Papers - MA Jian Feng

Elevated expression of SaMTP8.1 is involved in internal Mn detoxification in the hyperaccumulating ecotype of Sedum alfredii

Jun Ge, Lingli Lu, Jian Feng Ma

The Plant Journal   2025.6

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DOI： 10.1111/tpj.70240

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Role of polar localization of the silicon transporter OsLsi1 in metalloid uptake by rice roots

Noriyuki Konishi, Namiki Mitani-Ueno, Jian Feng Ma

Plant Physiology   2025.4

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DOI： 10.1093/plphys/kiaf196

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Symplastic and apoplastic pathways for local distribution of silicon in rice leaves

Sheng Huang, Naoki Yamaji, Noriyuki Konishi, Namiki Mitani‐Ueno, Jian Feng Ma

New Phytologist   2025.4

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Publishing type：Research paper (scientific journal)  

DOI： 10.1111/nph.70110

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Shoot-Silicon-Signal protein to regulate root silicon uptake in rice

Naoki Yamaji, Namiki Mitani-Ueno, Toshiki Fujii, Tomonori Shinya, Ji Feng Shao, Shota Watanuki, Yasunori Saitoh, Jian Feng Ma

Nature Communications   2024.12

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DOI： 10.1038/s41467-024-55322-7

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OsHAK4 functions in retrieving sodium from the phloem at the reproductive stage of rice

Jing Che, Naoki Yamaji, Shao Fei Wang, Yue Xia, Shun Ying Yang, Yan Hua Su, Ren Fang Shen, Jian Feng Ma

The Plant Journal   2024.10

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Publishing type：Research paper (scientific journal)  

DOI： 10.1111/tpj.16971

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Breeding for an elite malting barley cultivar with acid soil tolerance

Sheng Huang, Kazuhiro Sato, Jian Feng Ma

Communications Biology   7 ( 1 )   2024.9

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Publishing type：Research paper (scientific journal)   Publisher：Springer Science and Business Media LLC  

DOI： 10.1038/s42003-024-06903-1

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Other Link： https://www.nature.com/articles/s42003-024-06903-1

Tissue-specific deposition, speciation and transport of antimony in rice

Hengliang Huang, Naoki Yamaji, Jian Feng Ma

Plant Physiology   2024.7

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DOI： 10.1093/plphys/kiae289

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Genetic background influences mineral accumulation in rice straw and grains under different soil pH conditions. International journal

Toshio Yamamoto, Kazunari Kashihara, Tomoyuki Furuta, Qian Zhang, En Yu, Jian Feng Ma

Scientific reports   14 ( 1 )   15139 - 15139   2024.7

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Mineral element accumulation in plants is influenced by soil conditions and varietal factors. We investigated the dynamic accumulation of 12 elements in straw at the flowering stage and in grains at the mature stage in eight rice varieties with different genetic backgrounds (Japonica, Indica, and admixture) and flowering times (early, middle, and late) grown in soil with various pH levels. In straw, Cd, As, Mn, Zn, Ca, Mg, and Cu accumulation was influenced by both soil pH and varietal factors, whereas P, Mo, and K accumulation was influenced by pH, and Fe and Ni accumulation was affected by varietal factors. In grains, Cd, As, Mn, Cu, Ni, Mo, Ca, and Mg accumulation was influenced by both pH and varietal factors, whereas Zn, Fe, and P accumulation was affected by varietal factors, and K accumulation was not altered. Only As, Mn, Ca and Mg showed similar trends in the straw and grains, whereas the pH responses of Zn, P, K, and Ni differed between them. pH and flowering time had synergistic effects on Cd, Zn, and Mn in straw and on Cd, Ni, Mo, and Mn in grains. Soil pH is a major factor influencing mineral uptake in rice straw and grains, and genetic factors, flowering stage factors, and their interaction with soil pH contribute in a combined manner.

DOI： 10.1038/s41598-024-66036-7

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An oligo peptide transporter family member, OsOPT7, mediates xylem unloading of Fe for its preferential distribution in rice

Naoki Yamaji, Yuma Yoshioka, Sheng Huang, Takaaki Miyaji, Akimasa Sasaki, Jian Feng Ma

New Phytologist   2024.6

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Publishing type：Research paper (scientific journal)  

DOI： 10.1111/nph.19756

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Diverse roles of the metal binding domains and transport mechanism of copper transporting P-type ATPases

Zongxin Guo, Fredrik Orädd, Viktoria Bågenholm, Christina Grønberg, Jian Feng Ma, Peter Ott, Yong Wang, Magnus Andersson, Per Amstrup Pedersen, Kaituo Wang, Pontus Gourdon

Nature Communications   2024.3

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DOI： 10.1038/s41467-024-47001-4

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Metal Transport Systems in Plants. International journal

Sheng Huang, Naoki Yamaji, Jian Feng Ma

Annual review of plant biology   2024.2

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Language：English   Publishing type：Research paper (scientific journal)  

Plants take up metals, including the essential micronutrients [iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn)] and the toxic heavy metal cadmium (Cd), from soil and accumulate these metals in their edible parts, which are direct and indirect intake sources for humans. Multiple transporters belonging to different families are required to transport a metal from the soil to different organs and tissues, but only a few of them have been fully functionally characterized. The transport systems (the transporters required for uptake, translocation, distribution, redistribution, and their regulation) differ with metals and plant species, depending on the physiological roles, requirements of each metal, and anatomies of different organs and tissues. To maintain metal homeostasis in response to spatiotemporal fluctuations of metals in soil, plants have developed sophisticated and tightly regulated mechanisms through the regulation of transporters at the transcriptional and/or posttranscriptional levels. The manipulation of some transporters has succeeded in generating crops rich in essential metals but low in Cd accumulation. A better understanding of metal transport systems will contribute to better and safer crop production. Expected final online publication date for the Annual Review of Plant Biology, Volume 75 is May 2024. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

DOI： 10.1146/annurev-arplant-062923-021424

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Transport of mineral elements in plants and me

Ma Jian Feng

Fertilizer Science   45 ( 45 )   109 - 139   2024.2

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Language：Japanese   Publisher：The Fertilization Research Foundation  

DOI： 10.57411/fertilizerscience.45.45_109

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Other Link： https://ndlsearch.ndl.go.jp/books/R000000004-I033381300

Knockout of a rice K5.2 gene increases Ca accumulation in the grain

Peitong Wang, Naoki Yamaji, Namiki Mitani‐Ueno, Jun Ge, Jian Feng Ma

Journal of Integrative Plant Biology   2024.2

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DOI： 10.1111/jipb.13587

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Local distribution of manganese to leaf sheath is mediated by OsNramp5 in rice

Sheng Huang, Noriyuki Konishi, Naoki Yamaji, Jian Feng Ma

New Phytologist   2024.2

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DOI： 10.1111/nph.19454

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Uptake and Accumulation of Cobalt Is Mediated by OsNramp5 in Rice

Hengliang Huang, Naoki Yamaji, Sheng Huang, Jian Feng Ma

Plant Cell and Environment   2024

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Cobalt (Co) contamination in soils potentially affects human health through the food chain. Although rice (Oryza sativa) as a staple food is a major dietary source of human Co intake, it is poorly understood how Co is taken up by the roots and accumulated in rice grain. In this study, we physiologically characterized Co accumulation and identified the transporter for Co2+ uptake in rice. A dose-dependent experiment showed that Co mainly accumulated in rice roots. Further analysis with LA-ICP-MS showed Co deposited in most tissue of the roots, including exodermis, endodermis and stele region. Co accumulation analysis using mutants defective in divalent cation uptake showed that Co2+ uptake in rice is mediated by the Mn2+/Cd2+/Pb2+ transporter OsNramp5, rather than OsIRT1 for Fe2+ and OsZIP9 for Zn2+. Knockout of OsNramp5 enhanced tolerance to Co toxicity. Heterologous expression of OsNramp5 showed transport activity for Co2+ in Saccharomyces cerevisiae. Co2+ uptake was inhibited by either Mn2+ or Cd2+ supply. At the reproductive stage, the Co concentration in the straw and grains of the OsNramp5 knockout lines was decreased by 41%–48% and 28%–36%, respectively, compared with that of the wild-type rice. The expression level of OsNramp5 in the roots was not affected by Co2+. Taken together, our results indicate that OsNramp5 is a major transporter for Co2+ uptake in rice, which ultimately mediates Co accumulation in the grains.

DOI： 10.1111/pce.15130

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Silicon transport and its “homeostasis” in rice

Sheng Huang, Jian Feng Ma

Quantitative Plant Biology   2024

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Publishing type：Research paper (scientific journal)  

DOI： 10.1017/qpb.2024.19

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Dissecting the promotional effect of zinc on cadmium translocation from roots to shoots in rice

Jia-Dong Chang, Sheng Huang, Indi Wiseno, Fu-Qing Sui, Fan Feng, Luqing Zheng, Jian Feng Ma, Fang-Jie Zhao

Journal of Experimental Botany   2023.11

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DOI： 10.1093/jxb/erad330

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A silicon transporter gene required for healthy growth of rice on land International journal

Namiki Mitani-Ueno, Naoki Yamaji, Sheng Huang, Yuma Yoshioka, Takaaki Miyaji, Jian Feng Ma

Nature Communications   14 ( 1 )   6522 - 6522   2023.10

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Silicon (Si) is the most abundant mineral element in the earth's crust. Some plants actively accumulate Si as amorphous silica (phytoliths), which can protect plants from stresses. Here, we report a gene (SIET4) that is required for the proper accumulation and cell-specific deposition of Si in rice and show that it is essential for normal growth. SIET4 is constitutively expressed in leaves and encodes a Si transporter. SlET4 polarly localizes at the distal side of epidermal cells and cells surrounding the bulliform cells (motor cells) of the leaf blade, where Si is deposited. Knockout of SIET4 leads to the death of rice in the presence but not absence of Si. Further analysis shows that SIET4 knockout induces abnormal Si deposition in mesophyll cells and the induction of hundreds of genes related to various stress responses. These results indicate that SIET4 is required for the proper export of Si from leaf cells to the leaf surface and for the healthy growth of rice on land.

DOI： 10.1038/s41467-023-42180-y

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Knockout of a gene encoding a Gγ protein boosts alkaline tolerance in cereal crops. International journal

Peitong Wang, Jian Feng Ma

aBIOTECH   4 ( 2 )   180 - 183   2023.6

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Sorghum is highly tolerant to alkaline stress, but the underlying mechanisms are not well understood. Here, based on genotypic difference in alkaline tolerance of sorghum, it was found that AT1 (Alkaline tolerance 1) encoding a G protein is involved in alkaline tolerance through negatively modulating the phosphorylation level of PIP2, an aquaporin with transport activity for H2O2. Knockout of AT1 releases its inhibition of PIP2, thereby resulting in an increased transport of H2O2 from the cytosol into the apoplast, subsequently boosting alkaline tolerance.

DOI： 10.1007/s42994-023-00106-8

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Polar localization of a rice silicon transporter requires isoleucine at both C- and N-termini as well as positively charged residues. International journal

Noriyuki Konishi, Namiki Mitani-Ueno, Naoki Yamaji, Jian Feng Ma

The Plant cell   35 ( 6 )   2232 - 2250   2023.5

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Silicon (Si) is important for stable and high yields in rice (Oryza sativa), a typical Si hyperaccumulator. The high Si accumulation is achieved by the cooperation of 2 Si transporters, LOW SILICON 1 (OsLsi1) and OsLsi2, which are polarly localized in cells of the root exodermis and endodermis. However, the mechanism underlying their polar localization is unknown. Here, we identified amino acid residues critical for the polar localization of OsLsi1. Deletion of both N- and C-terminal regions resulted in the loss of its polar localization. Furthermore, the deletion of the C-terminus inhibited its trafficking from the endoplasmic reticulum to the plasma membrane. Detailed site-directed mutagenesis analysis showed that Ile18 at the N-terminal region and Ile285 at the C-terminal region were essential for the polar localization of OsLsi1. Moreover, a cluster of positively charged residues at the C-terminal region is also required for polar localization. Phosphorylation and Lys modifications of OsLsi1 are unlikely to be involved in its polar localization. Finally, we showed that the polar localization of OsLsi1 is required for the efficient uptake of Si. Our study not only identified critical residues required for the polar localization of OsLsi1, but also provided experimental evidence for the importance of transporter polarity for efficient nutrient uptake.

DOI： 10.1093/plcell/koad073

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ART1 and putrescine contribute to rice aluminum resistance via OsMYB30 in cell wall modification. International journal

Li Jun Gao, Xiang Pei Liu, Ke Ke Gao, Meng Qi Cui, Hui Hui Zhu, Gui Xin Li, Jing Ying Yan, Yun Rong Wu, Zhong Jie Ding, Xue Wei Chen, Jian Feng Ma, Nicholas P Harberd, Shao Jian Zheng

Journal of integrative plant biology   65 ( 4 )   934 - 949   2023.4

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Cell wall is the first physical barrier to aluminum (Al) toxicity. Modification of cell wall properties to change its binding capacity to Al is one of the major strategies for plant Al resistance; nevertheless, how it is regulated in rice remains largely unknown. In this study, we show that exogenous application of putrescines (Put) could significantly restore the Al resistance of art1, a rice mutant lacking the central regulator Al RESISTANCE TRANSCRIPTION FACTOR 1 (ART1), and reduce its Al accumulation particularly in the cell wall of root tips. Based on RNA-sequencing, yeast-one-hybrid and electrophoresis mobility shift assays, we identified an R2R3 MYB transcription factor OsMYB30 as the novel target in both ART1-dependent and Put-promoted Al resistance. Furthermore, transient dual-luciferase assay showed that ART1 directly inhibited the expression of OsMYB30, and in turn repressed Os4CL5-dependent 4-coumaric acid accumulation, hence reducing the Al-binding capacity of cell wall and enhancing Al resistance. Additionally, Put repressed OsMYB30 expression by eliminating Al-induced H2 O2 accumulation, while exogenous H2 O2 promoted OsMYB30 expression. We concluded that ART1 confers Put-promoted Al resistance via repression of OsMYB30-regulated modification of cell wall properties in rice.

DOI： 10.1111/jipb.13429

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Linking root morphology and anatomy with transporters for mineral element uptake in plants

Yu En, Naoki Yamaji, Jian Feng Ma

Plant and Soil   2023.3

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Publishing type：Research paper (scientific journal)  

DOI： 10.1007/s11104-022-05692-y

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100 essential questions for the future of agriculture

Yuming Hu, Taolan Zhao, Yafang Guo, Meng Wang, Kerstin Brachhold, Chengcai Chu, Andrew Hanson, Sachin Kumar, Rongcheng Lin, Wenjin Long, Ming Luo, Jian Feng Ma, Yansong Miao, Shaoping Nie, Yu Sheng, Weiming Shi, James Whelan, Qingyu Wu, Ziping Wu, Wei Xie, Yinong Yang, Chao Zhao, Lei Lei, Yong‐Guan Zhu, Qifa Zhang

Modern Agriculture   1 ( 1 )   4 - 12   2023.3

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Publishing type：Research paper (scientific journal)   Publisher：Wiley  

Abstract

The world is at a crossroad when it comes to agriculture. The global population is growing, and the demand for food is increasing, putting a strain on our agricultural resources and practices. To address this challenge, innovative, sustainable, and inclusive approaches to agriculture are urgently required. In this paper, we launched a call for Essential Questions for the Future of Agriculture and identified a priority list of 100 questions. We focus on 10 primary themes: transforming agri‐food systems, enhancing resilience of agriculture to climate change, mitigating climate change through agriculture, exploring resources and technologies for breeding, advancing cultivation methods, sustaining healthy agroecosystems, enabling smart and controlled‐environment agriculture for food security, promoting health and nutrition‐driven agriculture, exploring economic opportunities and addressing social challenges, and integrating one health and modern agriculture. We emphasise the critical importance of interdisciplinary and multidisciplinary research that integrates both basic and applied sciences and bridges the gaps among various stakeholders for achieving sustainable agriculture.

DOI： 10.1002/moda.5

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The ferroxidases LPR1 and LPR2 control iron translocation in the xylem of Arabidopsis plants. International journal

Zhong-Rui Xu, Mei-Ling Cai, Ying Yang, Ting-Ting You, Jian Feng Ma, Peng Wang, Fang-Jie Zhao

Molecular plant   15 ( 12 )   1962 - 1975   2022.12

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Language：English   Publishing type：Research paper (scientific journal)  

Iron (Fe) deficiency is common in agricultural crops and affects millions of people worldwide. Translocation of Fe in the xylem is a key step for Fe distribution in plants. The mechanism controlling this process remains largely unknown. Here, we report that two Arabidopsis ferroxidases, LPR1 and LPR2, play a crucial and redundant role in controlling Fe translocation in the xylem. LPR1 and LPR2 are mainly localized in the cell walls of xylem vessels and the surrounding cells in roots, leaves, and stems. Knockout of both LPR1 and LPR2 increased the proportion of Fe(II) in the xylem sap, and caused Fe deposition along the vascular bundles especially in the petioles and main veins of leaves, which was alleviated by blocking blue light. The lpr1 lpr2 double mutant displayed constitutive expression of Fe deficiency response genes and overaccumulation of Fe in the roots and mature leaves under Fe-sufficient supply, but Fe deficiency chlorosis in the new leaves and inflorescences under low Fe supply. Moreover, the lpr1 lpr2 double mutant showed lower Fe concentrations in the xylem and phloem saps, and impaired 57Fe translocation along the xylem. In vitro assays showed that Fe(III)-citrate, the main form of Fe in xylem sap, is easily photoreduced to Fe(II)-citrate, which is unstable and prone to adsorption by cell walls. Taken together, these results indicate that LPR1 and LPR2 are required to oxidize Fe(II) and maintain Fe(III)-citrate stability and mobility during xylem translocation against photoreduction. Our study not only uncovers an essential physiological role of LPR1 and LPR2 but also reveals a new mechanism by which plants maintain Fe mobility during long-distance translocation in the xylem.

DOI： 10.1016/j.molp.2022.11.003

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FE UPTAKE‐INDUCING PEPTIDE1 maintains Fe translocation by controlling Fe deficiency response genes in the vascular tissue of Arabidopsis International journal

Satoshi Okada, Gui J. Lei, Naoki Yamaji, Sheng Huang, Jian F. Ma, Keiichi Mochida, Takashi Hirayama

Plant, Cell &Environment   45 ( 11 )   3322 - 3337   2022.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Wiley  

FE UPTAKE-INDUCING PEPTIDE1 (FEP1), also named IRON MAN3 (IMA3) is a short peptide involved in the iron deficiency response in Arabidopsis thaliana. Recent studies uncovered its molecular function, but its physiological function in the systemic Fe response is not fully understood. To explore the physiological function of FEP1 in iron homoeostasis, we performed a transcriptome analysis using the FEP1 loss-of-function mutant fep1-1 and a transgenic line with oestrogen-inducible expression of FEP1. We determined that FEP1 specifically regulates several iron deficiency-responsive genes, indicating that FEP1 participates in iron translocation rather than iron uptake in roots. The iron concentration in xylem sap under iron-deficient conditions was lower in the fep1-1 mutant and higher in FEP1-induced transgenic plants compared with the wild type (WT). Perls staining revealed a greater accumulation of iron in the cortex of fep1-1 roots than in the WT root cortex, although total iron levels in roots were comparable in the two genotypes. Moreover, the fep1-1 mutation partially suppressed the iron overaccumulation phenotype in the leaves of the oligopeptide transporter3-2 (opt3-2) mutant. These data suggest that FEP1 plays a pivotal role in iron movement and in maintaining the iron quota in vascular tissues in Arabidopsis.

DOI： 10.1111/pce.14424

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Other Link： https://onlinelibrary.wiley.com/doi/full-xml/10.1111/pce.14424

Plant Hormone and Inorganic Ion Concentrations in the Xylem Exudate of Grafted Plants Depend on the Scion–Rootstock Combination International journal

Kohei Kawaguchi, Makoto Nakaune, Jian Feng Ma, Mikiko Kojima, Yumiko Takebayashi, Hitoshi Sakakibara, Shungo Otagaki, Shogo Matsumoto, Katsuhiro Shiratake

Plants   11 ( 19 )   2594 - 2594   2022.10

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：MDPI AG  

In grafted plants, inorganic ions and plant hormones in the xylem exudate transported from the rootstock to the scion directly or indirectly affect the scion, thereby improving the traits. Therefore, the concentration of these components in the xylem exudate of grafted plants may be an indicator for rootstock selection. On the other hand, few reports have presented a comprehensive analysis of substances transferred from the rootstock to the scion in plants grafted onto different rootstocks, primarily commercial cultivars. In this study, we measured inorganic ions and plant hormones in the xylem exudate from the rootstock to the scion in various grafted plants of tomato and eggplant. The results revealed that the concentrations of inorganic ions and plant hormones in the xylem exudate significantly differed depending on the type of rootstock. In addition, we confirmed the concentration of the inorganic ions and plant hormones in the xylem exudate of plants grafted onto the same tomato rootstock cultivars as rootstock with tomato or eggplant as the scions. As a result, the concentrations of inorganic ions and plant hormones in the xylem exudate were significantly different in the grafted plants with eggplant compared with tomato as the scion. These results suggest that signals from the scion (shoot) control the inorganic ions and plant hormones transported from the rootstock (root).

DOI： 10.3390/plants11192594

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Duplication of a manganese/cadmium transporter gene reduces cadmium accumulation in rice grain International journal

En Yu, Wenguang Wang, Naoki Yamaji, Shuichi Fukuoka, Jing Che, Daisei Ueno, Tsuyu Ando, Fenglin Deng, Kiyosumi Hori, Masahiro Yano, Ren Fang Shen, Jian Feng Ma

Nature Food   68 ( 8 )   597 - 607   2022.8

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Global contamination of soils with toxic cadmium (Cd) is a serious health threat. Here we found that a tandem duplication of a gene encoding a manganese/Cd transporter, OsNramp5, was responsible for low-Cd accumulation in Pokkali, an old rice cultivar. This duplication doubled the expression of OsNramp5 gene but did not alter its spatial expression pattern and cellular localization. Higher expression of OsNramp5 increased uptake of Cd and Mn into the root cells but decreased Cd release to the xylem. Introgression of this allele into Koshihikari, an elite rice cultivar, through backcrossing significantly reduced Cd accumulation in the grain when cultivated in soil heavily contaminated with Cd but did not affect both grain yield and eating quality. This study not only reveals the molecular mechanism underlying low-Cd accumulation but also provides a useful target for breeding rice cultivars with low-Cd accumulation.

DOI： 10.1038/s43016-022-00569-w

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A novel kinase subverts aluminium resistance by boosting ornithine decarboxylase‐dependent putrescine biosynthesis

Xiang P. Liu, Li J. Gao, Ben T. She, Gui X. Li, Yun R. Wu, Ji M. Xu, Zhong J. Ding, Jian F. Ma, Shao J. Zheng

Plant, Cell & Environment   2022.8

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Publishing type：Research paper (scientific journal)   Publisher：Wiley  

DOI： 10.1111/pce.14371

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A Golgi‐localized glycosyltransferase, OsGT14;1, is required for growth of both roots and shoots in rice

Peitong Wang, Naoki Yamaji, Jian Feng Ma

The Plant Journal   2022.8

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Publishing type：Research paper (scientific journal)  

DOI： 10.1111/tpj.15897

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A tonoplast-localized magnesium transporter is crucial for stomatal opening in Arabidopsis under high Mg2+ conditions. International journal

Shin-Ichiro Inoue, Maki Hayashi, Sheng Huang, Kengo Yokosho, Eiji Gotoh, Shuka Ikematsu, Masaki Okumura, Takamasa Suzuki, Takumi Kamura, Toshinori Kinoshita, Jian Feng Ma

The New phytologist   2022.7

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Plant stomata play an important role in CO2 uptake for photosynthesis and transpiration, but the mechanisms underlying stomatal opening and closing under changing environmental conditions are still not completely understood. Through large-scale genetic screening, we isolated an Arabidopsis mutant (closed stomata2 (cst2)) that is defective in stomatal opening. We cloned the causal gene (MGR1/CST2) and functionally characterized this gene. The mutant phenotype was caused by a mutation in a gene encoding an unknown protein with similarities to the human magnesium (Mg2+ ) efflux transporter ACDP/CNNM. MGR1/CST2 was localized to the tonoplast and showed transport activity for Mg2+ . This protein was constitutively and highly expressed in guard cells. Knockout of this gene resulted in stomatal closing, decreased photosynthesis and growth retardation, especially under high Mg2+ conditions, while overexpression of this gene increased stomatal opening and tolerance to high Mg2+ concentrations. Furthermore, guard cell-specific expression of MGR1/CST2 in the mutant partially restored its stomatal opening. Our results indicate that MGR1/CST2 expression in the leaf guard cells plays an important role in maintaining cytosolic Mg2+ concentrations through sequestering Mg2+ into vacuoles, which is required for stomatal opening, especially under high Mg2+ conditions.

DOI： 10.1111/nph.18410

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NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis

Lun Li, Zongzheng Zhu, Yonghui Liao, Changhong Yang, Ni Fan, Jie Zhang, Naoki Yamaji, Léon Dirick, Jian Feng Ma, Catherine Curie, Chao‐Feng Huang

The Plant Journal   2022.6

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Publishing type：Research paper (scientific journal)   Publisher：Wiley  

DOI： 10.1111/tpj.15754

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根におけるミネラルとその輸送体の可視化 Invited Reviewed

馬 建鋒, 山地直樹

アグリバイオ   6 ( 6 )   502 - 506   2022.6

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Authorship：Lead author,　Corresponding author   Language：Japanese   Publisher：東京 : 北隆館  

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Other Link： https://ndlsearch.ndl.go.jp/books/R000000004-I032231532

Cell-Type-Dependent but CME-Independent Polar Localization of Silicon Transporters in Rice

Noriyuki Konishi, Sheng Huang, Naoki Yamaji, Jian Feng Ma

Plant and Cell Physiology   63 ( 5 )   699 - 712   2022.5

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Publishing type：Research paper (scientific journal)   Publisher：Oxford University Press ({OUP})  

DOI： 10.1093/pcp/pcac032

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A pericycle‐localized silicon transporter for efficient xylem loading in rice

Sheng Huang, Naoki Yamaji, Gen Sakurai, Namiki Mitani‐Ueno, Noriyuki Konishi, Jian Feng Ma

New Phytologist   234 ( 1 )   197 - 208   2022.4

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Publishing type：Research paper (scientific journal)   Publisher：Wiley  

DOI： 10.1111/nph.17959

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A crucial role for a node‐localized transporter, HvSPDT, in loading phosphorus into barley grains International journal

Mian Gu, Hengliang Huang, Hiroshi Hisano, Guangda Ding, Sheng Huang, Namiki Mitani‐Ueno, Kengo Yokosho, Kazuhiro Sato, Naoki Yamaji, Jian Feng Ma

New Phytologist   2022.3

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Wiley  

Grains are the major sink of phosphorus (P) in cereal crops, accounting for 60-85% of total plant P, but the mechanisms underlying P loading into the grains are poorly understood. We functionally characterized a transporter gene required for the distribution of P to the grains in barley (Hordeum vulgare), HvSPDT (SULTR-like phosphorus distribution transporter). HvSPDT encoded a plasma membrane-localized Pi/H+ cotransporter. It was mainly expressed in the nodes at both the vegetative and reproductive stages. Furthermore, its expression was induced by inorganic phosphate (Pi) deficiency. In the nodes, HvSPDT was expressed in both the xylem and phloem region of enlarged and diffuse vascular bundles. Knockout of HvSPDT decreased the distribution of P to new leaves, but increased the distribution to old leaves at the vegetative growth stage under low P supply. However, knockout of HvSPDT did not alter the redistribution of P from old to young organs. At the reproductive stage, knockout of HvSPDT significantly decreased P allocation to the grains, resulting in a considerable reduction in grain yield, especially under P-limited conditions. Our results indicate that node-based HvSPDT plays a crucial role in loading P into barley grains through preferentially distributing P from the xylem and further to the phloem.

DOI： 10.1111/nph.18057

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Boron uptake in rice is regulated post-translationally via a clathrin-independent pathway

Sheng Huang, Noriyuki Konishi, Naoki Yamaji, Ji Feng Shao, Namiki Mitani-Ueno, Jian Feng Ma

Plant Physiology   188 ( 3 )   1649 - 1664   2022.3

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Publishing type：Research paper (scientific journal)   Publisher：Oxford University Press ({OUP})  

<title>Abstract</title>
Uptake of boron (B) in rice (Oryza sativa) is mediated by the Low silicon rice 1 (OsLsi1) channel, belonging to the NOD26-like intrinsic protein III subgroup, and the efflux transporter B transporter 1 (OsBOR1). However, it is unknown how these transporters cooperate for B uptake and how they are regulated in response to B fluctuations. Here, we examined the response of these two transporters to environmental B changes at the transcriptional and posttranslational level. OsBOR1 showed polar localization at the proximal side of both the exodermis and endodermis of mature root region, forming an efficient uptake system with OsLsi1 polarly localized at the distal side of the same cell layers. Expression of OsBOR1 and OsLsi1 was unaffected by B deficiency and excess. However, although OsLsi1 protein did not respond to high B at the protein level, OsBOR1 was degraded in response to high B within hours, which was accompanied with a significant decrease of total B uptake. The high B-induced degradation of OsBOR1 was inhibited in the presence of MG-132, a proteasome inhibitor, without disturbance of the polar localization. In contrast, neither the high B-induced degradation of OsBOR1 nor its polarity was affected by induced expression of dominant-negative mutated dynamin-related protein 1A (OsDRP1AK47A) or knockout of the mu subunit (AP2M) of adaptor protein-2 complex, suggesting that clathrin-mediated endocytosis is not involved in OsBOR1 degradation and polar localization. These results indicate that, in contrast to Arabidopsis thaliana, rice has a distinct regulatory mechanism for B uptake through clathrin-independent degradation of OsBOR1 in response to high B.

DOI： 10.1093/plphys/kiab575

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Role of calcium signaling in aluminum tolerance in Arabidopsis

Sheng Huang, Jian Feng Ma

New Phytologist   233 ( 6 )   2327 - 2329   2022.3

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DOI： 10.1111/nph.17953

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Metalloid transporters and their regulation in plants

Naoki Yamaji, Jian Feng Ma

Plant Physiology   187 ( 4 )   1929 - 1939   2021.12

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DOI： 10.1093/plphys/kiab326

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Acetic-acid-induced jasmonate signaling in root enhances drought avoidance in rice

Daisuke Ogawa, Yuya Suzuki, Takayuki Yokoo, Etsuko Katoh, Miyu Teruya, Masayuki Muramatsu, Jian Feng Ma, Yuri Yoshida, Shunsaku Isaji, Yuko Ogo, Mitsue Miyao, Jong-Myong Kim, Mikiko Kojima, Yumiko Takebayashi, Hitoshi Sakakibara, Shin Takeda, Kazunori Okada, Naoki Mori, Motoaki Seki, Yoshiki Habu

Scientific Reports   11 ( 1 )   2021.12

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Conferring drought resistant traits to crops is one of the major aims of current breeding programs in response to global climate changes. We previously showed that exogenous application of acetic acid to roots of various plants could induce increased survivability under subsequent drought stress conditions, but details of the metabolism of exogenously applied acetic acid, and the nature of signals induced by its application, have not been unveiled. In this study, we show that rice rapidly induces jasmonate signaling upon application of acetic acid, resulting in physiological changes similar to those seen under drought. The major metabolite of the exogenously applied acetic acid in xylem sap was determined as glutamine-a common and abundant component of xylem sap-indicating that acetic acid is not the direct agent inducing the observed physiological responses in shoots. Expression of drought-responsive genes in shoot under subsequent drought conditions was attenuated by acetic acid treatment. These data suggest that acetic acid activates root-to-shoot jasmonate signals that partially overlap with those induced by drought, thereby conferring an acclimated state on shoots prior to subsequent drought.

DOI： 10.1038/s41598-021-85355-7

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Structural basis for high selectivity of a rice silicon channel Lsi1

Yasunori Saitoh, Namiki Mitani-Ueno, Keisuke Saito, Kengo Matsuki, Sheng Huang, Lingli Yang, Naoki Yamaji, Hiroshi Ishikita, Jian-Ren Shen, Jian Feng Ma, Michihiro Suga

Nature Communications   12 ( 1 )   2021.12

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<title>Abstract</title>Silicon (Si), the most abundant mineral element in the earth’s crust, is taken up by plant roots in the form of silicic acid through Low silicon rice 1 (Lsi1). Lsi1 belongs to the Nodulin 26-like intrinsic protein subfamily in aquaporin and shows high selectivity for silicic acid. To uncover the structural basis for this high selectivity, here we show the crystal structure of the rice Lsi1 at a resolution of 1.8 Å. The structure reveals transmembrane helical orientations different from other aquaporins, characterized by a unique, widely opened, and hydrophilic selectivity filter (SF) composed of five residues. Our structural, functional, and theoretical investigations provide a solid structural basis for the Si uptake mechanism in plants, which will contribute to secure and sustainable rice production by manipulating Lsi1 selectivity for different metalloids.

DOI： 10.1038/s41467-021-26535-x

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Other Link： https://www.nature.com/articles/s41467-021-26535-x

Zinc Transport in Rice: Dilemma between optimal plant requirement and human nutrition. International journal

Sheng Huang, Naoki Yamaji, Jian Feng Ma

Journal of experimental botany   73 ( 6 )   1800 - 1808   2021.11

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Zinc (Zn) is an essential micronutrient for both plants and animals, while Zn deficiency in crops and humans is a global problem affecting crop productivity and human health. Since plants and humans differ in their Zn requirement, there is a dilemma between plant nutrition and human nutrition. In this review, we focus on the transport system of Zn from soil to grain in rice (Oryza sativa), which is a major dietary source of Zn for people subsiding on rice-based diets. We describe transporters belonging to different family, which are involved in the uptake, vacuolar sequestration, root-to-shoot translocation and distribution of Zn. We also discuss the possible regulation mechanism of these transporters. Several examples are given on enhancing Zn accumulation and bioavailability in rice grains through manipulation of genes highly expressed in the nodes, where Zn is highly deposited. We finally provide our perspectives toward breeding rice cultivars with both increased tolerance to Zn-deficiency stress and high Zn density in rice grains.

DOI： 10.1093/jxb/erab478

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Lateral roots but not root hairs contribute to high uptake of manganese and cadmium in rice. International journal

En Yu, Naoki Yamaji, Chuanzao Mao, Hua Wang, Jian Feng Ma

Journal of experimental botany   72 ( 20 )   7219 - 7228   2021.10

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Rice (Oryza sativa L.) can accumulate high manganese (Mn) in the shoots through uptake by the roots, which consist of crown roots, lateral roots and root hairs. We investigated the role of lateral roots and root hairs in Mn and cadmium (Cd) uptake by using two indica rice mutants defective in formation of lateral roots (osiaa11) and root hairs (osrhl1). The uptake of Mn and Cd in osiaa11 was significantly lower than that in wild type 'Kasalath', but there was no difference between wild type and osrhl1. Furthermore, a kinetic study showed that Mn uptake in osiaa11 was much lower than that in wild type and osrhl1 across a wide range of Mn concentrations. The role of lateral roots in Mn and Cd uptake was further confirmed in a japonica rice mutant defective in lateral root formation. We found that expression of Mn transporter gene Natural Resistance-Associated Macrophage Protein 5 (OsNRAMP5), but not of Metal Tolerance Protein 9 (OsMTP9), was lower in osiaa11 than in wild type; however, there were no differences between osrhl1 and the wild type. Immunostaining showed that OsNRAMP5 and OsMTP9 were localized in the exodermis and endodermis of crown roots and lateral roots, but not in the root hairs. Taken together, our results indicate that lateral roots, but not root hairs, play an important role in high Mn and Cd uptake in rice.

DOI： 10.1093/jxb/erab329

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Transport Systems of Mineral Elements in Plants: Transporters, Regulation and Utilization

Jian Feng Ma, Yi-Fang Tsay

Plant and Cell Physiology   62 ( 4 )   539 - 540   2021.9

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DOI： 10.1093/pcp/pcab026

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Germplasm evaluation for crop improvement: Analysis of grain quality and cadmium accumulation in barley

Kazuhiro Sato, Kazuyoshi Takeda, Jian Feng Ma

Journal of Cereal Science   101   103297 - 103297   2021.9

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Publishing type：Research paper (scientific journal)   Publisher：Elsevier {BV}  

Evaluating genetic variation in barley (Hordeum vulgare) germplasm, combined with genome-wide genotyping, is vital for identifying genes controlling important grain-quality traits. For example, in addition to traditional grain quality properties such as starch and protein contents, grain safety parameters such as heavy metal content, are important in the use of barley for human food and animal feed. A number of genes affecting grain quality have been identified by map-based cloning strategies and functionally analyzed by genetic transformation experiments. Moreover, germplasm evaluation yielded information that enabled the introgression of a key gene controlling grain cadmium accumulation into an elite barley cultivar, reducing the content of this heavy metal in grain. Genotyping of molecular markers and resequencing of germplasm accessions may provide information about how grain quality–related loci evolved and how the current allelic diversity was established. In this review, we describe germplasm resources for barley grain quality–related traits and the methods used to analyze the functions of genes controlling these traits, illustrating cadmium accumulation as an example. We also discuss future directions for the efficient identification of grain quality–related genes.

DOI： 10.1016/j.jcs.2021.103297

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Role of qGZn9a in controlling grain zinc concentration in rice, Oryza sativa L.

Miki Ogasawara, Naoya Miyazaki, Gotaro Monden, Kenta Taniko, Sathya Lim, Masahide Iwata, Takashige Ishii, Jian Feng Ma, Ryo Ishikawa

Theoretical and Applied Genetics   134 ( 9 )   3013 - 3022   2021.9

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Key message: A candidate gene responsible for higher grain zinc accumulation in rice was identified, which was probably associated with a partial defect in anther dehiscence. Abstract: Zinc (Zn) is an essential mineral element in many organisms. Zn deficiency in humans causes various health problems; therefore, an adequate dietary Zn intake is required daily. Rice, Oryza sativa, is one of the main crops cultivated in Asian countries, and one of the breeding scopes of rice is to increase the grain Zn levels. Previously, we found that an Australian wild rice strain, O. meridionalis W1627, exhibits higher grain Zn levels than cultivated rice, O. sativa Nipponbare, and identified responsible genomic loci. An increase in grain Zn levels caused by one of the loci, qGZn9a, is associated with fertility reduction, but how this negative effect on grain productivity is regulated remains unknown. In this study, we artificially trimmed spikelets on the flowering day and found that a reduction in number of seeds was associated with an increase in the grain Zn levels. We also found that a partial defect in anther dehiscence correlated with the increase in grain Zn levels in plants carrying the W1627 chromosomal segment at qGZn9a in a Nipponbare genetic background. Among eight candidate genes in the qGZn9a region, three were absent from the corresponding region of W1627; one of these, Os09g0384900, encoding a DUF295 protein with an unknown function, was found to be specifically expressed in the developing anther, thereby suggesting that the gene may be involved in the regulation of anther dehiscence. As fertility and grain Zn levels are essential agronomic traits in rice, our results highlight the importance of balancing these two traits.

DOI： 10.1007/s00122-021-03873-4

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Three polarly localized ammonium transporter 1 members are cooperatively responsible for ammonium uptake in rice under low ammonium condition

Noriyuki Konishi, Jian Feng Ma

New Phytologist   232 ( 4 )   1778 - 1792   2021.8

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Ammonium is a preferential nitrogen form for rice (Oryza sativa) grown in paddy field, but the molecular mechanisms for ammonium uptake have not been well understood. We functionally characterized three members belonging to ammonium transporter 1 (AMT1) and investigated their contributions to ammonium uptake. Spatial expression analysis showed that the upregulated expression of OsAMT1;1 and OsAMT1;2 and downregulated expression of OsAMT1;3 by ammonium were higher in the root mature region than in the root tips. All OsAMT1 members were polarly localized at the distal side of exodermis in the mature region of crown roots and lateral roots. Upon exposure to ammonium, localization of OsAMT1;1 and OsAMT1;2 was also observed in the endoplasmic reticulum, but their abundance in the plasma membrane was not changed. Single knockout of either gene did not affect ammonium uptake, but knockout of all three genes resulted in 95% reduction of ammonium uptake. However, the nitrogen uptake did not differ between the wild-type rice and triple mutants at high ammonium and nitrate supply. Our results indicate that three OsAMT1 members are cooperatively required for uptake of low ammonium in rice roots and that they undergo a distinct regulatory mechanism in response to ammonium.

DOI： 10.1111/nph.17679

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LYSINE KETOGLUTARATE REDUCTASE TRANS-SPLICING RELATED 1 is involved in temperature-dependent root growth in rice

En Yu, Naoki Yamaji, Keiich Mochida, Ivan Galis, Kanatani Asaka, Jian Feng Ma, Hideki Takahashi

Journal of Experimental Botany   72 ( 18 )   6336 - 6349   2021.5

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Root length is an important root parameter directly related to the uptake of water and nutrients. However, the molecular mechanisms controlling root length are still not fully understood. Here, we isolated a short-root mutant of rice, dice2 (defective in cell elongation 2). The cell length and meristem size of the roots were decreased in dice2, but the root function in terms of mineral element uptake, root cell width, and root anatomy were hardly altered compared with wild-type (WT) rice. The root growth defect in dice2 could be partially rescued by high temperature. Map-based cloning combined with a complementation test revealed that the short-root phenotype was caused by a nonsense mutation in a gene which was annotated to encode Lysine Ketoglutarate Reductase Trans-Splicing related 1 (OsLKRT1). OsLKRT1, encoding a cytosol-localized protein, was expressed in all cells of the root tip and elongation region as well as the shoot. RNA-seq analysis showed that there was no difference between dice2 and the WT in the expression level of genes involved in root development identified so far. These results indicate that OsLKRT1 is involved in a novel pathway required for root cell elongation in rice, although its exact role remains to be further investigated.

DOI： 10.1093/jxb/erab240

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ANAC044 is associated with P reutilization in P deficient Arabidopsis thaliana root cell wall in an ethylene dependent manner

Xiao Long Zhang, Qi Wu, Ye Tao, Xiao Fang Zhu, Naoki Takahashi, Masaaki Umeda, Ren Fang Shen, Jian Feng Ma

Environmental and Experimental Botany   185   104386 - 104386   2021.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Elsevier {BV}  

Phosphorus (P) deficiency is a major problem in agriculture, thus identifying mechanisms affecting plant's ability to reutilize previously assimilated P is a prerequisite for improving the P homeostasis in crops grown with P deficient soil. Here, we reported the involvement of a NAC (No apical meristem [NAM], Arabidopsis transcription activation factor [ATAF] and Cup-shaped cotyledon [CUC]) transcription factor in response to P deficiency. Compared to the wild type (WT, Col-0) and two independent complementary lines, the anac044 mutant displayed P deficiency resistant phenotype, together with the increased root length, root and shoot biomass under P deficiency. In addition, ANAC044 was highly expressed in root and silique. Upon P deficient treatment even within 1 d, ANAC044 transcript accumulation was strongly up-regulated. Further analysis revealed that, under P-deficient condition, the cell wall, particularly the pectin of anac044, released more P than that of WT and complementary lines, accompanied by an increment of ethylene production, as a result, more soluble and total P were available in anac044 root and shoot. Thus, the study here uncovers the role of ANAC044-regulated cell wall P remobilization through ethylene signaling under P deficiency.

DOI： 10.1016/j.envexpbot.2021.104386

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Role of a vacuolar iron transporter OsVIT2 in the distribution of iron to rice grains

Jing Che, Naoki Yamaji, Jian Feng Ma

New Phytologist   230 ( 3 )   1049 - 1062   2021.5

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Iron (Fe) from rice grains is an important source of dietary intake; however, the molecular mechanisms responsible for loading of Fe to the grains are poorly understood. We functionally characterized a vacuolar iron transporter gene, OsVIT2 in terms of expression pattern, cellular localization, and mutant phenotypes. OsVIT2 was expressed in the parenchyma cell bridges of nodes, in the mestome sheath of leaf sheath and aleurone of the caryopsis. Mutation of OsVIT2 resulted in decreased Fe distribution to the leaf sheath, nodes, and aleurone, but increased Fe to the leaf blade and grains. Furthermore, Fe was heavily deposited in the parenchyma cell bridges, mestome sheath and aleurone in the wild-type rice, but this accumulation was decreased in the knockout lines. Conversely, heavier deposition of Fe was observed in the embryo and endosperm of the grains of knockout lines compared with the wild-type rice, resulting in increased Fe accumulation in the polished rice without yield penalty. These results indicate that OsVIT2 is involved in the distribution of Fe to the grains through sequestering Fe into vacuoles in mestome sheath, nodes, and aleurone layer and that knockout of this gene provides a potential way for Fe biofortification without yield penalty.

DOI： 10.1111/nph.17219

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Expression Level of Transcription Factor ART1 Is Responsible for Differential Aluminum Tolerance in Indica Rice

Li Ming Sun, Jing Che, Jian Feng Ma, Ren Fang Shen

PLANTS-BASEL   10 ( 4 )   2021.4

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：MDPI  

Rice is the most aluminum (Al)-tolerant species among the small grain cereals, but there are great variations in the Al tolerance between subspecies, with higher tolerance in japonica subspecies than indica subspecies. Here, we performed a screening of Al tolerance using 65 indica cultivars and found that there was also a large genotypic difference in Al tolerance among indica subspecies. Further characterization of two cultivars contrasting in Al tolerance showed that the expression level of ART1 (ALUMINUM RESISTANCE TRANSCRIPTION FACTOR 1) encoding a C2H2-type Zn-finger transcription factor, was higher in an Al-tolerant indica cultivar, Jinguoyin, than in an Al-sensitive indica cultivar, Kasalath. Furthermore, a dose-response experiment showed that ART1 expression was not induced by Al in both cultivars, but Jinguoyin always showed 5.9 to 11.4-fold higher expression compared with Kasalath, irrespectively of Al concentrations. Among genes regulated by ART1, 19 genes showed higher expression in Jinguoyin than in Kasalath. This is associated with less Al accumulation in the root tip cell wall in Jinguoyin. Sequence comparison of the 2-kb promoter region of ART1 revealed the extensive sequence polymorphism between two cultivars. Whole transcriptome analysis with RNA-seq revealed that more genes were up- and downregulated by Al in Kasalath than in Jinguoyin. Taken together, our results suggest that there is a large genotypic variation in Al tolerance in indica rice and that the different expression level of ART1 is responsible for the genotypic difference in the Al tolerance.

DOI： 10.3390/plants10040634

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Fine regulation system for distribution of boron to different tissues in rice

Ji Feng Shao, Naoki Yamaji, Sheng Huang, Jian Feng Ma

NEW PHYTOLOGIST   230 ( 2 )   656 - 668   2021.2

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Boron (B) is essential for growth and development, with the B requirement differing depending on the particular organs and tissues, but the molecular mechanisms underlying the preferential distribution of B to different tissues are poorly understood.We investigated the role of a rice gene (OsBOR1) encoding a B efflux transporter in the distribution of B to different tissues under different B supplies.OsBOR1 was highly expressed in the nodes at all growth stages. The OsBOR1 protein shows polar localization at the distal side of bundle sheath cells in nodes and xylem parenchyma cells of elongating leaf sheath, but in the mature leaf sheath and blade at the proximal side of bundle sheath cells. Furthermore, the expression of OsBOR1 was not affected by external B fluctuations, but the OsBOR1 protein was gradually degraded in response to high B. Knockout of this gene altered B distribution, decreasing the distribution of B to new leaves and panicles but increasing B distribution to old leaves.These results indicate that OsBOR1 expressed in nodes and leaf sheath is involved in the preferential distribution of B to different tissues in rice. Furthermore, the OsBOR1 undergoes degradation in response to high B for fine regulation of B distribution to different tissues.

DOI： 10.1111/nph.17169

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A transporter for delivering zinc to the developing tiller bud and panicle in rice

Shuai Mu, Naoki Yamaji, Akimasa Sasaki, Le Luo, Binbin Du, Jing Che, Huichao Shi, Haoqiang Zhao, Sheng Huang, Fenglin Deng, Zhenguo Shen, Mary Lou Guerinot, Luqing Zheng, Jian Feng Ma

Plant Journal   105 ( 3 )   786 - 799   2021.2

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Tiller number is one of the most important agronomic traits that determine rice (Oryza sativa) yield. Active growth of tiller bud (TB) requires high amount of mineral nutrients; however, the mechanism underlying the distribution of mineral nutrients to TB with low transpiration is unknown. Here, we found that the distribution of Zn to TB is mediated by OsZIP4, one of the ZIP (ZRT, IRT-like protein) family members. The expression of OsZIP4 was highly detected in TB and nodes, and was induced by Zn deficiency. Immunostaining analysis revealed that OsZIP4 was mainly expressed in phloem of diffuse vascular bundles in the nodes and the axillary meristem. The mutation of OsZIP4 did not affect the total Zn uptake, but altered Zn distribution; less Zn was delivered to TB and new leaf, but more Zn was retained in the basal stems at the vegetative growth stage. Bioimaging analysis showed that the mutant aberrantly accumulated Zn in enlarged and transit vascular bundles of the basal node, whereas in wild-type high accumulation of Zn was observed in the meristem part. At the reproductive stage, mutation of OsZIP4 resulted in delayed panicle development, which is associated with decreased Zn distribution to the panicles. Collectively, OsZIP4 is involved in transporting Zn to the phloem of diffuse vascular bundles in the nodes for subsequent distribution to TBs and other developing tissues. It also plays a role in transporting Zn to meristem cells in the TBs.

DOI： 10.1111/tpj.15073

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Transport of cadmium from soil to grain in cereal crops: A review

Jian Feng MA, Ren Fang SHEN, Ji Feng SHAO

Pedosphere   31 ( 1 )   3 - 10   2021.2

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Due to rapid urbanization and industrialization, many soils for crop production are contaminated by cadmium (Cd), a heavy metal highly toxic to many organisms. Cereal crops such as rice, wheat, maize, and barley are the primary dietary source of Cd for humans, and reducing Cd transfer from soil to their grains is therefore an important issue for food safety. During the last decade, great progress has been made in elucidating the molecular mechanisms of Cd transport, particularly in rice. Inter- and intraspecific variations in Cd accumulation have been observed in cereal crops. Transporters for Cd have been identified in rice and other cereal crops using genotypic differences in Cd accumulation and mutant approaches. These transporters belong to different transporter families and are involved in the uptake, vacuolar sequestration, root-to-shoot translocation, and distribution of Cd. Attempts have been made to reduce Cd accumulation in grains by manipulating these transporters through overexpression or knockout of the transporter genes, as well as through marker-assisted selection breeding based on genotypic differences in Cd accumulation in the grains. In this review, we describe recent progress on molecular mechanisms of Cd accumulation in cereal crops and compare different molecular strategies for minimizing Cd accumulation in grains.

DOI： 10.1016/S1002-0160(20)60015-7

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Cadmium transfer in contaminated soil-rice systems: Insights from solid-state speciation analysis and stable isotope fractionation

Matthias Wiggenhauser, Anne Marie Aucour, Sarah Bureau, Sylvain Campillo, Philippe Telouk, Marco Romani, Jian Feng Ma, Gautier Landrot, Géraldine Sarret

Environmental Pollution   269   2021.1

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Initial Cadmium (Cd) isotope fractionation studies in cereals ascribed the retention of Cd and its light isotopes to the binding of Cd to sulfur (S). To better understand the relation of Cd binding to S and Cd isotope fractionation in soils and plants, we combined isotope and XAS speciation analyses in soil-rice systems that were rich in Cd and S. The systems included distinct water management (flooded vs. non-flooded) and rice accessions with (excluder) and without (non-excluder) functional membrane transporter OsHMA3 that transports Cd into root vacuoles. Initially, 13% of Cd in the soil was bound to S. Through soil flooding, the proportion of Cd bound to S increased to 100%. Soil flooding enriched the rice plants towards heavy isotopes (δ114/110Cd = −0.37 to −0.39%) compared to the plants that grew on non-flooded soils (δ114/110Cd = −0.45 to −0.56%) suggesting that preferentially light Cd isotopes precipitated into Cd sulfides. Isotope compositions in CaCl2 root extracts indicated that the root surface contributed to the isotope shift between soil and plant during soil flooding. In rice roots, Cd was fully bound to S in all treatments. The roots in the excluder rice strongly retained Cd and its lights isotopes while heavy isotopes were transported to the shoots (Δ114/110Cdshoot-root 0.16–0.19‰). The non-excluder rice accumulated Cd in shoots and the apparent difference in isotope composition between roots and shoots was smaller than that of the excluder rice (Δ114/110Cdshoot-root −0.02 to 0.08‰). We ascribe the retention of light Cd isotopes in the roots of the excluder rice to the membrane transport of Cd by OsHMA3 and/or chelating Cd–S complexes in the vacuole. Cd–S was the major binding form in flooded soils and rice roots and partly contributed to the immobilization of Cd and its light isotopes in soil-rice systems.

DOI： 10.1016/j.envpol.2020.115934

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Jian Feng Ma

Jian Feng Ma

NEW PHYTOLOGIST   229 ( 2 )   673 - 674   2021.1

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DOI： 10.1111/nph.17066

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Two metallothionein genes highly expressed in rice nodes are involved in distribution of Zn to the grain

Gui Jie Lei, Naoki Yamaji, Jian Feng Ma

NEW PHYTOLOGIST   229 ( 2 )   1007 - 1020   2021.1

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A rice node is a hub for distribution of mineral elements; however, most genes highly expressed in the node have not been functionally characterized. Transcriptomic analysis of a rice node revealed that two metallothionein genes,OsMT2bandOsMT2c, were highly expressed in the node I. We functionally characterized these genes in terms of gene expression pattern, cellular and subcellular localization, phenotypic analysis of the single and double knockout mutants and metal-binding ability. BothOsMT2bandOsMT2cwere mainly and constitutively expressed in the phloem region of enlarged and diffuse vascular bundles in the nodes and of the anther. Knockout of eitherOsMT2borOsMT2cincreased zinc (Zn) accumulation in the nodes, but decreased Zn distribution to the panicle, resulting in decreased grain yield. A double mutant,osmt2bmt2c, showed further negative effects on the Zn distribution and grain yield. By contrast, knockout ofOsMT2bhad a small effect on copper (Cu) accumulation. Both OsMT2b and OsMT2c showed binding ability with Zn, whereas only OsMT2b showed binding ability with Cu in yeast. Our results suggest that bothOsMT2bandOsMT2cplay an important role mainly in the distribution of Zn to grain through chelation and subsequent transport of Zn in the phloem in rice.

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Linking transport system of silicon with its accumulation in different plant species

Namiki Mitani-Ueno, Jian Feng Ma

Soil Science and Plant Nutrition   67 ( 1 )   10 - 17   2021

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Silicon (Si) is a beneficial element for plants, which helps to mitigate various biotic and abiotic stresses. Since the last review on Si published in this journal in 2004, great progress has been made in understanding transport system of Si in different plant species. The discovery of two different transporters for Si (Lsi1 and Lsi2) in rice led to intensive investigation of Si transporters in other plant species. Lsi1 belongs to the Nodulin 26-like intrinsic proteins (NIPs) subfamily in the aquaporin (AQP) family and functions as an influx transporter for Si. By contrast, Lsi2 belongs to the anion transporter superfamily and functions as an efflux transporter of Si. They are polarly localized at the distal and proximal sides, respectively, of both exodermis and endodermis of rice roots and are required for efficient uptake of Si. So far, homologs of Lsi1 and Lsi2 are identified not only in monocots, but also in dicots, which greatly differ in Si accumulation in the aboveground parts. However, the expression pattern, cell-type-specific expression, and polar localization of these transporters differ with plant species. In this review, we focus on recent progress in Si transporters identified in different plant species. We link these transporters with an accumulation of Si in different plant species in terms of expression pattern, cell-type-specific expression, polar localization of these transporters and propose three uptake systems of Si in different plant species. We also provide the perspectives toward a better understanding of Si transport system in different plant species and discuss its essentiality for plant growth.

DOI： 10.1080/00380768.2020.1845972

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Buckwheat FeNramp5 Mediates High Manganese Uptake in Roots

Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

Plant and Cell Physiology   62 ( 4 )   600 - 609   2020.12

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Manganese (Mn) is an essential element for plant growth and development, but transporters required for Mn uptake have only been identified in a few plant species. Here, we functionally characterized a member of the natural resistance-associated macrophage proteins (Nramps) family, FeNramp5 in buckwheat (Fagopyrum esculentum Moench), which is known as a species well adapted to acidic soils. FeNramp5 was mainly expressed in the roots, and its expression was upregulated by the deficiency of Mn and Fe. Furthermore, spatial and tissue-specific expression analysis showed that FeNramp5 was expressed in all tissues of the basal root regions. FeNramp5-GFP protein was localized to the plasma membrane when transiently expressed in buckwheat leaf protoplast. FeNramp5 showed the transport activity for Mn2+ and Cd2+ but not for Fe2+ when expressed in yeast. Furthermore, the transport activity for Mn2+ was higher in yeast expressing FeNramp5 than in yeast expressing AtNramp1. FeNramp5 was also able to complement the phenotype of Arabidopsis atnramp1 mutant in terms of the growth and accumulation of Mn and Cd. The absolute expression level of AtNramp1 was comparable to that of FeNramp5 in the roots, but buckwheat accumulated higher Mn than Arabidopsis when grown under the same condition. Further analysis showed that at least motif B in FeNramp5 seems important for its high transport activity for Mn. These results indicate that FeNramp5 is a transporter for the uptake of Mn and Cd and its higher transport activity for Mn is probably associated with higher Mn accumulation in buckwheat.

DOI： 10.1093/pcp/pcaa153

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Silicon suppresses zinc uptake through down-regulating zinc transporter gene in rice

Sheng Huang, Jian Feng Ma

PHYSIOLOGIA PLANTARUM   170 ( 4 )   580 - 591   2020.12

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One of the beneficial effects of silicon (Si) is to improve nutrient imbalance including deficiency and excess of nutrients, however the molecular mechanisms underlying this effect are still poorly understood. In this study, we investigated the interaction between Si and zinc (Zn) in rice by using a mutant (lsi1) defective in Si uptake and its wild-type (WT, cv. Oochikara) at different Zn levels. High Zn inhibited the root elongation of both WT andlsi1mutant, but Si did not alleviate this inhibition in both lines. By contrast, Si supply decreased Zn concentration in both the roots and shoots of the WT, but not in thelsi1mutant. A short-term (24 h) labeling experiment with stable isotope(67)Zn showed that Si decreased(67)Zn uptake, but did not affect the root-to-shoot translocation and distribution ratio to different organs of(67)Zn in the WT. Furthermore, Si accumulated in the shoots, rather than Si in the external solution, is required for suppressing Zn uptake, but this was not caused by Si-decreased transpiration. A kinetic study showed that Si did not affect K(m)value of root Zn uptake, but decreased V(max)value in the WT. Analysis of genes related with Zn transport showed that among ZIP family genes, the expression of onlyOsZIP1implicated in Zn uptake, was down-regulated by Si in the WT, but not in thelsi1mutant. These results indicate that Si accumulated in the shoots suppresses the Zn uptake through down-regulating the transporter gene involved in Zn uptake in rice.

DOI： 10.1111/ppl.13196

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The grapevine NIP2;1 aquaporin is a silicon channel

Henrique Noronha, Angelica Silva, Namiki Mitani-Ueno, Carlos Conde, Farzana Sabir, Catarina Prista, Graca Soveral, Paul Isenring, Jian Feng Ma, Richard R. Belanger, Hernani Geros

JOURNAL OF EXPERIMENTAL BOTANY   71 ( 21 )   6789 - 6798   2020.12

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Silicon (Si) supplementation has been shown to improve plant tolerance to different stresses, and its accumulation in the aerial organs is mediated by NIP2;1 aquaporins (Lsi channels) and Lsi2-type exporters in roots. In the present study, we tested the hypothesis that grapevine expresses a functional NIP2;1 that accounts for root Si uptake and, eventually, Si accumulation in leaves. Own-rooted grapevine cuttings of the cultivar Vinhao accumulated >0.2% Si (DW) in leaves when irrigated with 1.5 mM Si for 1 month, while Si was undetected in control leaves. Real-time PCR showed that VvNIP2;1 was highly expressed in roots and in green berries. The transient transformation of tobacco leaf epidermal cells mediated by Agrobacterium tumefaciens confirmed VvNIP2;1 localization at the plasma membrane. Transport experiments in oocytes showed that VvNIP2;1 mediates Si and arsenite uptake, whereas permeability studies revealed that VvNIP2;1 expressed in yeast is unable to transport water and glycerol. Si supplementation to pigmented grape cultured cells (cv. Gamay Freaux) had no impact on the total phenolic and anthocyanin content, or on the growth rate and VvNIP2;1 expression. Long-term experiments should help determine the extent of Si uptake over time and whether grapevine can benefit from Si fertilization.

DOI： 10.1093/jxb/eraa294

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Simultaneous changes in seed size, oil content and protein content driven by selection of SWEET homologues during soybean domestication

Shoudong Wang, Shulin Liu, Jie Wang, Kengo Yokosho, Bin Zhou, Ya-Chi Yu, Zhi Liu, Wolf B. Frommer, Jian Feng Ma, Li-Qing Chen, Yuefeng Guan, Huixia Shou, Zhixi Tian

NATIONAL SCIENCE REVIEW   7 ( 11 )   1776 - 1786   2020.11

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Soybean accounts for more than half of the global production of oilseed and more than a quarter of the protein used globally for human food and animal feed. Soybean domestication involved parallel increases in seed size and oil content, and a concomitant decrease in protein content. However, science has not yet discovered whether these effects were due to selective pressure on a single gene or multiple genes. Here, re-sequencing data from >800 genotypes revealed a strong selection during soybean domestication on GmSWEET10a. The selection of GmSWEET10a conferred simultaneous increases in soybean-seed size and oil content as well as a reduction in the protein content. The result was validated using both near-isogenic lines carrying substitution of haplotype chromosomal segments and transgenic soybeans. Moreover, GmSWEET10b was found to be functionally redundant with its homologue GmSWEET10a and to be undergoing selection in current breeding, leading the the elite allele GmSWEET10b, a potential target for present-day soybean breeding. Both GmSWEET10a and GmSWEET10b were shown to transport sucrose and hexose, contributing to sugar allocation from seed coat to embryo, which consequently determines oil and protein contents and seed size in soybean. We conclude that past selection of optimal GmSWEET10a alleles drove the initial domestication of multiple soybean-seed traits and that targeted selection of the elite allele GmSWEET10b may further improve the yield and seed quality of modem soybean cultivars.

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OsNRAMP1transporter contributes to cadmium and manganese uptake in rice

Jia-Dong Chang, Sheng Huang, Naoki Yamaji, Wenwen Zhang, Jian Feng Ma, Fang-Jie Zhao

PLANT CELL AND ENVIRONMENT   43 ( 10 )   2476 - 2491   2020.10

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Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, thein plantafunction of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As.OsNRAMP1was mainly expressed in roots and leaves and encoded a plasma membrane-localized protein.OsNRAMP1expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout ofOsNRAMP1resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout ofOsNRAMP1had smaller effects on Cd and Mn uptake than knockout ofOsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant.

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Overexpression of the manganese/cadmium transporter OsNRAMP5 reduces cadmium accumulation in rice grain

Jia-Dong Chang, Sheng Huang, Noriyuki Konishi, Peng Wang, Jie Chen, Xin-Yuan Huang, Jian Feng Ma, Fang-Jie Zhao

JOURNAL OF EXPERIMENTAL BOTANY   71 ( 18 )   5705 - 5715   2020.9

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Rice is a major dietary source of the toxic metal cadmium (Cd), and reducing its accumulation in the grain is therefore important for food safety. We selected two cultivars with contrasting Cd accumulation and generated transgenic lines overexpressing OsNRAMP5, which encodes a major influx transporter for manganese (Mn) and Cd. We used two different promoters to control the expression, namely OsActin1 and maize Ubiquitin. Overexpression of OsNRAMP5 increased Cd and Mn uptake into the roots, but markedly decreased Cd accumulation in the shoots, whilst having a relatively small effect on Mn accumulation in the shoots. The overexpressed OsNRAMP5 protein was localized to the plasma membrane of all cell types in the root tips and lateral root primordia without polarity. Synchrotron X-ray fluorescence mapping showed that the overexpression lines accumulated more Cd in the root tips and lateral root primordia compared with the wild-type. When grown in three Cd-contaminated paddy soils, overexpression of OsNRAMP5 decreased concentration of Cd in the grain by 49-94% compared with the wild type. OsNRAMP5-overexpression plants had decreased Cd translocation from roots to shoots as a result of disruption of its radial transport into the stele for xylem loading, demonstrating the effect of transporter localization and polarity on ion homeostasis.

DOI： 10.1093/jxb/eraa287

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Effect of ferritin on nitrogen fixation in Lotus japonicus nodules under various iron concentrations

Yamikani Frank Chikoti, Supriadi, Mallika Duangkhet, Sirinapa Chungopast, Shigeyuki Tajima, Jian Feng Ma, Mika Nomura

JOURNAL OF PLANT PHYSIOLOGY   252   2020.9

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：ELSEVIER GMBH  

In the nitrogen fixation process, iron plays a vital role by being part of many symbiotic proteins, such as nitrogenase and leghemoglobin, in an active symbiosis. Excess or insufficient iron in active nitrogen fixation negatively affects the entire process. In Lotus japonicus nodules, ferritin is expressed at the initial stages of nodule development and increases at the nodule senescence stage to mobilize iron release during that stage. In this study, we investigated the effects of overexpressing and suppressing ferritin on nitrogen fixation. Acetylene reduction activity revealed that nitrogen fixation is affected by the overexpression of ferritin at high iron concentrations, but at low iron concentrations, higher nitrogen fixation was observed in ferritin-suppressed plants. qRT-PCR data indicated that suppression of ferritin in nodules induces antioxidant genes, such as superoxide dismutase, dehydroascorbate reductase and ascorbate peroxidase, to detoxify reactive oxygen species. Our data suggest that suppressing ferritin in the nodules is effective for higher nitrogen fixation under iron deficient conditions. Overaccumulated ferritin in nodule is effective under the higher iron conditions, such as senescence state.

DOI： 10.1016/j.jplph.2020.153247

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Node-Localized Transporters of Phosphorus Essential for Seed Development in Rice

Jing Che, Naoki Yamaji, Takaaki Miyaji, Namiki Mitani-Ueno, Yuri Kato, Ren Fang Shen, Jian Feng Ma

Plant and Cell Physiology   61 ( 8 )   1387 - 1398   2020.8

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About 60-85% of total phosphorus (P) in cereal crops is finally allocated to seeds, where it is required for seed development, germination and early growth. However, little is known about the molecular mechanisms underlying P allocation to seeds. Here, we found that two members (OsPHO1;1 and OsPHO1;2) of the PHO1 gene family are involved in the distribution of P to seeds in rice. Both OsPHO1;1 and OsPHO1;2 were localized to the plasma membrane and showed influx transport activities for inorganic phosphate. At the reproductive stage, both OsPHO1;1 and OsPHO1;2 showed higher expression in node I, the uppermost node connecting to the panicle. OsPHO1;1 was mainly localized at the phloem region of diffuse vascular bundles (DVBs) of node I, while OsPHO1;2 was expressed in the xylem parenchyma cells of the enlarged vascular bundles (EVBs). In addition, they were also expressed in the ovular vascular trace, the outer layer of the inner integument (OsPHO1;1) and in the nucellar epidermis (OsPHO1;2) of caryopses. Knockout of OsPHO1;2, as well as OsPHO1;1 to a lesser extent, decreased the distribution of P to the seed, resulting in decreased seed size and delayed germination. Taken together, OsPHO1;2 expressed in node I is responsible for the unloading of P from the xylem of EVBs, while OsPHO1;1 is involved in reloading P into the phloem of DVBs for subsequent allocation of P to seeds. Furthermore, OsPHO1;1 and OsPHO1;2 expression in the caryopsis is important for delivering P from the maternal tissues to the filial tissues for seed development.

DOI： 10.1093/pcp/pcaa074

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Breeding for low cadmium barley by introgression of a Sukkula-like transposable element

Gui Jie Lei, Miho Fujii-Kashino, De Zhi Wu, Hiroshi Hisano, Daisuke Saisho, Fenglin Deng, Naoki Yamaji, Kazuhiro Sato, Fang-Jie Zhao, Jian Feng Ma

NATURE FOOD   1 ( 8 )   489 - U17   2020.8

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：SPRINGERNATURE  

Barley is the fourth most produced cereal crop in the world and one of the major dietary sources of cadmium (Cd), which poses serious threats to human health. Here, we identify a gene that encodes a P-type heavy metal ATPase 3 (HvHMA3) responsible for grain Cd accumulation in barley. HvHMA3 from the high Cd barley variety Haruna Nijo in Japan and the low Cd variety BCS318 in Afghanistan shared 97% identity at the amino acid level. In addition, the HvHMA3 from both varieties showed similar transport activity for Cd and the same subcellular localization at the tonoplast. However, the expression of HvHMA3 was double in BCS318 than in Haruna Nijo. A 3.3-kilobase Sukkula-like transposable element was found to be inserted upstream of the gene in the low Cd variety, which functioned as a promoter and enhanced the expression of HvHMA3. Introgression of this insertion to an elite barley cultivar through backcrossing resulted in decreased Cd accumulation in the grain grown in Cd-contaminated soil without yield penalty. The decreased Cd accumulation resulting from the insertion was also found in some other barley landraces in the world. Our results indicate that insertion of the Sukkula-like transposable element plays an important role in upregulating HvHMA3 expression.The primary source of human exposure to the highly toxic heavy metal cadmium (Cd) is diet. This study identified a gene encoding a P-type heavy metal ATPase 3 (HvHMA3) that is responsible for Cd accumulation in barley grain. A Sukkula-like transposable element was found to play an important role in upregulating the expression of HvHMA3, thereby decreasing Cd accumulation in the grain.

DOI： 10.1038/s43016-020-0130-x

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Diel magnesium fluctuations in chloroplasts contribute to photosynthesis in rice

Jian Li, Kengo Yokosho, Sheng Liu, Hong Rui Cao, Naoki Yamaji, Xin Guang Zhu, Hong Liao, Jian Feng Ma, Zhi Chang Chen

NATURE PLANTS   6 ( 7 )   848 - +   2020.7

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Photosynthesis in plants responds to light fluctuations and displays circadian rhythms in various aspects. Here a new regulator of photosynthetic rhythms is identified in rice and shown to control diurnal magnesium fluctuations in the chloroplast. Further engineering attempts yield enhanced rice growth and photosynthesis.Photosynthesis provides food, fibre and fuel that support our society; understanding the mechanisms controlling dynamic changes in this process helps identify new options to improve photosynthesis. Photosynthesis shows diel changes, which have been largely attributed to external light/dark conditions, as well as internal gene expression and the post-translational modification of critical enzymes. Here we report diel fluctuations of magnesium (Mg) in rice (Oryza sativa) chloroplasts, which may function as a rhythm regulator contributing to the post-translational regulation of photosynthetic CO(2)assimilation in rice. We found that a chloroplast-localized Mg(2+)transporter gene,OsMGT3, which is rhythmically expressed in leaf mesophyll cells, partly modulates Mg fluctuations in rice chloroplasts. Knockout ofOsMGT3substantially reduced Mg(2+)uptake, as well as the amplitude of free Mg(2+)fluctuations in chloroplasts, which was closely associated with a decrease in ribulose 1,5-bisphosphate carboxylase activity in vivo and a consequent decline in the photosynthetic rate. In addition, the mesophyll-specific overexpression ofOsMGT3remarkably improved photosynthetic efficiency and growth performance in rice. Taken together, these observations demonstrate that OsMGT3-dependent diel Mg fluctuations in chloroplasts may contribute to Mg-dependent enzyme activities for photosynthesis over the daily cycle. Enhancing Mg(2+)input to chloroplasts could be a potential approach to improving photosynthetic efficiency in plants.

DOI： 10.1038/s41477-020-0686-3

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The ZIP Transporter Family Member OsZIP9 Contributes To Root Zinc Uptake in Rice under Zinc-Limited Conditions(1)([OPEN])

Sheng Huang, Akimasa Sasaki, Naoki Yamaji, Haruka Okada, Namiki Mitani-Ueno, Jian Feng Ma

PLANT PHYSIOLOGY   183 ( 3 )   1224 - 1234   2020.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER SOC PLANT BIOLOGISTS  

Zinc (Zn) is an important essential micronutrient for plants and humans; however, the exact transporter responsible for root zinc uptake from soil has not been identified. Here, we found that OsZIP9, a member of the ZRT-IRT-related protein, is involved in Zn uptake in rice (Oryza sativa) under Zn-limited conditions. OsZIP9 was mainly localized to the plasma membrane and showed transport activity for Zn in yeast (Saccharomyces cerevisiae). Expression pattern analysis showed thatOsZIP9was mainly expressed in the roots throughout all growth stages and its expression was upregulated by Zn-deficiency. Furthermore,OsZIP9was expressed in the exodermis and endodermis of root mature regions. For plants grown in a hydroponic solution with low Zn concentration, knockout ofOsZIP9significantly reduced plant growth, which was accompanied by decreased Zn concentrations in both the root and shoot. However, plant growth and Zn accumulation did not differ between knockout lines and wild-type rice under Zn-sufficient conditions. When grown in soil, Zn concentrations in the shoots and grains of knockout lines were decreased to half of wild-type rice, whereas the concentrations of other mineral nutrients were not altered. A short-term kinetic experiment with stable isotope(67)Zn showed that(67)Zn uptake in knockout lines was much lower than that in wild-type rice. Combined, these results indicate that OsZIP9 localized at the root exodermis and endodermis functions as an influx transporter of Zn and contributes to Zn uptake under Zn-limited conditions in rice.The zinc transporter OsZIP9, expressed at the exodermis and endodermis of root mature region, contributes to Zn uptake from soil in rice.

DOI： 10.1104/pp.20.00125

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Plant Nutrition for Human Nutrition: Hints from Rice Research and Future Perspectives

Sheng Huang, Peitong Wang, Naoki Yamaji, Jian Feng Ma

MOLECULAR PLANT   13 ( 6 )   825 - 835   2020.6

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Both plants and humans require mineral elements for their healthy growth and development. Mineral elements in the soil are taken up by the plant roots and transported to the edible parts for human consumption through various different transporters. An ideal future crop for human health should be rich in essential mineral elements but with less toxic elements in the edible parts. However, due to the great difference in the numbers and amounts of mineral elements required between plants and humans, it is a challenge to balance plant growth and nutrient requirement for humans. In this article, we mainly focus on the transport system of mineral elements from soil to grain in rice, a staple food for half of the world's population, and discuss recent progress on the underlying genetic and physiological mechanisms. Examples are given for silicon, zinc, and iron essential/beneficial for both plants and humans, selenium and iodine only essential for humans, and toxic cadmium and arsenic for all organisms. Manipulation of some transporters for these elements, especially those localized in the node for allocation of mineral elements to the grain, has been successful in generating rice with higher density and bioavailability of essential elements but with less accumulation of toxic elements. We provide our perspectives toward breeding future crops for human health.

DOI： 10.1016/j.molp.2020.05.007

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OASTL-A1 functions as a cytosolic cysteine synthase and affects arsenic tolerance in rice

Chengcheng Wang, Lihua Zheng, Zhong Tang, Shengkai Sun, Jian Feng Ma, Xin-Yuan Huang, Fang-Jie Zhao

JOURNAL OF EXPERIMENTAL BOTANY   71 ( 12 )   3678 - 3689   2020.6

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Arsenic (As) contamination in paddy soil can cause phytotoxicity and elevated As accumulation in rice grains. Arsenic detoxification is closely linked to sulfur assimilation, but the genes involved have not been described in rice. In this study, we characterize the function of OASTL-A1, an O-acetylserine(thiol) lyase, in cysteine biosynthesis and detoxification of As in rice. Tissue expression analysis revealed that OsOASTL-A1 is mainly expressed in roots at the vegetative growth stage and in nodes at the reproductive stage. Furthermore, the expression of OsOASTL-A1 in roots was strongly induced by As exposure. Transgenic rice plants expressing pOsOASTL-A1::GUS (beta-glucuronidase) indicated that OsOASTL-A1 was strongly expressed in the outer cortex and the vascular cylinder in the root mature zone. Subcellular localization using OsOASTL-A1:eGFP (enhanced green fluorescent protein) fusion protein showed that OsOASTL-A1 was localized to the cytosol. In vivo and in vitro enzyme activity assays showed that OsOASTL-A1 possessed the O-acetylserine(thiol) lyase activity. Knockout of OsOASTL-A1 led to significantly lower levels of cysteine, glutathione, and phytochelatins in roots and increased sensitivity to arsenate stress. Furthermore, the osoastl-al knockout mutants reduced As accumulation in the roots, but increased As accumulation in shoots. We conclude that OsOASTL-A1 is the cytosolic O-acetylserine(thiol) lyase that plays an important role in non-protein thiol biosynthesis in roots for As detoxification.

DOI： 10.1093/jxb/eraa113

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Plastic transport systems of rice for mineral elements in response to diverse soil environmental changes

Peitong Wang, Naoki Yamaji, Komaki Inoue, Keiich Mochida, Jian Feng Ma

NEW PHYTOLOGIST   226 ( 1 )   156 - 169   2020.4

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Climate change will increase frequency of drought and flooding, which threaten global crop productivity and food security. Rice (Oryza sativa) is unique in that it is able to grow in both flooded and upland conditions, which have large differences in the concentrations and chemical forms of mineral elements available to plants. To comprehensively understand the mechanisms of rice for coping with different water status, we performed ionomics and transcriptomics analysis of the roots, nodes and leaves of rice grown in flooded and upland conditions. Focusing the analysis on genes encoding proteins involved in transport functions for mineral elements, it was found that, although rice plants maintained similar levels of each element in the shoots for optimal growth, different transporters for mineral elements were utilised for nitrogen, iron, copper and zinc to deal with different soil water conditions. For example, under flooded conditions, rice roots take up nitrogen using transporters for both ammonium (OsAMT1/2) and nitrate (OsNPF2.4, OsNRT1.1A and OsNRT2.3), whereas under upland conditions, nitrogen uptake is mediated by different nitrate transporters (OsNRT1.1B and OsNRT1.5A). This study shows that rice possesses plastic transport systems for mineral elements in response to different water conditions (upland and flooding).

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Tomato roots have a functional silicon influx transporter but not a functional silicon efflux transporter

Hao Sun, Yaoke Duan, Namiki Mitani-Ueno, Jing Che, Jianhua Jia, Jiaqi Liu, Jia Guo, Jian Feng Ma, Haijun Gong

PLANT CELL AND ENVIRONMENT   43 ( 3 )   732 - 744   2020.3

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Silicon (Si) accumulation in shoots differs greatly with plant species, but the molecular mechanisms for this interspecific difference are unknown. Here, we isolated homologous genes of rice Si influx (SlLsi1) and efflux (SlLsi2) transporter genes in tomato (Solanum lycopersicum L.) and functionally characterized these genes. SlLsi1 showed transport activity for Si when expressed in both rice lsi1 mutant and Xenopus laevis oocytes. SlLsi1 was constitutively expressed in the roots. Immunostaining showed that SlLsi1 was localized at the plasma membrane of both root tip and basal region without polarity. Furthermore, overexpression of SlLsi1 in tomato increased Si concentration in the roots and root cell sap but did not alter the Si concentration in the shoots. By contrast, two Lsi2-like proteins did not show efflux transport activity for Si in Xenopus oocytes. However, when functional CsLsi2 from cucumber was expressed in tomato, the Si uptake was significantly increased, resulting in higher Si accumulation in the leaves and enhanced tolerance of the leaves to water deficit and high temperature. Our results suggest that the low Si accumulation in tomato is attributed to the lack of functional Si efflux transporter Lsi2 required for active Si uptake although SlLsi1 is functional.

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Altered Root Structure Affects Both Expression and Cellular Localization of Transporters for Mineral Element Uptake in Rice

En Yu, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   61 ( 3 )   481 - 491   2020.3

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

One of the most important roles of plant roots is to take up mineral elements for their growth. Although several genes involved in root growth have been identified, the association between root structure and mineral element uptake is less investigated. In this study, we isolated a rice mutant (dice1, defective in cell elongation 1) with short-root phenotype. This mutant was characterized by partial defect in the formation of root outer cell layers. Mapping of the responsible gene revealed that the short-root phenotype in the mutant was caused by a single-nucleotide substitution of a gene encoding a membrane-anchored endo-1,4-beta-glucanase (OsGlu3). The growth of both the roots and shoots was partially recovered with increasing strength of nutrient solution and glucose in the mutant. The mutant showed a decreased uptake (normalized by root dry weight) for Mg, Mn, Fe, Cu, Zn, Cd, As and Ge but increased uptake for K and Ca. The expression level of some transporter genes including OsLsi1 and OsLsi2 for Si uptake and OsNromp5 for Mn uptake was significantly decreased in the mutant compared with the wild-type (WT) rice. Furthermore, the cellular localization of OsLsi1 was altered; OsLsi1 localized at the root exodermis of the WT rice was changed to be localized to other cell layers of the mutant roots. However, this localization became normal in the presence of exogenous glucose in the mutant. Our results indicate that a normal root structure is required for maintaining the expression and localization of transporters involved in the mineral element uptake.

DOI： 10.1093/pcp/pcz213

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A transcription factor OsbHLH156 regulates Strategy II iron acquisition through localising IRO2 to the nucleus in rice

Shoudong Wang, Lin Li, Yinghui Ying, Jin Wang, Ji Feng Shao, Naoki Yamaji, James Whelan, Jian Feng Ma, Huixia Shou

NEW PHYTOLOGIST   225 ( 3 )   1247 - 1260   2020.2

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Plants have evolved two strategies to acquire ferrous (Strategy I) or ferric (Strategy II) iron from soil. The iron-related bHLH transcription factor 2 (IRO2) has been identified as a key regulator of iron acquisition (Strategy II) in rice. However, its mode of action, subcellular localisation and binding partners are not clearly defined. Using RNA-seq analyses, we identified a novel bHLH-type transcription factor, OsbHLH156. The function of OsbHLH156 in Fe homeostasis was analysed by characterisation of the phenotypes, elemental content, transcriptome, interaction and subcellular localisation of OsbHLH156 and IRO2. OsbHLH156 is primarily expressed in the roots and transcript abundance is greatly increased by Fe deficiency. Loss of function of OsbHLH156 resulted in Fe-deficiency-induced chlorosis and reduced Fe concentration in the shoots under upland or Fe(III) supplied conditions. Transcriptome analyses revealed that the expression of most Fe-deficiency-responsive genes involved in Strategy II were not induced in the osbhlh156-1 mutant. Furthermore, OsbHLH156 was required for nuclear localisation of IRO2. We conclude that OsbHLH156 is required for a Strategy II uptake mechanism in rice, partnering with a previously identified 'master' regulator IRO2. Mechanistically it is required for the nuclear localisation of IRO2.

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Functional evolution of nodulin 26-like intrinsic proteins: from bacterial arsenic detoxification to plant nutrient transport

Benjamin Pommerrenig, Till A. Diehn, Nadine Bernhardt, Manuela D. Bienert, Namiki Mitani-Ueno, Jacqueline Fuge, Annett Bieber, Christoph Spitzer, Andrea Braeutigam, Jian Feng Ma, Francois Chaumont, Gerd P. Bienert

NEW PHYTOLOGIST   225 ( 3 )   1383 - 1396   2020.2

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Nodulin 26-like intrinsic proteins (NIPs) play essential roles in transporting the nutrients silicon and boron in seed plants, but the evolutionary origin of this transport function and the co-permeability to toxic arsenic remains enigmatic. Horizontal gene transfer of a yet uncharacterised bacterial AqpN-aquaporin group was the starting-point for plant NIP evolution. We combined intense sequence, phylogenetic and genetic context analyses and a mutational approach with various transport assays in oocytes and plants to resolve the transorganismal and functional evolution of bacterial and algal and terrestrial plant NIPs and to reveal their molecular transport specificity features. We discovered that aqpN genes are prevalently located in arsenic resistance operons of various prokaryotic phyla. We provided genetic and functional evidence that these proteins contribute to the arsenic detoxification machinery. We identified NIPs with the ancestral bacterial AqpN selectivity filter composition in algae, liverworts, moss, hornworts and ferns and demonstrated that these archetype plant NIPs and their prokaryotic progenitors are almost impermeable to water and silicon but transport arsenic and boron. With a mutational approach, we demonstrated that during evolution, ancestral NIP selectivity shifted to allow subfunctionalisations. Together, our data provided evidence that evolution converted bacterial arsenic efflux channels into essential seed plant nutrient transporters.

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Vascular Cambium-Localized AtSPDT Mediates Xylem-to-Phloem Transfer of Phosphorus for Its Preferential Distribution in Arabidopsis

Guangda Ding, Gui Jie Lei, Naoki Yamaji, Kengo Yokosho, Namiki Mitani-Ueno, Sheng Huang, Jian Feng Ma

MOLECULAR PLANT   13 ( 1 )   99 - 111   2020.1

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During plant growth and development mineral elements are preferentially delivered to different organs and tissues to meet the differential demand. It has been shown that the preferential distribution of mineral nutrients in gramineous plants is mediated by node-based transporters, but the mechanisms of preferential distribution in dicots are poorly understood. Here, we report a distinct mechanism for the preferential distribution of phosphorus (P) in Arabidopsis plants, revealed by detailed functional analysis of AtSPDT/AtSULTR3;4 (SULTR-like P Distribution Transporter), a homolog of rice OsSPDT. Like OsSPDT, AtSPDT is localized at the plasma membrane and showed proton-dependent transport activity for P. Interestingly, we found that AtSPDT is mainly expressed in the rosette basal region and leaf petiole, and its expression is up-regulated by P deficiency. Tissue-specific analysis showed that AtSPDT is mainly located in the vascular cambium of different organs, as well as in the parenchyma tissues of both xylem and phloem regions. Knockout of AtSPDT inhibited the growth of new leaves under low P due to decreased P distribution to those organs. The seed yields of the wild-type and atspdt mutant plants are similar, but the seeds of mutant plants contain - less P. These results indicate that AtSPDT localized in the vascular cambium is involved in preferential distribution of P to the developing tissues, through xylem-to-phloem transfer mainly at the rosette basal region and leaf petiole.

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Silicon accumulation in rice plant aboveground biomass affects leaf carbon quality

Jorg Schaller, Robin Heimes, Jian Feng Ma, Jean-Dominique Meunier, Ji Feng Shao, Miho Fujii-Kashino, Klaus Holger Knorr

PLANT AND SOIL   444 ( 1-2 )   399 - 407   2019.11

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Background and aim Silicon is known to be able to substitute carbon in plant biomass, especially in cellulose, lignin and phenols. However, a more comprehensive picture regarding the effect of silicon accumulation on plant carbon quality (cellulose, lignin, phenol, wax, lipids, and free organic acids content) with regard to potential decomposability is still missing. Methods Two different rice varieties (French brown and red rice cultivars) were cultivated under five different soil silicon availabilities. After maturity we harvested the plants and analyzed them regarding carbon quality by FTIR spectroscopy and regarding plant silicon concentrations. Results Silicon accumulation was found to be dependent on silicon availability and on the specific rice cultivar. The lowering of carbon compounds content by silicon was found not to be restricted to cellulose, lignin and phenol. Silicon accumulation was able to decrease other carbon compounds such as fat, wax, lipids, and free organic acids, too. Conclusions Consequently, silicon is important for the carbon quality of silicon accumulating plants. Furthermore, silicon accumulation in plants is interfering with a large range of different carbon compounds potentially altering the leaf economic spectra, decomposability, and thus potentially interfering with the whole performance of ecosystems dominated by silicon accumulating plant species.

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The ABC transporter ABCG36 is required for cadmium tolerance in rice

Shan Fu, Youshe Lu, Xiang Zhang, Guangzhe Yang, Dong Chao, Zhigang Wang, Mingxing Shi, Jiugeng Chen, Dai-Yin Chao, Rongbai Li, Jian Feng Ma, Jixing Xia

JOURNAL OF EXPERIMENTAL BOTANY   70 ( 20 )   5909 - 5918   2019.10

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Cadmium (Cd) is a highly toxic heavy metal in nature, which causes severe damage to plant growth. The molecular mechanisms for Cd detoxification are poorly understood. Here, we report that a G-type ATP-binding cassette transporter, OsABCG36, is involved in Cd tolerance in rice. OsABCG36 was expressed in both roots and shoots at a low level, but expression in the roots rather than the shoots was greatly up-regulated by a short exposure to Cd. A spatial expression analysis showed that Cd-induced expression of OsABCG36 was found in both the root tip and the mature root region. Transient expression of OsABCG36 in rice protoplast cells showed that it was localized to the plasma membrane. Immunostaining showed that OsABCG36 was localized in all root cells except the epidermal cells. Knockout of OsABCG36 resulted in increased Cd accumulation in root cell sap and enhanced Cd sensitivity, but did not affect tolerance to other metals including Al, Zn, Cu, and Pb. The concentration of Cd in the shoots was similar between the knockout lines and wild-type rice. Heterologous expression of OsABCG36 in yeast showed an efflux activity for Cd, but not for Zn. Taken together, our results indicate that OsABCG36 is not involved in Cd accumulation in the shoots, but is required for Cd tolerance by exporting Cd or Cd conjugates from the root cells in rice.

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A Vacuolar Phytosiderophore Transporter Alters Iron and Zinc Accumulation in Polished Rice Grains

Jing Che, Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

PLANT PHYSIOLOGY   181 ( 1 )   276 - 288   2019.9

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Essential metals, such as iron (Fe) and zinc (Zn), in grains are important sources for seed germination and nutritional requirements, but the molecular mechanisms underlying their loading into grains are poorly understood. Recently, nodes in rice (Oryza sativa) were reported to play an important role in the preferential distribution of mineral elements to the grains. In this study, we functionally characterized a rice gene highly expressed in nodes, OsVMT (VACUOLAR MUGINEIC ACID TRANSPORTER), belonging to a major facilitator superfamily. OsVMT is highly expressed in the parenchyma cell bridges of node I, where Fe and Zn are highly deposited. The expression of OsVMT was induced by Fe deficiency in the roots but not in the shoot basal region and uppermost node. OsVMT localized to the tonoplast and showed efflux transport activity for 2'-deoxymugineic acid (DMA). At the vegetative stage, knockout of OsVMT resulted in decreased DMA but increased ferric Fe in the root cell sap. As a result, the concentration of DMA in the xylem sap increased but that of ferric Fe decreased in the xylem sap in the mutants. In the polished rice grain, the mutants accumulated 1.8- to 2.1-fold, 1.5- to 1.6-fold, and 1.4- to 1.5-fold higher Fe, Zn, and DMA, respectively, than the wild type. Taken together, our results indicate that OsVMT is involved in sequestering DMA into the vacuoles and that knockout of this gene enhances the accumulation of Fe and Zn in polished rice grains through DMA-increased solubilization of Fe and Zn deposited in the node.

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Magnesium Deficiency Triggers SGR-Mediated Chlorophyll Degradation for Magnesium Remobilization

Yu Yang Peng, Li Li Liao, Sheng Liu, Miao Miao Nie, Jian Li, Lu Dan Zhang, Jian Feng Ma, Zhi Chang Chen

PLANT PHYSIOLOGY   181 ( 1 )   262 - 275   2019.9

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Magnesium (Mg) is a relatively mobile element that is remobilized in plants under Mg-limited conditions through transport from old to young tissues. However, the physiological and molecular mechanisms underlying Mg remobilization in plants remain poorly understood. In this study, we investigated Mg remobilization in rice (Oryza sativa) as facilitated through a Mg dechelatase gene involved in chlorophyll degradation, STAY-GREEN (OsSGR). We first observed that mid-aged leaves of rice are more susceptible to Mg deficiency. Expression of OsSGR was specifically upregulated by Mg deficiency, and the response was more pronounced in mid-aged leaves. Knockout of OsSGR exhibited the stay-green phenotype, which hindered the mobility of Mg from mid-aged leaves to young developing leaves. This decline in Mg mobility was associated with inhibited growth of developing leaves in mutants under Mg-limited conditions. Furthermore, Mg deficiency enhanced reactive oxygen species (ROS) generation in mid-aged leaves. ROS levels, particularly hydrogen peroxide, in turn, positively regulated OsSGR expression, probably through chloroplast-to-nucleus signaling, which triggers chlorophyll degradation to protect mid-aged leaves from photodamage. Taken together, these results show that OsSGR-mediated chlorophyll degradation contributes to not only internal remobilization of Mg from mid-aged leaves to developing leaves, but also photooxidative protection of mid-aged leaves under Mg-limited conditions. ROS appear to act as feedback regulators of OsSGR expression to precisely govern chlorophyll degradation in mid-aged leaves where Mg and photosynthetic capacities are relatively high.

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Bioimaging of multiple elements by high-resolution LA-ICP-MS reveals altered distribution of mineral elements in the nodes of rice mutants Reviewed

Naoki Yamaji, Jian Feng Ma

PLANT JOURNAL   99 ( 6 )   1254 - 1263   2019.9

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Inter-vascular transfer in rice (Oryza sativa) nodes is required for delivering mineral elements to developing tissues, which is mediated by various transporters in the nodes. However, the effect of these transporters on distribution of mineral elements in the nodes at a cellular level is still unknown. Here, we established a protocol for bioimaging of multiple elements at a cellular level in rice node by laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS), and compared the mineral distribution profile between wild-type (WT) rice and mutants. Both relative comparison of mineral distribution normalized by endogenous C-13 and quantitative analysis using spiked standards combined with soft ablation gave valid results. Overall, macro-nutrients such as K and Mg were accumulated more in the phloem region, while micro-nutrients such as Fe and Zn were highly accumulated at the inter-vascular tissues of the node. In mutants of nodal Zn transporter OsHMA2, Zn localization pattern in the node tissues did not differ from that of WT; however, Zn accumulation in the inter-vascular tissues was lower in uppermost node I but higher in the third upper node III compared with the WT. In contrast, Si deposition in the mutants of three nodal Si transporters Lsi2, Lsi3 and Lsi6 showed different patterns, which are consistent with the localization of these transporters. This improved LA-ICP-MS analysis combined with functional characterization of transporters will provide further insight into mineral element distribution mechanisms in rice and other plant species.

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The Soybean Sugar Transporter GmSWEET15 Mediates Sucrose Export from Endosperm to Early Embryo

Shoudong Wang, Kengo Yokosho, Runze Guo, James Whelan, Yong-Ling Ruan, Jian Feng Ma, Huixia Shou

PLANT PHYSIOLOGY   180 ( 4 )   2133 - 2141   2019.8

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Soybean (Glycine max) seed is primarily composed of a mature embryo that provides a major source of protein and oil for humans and other animals. Early in development, the tiny embryos grow rapidly and acquire large quantities of sugars from the liquid endosperm of developing seeds. An insufficient supply of nutrients from the endosperm to the embryo results in severe seed abortion and yield reduction. Hence, an understanding of the molecular basis and regulation of assimilate partitioning involved in early embryo development is important for improving soybean seed yield and quality. Here, we used expression profiling analysis to show that two paralogous sugar transporter genes from the SWEET (Sugars Will Eventually be Exported Transporter) family, GmSWEET15a and GmSWEET15b, were highly expressed in developing soybean seeds. In situ hybridization and quantitative real-time PCR showed that both genes were mainly expressed in the endosperm at the cotyledon stage. GmSWEET15b showed both efflux and influx activities for sucrose in Xenopus oocytes. In Arabidopsis (Arabidopsis thaliana), knockout of three AtSWEET alleles is required to see a defective, but not lethal, embryo phenotype, whereas knockout of both GmSWEET15 genes in soybean caused retarded embryo development and endosperm persistence, resulting in severe seed abortion. In addition, the embryo sugar content of the soybean knockout mutants was greatly reduced. These results demonstrate that the plasma membrane sugar transporter, GmSWEET15, is essential for embryo development in soybean by mediating Suc export from the endosperm to the embryo early in seed development.

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In defence of the selective transport and role of silicon in plants

Devrim Coskun, Rupesh Deshmukh, Humira Sonah, James G. Menzies, Olivia Reynolds, Jian Feng Ma, Herbert J. Kronzucker, Richard R. Belanger

NEW PHYTOLOGIST   223 ( 2 )   514 - 516   2019.7

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DOI： 10.1111/nph.15764

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Producing cadmium-free Indica rice by overexpressing OsHMA3

Chenni Lu, Lingxiao Zhang, Zhong Tang, Xin-Yuan Huang, Jian Feng Ma, Fang-Jie Zhao

ENVIRONMENT INTERNATIONAL   126   619 - 626   2019.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：PERGAMON-ELSEVIER SCIENCE LTD  

Background: Considerable proportions of rice grains produced in some areas in southern China contain high concentrations of cadmium (Cd), leading to unsafe levels of dietary Cd intake. Cultivars of Indica rice, widely grown in southern China, are particularly prone to high Cd accumulation in the grain. Effective methods are needed to decrease Cd accumulation in Indica rice.Methods: OsHMA3, encoding a tonoplast Cd transporter, was overexpressed in an elite Indica rice cultivar (Zhongjiazao 17) driven by CaMV 35S promoter. The effects on Cd translocation, accumulation and tolerance, as well as on the agronomic traits and micronutrient concentrations were evaluated.Results: OsHMA3 overexpression markedly decreased Cd translocation from roots to shoots and increased Cd tolerance. OsHMA3 overexpression decreased Cd concentrations in brown rice by 94-98%, to levels just above the detection limit, when rice plants were grown in two Cd-contaminated paddy soils. OsHMA3 overexpression generally had no significant effect on grain yield and the concentrations of the essential micronutrients including zinc, iron, copper and manganese in field trials.Conclusion: Overexpression of OsHMA3 is a highly effective method to reduce Cd accumulation in Indica rice, producing rice grains that were almost Cd free with little effect on grain yield or essential micronutrient concentrations.

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The tonoplast-localized transporter OsHMA3 plays an important role in maintaining Zn homeostasis in rice

Hongmei Cai, Sheng Huang, Jing Che, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   70 ( 10 )   2717 - 2725   2019.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

In order to respond to fluctuating zinc (Zn) in the environment, plants must have a system to control Zn homeostasis. However, how plants maintain an appropriate level of Zn during their growth and development is still poorly understood. In this study, we found that OsHMA3, a tonoplast-localized transporter for Zn/Cd, plays an important role in Zn homeostasis in rice. Accessions with the functional allele of OsHMA3 showed greater tolerance to high Zn than those with the non-functional allele based on root elongation test. A 67Zn-labeling experiment showed that accessions with loss of function of OsHMA3 had lower Zn accumulation in the roots but similar concentrations in the shoots compared with functional OsHMA3 accessions. When exposed to Zn-free growing medium, the concentration in the root cell sap was rapidly decreased in accessions with functional OsHMA3, but less dramatic changes were observed in non-functional accessions. A mobility experiment showed that more Zn in the roots was translocated to the shoots in accessions with functional OsHMA3. Higher expression levels of OsZIP4, OsZIP5, OsZIP8, and OsZIP10 were found in the roots of accessions with functional OsHMA3 in response to Zn deficiency. Taken together, our results indicate that OsHMA3 plays an important role in rice roots in both Zn detoxification and storage by sequestration into the vacuoles, depending on Zn concentration in the environment.

DOI： 10.1093/jxb/erz091

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A nodule-localized phosphate transporter GmPT7 plays an important role in enhancing symbiotic N-2 fixation and yield in soybean Reviewed

Liyu Chen, Lu Qin, Lili Zhou, Xinxin Li, Zhichang Chen, Lili Sun, Wenfei Wang, Zhihao Lin, Jing Zhao, Naoki Yamaji, Jian Feng Ma, Mian Gu, Guohua Xu, Hong Liao

NEW PHYTOLOGIST   221 ( 4 )   2013 - 2025   2019.3

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Symbiotic nitrogen (N-2) fixation plays a vital role in sustainable agriculture. Efficient N-2 fixation requires various materials, including phosphate (Pi); however, the molecular mechanism underlying the transport of Pi into nodules and bacteroids remains largely unknown. A nodule-localized Pi transporter, GmPT7, was functionally characterized in soybean (Glycine max) and its role in N-2 fixation and yield was investigated via composite and whole transgenic plants. GmPT7 protein was localized to the plasma membrane and showed transport activity for Pi in yeast. Altered expression of GmPT7 changed (33)Pi uptake from rhizosphere and translocation to bacteroids. GmPT7 was mainly localized to the outer cortex and fixation zones of the nodules. Overexpression of GmPT7 promoted nodulation, and increased plant biomass, shoot nitrogen and phosphorus content, resulting in improved soybean yield by up to 36%. Double suppression of GmPT5 and GmPT7 led to nearly complete elimination of nodulation and over 50% reduction in plant biomass, shoot nitrogen and phosphorus content, indicating that both GmPT7 and GmPT5 contribute to Pi transport for N-2 fixation. Taken together, our results indicate that GmPT7 is a transporter responsible for direct Pi entry to nodules and further to fixation zones, which is required for enhancing symbiotic N-2 fixation and grain yield of soybean.

DOI： 10.1111/nph.15541

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OsPHT1;3 Mediates Uptake, Translocation, and Remobilization of Phosphate under Extremely Low Phosphate Regimes Reviewed

Ming Xing Chang, Mian Gu, Yu Wei Xia, Xiao Li Dai, Chang Rong Dai, Jun Zhang, Shi Chao Wang, Hong Ye Qu, Naoki Yamaji, Jian Feng Ma, Guo Hua Xu

PLANT PHYSIOLOGY   179 ( 2 )   656 - 670   2019.2

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Plant roots rely on inorganic orthophosphate (Pi) transporters to acquire soluble Pi from soil solutions that exists at micromolar levels in natural ecosystems. Here, we functionally characterized a rice (Oryza sativa) Pi transporter, Os Phosphate Transporter1;3 (OsPHT1;3), that mediates Pi uptake, translocation, and remobilization. OsPHT1;3 was directly regulated by Os Phosphate Starvation Response-2 and, in response to Pi starvation, showed enhanced expression in young leaf blades and shoot basal regions and even more so in roots and old leaf blades. OsPHT1;3 was able to complement a yeast mutant strain defective in five Pi transporters and mediate Pi influx in Xenopus laevis oocytes. Overexpression of OsPHT1;3 led to increased Pi concentration both in roots and shoots. However, unlike that reported for other known OsPHT1 members that facilitate Pi uptake at relatively higher Pi levels, mutation of OsPHT1;3 impaired Pi uptake and root-to-shoot Pi translocation only when external Pi concentration was below 5 mu M. Moreover, in basal nodes, the expression of OsPHT1;3 was restricted to the phloem of regular vascular bundles and enlarged vascular bundles. An isotope labeling experiment with P-32 showed that ospht1;3 mutant lines were impaired in remobilization of Pi from source to sink leaves. Furthermore, overexpression and mutation of OsPHT1;3 led to reciprocal alteration in the expression of OsPHT1;2 and several other OsPHT1 genes. Yeast-two-hybrid, bimolecular fluorescence complementation, and coimmunoprecipitation assays all demonstrated a physical interaction between OsPHT1;3 and OsPHT1;2. Taken together, our results indicate that OsPHT1;3 acts as a crucial factor for Pi acquisition, root-to-shoot Pi translocation, and redistribution of phosphorus in plants growing in environments with extremely low Pi levels.

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The controversies of silicon's role in plant biology

Devrim Coskun, Rupesh Deshmukh, Humira Sonah, James G. Menzies, Olivia Reynolds, Jian Feng Ma, Herbert J. Kronzucker, Richard R. Belanger

NEW PHYTOLOGIST   221 ( 1 )   67 - 85   2019.1

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Silicon (Si) is not classified as an essential plant nutrient, and yet numerous reports have shown its beneficial effects in a variety of species and environmental circumstances. This has created much confusion in the scientific community with respect to its biological roles. Here, we link molecular and phenotypic data to better classify Si transport, and critically summarize the current state of understanding of the roles of Si in higher plants. We argue that much of the empirical evidence, in particular that derived from recent functional genomics, is at odds with many of the mechanistic assertions surrounding Si's role. In essence, these data do not support reports that Si affects a wide range of molecular-genetic, biochemical and physiological processes. A major reinterpretation of Si's role is therefore needed, which is critical to guide future studies and inform agricultural practice. We propose a working model, which we term the 'apoplastic obstruction hypothesis', which attempts to unify the various observations on Si's beneficial influences on plant growth and yield. This model argues for a fundamental role of Si as an extracellular prophylactic agent against biotic and abiotic stresses (as opposed to an active cellular agent), with important cascading effects on plant form and function.

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OsCASP1 is required for casparian strip formation at endodermal cells of rice roots for selective uptake of mineral elements

Zhigang Wang, Naoki Yamaji, Sheng Huang, Xiang Zhang, Mingxing Shi, Shan Fu, Guangzhe Yang, Jian Feng Ma, Jixing Xia

Plant Cell   31 ( 11 )   2636 - 2648   2019

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In response to diverse environmental conditions, rice (Oryza sativa) roots have developed one Casparian strip (CS) at the exodermis and one CS at the endodermis. Here, we functionally characterized OsCASP1 (Casparian strip domain protein 1) in rice. OsCASP1 was mainly expressed in the root elongation zone, and the protein encoded was first localized to all sides of the plasma membrane of endodermal cells without CS, followed by the middle of the anticlinal side of endodermal cells with CS. Knockout of OsCASP1 resulted in a defect of CS formation at the endodermis and decreased growth under both soil and hydroponic conditions. Mineral analysis showed that the oscasp1 mutants accumulated more Ca, but less Mn, Zn, Fe, Cd, and As in the shoots compared with the wild type. The growth inhibition of the mutants was further aggravated by high Ca in growth medium. The polar localization of the Si transporter Low Si 1 at the distal side of the endodermis was not altered in the mutant, but the protein abundance was decreased, resulting in a substantial reduction in silicon uptake. These results indicated that OsCASP1 is required for CS formation at the endodermis and that the CS in rice plays an important role in root selective uptake of mineral elements, especially Ca and Si.

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Two Genes Encoding a Bacterial-Type ATP-Binding Cassette Transporter are Implicated in Aluminum Tolerance in Buckwheat

Jing Che, Naoki Yamaji, Kengo Yokosho, Ren Fang Shen, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   59 ( 12 )   2502 - 2511   2018.12

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Buckwheat (Fagopyrum esculentum Moench) shows high tolerance to aluminum (Al) toxicity, but the molecular mechanisms underlying its high Al tolerance are poorly understood. Here, we functionally characterized two genes (FeSTAR1 and FeSTAR2), which encode a nucleotide-binding domain and a membrane domain, respectively, of a bacterial-type ATP-binding cassette (ABC) transporter. The expression of FeSTAR1 and FeSTAR2 was induced by Al in both roots and leaves with higher expression in the roots. Spatial and tissue-specific expression analysis showed that the Al-induced expression of these two genes was found in both the root tips and basal root regions with higher expression in the root outer cell layers. The expression was neither induced by other metals including Cd and La nor by low pH and phosphorus-deficiency. FeSTAR1 and FeSTAR2 were present in a single copy in the genome, but the Al-induced transcript copy number of FeSTAR1 and FeSTAR2 was much higher than their homologous genes in rice and Arabidopsis. FeSTAR1 and FeSTAR2 form a complex when co-expressed in onion epidermal cells. Introduction of FeSTAR1 and FeSTAR2 into Arabidopsis mutants atstar1 and als3/atstar2, respectively, rescued the sensitivity of the mutants to Al. Taken together, our results indicate that FeSTAR1 and FeSTAR2 are involved in Al tolerance and that their high expression level may contribute to high Al tolerance in buckwheat.

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Retrotransposon Insertion and DNA Methylation Regulate Aluminum Tolerance in European Barley Accessions Reviewed International journal

Miho Kashino-Fujii, Kengo Yokosho, Naoki Yamaji, Miki Yamane, Daisuke Saisho, Kazuhiro Sato, Jian Feng Ma

PLANT PHYSIOLOGY   178 ( 2 )   716 - 727   2018.10

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Aluminum (Al) toxicity is a major stress factor limiting crop productivity in acid soil. Although there is great genotypic variation in tolerance to Al toxicity, the underlying molecular mechanisms are poorly understood. Here, we report that, in barley (Hordeum vulgare), the fourth largest cereal crop produced in the world, both retrotransposon insertion and DNA methylation are involved in regulating differential Al tolerance. HvAACT1 is a major gene responsible for citrate secretion from the roots for external detoxification of Al. A multiretrotransposon-like (MRL) sequence insertion at least 15.3 kb in length was detected in the upstream genomic region of HvAACT1 that displayed promoter activity and significantly enhanced HvAACT1 expression, especially in the root tips of Al-tolerant accessions. Furthermore, in a number of accessions with low levels of HvAACT1 expression, this MRL insertion was present but highly methylated. Geographical analysis showed that accessions with this MRL insertion are distributed mainly in European areas with acid soils. Two wild barley accessions were found to possess this MRL insertion, but with a high degree of methylation. These results indicate that the MRL insertion and its degree of DNA methylation influence HvAACT1 expression and that demethylation of this MRL insertion, which facilitates adaptation to acid soils, occurred following barley domestication. Moreover, our results indicate that barley accessions in East Asia and Europe have developed independent but equivalent strategies to withstand Al toxicity in acid soils.

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OsYSL16 is Required for Preferential Cu Distribution to Floral Organs in Rice

Chang Zhang, Wenhui Lu, Yang Yang, Zhenguo Shen, Jian Feng Ma, Luqing Zheng

PLANT AND CELL PHYSIOLOGY   59 ( 10 )   2039 - 2051   2018.10

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Deficiency of copper (Cu) causes low fertility in many plant species, but the molecular mechanisms underlying distribution of Cu to the floral organs are poorly understood. Here, we found that a member of yellow-stripe like (YSL) family, YSL16 encoding the Cu-nicotianamine (Cu-NA) transporter, was highly expressed in the rachilla, with less expression in the palea and lemma of rice (Oryza sativa). beta-Glucuronidase (GUS) staining of transgenic rice carrying the OsYSL16 promoter-GUS showed that OsYSL16 was mainly expressed in vascular bundles of the rachilla as well as the palea and lemma. Knockout of OsYSL16 resulted in decreased Cu distribution to the stamens, but increased distribution to the palea and lemma. A short-term (24 h) Cu-65 labeling experiment confirmed increased Cu concentration of palea and lemma in the mutant. Furthermore, we found that redistribution of Cu from the palea and lemma was impaired in the osysl16 mutant after exposure to Cu-free solution. The osysl16 mutant showed low pollen germination, but this was rescued by addition of Cu in the medium. Our results indicate that OsYSL16 expressed in the vascular bundles of the rachilla is important for preferential distribution of Cu to the stamens, while OsYSL16 in vascular bundles of the palea and lemma is involved in Cu redistribution under Cu-limited conditions in rice.

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Functional characterization of an aluminum (Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice Reviewed

Jing Che, Tomokazu Tsutsui, Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

NEW PHYTOLOGIST   220 ( 1 )   209 - 218   2018.10

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High aluminum (Al) tolerance in rice (Oryza sativa) is controlled by a Cys2His2-type zinc finger transcription factor ART1 (Al resistance transcription factor1). There are five close homologs of ART1 in the rice genome, but the role of these homologs is unknown.We functionally characterized one of the ART1 homologs, ART2, in terms of tissue and spatial expression, subcellular localization, transcriptional activation activity, and phenotypic analysis of the knockout lines.ART2 was localized to the nucleus and showed a transcriptional activation potential in yeast. ART2 was mainly expressed in the roots, but the expression level was much lower than that of ART1. The ART2 expression was rapidly induced by Al in the roots of the wild-type rice, but not in art1 mutant. Knockout of ART2 resulted in increased sensitivity to Al toxicity, but did not alter sensitivity to different pH values. Expression profile analysis by RNA-sequencing showed that ART2 was not involved in activation of genes regulated by ART1; however, four genes seems to be regulated by ART2, which are implicated in Al tolerance.These results indicate that ART1 and ART2 regulate different pathways leading to Al tolerance, and ATR2 plays a supplementary role in Al tolerance in rice.

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Engineering rice with lower grain arsenic

Fenglin Deng, Naoki Yamaji, Jian Feng Ma, Sang-Kyu Lee, Jong-Seong Jeon, Enrico Martinoia, Youngsook Lee, Won-Yong Song

PLANT BIOTECHNOLOGY JOURNAL   16 ( 10 )   1691 - 1699   2018.10

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Arsenic (As) is a poisonous element that causes severe skin lesions and cancer in humans. Rice (Oryza sativa L.) is a major dietary source of As in humans who consume this cereal as a staple food. We hypothesized that increasing As vacuolar sequestration would inhibit its translocation into the grain and reduce the amount of As entering the food chain. We developed transgenic rice plants expressing two different vacuolar As sequestration genes, ScYCF1 and OsABCC1, under the control of the RCc3 promoter in the root cortical and internode phloem cells, along with a bacterial gamma-glutamylcysteine synthetase driven by the maize UBI promoter. The transgenic rice plants exhibited reduced root-to-shoot and internode-to-grain As translocation, resulting in a 70% reduction in As accumulation in the brown rice without jeopardizing agronomic traits. This technology could be used to reduce As intake, particularly in populations of South East Asia suffering from As toxicity and thereby improve human health.

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The Putative Peptide Gene FEP1 Regulates Iron Deficiency Response in Arabidopsis

Takashi Hirayama, Gui Jie Lei, Naoki Yamaji, Naoki Nakagawa, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   59 ( 9 )   1739 - 1752   2018.9

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Iron is an essential element for all organisms, and plants have developed sophisticated systems to acquire iron and maintain iron homeostasis. We found that an Arabidopsis thaliana ABA-hypersensitive mutant, aba hypersensitive germination2-1 (ahg2-1), that is known to be defective in mitochondrial mRNA regulation, had increased expression of iron deficiency response genes. The ahg2-1 mutant had lower heme levels than the wild type. Transcriptome data further revealed that novel genes encoding short polypeptides were highly expressed in this mutant. The expression of one of these genes, which we named FE-UPTAKE-INDUCING PEPTIDE 1 (FEP1), was induced under iron-deficient conditions and was observed in the vascular tissues of the leaves and roots, as well as in leaf mesophyll cells. Notably, deletion or insertion mutations of FEN exhibited impaired iron accumulation in shoots but normal iron levels in roots. Artificially induced expression of FEP1 was sufficient to induce iron deficiency response genes, such as basic HELIX- LOOP-HELIX 38 (bHLH38), bHLH39, IRON-REGULATED TRANSPORTERI (IRT1) and FERRIC REDUCTION OXIDASE2 (FRO2), and led to iron accumulation in planta. Further analysis confirmed that the encoded peptide, but not the FEP1 RNA, was responsible for this activity. Remarkably, the activation of bHLH39 by FEP1 was independent of FER-LIKE IRON DEFICIENCY INDUCED (FIT), a key transcription factor in the iron deficiency response. Taken together, our results indicate that FEP1 functions in iron homeostasis through a previously undescribed regulatory mechanism for iron acquisition in Arabidopsis.

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A member of cation diffusion facilitator family, MTP11, is required for manganese tolerance and high fertility in rice Reviewed

Yuta Tsunemitsu, Mayuko Genga, Tomoyuki Okada, Naoki Yamaji, Jian Feng Ma, Akira Miyazaki, Shin-ichiro Kato, Kozo Iwasaki, Daisei Ueno

PLANTA   248 ( 1 )   231 - 241   2018.7

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Rice MTP11 is the trans-Golgi-localized transporter that is involved in Mn tolerance with MTP8.1, and it is required for normal fertility.Rice (Oryza sativa L.) is one of the most manganese (Mn)-tolerant species, and it is able to accumulate high levels of this metal in the leaves without showing toxic symptoms. The metal tolerance protein 8.1 (MTP8.1), a member of the Mn-cation diffusion facilitator (CDF) family, has been shown to play a central role in high Mn tolerance by sequestering Mn into vacuoles. Recently, rice MTP11 was identified as an Mn transporter that is localized to Golgi-associated compartments, but its exact role in Mn tolerance in planta has not yet been understood. Here, we investigated the role of MTP11 in rice Mn tolerance using knockout lines. Old leaves presented higher levels of constitutively expressed MTP11 than other tissues and MTP11 expression was also found in reproductive organs. Fused MTP11:green fluorescent protein was co-localized to trans-Golgi markers and differentiated from other Golgi-associated markers. Knockout of MTP11 in wild-type rice did not affect tolerance and accumulation of Mn and other heavy metals, but knockout in the mtp8.1 mutant showed exacerbated Mn sensitivity at the vegetative growth stage. Knockout of MTP11 alone resulted in decreased grain yield and fertility at the reproductive stage. Thus, MTP11 is a trans-Golgi localized transporter for Mn, which plays a role in Mn tolerance through intracellular Mn compartmentalization. It is also required for maintaining high fertility in rice.

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Decreasing arsenic accumulation in rice by overexpressing OsNIP1;1 and OsNIP3;3 through disrupting arsenite radial transport in roots

Sheng-Kai Sun, Yi Chen, Jing Che, Noriyuki Konishi, Zhong Tang, Anthony J. Miller, Jian Feng Ma, Fang-Jie Zhao

NEW PHYTOLOGIST   219 ( 2 )   641 - 653   2018.7

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Rice is a major dietary source of the toxic metalloid arsenic. Reducing arsenic accumulation in rice grain is important for food safety.We generated transgenic rice overexpressing two aquaporin genes, OsNIP1;1 and OsNIP3;3, under the control of a maize ubiquitin promoter or the rice OsLsi1 promoter, and tested the effect on arsenite uptake and translocation.OsNIP1;1 and OsNIP3;3 were highly permeable to arsenite in Xenopus oocyte assays. Both transporters were localized at the plasma membrane. Knockout of either gene had little effect on arsenite uptake or translocation. Overexpression of OsNIP1;1 or OsNIP3;3 in rice did not affect arsenite uptake but decreased root-to-shoot translocation of arsenite and shoot arsenic concentration markedly. The overexpressed OsNIP1;1 and OsNIP3;3 proteins were localized in all root cells without polarity. Expression of OsNIP1;1 driven by the OsLsi1 promoter produced similar effects. When grown in two arsenic-contaminated paddy soils, overexpressing lines contained significantly lower arsenic concentration in rice grain than the wild-type without compromising plant growth or the accumulation of essential nutrients.Overexpression of OsNIP1;1 or OsNIP3;3 provides a route for arsenite to leak out of the stele, thus restricting arsenite loading into the xylem. This strategy is effective in reducing arsenic accumulation in rice grain.

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Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice (Oryza sativa) Reviewed

Ge Zi Li, Zhan Qi Wang, Kengo Yokosho, Bing Ding, Wei Fan, Qiao Qiao Gong, Gui Xin Li, Yun Rong Wu, Jian Li Yang, Jian Feng Ma, Shao Jian Zheng

NEW PHYTOLOGIST   219 ( 1 )   149 - 162   2018.7

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Whilst WRKY transcription factors are known to be involved in diverse plant responses to biotic stresses, their involvement in abiotic stress tolerance is poorly understood. OsFRDL4, encoding a citrate transporter, has been reported to be regulated by ALUMINUM (Al) RESISTANCE TRANSCRIPTION FACTOR 1 (ART1) in rice, but whether it is also regulated by other transcription factors is unknown.We define the role of OsWRKY22 in response to Al stress in rice by using mutation and transgenic complementation assays, and characterize the regulation of OsFRDL4 by OsWRKY22 via yeas one-hybrid, electrophoretic mobility shift assay and ChIP-quantitative PCR.We demonstrate that loss of OsWRKY22 function conferred by the oswrky22 T-DNA insertion allele causes enhanced sensitivity to Al stress, and a reduction in Al-induced citrate secretion. We next show that OsWRKY22 is localized in the nucleus, functions as a transcriptional activator and is able to bind to the promoter of OsFRDL4 via W-box elements. Finally, we find that both OsFRDL4 expression and Al-induced citrate secretion are significantly lower in art1 oswrky22 double mutants than in the respective single mutants.We conclude that OsWRKY22 promotes Al-induced increases in OsFRDL4 expression, thus enhancing Al-induced citrate secretion and Al tolerance in rice.

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Efficient and flexible uptake system for mineral elements in plants Reviewed

Jing Che, Naoki Yamaji, Jian Feng Ma

NEW PHYTOLOGIST   219 ( 2 )   513 - 517   2018.7

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Mineral elements required for plant growth and development must first be taken up by the roots from soil. Plants have developed an efficient uptake system for the radial transport of mineral elements from soil to central stele through the allocation of various transporters at different root cells. These transporters are regulated at transcriptional, translational and/or post-translational level to cope with the fluctuation of mineral elements in soil. In this insight, we describe an efficient uptake system for mineral elements formed by influx and efflux transporters, regulatory mechanisms and polarity of these transporters, and sensing and signal pathways, in response to spatial and temporal changes of mineral elements in soil. An understanding of the mineral element uptake system in different plant species, and its regulatory network, will contribute to high and safe crop production under varying environments.

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Plant nutrition for global green growth

Jan K. Schjoerring, Jian F. Ma, Nicolaus von Wirén

Physiologia Plantarum   163 ( 3 )   268   2018.7

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DOI： 10.1111/ppl.12757

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Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter Reviewed

Ji Feng Shao, Jixing Xia, Naoki Yamaji, Ren Fang Shen, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   69 ( 10 )   2743 - 2752   2018.4

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Reducing cadmium (Cd) accumulation in rice grain is an important issue for human health. The aim of this study was to manipulate both expression and tissue localization of OsHMA3, a tonoplast-localized Cd transporter, in the roots by expressing it under the control of the OsHMA2 promoter, which shows high expression in different organs including roots, nodes, and shoots. In two independent transgenic lines, the expression of OsHMA3 was significantly enhanced in all organs compared with non-transgenic rice. Furthermore, OsHMA3 protein was detected in the root pericycle cells and phloem region of both the diffuse vascular bundle and the enlarged vascular bundle of the nodes. At the vegetative stage, the Cd concentration in the shoots and xylem sap of the transgenic rice was significantly decreased, but that of the whole roots and root cell sap was increased. At the reproductive stage, the concentration of Cd, but not other essential metals, in the brown rice of transgenic lines was decreased to less than one-tenth that of the non-transgenic rice. These results indicate that expression of OsHMA3 under the control of the OsHMA2 promoter can effectively reduce Cd accumulation in rice grain through sequestering more Cd into the vacuoles of various tissues.

DOI： 10.1093/jxb/ery107

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Transport system of mineral elements in rice

Namiki Mitani-Ueno, Naoki Yamaji, Jian Feng Ma

Rice Genomics, Genetics and Breeding   223 - 240   2018.3

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Plant requires 14 mineral elements for their growth and development. These elements in the soil are taken up by the roots, translocated from the roots to the shoots, and distributed to different organs depending on their demands (Marschner P, Mineral nutrition of higher plants, 3rd edn. Academic, London, 2012). In addition to these essential elements, toxic elements such as Cd and As are also transported from the soils to aboveground parts. All these processes require various transporters (membrane proteins). During the last decades, a number of transporters for uptake, translocation, and distribution of mineral elements have been identified, especially in model plants such as Arabidopsis and rice; however, most transporters remain to be identified. In this chapter, transporters identified so far in rice are described, and the regulation mechanisms of transporters in response to environmental changes are also discussed.

DOI： 10.1007/978-981-10-7461-5_13

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Saving Water and Associated Energy from Distribution Networks by Considering Landscape Factors in Pressure Management and Use of District Metered Areas

Q. Xu, Q. W. Chen, S. P. Zhao, K. Liu, J. F. Ma

JOURNAL OF ENVIRONMENTAL INFORMATICS   31 ( 1 )   65 - 73   2018.3

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Controlling water loss in distribution systems is attracting increasing interest due to our increasingly limited water resources, exacerbated by rapid population growth, fast urbanization and climate change. Much has been invested in the management of water distribution networks to reduce water loss. However, the efficiency of management measures depends on spatiotemporal patterns of water loss, which are significantly influenced by the urban landscape. It is therefore important to consider urban landscape factors when designing and operating water distribution networks in order to reduce water loss and energy consumption. We investigated how the urban landscape, in particular urban topography and layout of water end users, impacts water loss and energy consumption. Topography was found to significantly influence the spatial pattern of average water pressure, while layout of end users influenced temporal variation of water pressure. A two-level water distribution network operating scheme (PMZ-DMA) was proposed to account for the influences of the two urban landscape factors. Application of the scheme efficiently reduced water loss, thereby generating significant environmental benefits, including reduction of energy consumption and greenhouse gas emissions.

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Preferential Distribution of Boron to Developing Tissues Is Mediated by the Intrinsic Protein OsNIP3 Reviewed

Ji Feng Shao, Naoki Yamaji, Xin Wei Liu, Kengo Yokosho, Ren Fang Shen, Jian Feng Ma

PLANT PHYSIOLOGY   176 ( 2 )   1739 - 1750   2018.2

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER SOC PLANT BIOLOGISTS  

Boron is especially required for the growth of meristem and reproductive organs, but the molecular mechanisms underlying the preferential distribution of B to these developing tissues are poorly understood. Here, we show evidence that a member of nodulin 26-like intrinsic protein (NIP), OsNIP3; 1, is involved in this preferential distribution in rice (Oryza sativa). OsNIP3; 1 was highly expressed in the nodes and its expression was up-regulated by B deficiency, but down-regulated by high B. OsNIP3; 1 was polarly localized at the xylem parenchyma cells of enlarged vascular bundles of nodes facing toward the xylem vessels. Furthermore, this protein was rapidly degraded within a few hours in response to high B. Knockout of this gene hardly affected the uptake and root-to-shoot translocation of B, but altered B distribution in different organs in the above-ground parts, decreased distribution of B to the new leaves, and increased distribution to the old leaves. These results indicate that OsNIP3; 1 located in the nodes is involved in the preferential distribution of B to the developing tissues by unloading B from the xylem in rice and that it is regulated at both transcriptional and protein level in response to external B level.

DOI： 10.1104/pp.17.01641

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OsNRT2.4 encodes a dual-affinity nitrate transporter and functions in nitrate-regulated root growth and nitrate distribution in rice Reviewed

Jia Wei, Yi Zheng, Huimin Feng, Hongye Qu, Xiaorong Fan, Naoki Yamaji, Jian Feng Ma, Guohua Xu

JOURNAL OF EXPERIMENTAL BOTANY   69 ( 5 )   1095 - 1107   2018.2

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Plant NRT2 nitrate transporters commonly require a partner protein, NAR2, for transporting nitrate at low concentrations, but their role in plants is not well understood. In this study, we characterized the gene for one of these transporters in the rice genome, OsNRT2.4, in terms of its activity and roles in rice grown in environments with different N supply. In Xenopus oocytes, OsNRT2.4 alone without OsNAR2 co-expression facilitated nitrate uptake showing biphasic kinetics at a wide concentration range, with high- and low-affinity K-M values of 0.15 and 4 mM, respectively. OsNRT2.4 did not have nitrate efflux or IAA influx activity. In rice roots, OsNRT2.4 was expressed mainly in the base of lateral root primordia. Knockout of OsNRT2.4 decreased lateral root number and length, and the total N uptake per plant at both 0.25 and 2.5 mM NO3- levels. In the shoots, OsNRT2.4 was expressed mainly in vascular tissues, and its knockout decreased the growth and NO3--N distribution. Knockout of OsNRT2.4, however, did not affect rice growth and N uptake under conditions without N or with only NH4+ supply. We conclude that OsNRT2.4 functions as a dual-affinity nitrate transporter and is required for nitrate-regulated root and shoot growth of rice.

DOI： 10.1093/jxb/erx486

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Silicon accumulated in the shoots results in down-regulation of phosphorus transporter gene expression and decrease of phosphorus uptake in rice

An Yong Hu, Jing Che, Ji Feng Shao, Kengo Yokosho, Xue Qiang Zhao, Ren Fang Shen, Jian Feng Ma

PLANT AND SOIL   423 ( 1-2 )   317 - 325   2018.2

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Silicon (Si) as a beneficial element can improve nutrient imbalance, but the molecular mechanism for this effect is poorly understood. The objective of this study is to examine the mechanism underlying Si-induced decrease of phosphorus (P) uptake in rice (Oryza sativa) at adequate/high P supply.A rice mutant (lsi1) defective in Si uptake and its wild type (cv. Oochikara) were used. The P uptake was compared in the presence and absence of Si and the expression of Pi transporter genes was quantified.Si addition in the nutrient solution significantly decreased shoot P concentration and uptake in the WT, but not in lsi1 mutant at two P levels, adequate (90 mu M) and high (210 mu M). Neither the root-to-shoot translocation of P nor the P distribution in different organs was altered by Si in both WT and lsi1. Heterogeneous expression of Lsi1 in Xenopus oocyte did not show transport activity for Pi. The expression of Pi transporter genes (OsPT1, 2 and 8) in the roots was hardly affected by Si in both WT and lsi1, but that of OsPT6 was down-regulated by Si in the WT roots, but not in the lsi1 roots. Furthermore, a split root experiment showed that Si accumulated in the shoots suppressed the expression of OsPT6. In rice grown in paddy field, lsi1 showed higher P concentration in the straw, husk and brown rice than the WT.Si decreased P uptake through down-regulating the expression of P transporter gene, OsPT6 in rice and Si accumulated in the shoot is required for this down-regulation.

DOI： 10.1007/s11104-017-3512-6

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T-DNA Tagging-Based Gain-of-Function of OsHKT1;4 Reinforces Na Exclusion from Leaves and Stems but Triggers Na Toxicity in Roots of Rice Under Salt Stress Reviewed

Yuuka Oda, Natsuko I. Kobayashi, Keitaro Tanoi, Jian Feng Ma, Yukiko Itou, Maki Katsuhara, Takashi Itou, Tomoaki Horie

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES   19 ( 1 )   2018.1

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The high affinity K+ transporter 1;4 (HKT1;4) in rice (Oryza sativa), which shows Na+ selective transport with little K+ transport activity, has been suggested to be involved in reducing Na in leaves and stems under salt stress. However, detailed physiological roles of OsHKT1;4 remain unknown. Here, we have characterized a transfer DNA (T-DNA) insertion mutant line of rice, which overexpresses OsHKT1;4, owing to enhancer elements in the T-DNA, to gain an insight into the impact of OsHKT1;4 on salt tolerance of rice. The homozygous mutant (the O/E line) accumulated significantly lower concentrations of Na in young leaves, stems, and seeds than the sibling WT line under salt stress. Interestingly, however, the mutation rendered the O/E plants more salt sensitive than WT plants. Together with the evaluation of biomass of rice lines, rhizosphere acidification assays using a pH indicator bromocresol purple and (NaCl)-Na-22 tracer experiments have led to an assumption that roots of O/E plants suffered heavier damages from Na which excessively accumulated in the root due to increased activity of Na+ uptake and Na+ exclusion in the vasculature. Implications toward the application of the HKT1-mediated Na+ exclusion system to the breeding of salt tolerant crop cultivars will be discussed.

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Both retrotransposon insertion and demethylation regulate aluminum tolerance of European barley for postdomestication expansion to acid soil.

Fujii-Kashino, M, Yamaji, N, Yamane, M, Saisho, D, Sato, K, Ma, J. F

Plant Physiology   2018

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Rice reduces Mn uptake in response to Mn stress Reviewed

Yuta Tsunemitsu, Naoki Yamaji, Jian Feng Ma, Shin-ichiro Kato, Kozo Iwasaki, Daisei Ueno

PLANT SIGNALING & BEHAVIOR   13 ( 1 )   2018

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Rice (Oryza sativa L) is one of the most Mn-tolerant crops that can grow in submerged paddy fields, where the Mn concentration in soil solution is very high due to reduction. Although a large part of Mn is transferred from the roots to the shoot in rice, the roots are constantly exposed to high Mn concentrations in submerged paddies. Thus, mechanisms for preventing Mn overaccumulation in the cytoplasm of root cells are necessary. Recently, we showed that two cation diffusion facilitators, MTP8.1 and MTP8.2, play a crucial role in Mn tolerance in rice roots by sequestering Mn in vacuoles. Moreover, we observed that disruption of MTP8.1 and MTP8.2 resulted in reduced Mn accumulation under excess Mn. In the present study, we examined the effects of disruption of MTP8.1 and MTP8.2 on Mn uptake and determined that this phenotype is caused by a rapid and significant reduction of Mn uptake in response to excess Mn. Previously, we showed that Mn export from root cells through MTP9 was promoted by high Mn. Together, these findings suggest that optimal Mn concentration in rice roots is maintained by reduced uptake, vacuolar sequestration, and extrusion by cation diffusion facilitators.

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Two MATE Transporters with Different Subcellular Localization are Involved in Al Tolerance in Buckwheat

Gui Jie Lei, Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   58 ( 12 )   2179 - 2189   2017.12

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Buckwheat (Fagopyrum esculentum) shows high tolerance to aluminum (Al) toxicity, but the molecular mechanisms responsible for this high Al tolerance are still poorly understood. Here, we investigated the involvement of two MATE (multi-drug and toxic compound extrusion) genes in Al tolerance. Both FeMATE1 and FeMATE2 showed efflux transport activity for citrate, but not for oxalate when expressed in Xenopus oocytes. A transient assay with buckwheat leaf protoplasts using green fluorescent protein (GFP) fusion showed that FeMATE1 was mainly localized to the plasma membrane, whereas FeMATE2 was localized to the trans-Golgi and Golgi. The expression of FeMATE1 was induced by Al only in the roots, but that of FeMATE2 was up-regulated in both the roots and leaves. Furthermore, the expression of both genes only responded to Al toxicity, but not to other stresses including low pH, cadmium (Cd) and lanthanum (La). Heterologous expression of FeMATE1 or FeMATE2 in the Arabidopsis mutant atmate partially rescued its Al tolerance. Expression of FeMATE1 also partially recovered the Al-induced secretion of citrate in the transgenic lines, whereas expression of FeMATE2 did not complement the citrate secretion. Further physiological analysis showed that buckwheat roots also secreted citrate in addition to oxalate in response to Al in a dose-responsive manner. Taken together, our results indicate that FeMATE1 is involved in the Al-activated citrate secretion in the roots, while FeMATE2 is probably responsible for transporting citrate into the Golgi system for the internal detoxification of Al in the roots and leaves of buckwheat.

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Root cone angle is enlarged in docs1 LRR-RLK mutants in rice

M. Bettembourg, M. Dal-Soglio, C. Bureau, A. Vernet, A. Dardoux, M. Portefaix, M. Bes, D. Meynard, D. Mieulet, B. Cayrol, C. Perin, B. Courtois, J. F. Ma, A. Dievart

RICE   10 ( 1 )   453 - 459   2017.12

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The DEFECTIVE IN OUTER CELL LAYER SPECIFICATION 1 (DOCS1) gene belongs to the Leucine-Rich Repeat Receptor-Like Kinase (LRR-RLK) subfamily. It has been discovered few years ago in Oryza sativa (rice) in a screen to isolate mutants with defects in sensitivity to aluminum. The c68 (docs1-1) mutant possessed a nonsense mutation in the C-terminal part of the DOCS1 kinase domain.
We have generated a new loss-of-function mutation in the DOCS1 gene (docs1-2) using the CRISPR-Cas9 technology. This new loss-of-function mutant and docs1-1 present similar phenotypes suggesting the original docs1-1 was a null allele. Besides the aluminum sensitivity phenotype, both docs1 mutants shared also several root phenotypes described previously: less root hairs and mixed identities of the outer cell layers. Moreover, our new results suggest that DOCS1 could also play a role in root cap development. We hypothesized these docs1 root phenotypes may affect gravity responses. As expected, in seedlings, the early gravitropic response was delayed. Furthermore, at adult stage, the root gravitropic set angle of docs1 mutants was also affected since docs1 mutant plants displayed larger root cone angles.
All these observations add new insights into the DOCS1 gene function in gravitropic responses at several stages of plant development.

DOI： 10.1186/s12284-017-0190-1

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A GDSL-motif esterase/acyltransferase/lipase is responsible for leaf water retention in barley

Chao Li, Guoxiong Chen, Kohei Mishina, Naoki Yamaji, Jian Feng Ma, Fumiko Yukuhiro, Akemi Tagiri, Cheng Liu, Mohammad Pourkheirandish, Nadia Anwar, Masaru Ohta, Pengshan Zhao, Udda Lundqvist, Xinrong Li, Takao Komatsuda

PLANT DIRECT   1 ( 5 )   1 - 12   2017.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：JOHN WILEY & SONS LTD  

The hydrophobic cuticle covers the surface of the most aerial organs of land plants. The barley mutant eceriferum-zv (cer-zv), which is hypersensitive to drought, is unable to accumulate a sufficient quantity of cutin in its leaf cuticle. The mutated locus has been mapped to a 0.02 cM segment in the pericentromeric region of chromosome 4H. As a map-based cloning approach to isolate the gene was therefore considered unlikely to be feasible, a comparison was instead made between the transcriptomes of the mutant and the wild type. In conjunction with extant genomic information, on the basis of predicted functionality, only two genes were considered likely to encode a product associated with cutin formation. When eight independent cer-zv mutant alleles were resequenced with respect to the two candidate genes, it was confirmed that the gene underlying the mutation in each allele encodes a Gly-Asp-Ser-Leu (GDSL)-motif esterase/acyltransferase/lipase. The gene was transcribed in the epidermis, and its product was exclusively deposited in cell wall at the boundary of the cuticle in the leaf elongation zone, coinciding with the major site of cutin deposition. CER-ZV is speculated to function in the deposition of cutin polymer. Its homologs were found in green algae, moss, and euphyllophytes, indicating that it is highly conserved in plant kingdom.

DOI： 10.1002/pld3.25

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Detection of quantitative trait loci controlling grain zinc concentration using Australian wild rice, Oryza meridionalis, a potential genetic resource for biofortification of rice

Ryo Ishikawa, Masahide Iwata, Kenta Taniko, Gotaro Monden, Naoya Miyazaki, Chhourn Orn, Yuki Tsujimura, Shusaku Yoshida, Jian Feng Ma, Takashige Ishii

PLOS ONE   12 ( 10 )   e0187224   2017.10

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Zinc (Zn) is one of the essential mineral elements for both plants and humans. Zn deficiency in human is one of the major causes of hidden hunger, a serious health problem observed in many developing countries. Therefore, increasing Zn concentration in edible part is an important issue for improving human Zn nutrition. Here, we found that an Australian wild rice O. meridionalis showed higher grain Zn concentrations compared with cultivated and other wild rice species. The quantitative trait loci (QTL) analysis was then performed to identify the genomic regions controlling grain Zn levels using backcross recombinant inbred lines derived from O. sativa 'Nipponbare' and O. meridionalis W1627. Four QTLs responsible for high grain Zn were detected on chromosomes 2, 9, and 10. The QTL on the chromosome 9 (named qGZn9), which showed the largest effect on grain Zn concentration was confirmed with the introgression line, which had a W1627 chromosomal segment covering the qGZn9 region in the genetic background of O. sativa 'Nipponbare'. Fine mapping of this QTL resulted in identification of two tightly linked loci, qGZn9a and qGZn9b. The candidate regions of qGZn9a and qGZn9b were estimated to be 190 and 950 kb, respectively. Furthermore, we also found that plants having a wild chromosomal segment covering qGZn9a, but not qGZn9b, is associated with fertility reduction. qGZn9b, therefore, provides a valuable allele for breeding rice with high Zn in the grains.

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Node-controlled allocation of mineral elements in Poaceae

Naoki Yamaji, Jian Feng Ma

CURRENT OPINION IN PLANT BIOLOGY   39   18 - 24   2017.10

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Mineral elements taken up by the roots will be delivered to different organs and tissues depending on their requirements. In Poaceae, this selective distribution is mainly mediated in the nodes, which have highly developed and fully organized vascular systems. Inter-vascular transfer of mineral elements from enlarged vascular bundles to diffuse vascular bundles is required for their preferential distribution to developing tissues and reproductive organs. A number of transporters involved in this inter-vascular transfer processes have been identified mainly in rice. They are localized at the different cell layers and form an efficient machinery within the node. Furthermore, some these transporters show rapid response to the environmental changes of mineral elements at the protein level. In addition to the node-based transporters, distinct nodal structures including enlarged xylem area, folded plasma membrane of xylem transfer cells and presence of an apoplastic barrier are also required for the efficient inter-vascular transfer. Manipulation of node-based transporters will provide a novel breeding target to improve nutrient use efficiency, productivity, nutritional value and safety in cereal crops.

DOI： 10.1016/j.pbi.2017.05.002

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Editorial: Role of Silicon in Plants

Rupesh K. Deshmukh, Jian F. Ma, Richard R. Belanger

FRONTIERS IN PLANT SCIENCE   8   1858   2017.10

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Silicon (Si), the second most abundant element on earth surface, is rapidly gaining attention in agriculture because of its many beneficial effects for plants. Hundreds of studies performed with several plant species and under diverse growth conditions have demonstrated the favorable benefits of Si fertilization, particularly in alleviating biotic and abiotic stresses (Fauteux et al., 2005, 2006). Ever since the breakthrough discovery of genes explaining the molecular mechanisms of Si uptake and transport in plants a decade ago (Ma et al., 2006, 2007), many research endeavors have tried to explain how and why Si presence in plants confers advantages. The most challenging aspect consists in defining a mechanistic model explaining the precise mechanisms involved in Si-derived stress tolerance. While many hypotheses have been proposed, there is no conclusive evidence showing exactly how Si plays a role in stress tolerance. Current efforts to resolve this enigma involve comprehensive analyses of the effect of Si supplementation on various abiotic and biotic stresses, biochemical and physiological parameters, mineral co-localization and distribution, and transcriptomic and metabolomic responses. At the same time, research activities are focused on improving Si fertilization and Si sources for crop cultivation. The present research topic compiles many aspects helpful to generate a better understanding required for the optimal utilization of Si to promote sustainable development and climate-adapted cropping.

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Silicon reduces cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in rice

Ji Feng Shao, Jing Che, Naoki Yamaji, Ren Fang Shen, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   68 ( 20 )   5641 - 5651   2017.9

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Silicon (Si) alleviates cadmium (Cd) toxicity and accumulation in a number of plant species, but the exact molecular mechanisms responsible for this effect are still poorly understood. Here, we investigated the effect of Si on Cd toxicity and accumulation in rice (Oryza sativa) by using two mutants (lsi1 and lsi2) defective in Si uptake and their wild types (WTs). Root elongation was decreased with increasing external Cd concentrations in both WTs and mutants, but Si did not show an alleviative effect on Cd toxicity in all lines. By contrast, the Cd concentration in both the shoots and roots was decreased by Si in the WTs, but not in the mutants. Furthermore, Si supply resulted in a decreased Cd concentration in the root cell sap and xylem sap in the WTs, but not in the mutants. Pre-treatment with Si also decreased Cd accumulation in the WTs, but not in the mutants. Silicon slightly decreased Cd accumulation in the cell wall of the roots. The expression level of OsNramp5 and OsHMA2 was down-regulated by Si in the WTs, but not in the mutants. These results indicate that the Si-decreased Cd accumulation was caused by down-regulating transporter genes involved in Cd uptake and translocation in rice.

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The Tonoplast-Localized Transporter MTP8.2 Contributes to Manganese Detoxification in the Shoots and Roots of Oryza sativa L.

Yuma Takemoto, Yuta Tsunemitsu, Miho Fujii-Kashino, Namiki Mitani-Ueno, Naoki Yamaji, Jian Feng Ma, Shin-ichiro Kato, Kozo Iwasaki, Daisei Ueno

PLANT AND CELL PHYSIOLOGY   58 ( 9 )   1573 - 1582   2017.9

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Manganese (Mn) cation diffusion facilitators (Mn-CDFs) play important roles in the Mn homeostasis of plants. In rice, the tonoplast-localized Mn-CDF metal tolerance protein 8.1 (MTP8.1) is involved in Mn detoxification in the shoots. This study functionally characterized the Mn-CDF MTP8.2 and determined its contribution to Mn tolerance. MTP8.2 was found to share 68% identity with MTP8.1 and was expressed in both the shoots and roots, but its transcription level was lower than that of MTP8.1. Transient expression of the MTP8.2:green fluorescent protein (GFP) fusion protein and immunoblotting studies indicated that MTP8.2 was also localized to the tonoplast. MTP8.2 expression in yeast conferred tolerance to Mn but not to Fe, Zn, Co, Ni or Cd. MTP8.2 knockdown caused further growth reduction of shoots and roots in the mtp8.1 mutant, which already exhibits stunted growth under conditions of excess Mn. In the presence of high Mn, the MTP8.2 knockdown lines of the mtp8.1 mutant showed lower root Mn concentrations, as well as lower root: total Mn ratios, than those of wild-type rice and the mtp8.1 mutant. These findings indicate that MTP8.2 mediates Mn tolerance along with MTP8.1 through the sequestration of Mn into the shoot and root vacuoles.

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Functional characterization of two half-size ABC transporter genes in aluminium-accumulating buckwheat

Gui Jie Lei, Kengo Yokosho, Naoki Yamaji, Miho Fujii-Kashino, Jian Feng Ma

NEW PHYTOLOGIST   215 ( 3 )   1080 - 1089   2017.8

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Buckwheat (Fagopyrum esculentum Moench) is able to detoxify high aluminium (Al) internally by sequestering it to the vacuoles in the leaves; however, the molecular mechanisms underlying this sequestration are unknown.We performed proteomic analysis with the leaf tonoplast-rich fraction and identified two half-size ABC transporters; FeASL1.1 and FeALS1.2. We investigated the gene expression patterns and subcellular localization. To demonstrate their physiological role, we expressed FeALS1.1 or FeALS1.2 in the Arabidopsis atals1 mutant under the control of AtALS1 promoter.FeALS1.1 expression was upregulated by Al in both the leaves and the roots, and its expression level in the roots was six times higher than its homologous gene (AtALS1) of Arabidopsis. FeALS1.2 expression, however, was not affected by Al but showed a 39 times higher expression level than AtALS1 in the leaves. When FeALS1.1 or FeALS1.2 was expressed in atals1, both of them recovered their Al tolerance through altering the subcellular localization of Al in root cells.Taken together, our results indicate that FeALS1.1 and FeALS1.2 are involved in the internal detoxification of Al in the roots and leaves, respectively, by sequestering Al into the vacuoles. Their high expression is probably required for high Al tolerance in buckwheat.

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OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice

Natsuko I. Kobayashi, Naoki Yamaji, Hiroki Yamamoto, Kaoru Okubo, Hiroki Ueno, Alex Costa, Keitaro Tanoi, Hideo Matsumura, Miho Fujii-Kashino, Tomoki Horiuchi, Mohammad Al Nayef, Sergey Shabala, Gynheung An, Jian Feng Ma, Tomoaki Horie

PLANT JOURNAL   91 ( 4 )   657 - 670   2017.8

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Salt tolerance quantitative trait loci analysis of rice has revealed that the SKC1 locus, which is involved in a higher K+/Na+ ratio in shoots, corresponds to the OsHKT1;5 gene encoding a Na+-selective transporter. However, physiological roles of OsHKT1;5 in rice exposed to salt stress remain elusive, and no OsHKT1;5 gene disruption mutants have been characterized to date. In this study, we dissected two independent TDNA insertional OsHKT1;5 mutants. Measurements of ion contents in tissues and 22 Na+ tracer imaging experiments showed that loss-of-function of OsHKT1;5 in salt-stressed rice roots triggers massive Na+ accumulation in shoots. Salt stress-induced increases in the OsHKT1;5 transcript were observed in roots and basal stems, including basal nodes. Immuno-staining using an anti-OsHKT1;5 peptide antibody indicated that OsHKT1;5 is localized in cells adjacent to the xylem in roots. Additionally, direct introduction of 22 Na+ tracer to leaf sheaths also demonstrated the involvement of OsHKT1;5 in xylem Na+ unloading in leaf sheaths. Furthermore, OsHKT1;5 was indicated to be present in the plasma membrane and found to localize also in the phloem of diffuse vascular bundles in basal nodes. Together with the characteristic 22 Na+ allocation in the blade of the developing immature leaf in the mutants, these results suggest a novel function of OsHKT1;5 in mediating Na+ exclusion in the phloem to prevent Na+ transfer to young leaf blades. Our findings further demonstrate that the function of OsHKT1;5 is crucial over growth stages of rice, including the protection of the next generation seeds as well as of vital leaf blades under salt stress.

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A Magnesium Transporter OsMGT1 Plays a Critical Role in Salt Tolerance in Rice(1[OPEN])

Zhi Chang Chen, Naoki Yamaji, Tomoaki Horie, Jing Che, Jian Li, Gynheung An, Jian Feng Ma

PLANT PHYSIOLOGY   174 ( 3 )   1837 - 1849   2017.7

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Salt stress is one of the major factors limiting rice (Oryza sativa) production globally. Although several transporters involved in salt tolerance have been identified in rice, the mechanisms regulating their transport activity are still poorly understood. Here, we show evidence that a rice Mg transporter OsMGT1 is required for salt tolerance probably by regulating transport activity of OsHKT1;5, a key transporter for the removal of Na+ from the xylem sap at the root mature zone. Knockout of OsMGT1 did not affect total Na uptake, but increased Na concentration in the shoots and xylem sap, resulting in a significant increase in salt sensitivity at low external Mg2+ concentration (20-200 mu M). However, such differences were abolished at a higher Mg2+ concentration (2 mM), although the total Na uptake was not altered. OsMGT1 was expressed in both the roots and shoots, but only that in the roots was moderately up-regulated by salt stress. Spatial expression analysis revealed that OsMGT1 was expressed in all root cells of the root tips but was highly expressed in the pericycle of root mature zone. OsMGT1 was also expressed in the phloem region of basal node, leaf blade, and sheath. When expressed in Xenopus laevis oocytes, the transport activity of OsHKT1;5 was enhanced by elevating external Mg2+ concentration. Furthermore, knockout of OsHKT1;5 in osmgt1 mutant background did not further increase its salt sensitivity. Taken together, our results suggest that Mg2+ transported by OsMGT1 in the root mature zone is required for enhancing OsHKT1;5 activity, thereby restricting Na accumulation to the shoots.

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Identification of a mammalian silicon transporter

Sarah Ratcliffe, Ravin Jugdaohsingh, Julien Vivancos, Alan Marron, Rupesh Deshmukh, Jian Feng Ma, Namiki Mitani-Ueno, Jack Robertson, John Wills, Mark V. Boekschoten, Michael Mueller, Robert C. Mawhinney, Stephen D. Kinrade, Paul Isenring, Richard R. Belanger, Jonathan J. Powell

AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY   312 ( 5 )   C550 - C561   2017.5

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Silicon (Si) has long been known to play a major physiological and structural role in certain organisms, including diatoms, sponges, and many higher plants, leading to the recent identification of multiple proteins responsible for Si transport in a range of algal and plant species. In mammals, despite several convincing studies suggesting that silicon is an important factor in bone development and connective tissue health, there is a critical lack of understanding about the biochemical pathways that enable Si homeostasis. Here we report the identification of a mammalian efflux Si transporter, namely Slc34a2 (also termed NaPiIIb), a known sodium-phosphate cotransporter, which was upregulated in rat kidney following chronic dietary Si deprivation. Normal rat renal epithelium demonstrated punctate expression of Slc34a2, and when the protein was heterologously expressed in Xenopus laevis oocytes, Si efflux activity (i.e., movement of Si out of cells) was induced and was quantitatively similar to that induced by the known plant Si transporter OsLsi2 in the same expression system. Interestingly, Si efflux appeared saturable over time, but it did not vary as a function of extracellular HPO42- or Na+ concentration, suggesting that Slc34a2 harbors a functionally independent transport site for Si operating in the reverse direction to the site for phosphate. Indeed, in rats with dietary Si depletion-induced upregulation of transporter expression, there was increased urinary phosphate excretion. This is the first evidence of an active Si transport protein in mammals and points towards an important role for Si in vertebrates and explains interactions between dietary phosphate and silicon.

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Polar Localization of the NIP5;1 Boric Acid Channel Is Maintained by Endocytosis and Facilitates Boron Transport in Arabidopsis Roots

Sheliang Wang, Akira Yoshinari, Tomoo Shimada, Ikuko Hara-Nishimura, Namiki Mitani-Ueno, Jian Feng Ma, Satoshi Naito, Junpei Takano

PLANT CELL   29 ( 4 )   824 - 842   2017.4

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Boron uptake in Arabidopsis thaliana is mediated by nodulin 26-like intrinsic protein 5;1 (NIP5;1), a boric acid channel that is located preferentially on the soil side of the plasma membrane in root cells. However, the mechanism underlying this polar localization is poorly understood. Here, we show that the polar localization of NIP5;1 in epidermal and endodermal root cells is mediated by the phosphorylation of Thr residues in the conserved TPG (ThrProGly) repeat in the N-terminal region of NIP5;1. Although substitutions of Ala for three Thr residues in the TPG repeat did not affect lateral diffusion in the plasma membrane, these substitutions inhibited endocytosis and strongly compromised the polar localization of GFP-NIP5;1. Consistent with this, the polar localization was compromised in m subunit mutants of the clathrin adaptor AP2. The Thr-to-Ala substitutions did not affect the boron transport activity of GFP-NIP5;1 in Xenopus laevis oocytes but did inhibit the ability to complement boron translocation to shoots and rescue growth defects in nip5;1-1 mutant plants under boron-limited conditions. These results demonstrate that the polar localization of NIP5;1 is maintained by clathrin-mediated endocytosis, is dependent on phosphorylation in the TPG repeat, and is necessary for the efficient transport of boron in roots.

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The Key to Vn Homeostasis in Plants: Regulation of Mn Transporters

Ji Feng Shao, Naoki Yamaji, Ren Fang Shen, Jian Feng Ma

TRENDS IN PLANT SCIENCE   22 ( 3 )   215 - 224   2017.3

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Plants only require small amounts of manganese (Mn) for healthy growth, but Mn concentrations in soil solution vary from sub-micromolar to hundreds of micromolar across the growth period. Therefore, plants must deal with large Mn concentration fluctuations, but the molecular mechanisms underlying how plants cope with low and high Mn concentrations are poorly understood. In this Opinion we discuss the role of Mn transporters in the uptake, distribution, and detoxification of Mn in response to changes in Mn concentrations through their regulation at the transcriptional and protein levels, mainly focusing on rice, an Mn-tolerant and accumulating species. We also propose mechanisms involved in the hyperaccumulation of Mn and future prospects for studying this specific trait.

DOI： 10.1016/j.tplants.2016.12.005

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Reducing phosphorus accumulation in rice grains with an impaired transporter in the node (vol 541, pg 92, 2017) Reviewed

Naoki Yamaji, Yuma Takemoto, Takaaki Miyaji, Namiki Mitani-Ueno, Kaoru T. Yoshida, Jian Feng Ma

NATURE   541 ( 7635 )   136 - 136   2017.1

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DOI： 10.1038/nature21404

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Iron-induced nitric oxide leads to an increase in the expression of ferritin during the senescence of Lotus japonicus nodules

Sirinapa Chungopast, Mallika Duangkhet, Shigeyuki Tajima, Jian Feng Ma, Mika Nomura

JOURNAL OF PLANT PHYSIOLOGY   208   40 - 46   2017.1

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Iron is an essential nutrient for legume-rhizobium symbiosis and accumulates abundantly in the nodules. However, the concentration of free iron in the cells is strictly controlled to avoid toxicity. It is known that ferritin accumulates in the cells as an iron storage protein. During nodule senescence, the expression of the ferritin gene, Ljfer1, was induced in Lotus japonicus. We investigated a signal transduction pathway leading to the increase of Ljfer1 in the nodule. The Ljfer1 promoter of L. japonicus contains a conserved Iron-Dependent Regulatory Sequence (IDRS). The expression of Ljfer1 was induced by the application of iron or sodium nitroprusside, which is a nitric oxide (NO) donor. The application of iron to the nodule increased the level of NO. These data strongly suggest that iron-induced NO leads to increased expression of Ljfer1 during the senescence of L. japonicus nodules. (C) 2016 Elsevier GmbH. All rights reserved.

DOI： 10.1016/j.jplph.2016.11.004

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Isolation and characterization of a rice line with high Cd accumulation for potential use in phytoremediation

Ji Feng Shao, Miho Fujii-Kashino, Naoki Yamaji, Shinichi Fukuoka, Ren Fang Shen, Jian Feng Ma

PLANT AND SOIL   410 ( 1-2 )   357 - 368   2017.1

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To reduce cadmium (Cd) intake, remediation of Cd-contaminated soil and breeding crops with low Cd accumulation are important. This study aims to isolate rice mutants with altered accumulation of Cd.We used rice seeds mutated by N-methyl-N-nitrosourea for screening. The mutant was physiologically, genetically, and molecularly characterized. Cd accumulation was compared among five rice varieties cultivated in a Cd-contaminated soil.From 1000 lines screened, we isolated a line (TCM213) with high Cd accumulation. There was no difference in the root Cd uptake, but a higher root-to-shoot translocation of Cd was found in TCM213 compared with a common rice cultivar, T-65. The expression and sequence of OsNramp5 and OsHMA2 did not differ between TCM213 and T-65. However, several SNPs and deletion were found in the sequence of OsHMA3, although its expression and tissue localization were similar to those of T-65. Genetic analysis of an F-2 population derived from T-65 and TCM213 showed that the variation of OsHMA3 explained 72 % of variation in total Cd accumulation. TCM213 accumulated the largest Cd amount in the shoots among five Cd-accumulating varieties.High Cd accumulation in TCM213 results from loss of function of OsHMA3, and its high Cd accumulation has potential for efficient phytoremediation of Cd-contaminated soil.

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A model of silicon dynamics in rice Reviewed

Gen Sakurai, Naoki Yamaji, Namiki Mitani-Ueno, Masayuki Yokozawa, Keisuke Ono, Jian Feng Ma

Frontiers in Plant Science   8   E31-E34   2017

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High Silicon Accumulation in the Shoot is Required for Down-Regulating the Expression of Si Transporter Genes in Rice

Namiki Mitani-Ueno, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   57 ( 12 )   2510 - 2518   2016.12

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Rice requires high silicon (Si) for its high and sustainable yield. The efficient uptake of Si in rice is mediated by two transporters OsLsi1 and OsLsi2, which function as influx and efflux transporters, respectively. Our previous studies showed that the mRNA expression levels of these transporter genes were down-regulated by Si. Herein we investigated the mechanism underlying regulation of OsLsi1 and OsLsi2 expression. There was a negative correlation between the expression level of OsLsi1 and OsLsi2 and shoot Si accumulation when the rice seedlings were exposed to different Si supply conditions. A split root experiment showed that the expression of both OsLsi1 and OsLsi2 was also downregulated in half the roots without direct Si exposure when the other half of the roots were exposed to Si. Analysis with transgenic rice carrying different lengths of OsLsi1 promoter regions fused with green fluorescent protein (GFP) as a reporter gene revealed that the region responsible for the Si response of OsLsi1 expression is present between -327 to -292 in the promoter. However, this region was not associated with the tissue and cellular localization of OsLsi1. In conclusion, the Si-induced down-regulation of Si transporter genes is controlled by shoot Si, not root Si, and the region between -327 and -292 in the OsLsi1 promoter is involved in this regulation of OsLsi1 expression in rice.

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Retrotransposon-Mediated Aluminum Tolerance through Enhanced Expression of the Citrate Transporter OsFRDL4

Kengo Yokosho, Naoki Yamaji, Miho Fujii-Kashino, Jian Feng Ma

PLANT PHYSIOLOGY   172 ( 4 )   2327 - 2336   2016.12

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High aluminum (Al) tolerance of rice (Oryza sativa) is controlled by multiple tolerance genes, but the regulatory mechanisms underlying the differential expression of these genes are poorly understood. Here, we investigated the factors regulating the expression of OsFRDL4, a gene encoding a citrate efflux transporter involved in Al-induced citrate secretion from the roots. Analysis with chromosome segment substitution lines derived from cv Nipponbare (high OsFRDL4 expression) and cv Kasalath (low OsFRDL4 expression) revealed that the differential expression of OsFRDL4 is responsible for the quantitative trait locus for Al tolerance detected previously on chromosome 1. Comparison of the OsFRDL4 gene structure in cv Nipponbare and cv Kasalath showed that there was no difference in the position of the transcriptional start site, but a 1.2-kb insertion showing high similarity to the solo long terminal repeat of the retrotransposon was found in the promoter region of OsFRDL4 in cv Nipponbare. This insertion showed higher promoter activity and contained nine cis-acting elements for ALUMINUM RESISTANCE TRANSCRIPTION FACTOR1 (ART1). However, this insertion did not alter the spatial expression or cellular localization of OsFRDL4. Furthermore, this insertion was found in most japonica varieties but was largely absent from indica varieties or wild rice species. These results indicate that the 1.2-kb insertion in the OsFRDL4 promoter region in japonica subspecies is responsible for their higher expression level of OsFRDL4 due to the increased number of cis-acting elements of ART1. Our results also suggest that this insertion event happened at the initial stage of domestication of japonica subspecies.

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The HvNramp5 Transporter Mediates Uptake of Cadmium and Manganese, But Not Iron International journal

Dezhi Wu, Naoki Yamaji, Miki Yamane, Miho Kashino-Fujii, Kazuhiro Sato, Jian Feng Ma

PLANT PHYSIOLOGY   172 ( 3 )   1899 - 1910   2016.11

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The Natural Resistance Associated Macrophage Protein (Nramp) represents a transporter family for metal ions in all organisms. Here, we functionally characterized a member of Nramp family in barley (Hordeum vulgare), HvNramp5. This member showed different expression patterns, transport substrate specificity, and cellular localization from its close homolog in rice (Oryza sativa), OsNramp5, although HvNramp5 was also localized to the plasma membrane. HvNramp5 was mainly expressed in the roots and its expression was not affected by Cd and deficiency of Zn, Cu, and Mn, but slightly up-regulated by Fe deficiency. Spatial expression analysis showed that the expression of HvNramp5 was higher in the root tips than that in the basal root regions. Furthermore, analysis with laser microdissection revealed higher expression of HvNramp5 in the outer root cell layers. HvNramp5 showed transport activity for both Mn2+ and Cd2+, but not for Fe2+ when expressed in yeast. Immunostaining with a HvNramp5 antibody showed that this protein was localized in the root epidermal cells without polarity. Knockdown of HvNramp5 in barley resulted in a significant reduction in the seedling growth at low Mn supply, but this reduction was rescued at high Mn supply. The concentration of Mn and Cd, but not other metals including Cu, Zn, and Fe, was decreased in both the roots and shoots of knockdown lines compared with the wild-type barley. These results indicate that HvNramp5 is a transporter required for uptake of Mn and Cd, but not for Fe, and that barley has a distinct uptake system from rice.

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OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice

Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   67 ( 18 )   5485 - 5494   2016.10

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OsFRDL1 expressed in the upper nodes is required for the distribution of Fe to the panicles through solubilizing Fe deposited in the apoplastic part of nodes in rice.Iron (Fe) is essential for plant growth and development, but the molecular mechanisms underlying its distribution to different organs are poorly understood. We found that OsFRDL1 (FERRIC REDUCTASE DEFECTIVE LIKE 1), a plasma membrane-localized transporter for citrate, was highly expressed in the upper nodes of rice at the reproductive growth stage. OsFRDL1 was expressed in most cells of enlarged vascular bundles, diffuse vascular bundles, and the interjacent parenchyma cell bridges of uppermost node I, as well as vascular tissues of the leaf blade, leaf sheath, peduncle, rachis, husk, and stamen. Knockout of OsFRDL1 decreased pollen viability and grain fertility when grown in a paddy field. Iron was deposited in the parenchyma cell bridges, a few of the cell layers of the parenchyma tissues outside of the bundle sheath of enlarged vascular bundles in node I in both the wild-type rice and osfrdl1 mutant, but the mutant accumulated more Fe than the wild-type rice in this area. A stem-fed experiment with stable isotope Fe-57 showed that the distribution of Fe in the anther and panicle decreased in the knockout line, but that in the flag leaf it increased compared with the wild-type rice. Taken together, our results show that OsFRDL1 expressed in the upper nodes is required for the distribution of Fe in the panicles through solubilizing Fe deposited in the apoplastic part of nodes in rice.

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A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain

Xin-Yuan Huang, Fenglin Deng, Naoki Yamaji, Shannon R. M. Pinson, Miho Fujii-Kashino, John Danku, Alex Douglas, Mary Lou Guerinot, David E. Salt, Jian Feng Ma

NATURE COMMUNICATIONS   7   2016.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATURE PUBLISHING GROUP  

Rice is a major source of calories and mineral nutrients for over half the world's human population. However, little is known in rice about the genetic basis of variation in accumulation of copper (Cu), an essential but potentially toxic nutrient. Here we identify OsHMA4 as the likely causal gene of a quantitative trait locus controlling Cu accumulation in rice grain. We provide evidence that OsHMA4 functions to sequester Cu into root vacuoles, limiting Cu accumulation in the grain. The difference in grain Cu accumulation is most likely attributed to a single amino acid substitution that leads to different OsHMA4 transport activity. The allele associated with low grain Cu was found in 67 of the 1,367 rice accessions investigated. Identification of natural allelic variation in OsHMA4 may facilitate the development of rice varieties with grain Cu concentrations tuned to both the concentration of Cu in the soil and dietary needs.

DOI： 10.1038/ncomms12138

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Transporters involved in mineral nutrient uptake in rice

Akimasa Sasaki, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   67 ( 12 )   3645 - 3653   2016.6

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One of the most important roles of plant roots is to take up essential mineral nutrients from the soil for use in plant growth and development. The uptake of mineral elements is mediated by various transporters belonging to different transporter families. Here we reviewed transporters for the uptake of macronutrients and micronutrients identified in rice, an important staple food for half of the world's population. Rice roots are characterized by having two Casparian strips on the exodermis and endodermis and by the formation of aerenchyma in the mature root zone. This distinct anatomical structure dictates that a pair of influx and efflux transporters at both the exodermis and endodermis is required for the radial transport of a mineral element from the soil solution to the stele. Some transporters showing polar localization at the distal and proximal sides of the exodermis and endodermis have been identified for silicon and manganese, forming an efficient uptake system. However, transporters for the uptake of most mineral elements remain to be identified.

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An Aluminum-Inducible IREG Gene is Required for Internal Detoxification of Aluminum in Buckwheat

Kengo Yokosho, Naoki Yamaji, Namiki Mitani-Ueno, Ren Fang Shen, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   57 ( 6 )   1169 - 1178   2016.6

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Buckwheat (Fagopyrum esculentum Moench) is able to detoxify aluminum (Al) both externally and internally, but the molecular mechanisms underlying its high Al tolerance are not understood. We functionally characterized a gene (FeIREG1) belonging to IRON REGULATED/ferroportin in buckwheat, which showed high expression in our previous genome-wide transcriptome analysis. FeIREG1 was mainly expressed in the roots, and its expression was up-regulated by Al, but not by other metals and low pH. Furthermore, in contrast to AtIREG1 and AtIREG2 in Arabidopsis, the expression of FeIREG1 was not induced by Fe deficiency. Spatial expression analysis showed that the Al-induced expression of FeIREG1 was found in the root tips and higher expression was detected in the outer layers of this part. Immunostaining also showed that FeIREG1 was localized at the outer cell layers in the root tip. A FeIREG1-green fluorescent protein (GFP) fusion protein was localized to the tonoplast when transiently expressed in onion epidermal cells. Overexpression of FeIREG1 in Arabidopsis resulted in increased Al tolerance, but did not alter the tolerance to Cd, Co and Fe. The tolerance to Ni was slightly enhanced in the overexpression lines. Mineral analysis showed that the accumulation of total root Al and other essential mineral elements was hardly altered in the overexpression lines. Taken together, our results suggest that FeIREG1 localized at the tonoplast plays an important role in internal Al detoxification by sequestering Al into the root vacuoles in buckwheat.

DOI： 10.1093/pcp/pcw065

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Oryza sativa H+-ATPase (OSA) is Involved in the Regulation of Dumbbell-Shaped Guard Cells of Rice

Yosuke Toda, Yin Wang, Akira Takahashi, Yuya Kawai, Yasuomi Tada, Naoki Yamaji, Jian Feng Ma, Motoyuki Ashikari, Toshinori Kinoshita

PLANT AND CELL PHYSIOLOGY   57 ( 6 )   1220 - 1230   2016.6

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The stomatal apparatus consists of a pair of guard cells and regulates gas exchange between the leaf and atmosphere. In guard cells, blue light (BL) activates H+-ATPase in the plasma membrane through the phosphorylation of its penultimate threonine, mediating stomatal opening. Although this regulation is thought to be widely adopted among kidney-shaped guard cells in dicots, the molecular basis underlying that of dumbbell-shaped guard cells in monocots remains unclear. Here, we show that H+-ATPases are involved in the regulation of dumbbell-shaped guard cells. Stomatal opening of rice was promoted by the H+-ATPase activator fusicoccin and by BL, and the latter was suppressed by the H+-ATPase inhibitor vanadate. Using H+-ATPase antibodies, we showed the presence of phosphoregulation of the penultimate threonine in Oryza sativa H+-ATPases (OSAs) and localization of OSAs in the plasma membrane of guard cells. Interestingly, we identified one H+-ATPase isoform, OSA7, that is preferentially expressed among the OSA genes in guard cells, and found that loss of function of OSA7 resulted in partial insensitivity to BL. We conclude that H+-ATPase is involved in BL-induced stomatal opening of dumbbell-shaped guard cells in monocotyledon species.

DOI： 10.1093/pcp/pcw070

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A Cation-Chloride Cotransporter Gene Is Required for Cell Elongation and Osmoregulation in Rice

Zhi Chang Chen, Naoki Yamaji, Miho Fujii-Kashino, Jian Feng Ma

PLANT PHYSIOLOGY   171 ( 1 )   494 - 507   2016.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER SOC PLANT BIOLOGISTS  

Rice (Oryza sativa) is characterized by having fibrous root systems; however, the molecular mechanisms underlying the root development are not fully understood. Here, we isolated a rice mutant with short roots and found that the mutant had a decreased cell size of the roots and shoots compared with wild-type rice. Map-based cloning combined with whole-genome sequencing revealed that a single nucleotide mutation occurred in a gene, which encodes a putative cation-chloride cotransporter (OsCCC1). Introduction of OsCCC1 cDNA into the mutant rescued the mutant growth, indicating that growth defects of both the roots and shoots are caused by loss of function of OsCCC1. Physiological analysis showed that the mutant had a lower concentration of Cl- and K+ and lower osmolality in the root cell sap than the wild type at all KCl supply conditions tested; however, the mutant only showed a lower Na+ concentration at high external Na+. Expression of OsCCC1 in yeast increased accumulation of K+, Na+, and Cl-. The expression of OsCCC1 was found in both the roots and shoots, although higher expression was found in the root tips. Furthermore, the expression in the roots did not respond to different Na+, K+, and Cl- supply. OsCCC1 was expressed in all cells of the roots, leaf, and basal node. Immunoblot analysis revealed that OsCCC1 was mainly localized to the plasma membrane. These results suggest that OsCCC1 is involved in the cell elongation by regulating ion (Cl-, K+, and Na+) homeostasis to maintain cellular osmotic potential.

DOI： 10.1104/pp.16.00017

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Functional Analysis of a MATE Gene OsFRDL2 Revealed its Involvement in Al-Induced Secretion of Citrate, but a Lower Contribution to Al Tolerance in Rice

Kengo Yokosho, Naoki Yamaji, Miho Fujii-Kashino, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   57 ( 5 )   976 - 985   2016.5

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The multidrug and toxic compound extrusion (MATE) transporters represent a large transporter family in plants, but the role of most genes in this family has not been examined. We functionally characterized a MATE family member, OsFRDL2, in rice (Oryza sativa). OsFRDL2 showed an efflux transport activity for citrate when it was expressed in both Xenopus oocytes and cultured tobacco cells. OsFRDL2 was mainly expressed in the roots and its expression was not induced by iron (Fe) deficiency, but it was rapidly up-regulated by aluminum (Al). Furthermore, the expression of OsFRDL2 was regulated by ART1, a C2H2-type zinc-finger transcription factor for Al tolerance. OsFRDL2 protein was localized at unidentified vesicles in the cytosol, but not co-localized with either mitochondria or peroxisomes when expressed in both onion epidermal cells and cultured tobacco cells. Knockout of OsFRDL2 decreased Al-induced secretion of citrate from the roots, but did not affect the internal citrate concentration. The Al-induced inhibition of root elongation was similar between the OsFRDL2 knockout line and its wild-type rice. Knockout of OsFRDL2 did not affect the translocation of Fe from the roots to the shoots. A double mutant between osfrdl2 and osfrdl4 or osfrdl1 did not further decrease the Al-induced citrate secretion and Fe translocation compared with the single mutant. Collectively, our results indicate that although OsFRDL2 is involved in the Al-induced secretion of citrate, its contribution to high Al tolerance is relatively small in rice.

DOI： 10.1093/pcp/pcw026

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Silicon decreases both uptake and root-to-shoot translocation of manganese in rice

Jing Che, Naoki Yamaji, Ji Feng Shao, Jian Feng Ma, Ren Fang Shen

JOURNAL OF EXPERIMENTAL BOTANY   67 ( 5 )   1535 - 1544   2016.3

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Silicon (Si) is known to alleviate manganese (Mn) toxicity in a number of plant species; however, the mechanisms responsible for this effect are poorly understood. Here, we investigated the interaction between Si and Mn in rice (Oryza sativa) by using a mutant defective in Si uptake. Silicon alleviated Mn toxicity in the wild-type (WT) rice, but not in the mutant exposed to high Mn. The Mn concentration in the shoots was decreased, but that in the roots was increased by Si in the WT. In contrast, the Mn concentration in the roots and shoots was unaffected by Si in the mutant. Furthermore, Si supply resulted in an increased Mn in the root cell sap, decreased Mn in the xylem sap in the WT, but these effects of Si were not observed in the mutant. A short-term labelling experiment with Mn-54 showed that the uptake of Mn was similar between plants with and without Si and between WT and the mutant. However, Si decreased root-to-shoot translocation of Mn in the WT, but not in the mutant. The expression of a Mn transporter gene for uptake, OsNramp5, was unaffected by a short exposure (< 1 d) to Si, but down-regulated by relatively long-term exposure to Si in WT. In contrast, the expression of OsNramp5 was unaffected by Si in the mutant. These results indicated that Si-decreased Mn accumulation results from both Si-decreased root-to-shoot translocation of Mn, probably by the formation of Mn-Si complex in root cells, and uptake by down-regulating Mn transporter gene.

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OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress

Kei Suzuki, Naoki Yamaji, Alex Costa, Eiji Okuma, Natsuko I. Kobayashi, Tatsuhiko Kashiwagi, Maki Katsuhara, Cun Wang, Keitaro Tanoi, Yoshiyuki Murata, Julian I. Schroeder, Jian Feng Ma, Tomoaki Horie

BMC PLANT BIOLOGY   16 ( 1 )   2016.1

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Background: Na+ exclusion from leaf blades is one of the key mechanisms for glycophytes to cope with salinity stress. Certain class I transporters of the high-affinity K+ transporter (HKT) family have been demonstrated to mediate leaf blade-Na+ exclusion upon salinity stress via Na+-selective transport. Multiple HKT1 transporters are known to function in rice (Oryza sativa). However, the ion transport function of OsHKT1;4 and its contribution to the Na+ exclusion mechanism in rice remain to be elucidated.Results: Here, we report results of the functional characterization of the OsHKT1; 4 transporter in rice. OsHKT1; 4 mediated robust Na+ transport in Saccharomyces cerevisiae and Xenopus laevis oocytes. Electrophysiological experiments demonstrated that OsHKT1; 4 shows strong Na+ selectivity among cations tested, including Li+, Na+, K+, Rb+, Cs+, and NH4+, in oocytes. A chimeric protein, EGFP-OsHKT1;4, was found to be functional in oocytes and targeted to the plasma membrane of rice protoplasts. The level of OsHKT1; 4 transcripts was prominent in leaf sheaths throughout the growth stages. Unexpectedly however, we demonstrate here accumulation of OsHKT1;4 transcripts in the stem including internode II and peduncle in the reproductive growth stage. Moreover, phenotypic analysis of OsHKT1;4 RNAi plants in the vegetative growth stage revealed no profound influence on the growth and ion accumulation in comparison with WT plants upon salinity stress. However, imposition of salinity stress on the RNAi plants in the reproductive growth stage caused significant Na+ overaccumulation in aerial organs, in particular, leaf blades and sheaths. In addition, Na-22(+) tracer experiments using peduncles of RNAi and WT plants suggested xylem Na+ unloading by OsHKT1;4.Conclusions: Taken together, our results indicate a newly recognized function of OsHKT1;4 in Na+ exclusion in stems together with leaf sheaths, thus excluding Na+ from leaf blades of a japonica rice cultivar in the reproductive growth stage, but the contribution is low when the plants are in the vegetative growth stage.

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Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods

Stephan Clemens, Jian Feng Ma

ANNUAL REVIEW OF PLANT BIOLOGY, VOL 67   67   489 - 512   2016

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Arsenic, cadmium, lead, and mercury are toxic elements that are almost ubiquitously present at low levels in the environment because of anthropogenic influences. Dietary intake of plant-derived food represents a major fraction of potentially health-threatening human exposure, especially to arsenic and cadmium. In the interest of better food safety, it is important to reduce toxic element accumulation in crops. A molecular understanding of the pathways responsible for this accumulation can enable the development of crop varieties with strongly reduced concentrations of toxic elements in their edible parts. Such understanding is rapidly progressing for arsenic and cadmium but is in its infancy for lead and mercury. Basic discoveries have been made in Arabidopsis, rice, and other models, and most advances in crops have been made in rice. Proteins mediating the uptake of arsenic and cadmium have been identified, and the speciation and biotransformations of arsenic are now understood. Factors controlling the efficiency of root-to-shoot translocation and the partitioning of toxic elements through the rice node have also been identified.

DOI： 10.1146/annurev-arplant-043015-112301

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A polarly localized transporter for efficient manganese uptake in rice

Daisei Ueno, Akimasa Sasaki, Naoki Yamaji, Takaaki Miyaji, Yumi Fujii, Yuma Takemoto, Sawako Moriyama, Jing Che, Yoshinori Moriyama, Kozo Iwasaki, Jian Feng Ma

NATURE PLANTS   1 ( 12 )   2015.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATURE PUBLISHING GROUP  

Manganese is an essential metal for plant growth. A number of transporters involved in the uptake of manganese from soils, and its translocation to the shoot, have been identified in Arabidopsis and rice. However, the transporter responsible for the radial transport of manganese out of root exodermis and endodermis cells and into the root stele remains unknown. Here, we show that metal tolerance protein 9 (MTP9), a member of the cation diffusion facilitator family, is a critical player in this process in rice (Oryza sativa). We find that MTP9 is mainly expressed in roots, and that the resulting protein is localized to the plasma membrane of exo- and endodermis cells, at the proximal side of these cell layers (opposite the manganese uptake transporter Nramp5, which is found at the distal side). We demonstrate that MTP9 has manganese transport activity by expression in proteoliposomes and yeast, and show that knockout of MTP9 in rice reduces manganese uptake and its translocation to shoots. We conclude that at least in rice MTP9 is required for manganese translocation to the root stele, and thereby manganese uptake.

DOI： 10.1038/NPLANTS.2015.170

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Genome-wide association mapping of cadmium accumulation in different organs of barley International journal

Dezhi Wu, Kazuhiro Sato, Jian Feng Ma

NEW PHYTOLOGIST   208 ( 3 )   817 - 829   2015.11

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The threshold value of cadmium (Cd) concentration in grains of barley (Hordeum vulgare) is the lowest among cereal crops; however, it is poorly understood how Cd accumulation in barley grain is genetically controlled.We investigated genotypic variation in Cd accumulation of different organs in 100 accessions from a subset of the barley core collection using both hydroponic and Cd-contaminated soil culture. We also performed a genome-wide association (GWA) mapping for Cd accumulation in different organs.A large genotypic variation in the Cd concentration was found in all organs. There was a good correlation between shoot Cd of solution and soil culture, the shoot Cd and grain Cd, but no correlation between the root Cd and grain Cd. GWA mapping detected 9 quantitative trait loci (QTL) for root Cd, 21 for shoot Cd, 14 for root-to-shoot translocation and 15 for grain Cd. A common QTL for the shoot Cd and root-to-shoot translocation was found at 132.6 cM on chromosome 5H. Two major QTL for grain Cd were identified on chromosome 2H and chromosome 5H.The genetic variation in Cd accumulation and major QTL detected provide useful information helpful for cloning candidate genes for Cd accumulation and breeding low-Cd barley cultivars in future.

DOI： 10.1111/nph.13512

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A node-localized transporter OsZIP3 is responsible for the preferential distribution of Zn to developing tissues in rice

Akimasa Sasaki, Naoki Yamaji, Namiki Mitani-Ueno, Miho Kashino, Jian Feng Ma

PLANT JOURNAL   84 ( 2 )   374 - 384   2015.10

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Developing tissues such as meristem with low transpiration require high Zn levels for their active growth, but the molecular mechanisms underlying the preferential distribution to these tissues are poorly understood. We found that a member of the ZIP (ZRT, IRT-like protein), OsZIP3, showed high expression in the nodes of rice (Oryza sativa). Immunostaining revealed that OsZIP3 was localized at the xylem intervening parenchyma cells and xylem transfer cells of the enlarged vascular bundle in both basal and upper nodes. Neither OsZIP3 gene expression nor encoded protein was affected by either deficiency or toxic levels of Zn. Knockdown of OsZIP3 resulted in significantly reduced Zn levels in the shoot basal region containing the shoot meristem and elongating zone, but increased Zn levels in the transpiration flow. A short-term experiment with the Zn-67 stable isotope showed that more Zn was distributed to the lower leaves, but less to the shoot elongating zone and nodes in the knockdown lines compared with the wild-type rice at both the vegetative and reproductive growth stages. Taken together, OsZIP3 located in the node is responsible for unloading Zn from the xylem of enlarged vascular bundles, which is the first step for preferential distribution of Zn to the developing tissues in rice.Significance Statement Zinc homeostasis is achieved by regulating diverse zinc transporters. Here we show that the zinc transporter OsZIP3 mediates the first step leading to preferential distribution of zinc in developing tissues, by unloading zinc from the xylem of enlarged vascular bundles.

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Effect of in planta phosphorus on aluminum-induced inhibition of root elongation in wheat

Ji Feng Shao, Jing Che, Rong Fu Chen, Jian Feng Ma, Ren Fang Shen

PLANT AND SOIL   395 ( 1-2 )   307 - 315   2015.10

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：SPRINGER  

Both aluminum (Al) toxicity and phosphorus (P) deficiency are limiting factors of crop production on acid soils. Although Al-P interaction has been extensively studied, the results are controversial. The aim of this study is to investigate the effect of in planta P on Al-induced inhibition of root elongation in wheat (Triticum aestivum L.).Roots of wheat (cv. Atlas 66) with different internal P concentrations were prepared by two methods; split-root and re-rooting in a hydroponic solution using three different P levels (0, 25 and 250 mu M) to avoid direct precipitation of Al-P in the solution. Al toxicity was evaluated by root elongation inhibition and callose induction. The Al and P concentrations in the root tips were also compared among different treatments.Both split-root and re-rooting methods generated roots with different P concentrations in the tips when exposed to different P levels. Lower P in the root tips resulted in less Al-induced inhibition of the root elongation, less callose content and less Al accumulation, while higher root P caused a higher Al-induced inhibition of the root elongation, increased callose content and Al accumulation in the root tips. Furthermore, Al in the root cell sap was not altered by different P concentrations, but Al in the root cell wall was increased with increasing in planta P concentrations.Al toxicity in wheat is associated with P in the root cell wall; lower root P enhanced Al tolerance, while higher root P aggravated Al toxicity in wheat.

DOI： 10.1007/s11104-015-2566-6

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Orchestration of three transporters and distinct vascular structures in node for intervascular transfer of silicon in rice

Naoki Yamaji, Gen Sakurai, Namiki Mitani-Ueno, Jian Feng Ma

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   112 ( 36 )   11401 - 11406   2015.9

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATL ACAD SCIENCES  

Requirement of mineral elements in different plant tissues is not often consistent with their transpiration rate; therefore, plants have developed systems for preferential distribution of mineral elements to the developing tissues with low transpiration. Here we took silicon (Si) as an example and revealed an efficient system for preferential distribution of Si in the node of rice (Oryza sativa). Rice is able to accumulate more than 10% Si of the dry weight in the husk, which is required for protecting the grains from water loss and pathogen infection. However, it has been unknown for a long time how this hyperaccumulation is achieved. We found that three transporters (Lsi2, Lsi3, and Lsi6) located at the node are involved in the intervascular transfer, which is required for the preferential distribution of Si. Lsi2 was polarly localized to the bundle sheath cell layer around the enlarged vascular bundles, which is next to the xylem transfer cell layer where Lsi6 is localized. Lsi3 was located in the parenchyma tissues between enlarged vascular bundles and diffuse vascular bundles. Similar to Lsi6, knockout of Lsi2 and Lsi3 also resulted in decreased distribution of Si to the panicles but increased Si to the flag leaf. Furthermore, we constructed a mathematical model for Si distribution and revealed that in addition to cooperation of three transporters, an apoplastic barrier localized at the bundle sheath cells and development of the enlarged vascular bundles in node are also required for the hyperaccumulation of Si in rice husk.

DOI： 10.1073/pnas.1508987112

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Improving Nitrogen Use Efficiency in Rice through Enhancing Root Nitrate Uptake Mediated by a Nitrate Transporter, NRT1.1B

Zhi Chang Chen, Jian Feng Ma

JOURNAL OF GENETICS AND GENOMICS   42 ( 9 )   463 - 465   2015.9

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DOI： 10.1016/j.jgg.2015.08.003

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The role of nodes in arsenic storage and distribution in rice

Yi Chen, Katie L. Moore, Anthony J. Miller, Steve P. McGrath, Jian Feng Ma, Fang-Jie Zhao

JOURNAL OF EXPERIMENTAL BOTANY   66 ( 13 )   3717 - 3724   2015.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Knowledge of arsenic (As) accumulation in rice (Oryza sativa L.) is important for minimizing As transfer to the food chain. The aim of this study was to investigate the role of rice nodes in As storage and distribution. Synchrotron mu X-ray fluorescence (mu-XRF) was used to map As distribution in the top node and internode of a lsi2 mutant defective in silicon/arsenite efflux carrier and its wild-type (WT) grown in soil. Lsi2 expression in different tissues during grain filling was investigated by quantitative RT-PCR. Arsenite or dimethylarsinic acid (DMA) was supplied to excised panicles to investigate the roles of Lsi2 and phytochelatins (PC) in As distribution. mu-XRF mapping revealed As storage in the phloem of different vascular bundles in the top node and internode. Soil-grown plants of lsi2 had markedly decreased As accumulation in the phloem compared with the WT. Lsi2 was strongly expressed, not only in the roots but also in the nodes. When excised panicles were exposed to As(III), the lsi2 mutant distributed more As to the node and flag leaf but less As to the grain compared with the WT, while there was no significant difference in DMA distribution. Inhibition of PC synthesis by L-buthionine-sulphoximine decreased As(III) deposition in the top node but increased As accumulation in the grain and flag leaf. The results suggest that rice nodes serve as a filter restricting As(III) distribution to the grain. Furthermore, Lsi2 plays a role in As(III) distribution in rice nodes and phytochelatins are important compounds for As(III) storage in the nodes.

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Altered cell wall properties are responsible for ammonium-reduced aluminium accumulation in rice roots

Wei Wang, Xue Qiang Zhao, Rong Fu Chen, Xiao Ying Dong, Ping Lan, Jian Feng Ma, Ren Fang Shen

PLANT CELL AND ENVIRONMENT   38 ( 7 )   1382 - 1390   2015.7

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The phytotoxicity of aluminium (Al) ions can be alleviated by ammonium (NH4+) in rice and this effect has been attributed to the decreased Al accumulation in the roots. Here, the effects of different nitrogen forms on cell wall properties were compared in two rice cultivars differing in Al tolerance. An in vitroAl-binding assay revealed that neither NH4+ nor NO3- altered the Al-binding capacity of cell walls, which were extracted from plants not previously exposed to N sources. However, cell walls extracted from NH4+-supplied roots displayed lower Al-binding capacity than those from NO3--supplied roots when grown in non-buffered solutions. Fourier-transform infrared microspectroscopy analysis revealed that, compared with NO3--supplied roots, NH4+-supplied roots possessed fewer Al-binding groups (-OH and COO-) and lower contents of pectin and hemicellulose. However, when grown in pH-buffered solutions, these differences in the cell wall properties were not observed. Further analysis showed that the Al-binding capacity and properties of cell walls were also altered by pHs alone. Taken together, our results indicate that the NH4+-reduced Al accumulation was attributed to the altered cell wall properties triggered by pH decrease due to NH4+ uptake rather than direct competition for the cell wall binding sites between Al3+ and NH4+.Ammonium (NH4+) is known to alleviate Al toxicity by reducing Al accumulation in rice roots, but the responsible mechanisms are poorly understood. In this study, we found that the NH4+-reduced accumulation of Al was associated with decreased Al-binding groups (-OH and COO-) and contents of pectin and hemicellulose in both Al-tolerant and Al-sensitive rice cultivars. Furthermore, these alterations of cell wall properties were caused by pH decrease due to uptake of NH4+.

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A cooperative system of silicon transport in plants

Jian Feng Ma, Naoki Yamaji

TRENDS IN PLANT SCIENCE   20 ( 7 )   435 - 442   2015.7

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The high accumulation of silicon (Si) protects plants from biotic and abiotic stresses. Two different types of Si transporter [Low Silicon 1 (Lsi1) and 2 (Lsi2)] involved in the uptake and distribution of Si have been identified. Lsi1, a Si permeable channel, belongs to the Nod26-like major intrinsic protein (NIP) III subgroup of the aquaporin membrane protein family with a distinct selectivity, whereas Lsi2, an efflux Si transporter, belongs to an uncharacterized anion transporter family. These transporters are localized to the plasma membrane, but, in different plant species, show different expression patterns and tissue or cellular localizations that are associated with different levels of Si accumulation. A recent mathematical modeling study revealed that cooperation of Lsi1 and Lsi2, which show a polarized localization, is required for the efficient transport of Si in rice.

DOI： 10.1016/j.tplants.2015.04.007

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In Silico Simulation Modeling Reveals the Importance of the Casparian Strip for Efficient Silicon Uptake in Rice Roots

Gen Sakurai, Akiko Satake, Naoki Yamaji, Namiki Mitani-Ueno, Masayuki Yokozawa, Francois Gabriel Feugier, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   56 ( 4 )   631 - 639   2015.4

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Silicon (Si) uptake by the roots is mediated by two different transporters, Lsi1 (passive) and Lsi2 (active), in rice (Oryza sativa). Both transporters are polarly localized in the plasma membranes of exodermal (outer) and endodermal (inner) cells with Casparian strips. However, it is unknown how rice is able to take up large amounts of Si compared with other plants, and why rice Si transporters have a characteristic cellular localization pattern. To answer these questions, we simulated Si uptake by rice roots by developing a mathematical model based on a simple diffusion equation that also accounts for active transport by Lsi2. In this model, we calibrated the model parameters using in vivo experimental data on the Si concentrations in the xylem sap and a Monte Carlo method. In our simulation experiments, we compared the Si uptake between roots with various transporter and Casparian strip locations and estimated the Si transport efficiency of roots with different localization patterns and quantities of the Lsi transporters. We found that the Si uptake by roots that lacked Casparian strips was lower than that of normal roots. This suggests that the doublelayer structure of the Casparian strips is an important factor in the high Si uptake by rice. We also found that among various possible localization patterns, the most efficient one was that of the wild-type rice; this may explain the high Si uptake capacity of rice.

DOI： 10.1093/pcp/pcv017

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The Rice CK2 Kinase Regulates Trafficking of Phosphate Transporters in Response to Phosphate Levels

Jieyu Chen, Yifeng Wang, Fei Wang, Jian Yang, Mingxing Gao, Changying Li, Yingyao Liu, Yu Liu, Naoki Yamaji, Jian Feng Ma, Javier Paz-Ares, Laurent Nussaume, Shuqun Zhang, Keke Yi, Zhongchang Wu, Ping Wu

PLANT CELL   27 ( 3 )   711 - 723   2015.3

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Phosphate transporters (PTs) mediate phosphorus uptake and are regulated at the transcriptional and posttranslational levels. In one key mechanism of posttranslational regulation, phosphorylation of PTs affects their trafficking from the endoplasmic reticulum (ER) to the plasma membrane. However, the kinase(s) mediating PT phosphorylation and the mechanism leading to ER retention of phosphorylated PTs remain unclear. In this study, we identified a rice (Oryza sativa) kinase subunit, CK2 beta 3, which interacts with PT2 and PT8 in a yeast two-hybrid screen. Also, the CK2 alpha 3/beta 3 holoenzyme phosphorylates PT8 under phosphate-sufficient conditions. This phosphorylation inhibited the interaction of PT8 with PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1, a key cofactor regulating the exit of PTs from the ER to the plasma membrane. Additionally, phosphorus starvation promoted CK2 beta 3 degradation, relieving the negative regulation of PT phosphorus-insufficient conditions. In accordance, transgenic expression of a nonphosphorylatable version of OsPT8 resulted in elevated levels of that protein at the plasma membrane and enhanced phosphorus accumulation and plant growth under various phosphorus regimes. Taken together, these results indicate that CK2 alpha 3/beta 3 negatively regulates PTs and phosphorus status regulates CK2 alpha 3/beta 3.

DOI： 10.1105/tpc.114.135335

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Exploring the power of plants to overcome environmental stresses

Motoyuki Ashikari, Jian Feng Ma

RICE   8 ( 1 )   10   2015.2

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DOI： 10.1186/s12284-014-0037-y

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A small RNA mediated regulation of a stress-activated retrotransposon and the tissue specific transposition during the reproductive period in Arabidopsis

Wataru Matsunaga, Naohiko Ohama, Noriaki Tanabe, Yukari Masuta, Seiji Masuda, Namiki Mitani, Kazuko Yamaguchi-Shinozaki, Jian F. Ma, Atsushi Kato, Hidetaka Ito

FRONTIERS IN PLANT SCIENCE   6 ( FEB )   48   2015.2

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Transposable elements (TEs) are key elements that facilitate genome evolution of the host organism. A number of studies have assessed the functions of TEs, which change gene expression in the host genome. Activation of TEs is controlled by epigenetic modifications such as DNA methylation and histone modifications. Several recent studies have reported that TEs can also be activated by biotic or abiotic stress in some plants. We focused on a Ty1/copia retrotransposon, ONSEN, that is activated by heat stress (HS) in Arabidopsis. We found that transcriptional activation of ONSEN was regulated by a small interfering RNA (siRNA)-related pathway, and the activation could also be induced by oxidative stress. Mutants deficient in siRNA biogenesis that were exposed to HS at the initial stages of vegetative growth showed transgenerational transposition. The transposition was also detected in the progeny, which originated from tissue that had differentiated after exposure to the HS. The results indicated that in some undifferentiated cells, transpositional activity could be maintained quite long after exposure to the HS.

DOI： 10.3389/fpls.2015.00048

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Foreword

Jian Feng Ma

Silicon and Plant Diseases   v - vi   2015.1

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DOI： 10.1007/978-3-319-22930-0

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Physiological characterization of aluminum tolerance and accumulation in tartary and wild buckwheat

Hua Wang, Rong Fu Chen, Takashi Iwashita, Ren Fang Shen, Jian Feng Ma

NEW PHYTOLOGIST   205 ( 1 )   273 - 279   2015.1

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：WILEY-BLACKWELL  

Ionic aluminum (Al) is toxic for plant growth, but some plant species are able to accumulate Al at high concentrations without showing toxicity symptoms. In order to determine whether other species in the genus Fagopyrum are able to accumulate Al like common buckwheat (Fagopyrum esculentum), we investigated the external and internal detoxification mechanisms of Al in two self-compatible species: tartary (Fagopyrum tataricum) and wild buckwheat (Fagopyrum homotropicum). Both tartary and wild buckwheat showed high Al tolerance comparable to common buckwheat. Furthermore, these two species also secreted oxalate rapidly from the roots in response to Al in a time-dependent manner. Both tartary and wild buckwheat accumulated >1mgg(-1) Al in the leaves after short-term exposure to Al. Analysis with Al-27-nuclear magnetic resonance (NMR) revealed that Al was present in the form of Al-oxalate (1:3 ratio) in the roots and leaves, but in the form of Al-citrate (1:1 ratio) in the xylem sap in both species. These results indicate that similar to common buckwheat, both tartary and wild buckwheat detoxify Al externally and internally, respectively, by secreting oxalate from the roots and by forming the Al-oxalate complex, which is a nonphytotoxic form. These features of Al response and accumulation may be conserved in genus Fagopyrum.

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AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis

Takaaki Miyaji, Takashi Kuromori, Yu Takeuchi, Naoki Yamaji, Kengo Yokosho, Atsushi Shimazawa, Eriko Sugimoto, Hiroshi Omote, Jian Feng Ma, Kazuo Shinozaki, Yoshinori Moriyama

NATURE COMMUNICATIONS   6   5928   2015.1

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Ascorbate is an antioxidant and coenzyme for various metabolic reactions in vivo. In plant chloroplasts, high ascorbate levels are required to overcome photoinhibition caused by strong light. However, ascorbate is synthesized in the mitochondria and the molecular mechanisms underlying ascorbate transport into chloroplasts are unknown. Here we show that AtPHT4;4, a member of the phosphate transporter 4 family of Arabidopsis thaliana, functions as an ascorbate transporter. In vitro analysis shows that proteoliposomes containing the purified AtPHT4; 4 protein exhibit membrane potential- and Cl- dependent ascorbate uptake. The AtPHT4; 4 protein is abundantly expressed in the chloroplast envelope membrane. Knockout of AtPHT4; 4 results in decreased levels of the reduced form of ascorbate in the leaves and the heat dissipation process of excessive energy during photosynthesis is compromised. Taken together, these observations indicate that the AtPHT4; 4 protein is an ascorbate transporter at the chloroplast envelope membrane, which may be required for tolerance to strong light stress.

DOI： 10.1038/ncomms6928

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Integrated research for crop improvement based on the molecular physiological strategies to global environmental changes

Saisho Daisuke, Horie Tomoaki, Kinoshita Toshinori, Feng Ma Jian

Breeding Research   17 ( 2 )   71 - 76   2015

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Language：Japanese   Publisher：Japanese Society of Breeding  

DOI： 10.1270/jsbbr.17.71

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Other Link： https://jlc.jst.go.jp/DN/JLC/20012694585?from=CiNii

Transcriptional activity and silencing of heat activated retrotransposon in Arabidopsis

Wataru Matsunaga, Yukari Masuta, Namiki Mitani, Ma Jian Feng, Atsushi Kato, Hidetaka Ito

GENES & GENETIC SYSTEMS   89 ( 6 )   316 - 316   2014.12

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Global Transcriptome Analysis of Al-Induced Genes in an Al-Accumulating Species, Common Buckwheat (Fagopyrum esculentum Moench)

Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   55 ( 12 )   2077 - 2091   2014.12

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Buckwheat (Fagopyrum esculentum Moench) is a species with high aluminum (Al) tolerance and accumulation. Although the physiological mechanisms for external and internal detoxification of Al have been well studied, the molecular mechanisms responsible are poorly understood. Here, we conducted a genome-wide transcriptome analysis of Al-responsive genes in the roots and leaves using RNA sequencing (RNA-Seq) technology. RNA-Seq generated reads ranging from 56 x 10(6) to 93 x 10(6). A total of 148,734 transcript contigs with an average length of 1,014 bp were assembled, generating 84,516 unigenes. Among them, 31,730 and 23,853 unigenes were annotated, respectively, in the NCBI plant database and TAIR database for Arabidopsis. Of the annotated genes, 4,067 genes in the roots and 2,663 genes in the leaves were up-regulated (>2-fold) by Al exposure, while 2,456 genes in the roots and 2,426 genes in the leaves were down-regulated (<2-fold) A few STOP1/ART1 (SENSITIVE TO PROTON RHIZOTOXICITY1/AL RESISTANCE TRANSCRIPTION FACTOR1)-regulated gene homologs including FeSTAR1, FeALS3 (ALUMINUM SENSITIVE3), FeALS1 (ALUMINUM SENSITIVE1), FeMATE1 and FeMATE2 (MULTIDRUG AND TOXIC COMPOUND EXTRUSION1 and 2) were also up-regulated in buckwheat, indicating some common Al tolerance mechanism across the species, although most STOP1/ART1-regulated gene homologs were not changed. Most genes involved in citric and oxalic acid biosynthesis were not significantly altered. Some transporter genes were highly expressed in the roots and leaves and responded to Al stress, implicating their role in Al tolerance and accumulation. Overall, our data provide a platform for further characterizing the functions of genes involved in Al tolerance and accumulation in buckwheat.

DOI： 10.1093/pcp/pcu135

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A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain

Won-Yong Song, Tomohiro Yamaki, Naoki Yamaji, Donghwi Ko, Ki-Hong Jung, Miho Fujii-Kashino, Gynheung An, Enrico Martinoia, Youngsook Lee, Jian Feng Ma

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   111 ( 44 )   15699 - 15704   2014.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATL ACAD SCIENCES  

Arsenic (As) is a chronic poison that causes severe skin lesions and cancer. Rice (Oryza sativa L.) is a major dietary source of As; therefore, reducing As accumulation in the rice grain and thereby diminishing the amount of As that enters the food chain is of critical importance. Here, we report that a member of the Oryza sativa C-type ATP-binding cassette (ABC) transporter (OsABCC) family, OsABCC1, is involved in the detoxification and reduction of As in rice grains. We found that OsABCC1 was expressed in many organs, including the roots, leaves, nodes, peduncle, and rachis. Expression was not affected when plants were exposed to low levels of As but was up-regulated in response to high levels of As. In both the basal nodes and upper nodes, which are connected to the panicle, OsABCC1 was localized to the phloem region of vascular bundles. Furthermore, OsABCC1 was localized to the tonoplast and conferred phytochelatin-dependent As resistance in yeast. Knockout of OsABCC1 in rice resulted in decreased tolerance to As, but did not affect cadmium toxicity. At the reproductive growth stage, the As content was higher in the nodes and in other tissues of wild-type rice than in those of OsABCC1 knockout mutants, but was significantly lower in the grain. Taken together, our results indicate that OsABCC1 limits As transport to the grains by sequestering As in the vacuoles of the phloem companion cells of the nodes in rice.

DOI： 10.1073/pnas.1414968111

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Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice

Akimasa Sasaki, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   65 ( 20 )   6013 - 6021   2014.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

As a member of the heavy metal ATPase (HMA) family, OsHMA3 is a tonoplast-localized transporter for Cd in the roots of rice (Oryza sativa). Overexpression of OsHMA3 selectively reduces Cd accumulation in the grain. Further characterization in the present study revealed that overexpression of OsHMA3 also enhances the tolerance to toxic Cd. The growth of both the roots and shoots was similar in the absence of Cd between an OsHMA3-overexpressed line and vector control, but the Cd-inhibited growth was significantly alleviated in the OsHMA3-overexpressed line. The over-expressed line showed higher Cd concentration in the roots, but lower Cd concentration in the shoots compared with the wild-type rice and vector control line, indicating that overexpression of OsHMA3 enhanced vacuolar sequestration of Cd in the roots. The Zn concentration in the roots of the OsHMA3-overexpressed line was constantly higher than that of vector control, but the Zn concentration in the shoots was similar between the overexpressed line and vector control. Five transporter genes belonging to the ZIP family were constitutively up-regulated in the OsHMA3-overexpressed line. These results suggest that shoot Zn level was maintained by up-regulating these genes involved in the Zn uptake/translocation. Taken together, overexpression of OsHMA3 is an efficient way to reduce Cd accumulation in the grain and to enhance Cd tolerance in rice.

DOI： 10.1093/jxb/eru340

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The node, a hub for mineral nutrient distribution in graminaceous plants

Naoki Yamaji, Jian Feng Ma

TRENDS IN PLANT SCIENCE   19 ( 9 )   556 - 563   2014.9

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Language：English   Publisher：ELSEVIER SCIENCE LONDON  

Mineral elements, including both essential and toxic elements, are delivered to different tissues after they are taken up from the roots, but the mechanism (or mechanisms) underlying the distribution remains poorly understood. In graminaceous plants, this distribution occurs in nodes, which have a complex, well-organized vascular system. A transfer of mineral elements between different vascular bundles is required, especially for preferential distribution to developing tissues that have low transpiration but high nutrient requirements. This intervascular transfer is mediated by various transporters localized at different cells in the node. In this opinion article, we propose four modes of distribution for different mineral elements: xylem-switch, phloem-tropic, phloem-kickback, and minimum-shift, based on specific molecular transport processes identified in the nodes mainly of rice (Oryza sativa). We also discuss the prospects for future studies on mineral nutrient distribution in the nodes.

DOI： 10.1016/j.tplants.2014.05.007

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Molecular mechanisms of Al tolerance in gramineous plants

Jian Feng Ma, Zhi Chang Chen, Ren Fang Shen

PLANT AND SOIL   381 ( 1-2 )   1 - 12   2014.8

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Aluminum (Al) toxicity has limited the productivity and expansion of cereal crops on acid soils; however, a number of plant species or cultivars have developed different strategies for detoxifying aluminum both internally and externally.This review focuses on recent progress on molecular mechanisms of Al tolerance in gramineous plants.A common mechanism in all gramineous plants is the secretion of organic acid anions (citrate and malate) from the roots. Genes belonging to ALMT (for Aluminum-activated malate transporter) and MATE (Multidrug and toxic compound extrusion) family involved in the secretion have been identified in several plant species; however, different plant species show different gene expression patterns including Al-induction, spatial and temporal expression, and tissue localization. Furthermore, the mechanisms regulating the gene expression also differ with plant species, which are achieved by increased tandem repeated element, increase of copy number, insertion of transposon, or alteration of cis-acting element. In addition to these common Al exclusion mechanisms, rice as a highly Al-tolerant species has developed a number of other mechanisms for detoxification of Al. A transcription factor for Al tolerance ART1 identified in rice regulates at least 30 genes implicated in internal and external detoxification of Al. These multiple genes may contribute to the high Al tolerance of rice. In the future, regulation mechanisms of Al-tolerance genes need to be further investigated.

DOI： 10.1007/s11104-014-2073-1

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Differential expression of Nrat1 is responsible for Al-tolerance QTL on chromosome 2 in rice

Jixing Xia, Naoki Yamaji, Jing Che, Ren Fang Shen, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   65 ( 15 )   4297 - 4304   2014.8

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Although rice (Oryza sativa) is the most Al-tolerant species among small-grain cereal crops, there is wide genotypic variation in its tolerance to Al toxicity. A number of quantitative trait loci (QTLs) for Al tolerance have been detected, but the responsible genes have not been identified. By using chromosome segment substitution lines, this work found that Nrat1, a gene encoding an Al transporter, is responsible for a QTL previously detected on chromosome 2. Substitution of the chromosome segment containing Nrat1 from Koshihikari (Al-tolerant variety) by that from Kasalath (Al-sensitive variety) decreased Nrat1 expression and Al uptake and tolerance, but increased binding of Al to the cell wall. Nrat1 in Kasalath showed tissue localization similar to Koshihikari in the roots. Although Koshihikari and Kasalath differed in four amino acids in Nrat1 protein, Nrat1 from Kasalath also showed transport activity for Al. Analysis with site-directed mutagenesis revealed that these differences did not affect the Al-transport activity much. Furthermore, there was no correlation between Al tolerance and the open-reading-frame sequence differences in other rice varieties. On the other hand, there was good correlation between Nrat1 expression and Al tolerance; however, sequence comparison of the promoter region up to 2.1 kb did not give a clear difference between the Al-tolerant and -sensitive varieties. Taken together, these results indicate that differential expression of Nrat1 is responsible for the QTL for Al tolerance on chromosome 2, although the mechanism controlling Nrat1 expression remains to be examined.

DOI： 10.1093/jxb/eru201

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Physiological and molecular characterization of Si uptake in wild rice species

Namiki Mitani-Ueno, Hisao Ogai, Naoki Yamaji, Jian Feng Ma

PHYSIOLOGIA PLANTARUM   151 ( 3 )   200 - 207   2014.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：WILEY-BLACKWELL  

Cultivated rice (Oryza sativa) accumulates high concentration of silicon (Si), which is required for its high and sustainable production. High Si accumulation in cultivated rice is achieved by a high expression of both influx (Lsi1) and efflux (Lsi2) Si transporters in roots. Herein, we physiologically investigated Si uptake, isolated and functionally characterized Si transporters in six wild rice species with different genome types. Si uptake by the roots was lower in Oryza rufipogon, Oryza barthii (AA genome), Oryza australiensis (EE genome) and Oryza punctata (BB genome), but similar in Oryza glumaepatula and Oryza meridionalis (AA genome) compared with the cultivated rice (cv. Nipponbare). However, all wild rice species and the cultivated rice showed similar concentration of Si in the shoots when grown in a field. All species with AA genome showed the same amino acid sequence of both Lsi1 and Lsi2 as O. sativa, whereas species with EE and BB genome showed several nucleotide differences in both Lsi1 and Lsi2. However, proteins encoded by these genes also showed transport activity for Si in Xenopus oocyte. The mRNA expression of Lsi1 in all wild rice species was lower than that in the cultivated rice, whereas the expression of Lsi2 was lower in O. rufipogon and O. barthii but similar in other species. Similar cellular localization of Lsi1 and Lsi2 was observed in all wild rice as the cultivated rice. These results indicate that superior Si uptake, the important trait for rice growth, is basically conserved in wild and cultivated rice species.

DOI： 10.1111/ppl.12125

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Knockdown of neuropilin-1 suppresses invasion, angiogenesis, and increases the chemosensitivity to doxorubicin in osteosarcoma cells - an in vitro study

B. Yue, J. -F. Ma, G. Yao, M. -D. Yang, H. Cheng, G. -Y. Liu

EUROPEAN REVIEW FOR MEDICAL AND PHARMACOLOGICAL SCIENCES   18 ( 12 )   1735 - 1741   2014.6

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：VERDUCI PUBLISHER  

OBJECTIVES: Neuropilin-1 (NRP-1) is a novel co-receptor for vascular endothelial growth factor (VEGF). NRP-1 expression in osteosarcoma tissues was significantly higher, and high NRP-1 expression was more frequently occurred in osteosarcoma tissues with advanced clinical stage, positive distant metastasis and poor response to chemotherapy. We tested a hypothesis that the NRP-1 gene plays a role in the invasiveness, angiogenesis and chemoresistance of human OS.MATERIALS AND METHODS: To determine the role of NRP-1 in OS, NRP-1 was stably transfected into the human OS cell line MG-63 to increase the NPR-1 level, and NRP-1 siRNA was stably transfected into the human OS cell line SaOS-2 to knockdown of NRP-1. The effect of NRP-1 on invasion and angiogenesis was assessed by Matrigel invasion assay and in vitro angiogenesis assay. Chemosensitivity to doxorubicin was assessed by MTT assay in the MG-63 and SaOS-2 cells following NRP-1 overexpression or siRNA-induced downregulation of NRP-1.RESULTS: The NRP-1 transfected MG-63 cells showed a markedly higher level of invasion in Matrigel invasion assay. The capillary-like structure formation of endothelial cells was also increased by coculture with the NRP-1 transfected MG-63 cells. On the contrary, the NRP-1 siRNA transfected SaOS-2 cells showed a markedly lower level of invasion in Matrigel invasion assay. The capillary-like structure formation of endothelial cells was also repressed by coculture with the NRP-1 siRNA transfected SaOS-2 cells. NRP-1 overexpression in MG-63 cells increased survival of cells after exposure to doxorubicin. In contrast, downregulation of NRP-1 expression in SaOS-2 cells markedly increased chemosensitivity after exposure to doxorubicin.CONCLUSIONS: We suggest that NRP-1 could be used as a biomarker for OS progression and a novel therapeutic or chemopreventive target for human OS treatment.

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Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation

Matthew J. Milner, Namiki Mitani-Ueno, Naoki Yamaji, Kengo Yokosho, Eric Craft, Zhangjun Fei, Stephen Ebbs, M. Clemencia Zambrano, Jian Feng Ma, Leon V. Kochian

PLANT JOURNAL   78 ( 3 )   398 - 410   2014.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：WILEY  

The Zn/Cd hyperaccumulator, Noccaea caerulescens, has been studied extensively for its ability to accumulate high levels of Zn and Cd in its leaves. Previous studies have indicated that the Zn and Cd hyperaccumulation trait exhibited by this species involves different transport and tolerance mechanisms. It has also been well documented that certain ecotypes of N.caerulescens are much better Cd hyperaccumulators than others. However, there does not seem to be much ecotypic variation for Zn hyperaccumulation in N.caerulescens. In this study we employed a comparative transcriptomics approach to look at root and shoot gene expression in Ganges and Prayon plants in response to Cd stress to identify transporter genes that were more highly expressed in either the roots or shoots of the superior Cd accumulator, Ganges. Comparison of the transcriptomes from the two ecotypes of Noccaea caerulescens identified a number of genes that encoded metal transporters that were more highly expressed in the Ganges ecotype in response to Cd stress. Characterization of one of these transporters, NcNramp1, showed that it is involved in the influx of Cd across the endodermal plasma membrane and thus may play a key role in Cd flux into the stele and root-to-shoot Cd transport. NcNramp1 may be one of the main transporters involved in Cd hyperaccumulation in N.caerulescens and copy number variation appears to be the main reason for high NcNramp1 gene expression underlying the increased Cd accumulation in the Ganges ecotype.

DOI： 10.1111/tpj.12480

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Normal root elongation requires arginine produced by argininosuccinate lyase in rice

Jixing Xia, Naoki Yamaji, Jing Che, Ren Fang Shen, Jian Feng Ma

PLANT JOURNAL   78 ( 2 )   215 - 226   2014.4

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：WILEY  

Plant roots play an important role in the uptake of water and nutrients, structural support and environmental sensing, but the molecular mechanisms involved in root development are poorly understood in rice (Oryza sativa), which is characterized by a dense fibrous root system. Here we report a rice mutant (red1 for root elongation defect 1) with short roots. Morphological and physiological analyses showed that the mutant had a shorter length from the quiescent center (QC) to the starting point of the elongation zone but a similar cell size and number of lateral and crown roots compared with the wild type. Furthermore, the mutant had similar radial structure and nutrient uptake patterns to the wild type. Map-based cloning revealed that the mutant phenotype was caused by a point mutation of a gene encoding an argininosuccinate lyase (ASL), catalyzing the last step of arginine biosynthesis. The OsASL1 gene has two distinct transcripts, OsASL1.1 and OsASL1.2, which result from different transcription start sites, but only OsASL1.1 was able to complement the mutant phenotype. OsASL1.1 was expressed in both the roots and shoots. The protein encoded by OsASL1.1 showed ASL activity in yeast. OsALS1.1 was localized to the plastid. The short root of the mutant was rescued by exogenous addition of arginine, but not by other amino acids. These results indicate that arginine produced by ASL is required for normal root elongation in rice.

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Rice grain resistance to brown spot and yield are increased by silicon

Leandro J. Dallagnol, Fabricio A. Rodrigues, Mateus V. B. Mielli, Jian F. Ma

TROPICAL PLANT PATHOLOGY   39 ( 1 )   56 - 63   2014.1

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：SOC BRASILEIRA FITOPATHOLOGIA  

Brown spot, caused by Bipolaris oryzae, is one of the most important diseases of rice and can cause a reduction in yield and grain quality. The effect of silicon (Si) on the resistance of rice grains to brown spot was investigated. Plants from cv. Oochikara and its mutant, defective in the Lsi1 transporter (lsi1 mutant), were grown in hydroponic culture either with Si (+ Si; 2 mM) or without Si (-Si). Panicle inoculation with B. oryzae was carried out at the beginning of the milk-grain stage. Panicles were harvested at physiological grain maturity. The supply of Si significantly increased Si concentration in husks compared to -Si plants. Si concentration in husks from cv. Oochikara was up to three times greater than the lsi1 mutant. In the presence of Si, brown spot severity was reduced by 88% in grains from cv. Oochikara and by 53% in grains from lsi1 mutant. Brown spot severity was 77% lower for grains of cv. Oochikara than for the lsi1 mutant, both plant types were grown in the presence of Si. Panicle inoculation reduced significantly the following yield components: number of grains per panicle, the weight of 1000 grains and the percentage of filled grains. Si significantly increased these yield components, especially for inoculated panicles. Considering kernel quality, the panicle inoculation with B. oryzae significantly reduced the yield of husked kernel, yield of whole kernel and kernel diameter, especially for grains from -Si plants. For panicles from + Si plants, the kernel quality was improved under inoculation, compared to -Si plants. Results from this study show that Si improved rice yield and kernel quality in panicles inoculated with B. oryzae. Furthermore the functional Lsi1 gene contributed significantly for increasing the yield of whole kernel and kernel diameter, possibly due to the increasing Si concentration in husks.

DOI： 10.1590/S1982-56762014005000003

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An appropriate concentration of arginine is required for normal root growth in rice

Jixing Xia, Naoki Yamaji, Jian Feng Ma

Plant Signaling and Behavior   9 ( APR )   e28717   2014

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Landes Bioscience  

Plant roots play an important role in uptake of water and nutrients, support of above-ground part and environmental sensing, but the molecular mechanisms underlying the root development are poorly understood in rice. We found that a gene (OsASL1) encoding argininosuccinate lyase is involved in normal root development of rice. OsASL1 cleaves argininosuccinate to arginine and fumarate reversibly, the last step in the arginine biosynthetic pathway. Here, we further characterized OsASL1 in terms of expression pattern, subcellular localization, and arginine effect on the root growth. A detailed expression analysis revealed that 2 transcripts of OsASL1, OsASL1.1 and OsASL1.2, showed different expression patterns
OsASL1.1 was expressed in most organs throughout the whole growth period, whereas OsASL1.2 was mainly expressed in the roots. In contrast to plastid-localized OsASL1.1, OsASL1.2 was localized to the cytosol and nucleus. The short-root phenotype of the mutant was not rescued by exogenous addition of the sodium nitroprusside, a nitric oxide donor, but rescued by an appropriate concentration of Arg. Our results indicate that the subcellular localization was determined by the N terminus of OsASL1 and that appropriate concentration of Arg is required for normal root elongation in rice. © 2014 Landes Bioscience.

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A Member of the Heavy Metal P-Type ATPase OsHMA5 Is Involved in Xylem Loading of Copper in Rice

Fenglin Deng, Naoki Yamaji, Jixing Xia, Jian Feng Ma

PLANT PHYSIOLOGY   163 ( 3 )   1353 - 1362   2013.11

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER SOC PLANT BIOLOGISTS  

Heavy metal-transporting P-type ATPase (HMA) has been implicated in the transport of heavy metals in plants. Here, we report the function and role of an uncharacterized member of HMA, OsHMA5 in rice (Oryza sativa). Knockout of OsHMA5 resulted in a decreased copper (Cu) concentration in the shoots but an increased Cu concentration in the roots at the vegetative stage. At the reproductive stage, the concentration of Cu in the brown rice was significantly lower in the mutants than in the wild-type rice; however, there was no difference in the concentrations of iron, manganese, and zinc between two independent mutants and the wild type. The Cu concentration of xylem sap was lower in the mutants than in the wild-type rice. OsHMA5 was mainly expressed in the roots at the vegetative stage but also in nodes, peduncle, rachis, and husk at the reproductive stage. The expression was up-regulated by excess Cu but not by the deficiency of Cu and other metals, including zinc, iron, and manganese, at the vegetative stage. Analysis of the transgenic rice carrying the OsHMA5 promoter fused with green fluorescent protein revealed that it was localized at the root pericycle cells and xylem region of diffuse vascular bundles in node I, vascular tissues of peduncle, rachis, and husk. Furthermore, immunostaining with an antibody against OsHMA5 revealed that it was localized to the plasma membrane. Expression of OsHMA5 in a Cu transport-defective mutant yeast (Saccharomyces cerevisiae) strain restored the growth. Taken together, OsHMA5 is involved in loading Cu to the xylem of the roots and other organs.

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Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family

Zonghui Chen, Yumi Fujii, Naoki Yamaji, Sakine Masuda, Yuma Takemoto, Takehiro Kamiya, Yusufujiang Yusuyin, Kozo Iwasaki, Shin-ichiro Kato, Masayoshi Maeshima, Jian Feng Ma, Daisei Ueno

JOURNAL OF EXPERIMENTAL BOTANY   64 ( 14 )   4375 - 4387   2013.11

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Manganese (Mn) is an essential micronutrient for plants, but is toxic when present in excess. The rice plant (Oryza sativa L.) accumulates high concentrations of Mn in the aerial parts; however, the molecular basis for Mn tolerance is poorly understood. In the present study, genes encoding Mn tolerance were screened for by expressing cDNAs of genes from rice shoots in Saccharomyces cerevisiae. A gene encoding a cation diffusion facilitator (CDF) family member, OsMTP8.1, was isolated, and its expression was found to enhance Mn accumulation and tolerance in S. cerevisiae. In plants, OsMTP8.1 and its transcript were mainly detected in shoots. High or low supply of Mn moderately induced an increase or decrease in the accumulation of OsMTP8.1, respectively. OsMTP8.1 was detected in all cells of leaf blades through immunohistochemistry. OsMTP8.1 fused to green fluorescent protein was localized to the tonoplast. Disruption of OsMTP8.1 resulted in decreased chlorophyll levels, growth inhibition in the presence of high concentrations of Mn, and decreased accumulation of Mn in shoots and roots. However, there was no difference in the accumulation of other metals, including Zn, Cu, Fe, Mg, Ca, and K. These results suggest that OsMTP8.1 is an Mn-specific transporter that sequesters Mn into vacuoles in rice and is required for Mn tolerance in shoots.

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LjMATE1: A Citrate Transporter Responsible for Iron Supply to the Nodule Infection Zone of Lotus japonicas (vol 54, pg 585, 2013)

Kojiro Takanashi, Kengo Yokosho, Kazuhiko Saeki, Akifumi Sugiyama, Shusei Sato, Satoshi Tabata, Jian Feng Ma, Kazufumi Yazaki

PLANT AND CELL PHYSIOLOGY   54 ( 10 )   1749 - 1749   2013.10

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DOI： 10.1093/pcp/pct118

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A plasma membrane-localized small peptide is involved in rice aluminum tolerance

Jixing Xia, Naoki Yamaji, Jian Feng Ma

PLANT JOURNAL   76 ( 2 )   345 - 355   2013.10

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A transcription factor for Al tolerance, ART1, regulates the expression of at least 30 genes in rice. Here we functionally characterized one of the downstream genes, OsCDT3, which encodes a predicted peptide of only 53 amino acid residues rich in cysteine. Knockdown of this gene resulted in decreased tolerance to Al, but did not affect the tolerance to Cd. The aluminum (Al) content in the root residues including cell wall and the plasma membrane of knockdown lines decreased, but the Al concentration in the root cell sap increased compared with those of the wild-type rice. OsCDT3 was mainly expressed in the roots and its expression was specifically induced by Al exposure, not by low pH and other metals. There was a small genotypic variation in OsCDT3 expression level, but no correlation between Al tolerance and the OsCDT3 variation was found among 17 rice cultivars. Analysis of pOsCDT3::GFP transgenic rice showed that OsCDT3 was expressed at all cells in the root tips. Transient expression of OsCDT3 fused with GFP at both N- and C-termini showed that OsCDT3 was anchored to the plasma membrane. Expression of OsCDT3 in yeast conferred tolerance to Al, but not to Cd. Furthermore, OsCDT3 did not show transport activity for Al in yeast, but was able to directly bind Al in vitro. Taken together, our results indicate that OsCDT3 anchoring to the plasma membrane may play a role in stopping entry of Al into the root cells by binding Al, therefore, contributing to high Al tolerance in rice.

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Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus

Zhi Chang Chen, Kengo Yokosho, Miho Kashino, Fang-Jie Zhao, Naoki Yamaji, Jian Feng Ma

PLANT JOURNAL   76 ( 1 )   10 - 23   2013.10

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Yorkshire fog (Holcus lanatus), which belongs to the Poaceae family and is a close relative of the agronomic crop oat (Avena sativa), is a widely adaptable grass species that is able to grow on highly acidic soils with high levels of Al, but the mechanism underlying the high Al tolerance is unknown. Here, we characterized two accessions of H.lanatus collected from an acid plot (soil pH 3.6, HL-A) and a neutral plot (pH 7.1, HL-N) in terms of Al tolerance, organic acid anion secretion and related gene expression. In response to Al (pH 4.5), the HL-A roots secreted approximately twice as much malate as the HL-N roots, but there was no difference in citrate secretion. Cloning of the gene HlALMT1 responsible for malate secretion showed that the encoded amino acid sequence did not differ between two accessions, but the expression level in the outer cell layers of the HL-A roots was twice as high as in the HL-N roots. This difference was not due to the genomic copy number, but was due to the number of cis-acting elements for an Al-responsive transcription factor (HlART1) in the promoter region of HlALMT1, as demonstrated by both a yeast one-hybrid assay and a transient assay in tobacco protoplasts. Furthermore, introduction of HlALMT1 driven by the HL-A promoter into rice resulted in significantly more Al-induced malate secretion than introduction of HlALMT1 driven by the HL-N promoter. These findings indicate that the adaptation of H.lanatus to acidic soils may be achieved by increasing number of cis-acting elements for ART1 in the promoter region of the HlALMT1 gene, enhancing the expression of HlALMT1 and the secretion of malate.

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A node-based switch for preferential distribution of manganese in rice

Naoki Yamaji, Akimasa Sasaki, Ji Xing Xia, Kengo Yokosho, Jian Feng Ma

NATURE COMMUNICATIONS   4   2442   2013.9

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Mineral nutrients, such as manganese, are required for the development of plants and their reproductive organs, but these can be toxic if accumulated at high concentrations. Therefore, plants must have a system for preferentially delivering an adequate amount of minerals to these organs for active growth and development, while preventing mineral overaccumulation in the face of changing environments. Here we show that a member of the Nramp transporter family, OsNramp3, functions as a switch in response to environmental Mn changes. OsNramp3 is constitutively expressed in the node, a junction of vasculatures connecting leaves, stems and panicles. At low Mn concentration, OsNramp3 preferentially transports Mn to young leaves and panicles. However, at high Mn concentration, the OsNramp3 protein is rapidly degraded within a few hours, resulting in the distribution of Mn to old tissues. Our results reveal the OsNramp3-mediated strategy of rice for adapting to a wide change of Mn in the environment.

DOI： 10.1038/ncomms3442

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Magnesium transporters and their role in Al tolerance in plants

Zhi Chang Chen, Jian Feng Ma

PLANT AND SOIL   368 ( 1-2 )   51 - 56   2013.7

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Magnesium (Mg) is an essential macronutrient for plant growth, which has diverse biological functions. However, little is known about the transport system of this nutrient in plants. In the genome of plants such as rice and Arabidopsis, there are homologues of bacterial Mg transporters (CorA) and some of them have been functionally characterized, but the physiological role of these transporters are poorly understood. On the other hand, Mg is able to alleviate Al toxicity in a number of plant species, but the mechanisms underlying this alleviation are not well understood. Recently, this alleviation has been associated with a Mg transporter in rice. In this paper, we present our opinions on Mg transporters, which are required for uptake, translocation, distribution and storage in plants. Possible mechanisms for Mg-mediated alleviation of Al toxicity are also discussed.

DOI： 10.1007/s11104-012-1433-y

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TWIN SISTER OF FT, GIGANTEA, and CONSTANS Have a Positive But Indirect Effect on Blue Light-Induced Stomatal Opening in Arabidopsis

Eigo Ando, Masato Ohnishi, Yin Wang, Tomonao Matsushita, Aiko Watanabe, Yuki Hayashi, Miho Fujii, Jian Feng Ma, Shin-ichiro Inoue, Toshinori Kinoshita

PLANT PHYSIOLOGY   162 ( 3 )   1529 - 1538   2013.7

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FLOWERING LOCUS T (FT) is the major regulatory component controlling photoperiodic floral transition. It is expressed in guard cells and affects blue light-induced stomatal opening induced by the blue-light receptor phototropins phot1 and phot2. Roles for other flowering regulators in stomatal opening have yet to be determined. We show in Arabidopsis (Arabidopsis thaliana) that TWIN SISTER OF FT (TSF), CONSTANS (CO), and GIGANTEA (GI) provide a positive effect on stomatal opening. TSF, which is the closest homolog of FT, was transcribed in guard cells, and light-induced stomatal opening was repressed in tsf-1, a T-DNA insertion mutant of TSF. Overexpression of TSF in a phot1 phot2 mutant background gave a constitutive open-stomata phenotype. Then, we examined whether CO and GI, which are upstream regulators of FT and TSF in photoperiodic flowering, are involved in stomatal opening. Similar to TSF, light-induced stomatal opening was suppressed in the GI and CO mutants gi-1 and co-1. A constitutive open-stomata phenotype was observed in GI and CO overexpressors with accompanying changes in the transcription of both FT and TSF. In photoperiodic flowering, photoperiod is sensed by photoreceptors such as the cryptochromes cry1 and cry2. We examined stomatal phenotypes in a cry1 cry2 mutant and in CRY2 overexpressors. Light-induced stomatal opening was suppressed in cry1 cry2, and the transcription of FT and TSF was down-regulated. In contrast, the stomata in CRY2 overexpressors opened even in the dark, and FT and TSF transcription was up-regulated. We conclude that the photoperiodic flowering components TSF, GI, and CO positively affect stomatal opening.

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Effect of silicon deficiency on secondary cell wall synthesis in rice leaf

Tsuyoshi Yamamoto, Atsuko Nakamura, Hiroaki Iwai, Tadashi Ishii, Jian Feng Ma, Ryusuke Yokoyama, Kazuhiko Nishitani, Shinobu Satoh, Jun Furukawa

JOURNAL OF PLANT RESEARCH   125 ( 6 )   771 - 779   2012.11

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Rice (Oryza sativa L.) is a typical Si-accumulating plant and is able to accumulate Si up to > 10 % of shoot dry weight. The cell wall has been reported to become thicker under Si-deficient condition. To clarify the relationship between Si accumulation and cell wall components, the physical properties of, and macromolecular components and Si content in, the pectic, hemicellulosic, and cellulosic fractions prepared from rice seedlings grown in hydroponics with or without 1.5 mM silicic acid were analyzed. In the absence of Si (the -Si condition), leaf blades drooped, but physical properties were enhanced. Sugar content in the cellulosic fraction and lignin content in the total cell wall increased under -Si condition. After histochemical staining, there was an increase in cellulose deposition in short cells and the cell layer just beneath the epidermis in the -Si condition, but no significant change in the pattern of lignin deposition. Expression of the genes involved in secondary cell wall synthesis, OsCesA4, OsCesA7, OsPAL, OsCCR1 and OsCAD6 was up-regulated under -Si condition, but expression of OsCesA1, involved in primary cell wall synthesis, did not increase. These results suggest that an increase in secondary cell wall components occurs in rice leaves to compensate for Si deficiency.

DOI： 10.1007/s10265-012-0489-3

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Functional Characterization of a Silicon Transporter Gene Implicated in Silicon Distribution in Barley

Naoki Yamaji, Yukako Chiba, Namiki Mitani-Ueno, Jian Feng Ma

PLANT PHYSIOLOGY   160 ( 3 )   1491 - 1497   2012.11

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Silicon (Si) is a beneficial element for plant growth. In barley (Hordeum vulgare), Si uptake by the roots is mainly mediated by a Si channel, Low Silicon1 (HvLsi1), and an efflux transporter, HvLsi2. However, transporters involved in the distribution of Si in the shoots have not been identified. Here, we report the functional characterization of a homolog of HvLsi1, HvLsi6. HvLsi6 showed permeability for Si and localized to the plasma membrane. At the vegetative growth stage, HvLsi6 was expressed in both the roots and shoots. The expression level was unaffected by Si supply. In the roots, HvLsi6 was localized in epidermis and cortex cells of the tips, while in the leaf blades and sheaths, HvLsi6 was only localized at parenchyma cells of vascular bundles. At the reproductive growth stage, high expression of HvLsi6 was also found in the nodes. HvLsi6 in node I was polarly located at the transfer cells surrounding the enlarged vascular bundles toward the numerous xylem vessels. These results suggest that HvLsi6 is involved in Si uptake in the root tips, xylem unloading of Si in leaf blade and sheath, and intervascular transfer of Si in the nodes. Furthermore, HvLsi2 was found to be localized at the parenchyma cell layer adjacent to the transfer cells with opposite polarity of HvLsi6, suggesting that the coupling of HvLsi6 and HvLsi2 is involved in the intervascular transfer of Si at the nodes. Si translocated via the enlarged vascular bundles is unloaded to the transfer cells by HvLsi6, followed by HvLsi2 to reload Si to the diffuse vascular bundles, which are connected to the upper part of the plant, especially the panicles, the ultimate Si sink.

DOI： 10.1104/pp.112.204578

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Cloning genes for mineral Uptake: Examples using rice mutants

J. F. Ma

Plant Mutation Breeding and Biotechnology   463 - 470   2012.10

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Comparative Genome-Wide Transcriptional Analysis of Al-Responsive Genes Reveals Novel Al Tolerance Mechanisms in Rice

Tomokazu Tsutsui, Naoki Yamaji, Chao Feng Huang, Ritsuko Motoyama, Yoshiaki Nagamura, Jian Feng Ma

PLOS ONE   7 ( 10 )   e48197   2012.10

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Rice (Oryza sativa) is the most aluminum (Al)-tolerant crop among small-grain cereals, but the mechanism underlying its high Al resistance is still not well understood. To understand the mechanisms underlying high Al-tolerance, we performed a comparative genome-wide transcriptional analysis by comparing expression profiling between the Al-tolerance cultivar (Koshihikari) and an Al-sensitive mutant star1 (SENSITIVE TO AL RHIZOTOXICITY 1) in both the root tips and the basal roots. Exposure to 20 mu M AlCl3 for 6 h resulted in up-regulation (higher than 3-fold) of 213 and 2015 genes including 185 common genes in the root tips of wild-type and the mutant, respectively. On the other hand, in the basal root, genes up-regulated by Al were 126 and 2419 including 76 common genes in the wild-type and the mutant, respectively. These results indicate that Al-response genes are not only restricted to the root tips, but also in the basal root region. Analysis with genes up-or down-regulated only in the wild-type reveals that there are other mechanisms for Al-tolerance except for a known transcription factor ART1-regulated one in rice. These mechanisms are related to nitrogen assimilation, secondary metabolite synthesis, cell-wall synthesis and ethylene synthesis. Although the exact roles of these putative tolerance genes remain to be examined, our data provide a platform for further work on Al-tolerance in rice.

DOI： 10.1371/journal.pone.0048197

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YSL16 Is a Phloem-Localized Transporter of the Copper-Nicotianamine Complex That Is Responsible for Copper Distribution in Rice

Luqing Zheng, Naoki Yamaji, Kengo Yokosho, Jian Feng Ma

PLANT CELL   24 ( 9 )   3767 - 3782   2012.9

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Cu is an essential element for plant growth, but the molecular mechanisms of its distribution and redistribution within the plants are unknown. Here, we report that Yellow stripe-like16 (YSL16) is involved in Cu distribution and redistribution in rice (Oryza sativa). Rice YSL16 was expressed in the roots, leaves, and unelongated nodes at the vegetative growth stage and highly expressed in the upper nodes at the reproductive stage. YSL16 was expressed at the phloem of nodes and vascular tissues of leaves. Knockout of this gene resulted in a higher Cu concentration in the older leaves but a lower concentration in the younger leaves at the vegetative stage. At the reproductive stage, a higher Cu concentration was found in the flag leaf and husk, but less Cu was present in the brown rice, resulting in a significant reduction in fertility in the knockout line. Isotope labeling experiments with Cu-65 showed that the mutant lost the ability to transport Cu-nicotianamine from older to younger leaves and from the flag leaf to the panicle. Rice YSL16 transported the Cu-nicotianamine complex in yeast. Taken together, our results indicate that Os-YSL16 is a Cu-nicotianamine transporter that is required for delivering Cu to the developing young tissues and seeds through phloem transport.

DOI： 10.1105/tpc.112.103820

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Up-Regulation of a Magnesium Transporter Gene OsMGT1 Is Required for Conferring Aluminum Tolerance in Rice

Zhi Chang Chen, Naoki Yamaji, Ritsuko Motoyama, Yoshiaki Nagamura, Jian Feng Ma

PLANT PHYSIOLOGY   159 ( 4 )   1624 - 1633   2012.8

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Magnesium (Mg)-mediated alleviation of aluminum (Al) toxicity has been observed in a number of plant species, but the mechanisms underlying the alleviation are still poorly understood. When a putative rice (Oryza sativa) Mg transporter gene, Oryza sativa MAGNESIUM TRANSPORTER1 (OsMGT1), was knocked out, the tolerance to Al, but not to cadmium and lanthanum, was decreased. However, this inhibition could be rescued by addition of 10 mu M Mg, but not by the same concentration of barium or strontium. OsMGT1 was expressed in both the roots and shoots in the absence of Al, but the expression only in the roots was rapidly up-regulated by Al. Furthermore, the expression did not respond to low pH and other metals including cadmium and lanthanum, and was regulated by an Al-responsive transcription factor, AL RESISTANCE TRANSCRIPTION FACTOR1. An investigation of subcellular localization showed that OsMGT1 was localized to the plasma membrane. A short-term (30 min) uptake experiment with stable isotope Mg-25 showed that knockout of OsMGT1 resulted in decreased Mg uptake, but that the uptake in the wild type was enhanced by Al. Mg concentration in the cell sap of the root tips was also increased in the wild-type rice, but not in the knockout lines in the presence of Al. A microarray analysis showed that transcripts of genes related to stress were more up- and down-regulated in the knockout lines. Taken together, our results indicate that OsMGT1 is a transporter for Mg uptake in the roots and that up-regulation of this gene is required for conferring Al tolerance in rice by increasing Mg concentration in the cell.

DOI： 10.1104/pp.112.199778

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Characterization of the high affinity Zn transporter from Noccaea caerulescens, NcZNT1, and dissection of its promoter for its role in Zn uptake and hyperaccumulation

Matthew J. Milner, Eric Craft, Naoki Yamaji, Emi Koyama, Jian Feng Ma, Leon V. Kochian

NEW PHYTOLOGIST   195 ( 1 )   113 - 123   2012.7

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In this paper, we conducted a detailed analysis of the ZIP family transporter, NcZNT1, in the zinc (Zn)/cadmium (Cd) hyperaccumulating plant species, Noccaea caerulescens, formerly known as Thlaspi caerulescens. NcZNT1 was previously suggested to be the primary root Zn/Cd uptake transporter. Both a characterization of NcZNT1 transport function in planta and in heterologous systems, and an analysis of NcZNT1 gene expression and NcZNT1 protein localization were carried out. We show that NcZNT1 is not only expressed in the root epidermis, but also is highly expressed in the root and shoot vasculature, suggesting a role in long-distance metal transport. Also, NcZNT1 was found to be a plasma membrane transporter that mediates Zn but not Cd, iron (Fe), manganese (Mn) or copper (Cu) uptake into plant cells. Two novel regions of the NcZNT1 promoter were identified which may be involved in both the hyperexpression of NcZNT1 and its ability to be regulated by plant Zn status. In conclusion, we demonstrate here that NcZNT1 plays a role in Zn and not Cd uptake from the soil, and based on its strong expression in the root and shoot vasculature, could be involved in long-distance transport of Zn from the root to the shoot via the xylem.

DOI： 10.1111/j.1469-8137.2012.04144.x

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Transcriptional regulation of aluminium tolerance genes

Emmanuel Delhaize, Jian Feng Ma, Peter R. Ryan

TRENDS IN PLANT SCIENCE   17 ( 6 )   341 - 348   2012.6

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Trivalent aluminium (Al3+) is the major toxin encountered by plants on acid soils. These cations inhibit root growth by damaging cells at the root apex. The physiology and genetics of Al3+ tolerance mechanisms involving organic anion efflux from roots have now been investigated in a range of species. Over the past decade, genes encoding these and other newly discovered mechanisms of tolerance have been cloned. In this review, we describe the genes controlling the genotypic variation in Al3+ tolerance for several important crop species. We focus on recent insights into the transcriptional regulation of these and other genes involved in Al3+ tolerance and discuss the pathways coordinating their expression in Arabidopsis and rice.

DOI： 10.1016/j.tplants.2012.02.008

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Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene

Jonatan Montpetit, Julien Vivancos, Namiki Mitani-Ueno, Naoki Yamaji, Wilfried Remus-Borel, Francois Belzile, Jian Feng Ma, Richard R. Belanger

PLANT MOLECULAR BIOLOGY   79 ( 1-2 )   35 - 46   2012.5

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Silicon (Si) is known to be beneficial to plants, namely in alleviating biotic and abiotic stresses. The magnitude of such positive effects is associated with a plant's natural ability to absorb Si. Many grasses can accumulate as much as 10% on a dry weight basis while most dicots, including Arabidopsis, will accumulate less than 0.1%. In this report, we describe the cloning and functional characterization of TaLsi1, a wheat Si transporter gene. In addition, we developed a heterologous system for the study of Si uptake in plants by introducing TaLsi1 and OsLsi1, its ortholog in rice, into Arabidopsis, a species with a very low innate Si uptake capacity. When expressed constitutively under the control of the CaMV 35S promoter, both TaLsi1 and OsLsi1 were expressed in cells of roots and shoots. Such constitutive expression of TaLsi1 or OsLsi1 resulted in a fourfold to fivefold increase in Si accumulation in transformed plants compared to WT. However, this Si absorption caused deleterious symptoms. When the wheat transporter was expressed under the control of a root-specific promoter (a boron transporter gene (AtNIP5;1) promoter), a similar increase in Si absorption was noted but the plants did not exhibit symptoms and grew normally. These results demonstrate that TaLsi1 is indeed a functional Si transporter as its expression in Arabidopsis leads to increased Si uptake, but that this expression must be confined to root cells for healthy plant development. The availability of this heterologous expression system will facilitate further studies into the mechanisms and benefits of Si uptake.

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Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice

Akimasa Sasaki, Naoki Yamaji, Kengo Yokosho, Jian Feng Ma

PLANT CELL   24 ( 5 )   2155 - 2167   2012.5

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Paddy rice (Oryza sativa) is able to accumulate high concentrations of Mn without showing toxicity; however, the molecular mechanisms underlying Mn uptake are unknown. Here, we report that a member of the Nramp (for the Natural Resistance-Associated Macrophage Protein) family, Nramp5, is involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice. Nramp5 was constitutively expressed in the roots and encodes a plasma membrane-localized protein. Nramp5 was polarly localized at the distal side of both exodermis and endodermis cells. Knockout of Nramp5 resulted in a significant reduction in growth and grain yield, especially when grown at low Mn concentrations. This growth reduction could be partially rescued by supplying high concentrations of Mn but not by the addition of Fe. Mineral analysis showed that the concentration of Mn and Cd in both the roots and shoots was lower in the knockout line than in wild-type rice. A short-term uptake experiment revealed that the knockout line lost the ability to take up Mn and Cd. Taken together, Nramp5 is a major transporter of Mn and Cd and is responsible for the transport of Mn and Cd from the external solution to root cells.

DOI： 10.1105/tpc.112.096925

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Acquisition of aluminium tolerance by modification of a single gene in barley. International journal

Miho Fujii, Kengo Yokosho, Naoki Yamaji, Daisuke Saisho, Miki Yamane, Hirokazu Takahashi, Kazuhiro Sato, Mikio Nakazono, Jian Feng Ma

Nature communications   3   713 - 713   2012.3

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Originating from the Fertile Crescent in the Middle East, barley has now been cultivated widely on different soil types including acid soils, where aluminium toxicity is a major limiting factor. Here we show that the adaptation of barley to acid soils is achieved by the modification of a single gene (HvAACT1) encoding a citrate transporter. We find that the primary function of this protein is to release citrate from the root pericycle cells to the xylem to facilitate the translocation of iron from roots to shoots. However, a 1-kb insertion in the upstream of the HvAACT1 coding region occurring only in the Al-tolerant accessions, enhances its expression and alters the location of expression to the root tips. The altered HvAACT1 has an important role in detoxifying aluminium by secreting citrate to the rhizosphere. Thus, the insertion of a 1-kb sequence in the HvAACT1 upstream enables barley to adapt to acidic soils.

DOI： 10.1038/ncomms1726

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A leucine-rich repeat receptor-like kinase gene is involved in the specification of outer cell layers in rice roots

Chao-Feng Huang, Naoki Yamaji, Kazuko Ono, Jian Feng Ma

PLANT JOURNAL   69 ( 4 )   565 - 576   2012.2

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Root outer cell layers of Oryza sativa (rice), which comprise the epidermis, exodermis and sclerenchyma, play an important role in protecting the roots from various stresses in soil, but the molecular mechanisms for the specification of these cell layers are poorly understood. In this work, we report on defective in outer cell layer specification 1 (Docs1), which is involved in the specification of outer cell layers in rice roots. Docs1 was isolated by map-based cloning using a mutant (c68) defective in the outer cell layers of primary roots. It encodes a leucine-rich repeat receptor-like kinase (LRR RLK). Docs1 mRNA was expressed in all tissues including roots, leaf blades and sheaths, and flowers. Immunostaining with an anti-Docs1 antibody showed that Docs1 was localized at the epidermis and exodermis, depending on the root region. Furthermore, Docs1 showed polar localization at the distal side. Subcellular examination showed that Docs1 was localized to the plasma membrane. Comparison of genome-wide transcriptional profiles between the wild-type and the knock-out mutant roots using microarray analysis showed that 61 and 41 genes were up- and downregulated in the mutant, including genes encoding putative transcription factors and genes potentially involved in cell wall metabolism. These results suggest that Docs1 might directly or indirectly regulate multiple genes involved in the proper development of root outer cell layers in rice.

DOI： 10.1111/j.1365-313X.2011.04824.x

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ABC transporter for Al tolerance Reviewed

Chao-Feng Huang, Naoki Yamaji, Zhichang Chen, Jian Feng Ma

The Plant Journal   69 ( 5 )   857 - 867   2012

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Chao-Feng Huang, Naoki Yamaji, Zhichang Chen, Jian Feng Ma, 2012, &#039;ABC transporter for Al tolerance&#039;, &lt;i&gt;The Plant Journal&lt;/i&gt;, vol. 69, no. 5, pp. 857-867

DOI： 10.1111/j.1365-313x.2011.04837.x

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Beneficial Elements

Martin Broadley, Patrick Brown, Ismail Cakmak, Jian Feng Ma, Zed Rengel, Fangjie Zhao

Marschner's Mineral Nutrition of Higher Plants   249 - 269   2012

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DOI： 10.1016/B978-0-12-384905-2.00008-X

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Silicon deficiency promotes lignin accumulation in rice

Shiro Suzuki, Jian Feng Ma, Naoki Yamamoto, Takefumi Hattori, Masahiro Sakamoto, Toshiaki Umezawa

PLANT BIOTECHNOLOGY   29 ( 4 )   391 - 394   2012

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：JAPANESE SOC PLANT CELL & MOLECULAR BIOLOGY  

Although both lignin and silica accumulate on cell walls and confer rigidity, mechanical strength, and resistance to pathogen invasion in rice, it remains unclear whether silicon deficiency affects lignin accumulation. We demonstrate that low silicon rice mutated in a silicon influx transporter, Lsi1, or a silicon efflux transporter, Lsi2, contained larger amounts of lignin in the rice straws. Furthermore, wild-type rice cultivated on low silicon media also accumulated larger amounts of lignin in shoots. Significant accumulation of guaiacyl lignin upon silicon deficiency was determined by nitrobenzene oxidation analysis. These data indicate a negative correlation between silicon accumulation and lignin deposition.

DOI： 10.5511/plantbiotechnology.12.0416a

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Identification and application of genes related to toxic element accumulation in rice

Ma Jian Feng

GENES & GENETIC SYSTEMS   86 ( 6 )   399 - 399   2011.12

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OsYSL6 Is Involved in the Detoxification of Excess Manganese in Rice

Akimasa Sasaki, Naoki Yamaji, Jixing Xia, Jian Feng Ma

PLANT PHYSIOLOGY   157 ( 4 )   1832 - 1840   2011.12

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Yellow Stripe-Like (YSL) proteins belong to the oligopeptide transporter family and have been implicated in metal transport and homeostasis in different plant species. Here, we functionally characterized a rice (Oryza sativa) YSL member, OsYSL6. Knockout of OsYSL6 resulted in decreased growth of both roots and shoots only in the high-manganese (Mn) condition. There was no difference in the concentration of total Mn and other essential metals between the wild-type rice and the knockout line, but the knockout line showed a higher Mn concentration in the leaf apoplastic solution and a lower Mn concentration in the symplastic solution than wild-type rice. OsYSL6 was constitutively expressed in both the shoots and roots, and the expression level was not affected by either deficiency or toxicity of various metals. Furthermore, the expression level increased with leaf age. Analysis with OsYSL6 promoter-green fluorescent protein transgenic rice revealed that OsYSL6 was expressed in all cells of both the roots and shoots. Heterogolous expression of OsYSL6 in yeast showed transport activity for the Mn-nicotianamine complex but not for the Mn-mugineic acid complex. Taken together, our results suggest that OsYSL6 is a Mn-nicotianamine transporter that is required for the detoxification of excess Mn in rice.

DOI： 10.1104/pp.111.186031

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An Al-inducible MATE gene is involved in external detoxification of Al in rice

Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

PLANT JOURNAL   68 ( 6 )   1061 - 1069   2011.12

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A number of plant species, including rice, secretes citrate from roots in response to Al stress. Here we characterized the functions of a gene, OsFRDL4 (Os01g0919100) that belongs to the multidrug and toxic compound extrusion (MATE) family in rice (Oryza sativa). Heterologous expression in Xenopus oocyte showed that the OsFRDL4 protein was able to transport citrate and was activated by Al. The expression level of the OsFRDL4 gene in roots was very low in the absence of Al, but was greatly enhanced by Al after short exposure. Furthermore, the OsFRDL4 expression was regulated by ART1, a C2H2-type zinc finger transcription factor for Al tolerance. Transient expression of OsFRDL4 in onion epidermal cells showed that it localized to the plasma membrane. Immunostaining showed that OsFRDL4 was localized in all cells in the root tip. These expression patterns and cell specificity of localization of OsFRDL4 are different from other MATE members identified previously. Knockout of OsFRDL4 resulted in decreased Al tolerance and decreased citrate secretion compared with the wild-type rice, but did not affect citrate concentration in the xylem sap. Furthermore, there is a positive correlation between OsFRDL4 expression level and the amount of citrate secretion in rice cultivars that are differing in Al tolerance. Taken together, our results show that OsFRDL4 is an Al-induced citrate transporter localized at the plasma membrane of rice root cells and is one of the components of high Al tolerance in rice.

DOI： 10.1111/j.1365-313X.2011.04757.x

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Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of Yellow Stripe-Like (YSL) transporters

Burcu K. Yordem, Sarah S. Conte, Jian Feng Ma, Kengo Yokosho, Kenneth A. Vasques, Srinivasa N. Gopalsamy, Elsbeth L. Walker

ANNALS OF BOTANY   108 ( 5 )   821 - 833   2011.10

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Background and Aims Brachypodium distachyon is a temperate grass with a small stature, rapid life cycle and completely sequenced genome that has great promise as a model system to study grass-specific traits for crop improvement. Under iron (Fe)-deficient conditions, grasses synthesize and secrete Fe(III)-chelating agents called phytosiderophores (PS). In Zea mays, Yellow Stripe1 (ZmYS1) is the transporter responsible for the uptake of Fe(III)-PS complexes from the soil. Some members of the family of related proteins called Yellow Stripe-Like (YSL) have roles in internal Fe translocation of plants, while the function of other members remains uninvestigated. The aim of this study is to establish brachypodium as a model system to study Fe homeostasis in grasses, identify YSL proteins in brachypodium and maize, and analyse their expression profiles in brachypodium in response to Fe deficiency.Methods The YSL family of proteins in brachypodium and maize were identified based on sequence similarity to ZmYS1. Expression patterns of the brachypodium YSL genes (BdYSL genes) were determined by quantitative RT-PCR under Fe-deficient and Fe-sufficient conditions. The types of PS secreted, and secretion pattern of PS in brachypodium were analysed by high-performance liquid chromatography.Key Results Eighteen YSL family members in maize and 19 members in brachypodium were identified. Phylogenetic analysis revealed that some YSLs group into a grass-specific clade. The Fe status of the plant can regulate expression of brachypodium YSL genes in both shoots and roots. 3-Hydroxy-2'-deoxymugineic acid (HDMA) is the dominant type of PS secreted by brachypodium, and its secretion is diurnally regulated.Conclusions PS secretion by brachypodium parallels that of related crop species such as barley and wheat. A single grass species-specific YSL clade is present, and expression of the BdYSL members of this clade could not be detected in shoots or roots, suggesting grass-specific functions in reproductive tissues. Finally, the Fe-responsive expression profiles of several YSLs suggest roles in Fe homeostasis.

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A functional cutin matrix is required for plant protection against water loss

Guoxiong Chen, Takao Komatsuda, Jian Feng Ma, Chao Li, Naoki Yamaji, Eviatar Nevo

Plant Signaling and Behavior   6 ( 9 )   1297 - 1299   2011.9

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The plant cuticle, a cutin matrix embedded with and covered by wax, seals the aerial organ's surface to protect the plant against uncontrolled water loss. The cutin matrix is essential for the cuticle to function as a barrier to water loss. Recently, we identified from wild barley a drought supersensitive mutant, eibi1, which is caused by a defective cutin matrix as the result of the loss of function of HvABCG31, an ABCG full transporter. Here, we report that eibi1 epidermal cells contain lipid-like droplets, which are supposed to consist of cutin monomers that have not been transported out of the cells. The eibi1 cuticle is fragile due to a defective cutin matrix. The rice ortholog of the EIBI1 gene has a similar pattern of expression, young shoot but not flag leaf blade, as the barley gene. The model of the function of Eibi1 is discussed. The HvABCG31 full transporter functions in the export of cutin components and contributed to land plant colonization, hence also to terrestrial life evolution. © 2011 Landes Bioscience.

DOI： 10.4161/psb.6.9.17507

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The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic

Namiki Mitani-Ueno, Naoki Yamaji, Fang-Jie Zhao, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   62 ( 12 )   4391 - 4398   2011.8

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Nodulin-26-like intrinsic proteins (NIPs) of the aquaporin family are involved in the transport of diverse solutes, but the mechanisms controlling the selectivity of transport substrates are poorly understood. The purpose of this study was to investigate how the aromatic/arginine (ar/R) selectivity filter influences the substrate selectivity of two NIP aquaporins; the silicic acid (Si) transporter OsLsi1 (OsNIP2;1) from rice and the boric acid (B) transporter AtNIP5;1 from Arabidopsis; both proteins are also permeable to arsenite. Native and site-directed mutagenized variants of the two genes were expressed in Xenopus oocytes and the transport activities for Si, B, arsenite, and water were assayed. Substitution of the amino acid at the ar/R second helix (H2) position of OsLsi1 did not affect the transport activities for Si, B, and arsenite, but that at the H5 position resulted in a total loss of Si and B transport activities and a partial loss of arsenite transport activity. Conversely, changes of the AtNIP5;1 ar/R selectivity filter and the NPA motifs to the OsLsi1 type did not result in a gain of Si transport activity. B transport activity was partially lost in the H5 mutant but unaffected in the H2 mutant of AtNIP5;1. In contrast, both the single and double mutations at the H2 and/or H5 positions of AtNIP5;1 did not affect arsenite transport activity. The results reveal that the residue at the H5 position of the ar/R filter of both OsLsi1 and AtNIP5;1 plays a key role in the permeability to Si and B, but there is a relatively low selectivity for arsenite.

DOI： 10.1093/jxb/err158

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An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice

Guoxiong Chen, Takao Komatsuda, Jian Feng Ma, Christiane Nawrath, Mohammad Pourkheirandish, Akemi Tagiri, Yin-Gang Hu, Mohammad Sameri, Xinrong Li, Xin Zhao, Yubing Liu, Chao Li, Xiaoying Ma, Aidong Wang, Sudha Nair, Ning Wang, Akio Miyao, Shun Sakuma, Naoki Yamaji, Xiuting Zheng, Eviatar Nevo

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   108 ( 30 )   12354 - 12359   2011.7

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Land plants have developed a cuticle preventing uncontrolled water loss. Here we report that an ATP-binding cassette (ABC) subfamily G (ABCG) full transporter is required for leaf water conservation in both wild barley and rice. A spontaneous mutation, eibi1.b, in wild barley has a low capacity to retain leaf water, a phenotype associated with reduced cutin deposition and a thin cuticle. Map-based cloning revealed that Eibi1 encodes an HvABCG31 full transporter. The gene was highly expressed in the elongation zone of a growing leaf (the site of cutin synthesis), and its gene product also was localized in developing, but not in mature tissue. A de novo wild barley mutant named "eibi1.c," along with two transposon insertion lines of rice mutated in the ortholog of HvABCG31 also were unable to restrict water loss from detached leaves. HvABCG31 is hypothesized to function as a transporter involved in cutin formation. Homologs of HvABCG31 were found in green algae, moss, and lycopods, indicating that this full transporter is highly conserved in the evolution of land plants.

DOI： 10.1073/pnas.1108444108

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Transport of silicon from roots to panicles in plants

Jian Feng Ma, Naoki Yamaji, Namiki Mitani-Ueno

PROCEEDINGS OF THE JAPAN ACADEMY SERIES B-PHYSICAL AND BIOLOGICAL SCIENCES   87 ( 7 )   377 - 385   2011.7

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Silicon (Si) is the most abundant minerals in soil and exerts beneficial effects on plant growth by alleviating various stresses. The transport of Si from soil to the panicles is mediated by different transporters. Lsi1, belonging to a NIP group of the aquaporin family, is responsible for the uptake of Si from soil into the root cells in both dicots and monocots although its expression patterns and cellular localization differ with plant species. The subsequent transport of Si out of the root cells towards the stele is medicated by an active efflux transporter, Lsi2. Lsi1. and Lsi2 are polarly localized at the distal and proximal sides, respectively, of both exodermis and endodermis in rice root. Silicon in the xylem sap is presented in the form of monosilicic acid and is unloaded by Lsi6, a homolog of Lsi1 in rice. Lsi6 is also involved in the inter-vascular transfer of Si at the node, which is necessary for preferential Si distribution to the panicles.

DOI： 10.2183/pjab.87.377

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Identification of a Cis-Acting Element of ART1, a C2H2-Type Zinc-Finger Transcription Factor for Aluminum Tolerance in Rice

Tomokazu Tsutsui, Naoki Yamaji, Jian Feng Ma

PLANT PHYSIOLOGY   156 ( 2 )   925 - 931   2011.6

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Rice (Oryza sativa) is one of the most aluminum (Al)-tolerant species among small-grain cereals. Recent identification of a transcription factor AL RESISTANCE TRANSCRIPTION FACTOR1 (ART1) revealed that this high Al tolerance in rice is achieved by multiple genes involved in detoxification of Al at different cellular levels. ART1 is a C2H2-type zinc-finger transcription factor and regulates the expression of 31 genes in the downstream. In this study, we attempted to identify a cis-acting element of ART1. We used the promoter region of SENSITIVE TO AL RHIZOTOXICITY1, an Al tolerance gene in the downstream of ART1. With the help of gel-shift assay, we were able to identify the cis-acting element as GGN(T/g/a/C)V(C/A/g)S(C/G). This element was found in the promoter region of 29 genes among 31 ART1-regulated genes. To confirm this cis-acting element in vivo, we transiently introduced this element one or five times tandemly repeated sequence with 35S minimal promoter and green fluorescent protein reporter together with or without ART1 gene in the tobacco (Nicotiana tabacum) mesophyll protoplasts. The results showed that the expression of green fluorescent protein reporter responded to ART1 expression. Furthermore, the expression increased with repetition of the cis-acting element. Our results indicate that the five nucleotides identified are the target DNA-binding sequence of ART1.

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Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens

Daisei Ueno, Matthew J. Milner, Naoki Yamaji, Kengo Yokosho, Emi Koyama, M. Clemencia Zambrano, Molly Kaskie, Stephen Ebbs, Leon V. Kochian, Jian Feng Ma

PLANT JOURNAL   66 ( 5 )   852 - 862   2011.6

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P>Cadmium (Cd) is a highly toxic heavy metal for plants, but several unique Cd-hyperaccumulating plant species are able to accumulate this metal to extraordinary concentrations in the aboveground tissues without showing any toxic symptoms. However, the molecular mechanisms underlying this hypertolerance to Cd are poorly understood. Here we have isolated and functionally characterized an allelic gene, TcHMA3 (heavy metal ATPase 3) from two ecotypes (Ganges and Prayon) of Thlaspi caerulescens contrasting in Cd accumulation and tolerance. The TcHMA3 alleles from the higher (Ganges) and lower Cd-accumulating ecotype (Prayon) share 97.8% identity, and encode a P-1B-type ATPase. There were no differences in the expression pattern, cell-specificity of protein localization and transport substrate-specificity of TcHMA3 between the two ecotypes. Both alleles were characterized by constitutive expression in the shoot and root, a tonoplast localization of the protein in all leaf cells and specific transport activity for Cd. The only difference between the two ecotypes was the expression level of TcHMA3: Ganges showed a sevenfold higher expression than Prayon, partly caused by a higher copy number. Furthermore, the expression level and localization of TcHMA3 were different from AtHMA3 expression in Arabidopsis. Overexpression of TcHMA3 in Arabidopsis significantly enhanced tolerance to Cd and slightly increased tolerance to Zn, but did not change Co or Pb tolerance. These results indicate that TcHMA3 is a tonoplast-localized transporter highly specific for Cd, which is responsible for sequestration of Cd into the leaf vacuoles, and that a higher expression of this gene is required for Cd hypertolerance in the Cd-hyperaccumulating ecotype of T. caerulescens.

DOI： 10.1111/j.1365-313X.2011.04548.x

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High-Resolution Secondary Ion Mass Spectrometry Reveals the Contrasting Subcellular Distribution of Arsenic and Silicon in Rice Roots

Katie L. Moore, Markus Schroeder, Zhongchang Wu, Barry G. H. Martin, Chris R. Hawes, Steve P. McGrath, Malcolm J. Hawkesford, Jian Feng Ma, Fang-Jie Zhao, Chris R. M. Grovenor

PLANT PHYSIOLOGY   156 ( 2 )   913 - 924   2011.6

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Rice (Oryza sativa) takes up arsenite mainly through the silicic acid transport pathway. Understanding the uptake and sequestration of arsenic (As) into the rice plant is important for developing strategies to reduce As concentration in rice grain. In this study, the cellular and subcellular distributions of As and silicon (Si) in rice roots were investigated using high-pressure freezing, high-resolution secondary ion mass spectrometry, and transmission electron microscopy. Rice plants, both the lsi2 mutant lacking the Si/arsenite efflux transporter Lsi2 and its wild-type cultivar, with or without an iron plaque, were treated with arsenate or arsenite. The formation of iron plaque on the root surface resulted in strong accumulation of As and phosphorous on the epidermis. The lsi2 mutant showed stronger As accumulation in the endodermal vacuoles, where the Lsi2 transporter is located in the plasma membranes, than the wild-type line. As also accumulated in the vacuoles of some xylem parenchyma cells and in some pericycle cells, particularly in the wild-type mature root zone. Vacuolar accumulation of As is associated with sulfur, suggesting that As may be stored as arsenite-phytochelatin complexes. Si was localized in the cell walls of the endodermal cells with little apparent effect of the Lsi2 mutation on its distribution. This study reveals the vacuolar sequestration of As in rice roots and contrasting patterns of As and Si subcellular localization, despite both being transported across the plasma membranes by the same transporters.

DOI： 10.1104/pp.111.173088

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Isolation and Characterization of a Barley Yellow Stripe-Like Gene, HvYSL5

Luqing Zheng, Miho Fujii, Naoki Yamaji, Akimasa Sasaki, Miki Yamane, Isamu Sakurai, Kazuhiro Sato, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   52 ( 5 )   765 - 774   2011.5

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Yellow stripe-like (YSL) family transporters, belonging to a novel subfamily of oligopeptide transporter (OPT), has been proposed to be involved in metal uptake and long-distance transport, but only a few of them have been functionally characterized so far. In the present study, we isolated an uncharacterized member of the YSL family, HvYSL5, in barley based on expressed sequence tag (EST) information. HvYSL5 shared 50% identity with HvYS1, a transporter for the ferric-mugineic acid complex, at the amino acid level. Promoter analysis showed that the HvYSL5 upstream sequence contains both iron deficiency response element 1 and 2 (IDE1 and 2). HvYSL5 was expressed in the roots and the expression was greatly induced by Fe deficiency, but not by deficiency of other metals including Zn, Cu and Mn. Spatial investigation showed that much higher expression of HvYSL5 was found in the mature zones of the roots, but not in the root tips. Furthermore, the expression showed a diurnal rhythm, being the highest in the morning, but with no expression in the afternoon. HvYSL5 was localized in all root cells, and subcellular localization analysis showed that HvYSL5 is likely to be localized in the vesicles. Knockdown of HvYSL5 did not result in any detectable phenotype changes. Although the exact role of HvYSL5 remains to be examined, our results suggest that it is involved in the transient storage of Fe or phytosiderophores.

DOI： 10.1093/pcp/pcr009

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Isolation and functional characterization of an influx silicon transporter in two pumpkin cultivars contrasting in silicon accumulation

Namiki Mitani, Naoki Yamaji, Yukiko Ago, Kozo Iwasaki, Jian Feng Ma

PLANT JOURNAL   66 ( 2 )   231 - 240   2011.4

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P>A high accumulation of silicon (Si) is required for overcoming abiotic and biotic stresses, but the molecular mechanisms of Si uptake, especially in dicotyledonous species, is poorly understood. Herein, we report the identification of an influx transporter of Si in two Cucurbita moschata (pumpkin) cultivars greatly differing in Si accumulation, which are used for the rootstocks of bloom and bloomless Cucumis sativus (cucumber), respectively. Heterogeneous expression in both Xenopus oocytes and rice mutant defective in Si uptake showed that the influx transporter from the bloom pumpkin rootstock can transport Si, whereas that from the bloomless rootstock cannot. Analysis with site-directed mutagenesis showed that, among the two amino acid residues differing between the two types of rootstocks, only changing a proline to a leucine at position 242 results in the loss of Si transport activity. Furthermore, all pumpkin cultivars for bloomless rootstocks tested have this mutation. The transporter is localized in all cells of the roots, and investigation of the subcellular localization with different approaches consistently showed that the influx Si transporter from the bloom pumpkin rootstock was localized at the plasma membrane, whereas the one from the bloomless rootstock was localized at the endoplasmic reticulum. Taken together, our results indicate that the difference in Si uptake between two pumpkin cultivars is probably the result of allelic variation in one amino acid residue of the Si influx transporter, which affects the subcellular localization and subsequent transport of Si from the external solution to the root cells.

DOI： 10.1111/j.1365-313X.2011.04483.x

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Physiological, genetic, and molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan

Daisei Ueno, Emi Koyama, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   62 ( 7 )   2265 - 2272   2011.4

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Cadmium (Cd) in rice is a major source of Cd intake for people on a staple rice diet. The mechanisms underlying Cd accumulation in rice plant are still poorly understood. Here, we characterized the physiology and genetics of Cd transport in a high-Cd-accumulating cultivar (Jarjan) of rice (Oryza sativa). Jarjan showed 5- to 34-fold higher Cd accumulation in the shoots and grains than the cultivar Nipponbare, when it was grown in either a non-Cd-contaminated or a Cd-contaminated soil. A short-term uptake experiment showed no significant difference in Cd uptake by the roots between the two cultivars. However, Jarjan translocated 49% of the total Cd taken up to the shoots, whereas Nipponbare retained most of the Cd in the roots. In both concentration- and time-dependent experiments, Jarjan showed a superior capacity for root-to-shoot translocation of Cd. These results indicate that the high-Cd-accumulation phenotype in Jarjan results from efficient translocation of Cd from roots to shoots. Genetic analysis using an F(2) population derived from Jarjan and Nipponbare revealed that plants showing high- and low-Cd-accumulation phenotypes segregated in a 1:3 ratio, indicating that high accumulation in Jarjan is controlled by a single recessive gene. Furthermore, we isolated OsHMA3, a gene encoding a tonoplast-localized Cd transporter from Jarjan. The OsHMA3 protein was localized in all roots cells, but the sequence has a mutation leading to loss of function. Therefore, failure to sequester Cd into the root vacuoles by OsHMA3 is probably responsible for high Cd accumulation in Jarjan.

DOI： 10.1093/jxb/erq383

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Further characterization of an aluminum influx transporter in rice

Jixing Xia, Naoki Yamaji, Jian Feng Ma

Plant Signaling and Behavior   6 ( 1 )   160 - 163   2011.1

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Nrat1 is a plasma membrane-localized aluminum transporter recently identified in rice, which is a member of Nramp family. Here, we further characterized this transporter in terms of transport substrate specificity. Heterologous assay in yeast showed that Al transport activity by Nrat1 was unaffected by the presence of high concentration of Ca, but significantly inhibited by trivalent ions including Yb and Ga, analogs of Al. Knockout of Nrat1 did not affect the uptake of Cd and Mn in rice. On the other hand, over expression of Nrat1 led to enhanced Al uptake by rice roots compared with wild-type rice, but did not affect Cd uptake. These results provide further evidence that unlike other Nramp members, Nrat1 is an influx transporter for trivalent Al ion. © 2011 Landes Bioscience.

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Further characterization of a rice Si efflux transporter, Lsi2.

Yamaji, N, Ma, J. F

Soil Science and Plant Nutrition   57   259 - 264   2011

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DOI： 10.1080/00380768.2011.565480

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Silicon efflux transporters isolated from two pumpkin cultivars contrasting in Si uptake

Namiki Mitani-Ueno, Naoki Yamaji, Jian Feng Ma

Plant Signaling and Behavior   6 ( 7 )   73 - 76   2011

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The accumulation of silicon (Si) differs greatly with plant species and cultivars due to different ability of the roots to take up Si. In Si accumulating plants such as rice, barley and maize, Si uptake is mediated by the influx (Lsi1) and efflux (Lsi2) transporters. Here we report isolation and functional analysis of two Si efflux transporters (CmLsi2-1 and CmLsi2-2) from two pumpkin (Cucurbita moschata Duch.) cultivars contrasting in Si uptake. These cultivars are used for rootstocks of bloom and bloomless cucumber, respectively. Different from mutations in the Si influx transporter CmLsi1, there was no difference in the sequence of either CmLsi2 between two cultivars. Both CmLsi2-1 and CmLsi2-2 showed an efflux transport activity for Si and they were expressed in both the roots and shoots. These results confirm our previous finding that mutation in CmLsi1, but not in CmLsi2-1 and CmLsi2-2 are responsible for bloomless phenotype resulting from low Si uptake. © 2011 Landes Bioscience.

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Plasma membrane-localized transporter for aluminum in rice

Jixing Xia, Naoki Yamaji, Tomonari Kasai, Jian Feng Ma

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   107 ( 43 )   18381 - 18385   2010.10

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATL ACAD SCIENCES  

Aluminum (Al) is the most abundant metal in the Earth's crust, but its trivalent ionic form is highly toxic to all organisms at low concentrations. How Al enters cells has not been elucidated in any organisms. Herein, we report a transporter, Nrat1 (Nramp aluminum transporter 1), specific for trivalent Al ion in rice. Nrat1 belongs to the Nramp (natural resistance-associated macrophage protein) family, but shares a low similarity with other Nramp members. When expressed in yeast, Nrat1 transports trivalent Al ion, but not other divalent ions, such as manganese, iron, and cadmium, or the Al-citrate complex. Nrat1 is localized at the plasma membranes of all cells of root tips except epidermal cells. Knockout of Nrat1 resulted in decreased Al uptake, increased Al binding to cell wall, and enhanced Al sensitivity, but did not affect the tolerance to other metals. Expression of Nrat1 is up-regulated by Al in the roots and regulated by a C2H2 zinc finger transcription factor (ART1). We therefore concluded that Nrat1 is a plasma membrane-localized transporter for trivalent Al, which is required for a prior step of final Al detoxification through sequestration of Al into vacuoles.

DOI： 10.1073/pnas.1004949107

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Gene limiting cadmium accumulation in rice

Daisei Ueno, Naoki Yamaji, Izumi Kono, Chao Feng Huang, Tsuyu Ando, Masahiro Yano, Jian Feng Ma

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   107 ( 38 )   16500 - 16505   2010.9

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Intake of toxic cadmium (Cd) from rice caused Itai-itai disease in the past and it is still a threat for human health. Therefore, control of the accumulation of Cd from soil is an important food-safety issue, but the molecular mechanism for the control is unknown. Herein, we report a gene (OsHMA3) responsible for low Cd accumulation in rice that was isolated from a mapping population derived from a cross between a high and low Cd-accumulating cultivar. The gene encodes a transporter belonging to the P(1B)-type ATPase family, but shares low similarity with other members. Heterologous expression in yeast showed that the transporter from the low-Cd cultivar is functional, but the transporter from the high-Cd cultivar had lost its function, probably because of the single amino acid mutation. The transporter is mainly expressed in the tonoplast of root cells at a similar level in both the low and high Cd-accumulating cultivars. Overexpression of the functional gene from the low Cd-accumulating cultivar selectively decreased accumulation of Cd, but not other micronutrients in the grain. Our results indicated that OsHMA3 from the low Cd-accumulating cultivar limits translocation of Cd from the roots to the above-ground tissues by selectively sequestrating Cd into the root vacuoles.

DOI： 10.1073/pnas.1005396107

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Involvement of Silicon Influx Transporter OsNIP2;1 in Selenite Uptake in Rice

Xue Qiang Zhao, Namiki Mitani, Naoki Yamaji, Ren Fang Shen, Jian Feng Ma

PLANT PHYSIOLOGY   153 ( 4 )   1871 - 1877   2010.8

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Rice (Oryza sativa) as a staple food, provides a major source of dietary selenium (Se) for humans, which essentially requires Se, however, the molecular mechanism for Se uptake is still poorly understood. Herein, we show evidence that the uptake of selenite, a main bioavailable form of Se in paddy soils, is mediated by a silicon (Si) influx transporter Lsi1 (OsNIP2;1) in rice. Defect of OsNIP2;1 resulted in a significant decrease in the Se concentration of the shoots and xylem sap when selenite was given. However, there was no difference in the Se concentration between the wild-type rice and mutant of OsNIP2;1 when selenate was supplied. A short-term uptake experiment showed that selenite uptake greatly increased with decreasing pH in the external solution. Si as silicic acid did not inhibit the Se uptake from selenite in both rice and yeast (Saccharomyces cerevisiae) at low pHs. Expression of OsNIP2;1 in yeast enhanced the selenite uptake at pH 3.5 and 5.5 but not at pH 7.5. On the other hand, defect of Si efflux transporter Lsi2 did not affect the uptake of Se either from selenite or selenate. Taken together, our results indicate that Si influx transporter OsNIP2;1 is permeable to selenite.

DOI： 10.1104/pp.110.157867

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Knockout of a Bacterial-Type ATP-Binding Cassette Transporter Gene, AtSTAR1, Results in Increased Aluminum Sensitivity in Arabidopsis

Chao-Feng Huang, Naoki Yamaji, Jian Feng Ma

PLANT PHYSIOLOGY   153 ( 4 )   1669 - 1677   2010.8

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ATP-binding cassette (ABC) transporters represent a large family in plants, but the functions of most of these transporters are unknown. Here we report a gene, AtSTAR1, only encoding an ATP-binding domain of a bacterial-type ABC transporter in Arabidopsis (Arabidopsis thaliana). AtSTAR1 is an ortholog of rice (Oryza sativa) OsSTAR1, which has been implicated in aluminum (Al) tolerance. Knockout of AtSTAR1 resulted in increased sensitivity to Al and earlier flowering. Unlike OsSTAR1, AtSTAR1 was expressed in both the roots and shoots and its expression was not induced by Al or other stresses. Investigation of tissue-specific localization of AtSTAR1 through beta-glucuronidase fusion revealed that AtSTAR1 was predominantly expressed at outer cell layers of root tips and developing leaves, whose localization is also different from those of OsSTAR1. However, introduction of OsSTAR1 into atstar1 mutant rescued the sensitivity of atstar1 to Al, indicating that AtSTAR1 has a similar function as OsSTAR1. Furthermore, we found that AtSTAR1 may interact with ALS3, a transmembrane-binding domain in Arabidopsis to form a complex because introduction of OsSTAR1, a functional substitute of AtSTAR1, into als3 mutant resulted in the loss of OsSTAR1 protein. All these findings indicate that AtSTAR1 is involved in the basic detoxification of Al in Arabidopsis.

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Silicon enhances growth independent of silica deposition in a low-silica rice mutant, lsi1

Mami Isa, Shuqin Bai, Takushi Yokoyama, Jian Feng Ma, Yushi Ishibashi, Takashi Yuasa, Mari Iwaya-Inoue

PLANT AND SOIL   331 ( 1-2 )   361 - 375   2010.6

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To examine whether silica bodies are essential for silicon-enhanced growth of rice seedlings, we investigated the response of rice, Oryza sativa L., to silicon treatment. Silicic acid treatment markedly enhanced the SPAD (soil plant analytical development) values of leaf blades and the growth and development of leaves and lateral roots in cvs. Hinohikari and Oochikara, and a low-silicon mutant, lsi1. Combination of ethanol-benzene displacement and staining with crystal violet lactone enabled more detailed histochemical analysis to visualize silica bodies in the epidermis under bright-field microscopy. Supply of silicon induced the development of motor cells and silica bodies in epidermal cells in Hinohikari and Oochikara but not or marginal in lsi1. X-ray analytical microscopy detected silicon specifically in the leaf sheath, the outermost part of the stem, and the leaf blade midrib, suggesting that silicon is distributed to tissues involved in maintaining rigidity of the plant to prevent lodging, rather than being passively deposited in growing tissues. Silicon supplied at high dose accumulated in all rice seedlings and enhanced growth and SPAD values with or without silica body formation. Silicon accumulated in the cell wall may play an important physiological role different from that played by the silica deposited in the motor cell and silica bodies.

DOI： 10.1007/s11104-009-0258-9

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Understanding how plants cope with acid soils

Jian Feng Ma, Peter R. Ryan

FUNCTIONAL PLANT BIOLOGY   37 ( 4 )   III - VI   2010

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Supplying food and fuel to meet the demands of a growing population is a challenge facing every society. Crop yields will need to increase significantly over the next 40 years to support an extra two billion people by 2050. Acid soils limit plant production around the world but especially in the tropical and sub-tropical latitudes where a large proportion of the population increases are expected to occur. Aluminium toxicity and phosphorus deficiency are two of the major stresses affecting plant growth on acid soils. How plants combat these stresses was a theme at the '7th International Symposium on Plant-Soil Interactions at Low pH', held in Guangzhou in 2009, and the focus of this issue of FPB. We provide an overview of recent progress in the area and introduce a selection of invited papers for this research front on acid soils.

DOI： 10.1071/FPv37n4_FO

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A specific transporter for iron(III)-phytosiderophore in barley roots (vol 46, pg 563, 2006) Reviewed

Murata Y, Ma J. F, Yamaji N, Ueno D, Nomoto K, Iwashita T

Plant Journal   61 ( 1 )   188 - 188   2010

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DOI： 10.1111/j.1365-313X.2009.04036.x

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Silicon Transporters in Higher Plants

Jian Feng Ma

MIPS AND THEIR ROLE IN THE EXCHANGE OF METALLOIDS   679   99 - 110   2010

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Silicon (Si) is the second most abundant element in the Earth's crust and exerts beneficial effects on plant growth and production by alleviating both biotic and abiotic stresses including diseases, pests, lodging, drought and nutrient imbalance. Silicon is taken up by the roots in the form of silicic acid, a noncharged molecule. Recently both influx (Lsi1) and efflux (Lsi2) transporters for silicic acid have been identified in gramineous plants including rice, barley and maize. Lsi1 and its homologs are influx Si transporters, which belong to a Nod26-like major intrinsic protein (NIP) subfamily in the aquaporin protein family. They are responsible for the transport of Si from the external solution to the root cells. On the other hand, Lsi2 and its homologs are efflux Si transporters, belonging to putative anion transporters and are responsible for the transport of Si out of the cells toward the xylem. All influx transporters show polar localization at the distal side. Among efflux transporters, Lsi2 in rice shows polar localization at the proximal side, but that in barley and maize does not show polar localization. The cell-specificity of localization of Si transporters and expression patterns are different between species. Rice Si transporters are also permeable to arsenite.

DOI： 10.1007/978-1-4419-6315-4_8

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Isolation and characterisation of two MATE genes in rye

Kengo Yokosho, Naoki Yamaji, Jian Feng Ma

FUNCTIONAL PLANT BIOLOGY   37 ( 4 )   296 - 303   2010

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Multidrug and toxic compound extrusion (MATE) proteins are widely present in bacteria, fungi, plants and mammals. Recent studies have showed that a group of plant MATE genes encodes citrate transporter, which are involved in the detoxification of aluminium or translocation of iron from the roots to the shoots. In this study, we isolated two homologous genes (ScFRDL1 and ScFRDL2) from this family in rye (Secale cereale L.). ScFRDL1 shared 94.2% identity with HvAACT1, an Al-activated citrate transporter in barley (Hordeum vulgare L.) and ScFRDL2 shared 80.6% identity with OsFRDL2, a putative Al-responsive protein in rice (Oryza sativa L.). Both genes were mainly expressed in the roots, however, they showed different expression patterns. Expression of ScFRDL1 was unaffected by Al treatment, but up-regulated by Fe-deficiency treatment. In contrast, expression of ScFRDL2 was greatly induced by Al but not by Fe deficiency. The Al-induced up-regulation of ScFRDL2 was found in both the root tips and basal roots. Furthermore, the expression pattern of ScFRDL2 was consistent with citrate secretion pattern. Immunostaining showed that ScFRDL1 was localised at all cells in the root tips and central cylinder and endodermis in the basal root. Taken together, our results suggest that ScFRDL1 was involved in efflux of citrate into the xylem for Fe translocation from the roots to the shoots, while ScFRDL2 was involved in Al-activated citrate secretion in rye.

DOI： 10.1071/FP09265

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The role of the rice aquaporin Lsi1 in arsenite efflux from roots

Fang-Jie Zhao, Yukiko Ago, Namiki Mitani, Ren-Ying Li, Yu-Hong Su, Naoki Yamaji, Steve P. McGrath, Jian Feng Ma

NEW PHYTOLOGIST   186 ( 2 )   392 - 399   2010

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When supplied with arsenate (As(V)), plant roots extrude a substantial amount of arsenite (As(III)) to the external medium through as yet unidentified pathways. The rice (Oryza sativa) silicon transporter Lsi1 (OsNIP2;1, an aquaporin channel) is the major entry route of arsenite into rice roots. Whether Lsi1 also mediates arsenite efflux was investigated.Expression of Lsi1 in Xenopus laevis oocytes enhanced arsenite efflux, indicating that Lsi1 facilitates arsenite transport bidirectionally.Arsenite was the predominant arsenic species in arsenate-exposed rice plants. During 24-h exposure to 5 mu M arsenate, rice roots extruded arsenite to the external medium rapidly, accounting for 60-90% of the arsenate uptake. A rice mutant defective in Lsi1 (lsi1) extruded significantly less arsenite than the wild-type rice and, as a result, accumulated more arsenite in the roots. By contrast, Lsi2 mutation had little effect on arsenite efflux to the external medium.We conclude that Lsi1 plays a role in arsenite efflux in rice roots exposed to arsenate. However, this pathway accounts for only 15-20% of the total efflux, suggesting the existence of other efflux transporters.

DOI： 10.1111/j.1469-8137.2010.03192.x

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Identification of a Novel Major Quantitative Trait Locus Controlling Distribution of Cd Between Roots and Shoots in Rice

Daisei Ueno, Emi Koyama, Izumi Kono, Tsuyu Ando, Masahiro Yano, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   50 ( 12 )   2223 - 2233   2009.12

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Accumulation of Cd in rice grain is a serious concern of food safety since rice as a staple food is a major source of Cd intake in Asian countries. However, the mechanisms controlling Cd accumulation in rice are still poorly understood. Herein, we report both physiological and genetic analysis of two rice cultivars contrasting in Cd accumulation, which were screened from a core collection of rice cultivars. The cultivar Anjana Dhan (Indica) accumulated much higher levels of Cd than Nipponbare (Japonica) in the shoots and grains when grown in both soil and solution culture. A short-term uptake experiment (20 min) showed that Cd uptake by Nipponbare was higher than that by Anjana Dhan. However, the concentration of Cd in the shoot and xylem sap was much higher in Anjana Dhan than in Nipponbare. Of the Cd taken up by the roots, <4% was translocated to the shoots in Nipponbare, compared with 10-25% in Anjana Dhan, indicating a higher root-to-shoot translocation of Cd in the latter. A quantitative trait locus (QTL) analysis for Cd accumulation was performed using an F-2 population derived from Anjana Dhan and Nipponbare. A QTL with large effect for Cd accumulation was detected on the short arm of chromosome 7, explaining 85.6 of the phenotypic variance in the shoot Cd concentration of the F-2 population. High accumulation is likely to be controlled by a single recessive gene. A candidate genomic region was defined to <1.9 Mb by means of substitution mapping.

DOI： 10.1093/pcp/pcp160

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Iron for plants and humans

Jian Feng Ma, Hong-Qing Ling

PLANT AND SOIL   325 ( 1-2 )   1 - 3   2009.12

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DOI： 10.1007/s11104-009-0203-y

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A Zinc Finger Transcription Factor ART1 Regulates Multiple Genes Implicated in Aluminum Tolerance in Rice

Naoki Yamaji, Chao Feng Huang, Sakiko Nagao, Masahiro Yano, Yutaka Sato, Yoshiaki Nagamura, Jian Feng Ma

PLANT CELL   21 ( 10 )   3339 - 3349   2009.10

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Aluminum (Al) toxicity is the major limiting factor of crop production on acid soils, but some plant species have evolved ways of detoxifying Al. Here, we report a C2H2-type zinc finger transcription factor ART1 (for Al resistance transcription factor 1), which specifically regulates the expression of genes related to Al tolerance in rice (Oryza sativa). ART1 is constitutively expressed in the root, and the expression level is not affected by Al treatment. ART1 is localized in the nucleus of all root cells. A yeast one-hybrid assay showed that ART1 has a transcriptional activation potential and interacts with the promoter region of STAR1, an important factor in rice Al tolerance. Microarray analysis revealed 31 downstream transcripts regulated by ART1, including STAR1 and 2 and a couple of homologs of Al tolerance genes in other plants. Some of these genes were implicated in both internal and external detoxification of Al at different cellular levels. Our findings shed light on comprehensively understanding how plants detoxify aluminum to survive in an acidic environment.

DOI： 10.1105/tpc.109.070771

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Secretion time of phytosiderophore differs in two perennial grasses and is controlled by temperature

Daisei Ueno, Jian Feng Ma

PLANT AND SOIL   323 ( 1-2 )   335 - 341   2009.10

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Some perennial grasses secrete phytosiderophores from the roots in response to Fe-deficiency. Here, we characterized the pattern of phytosiderophore secretion by Lolium perenne (cv. 'Tove') and Poa pratensis (cv. 'Baron'), which are used to correct iron-deficiency induced chlorosis in fruit trees grown on calcareous soils. Both species showed a distinct diurnal rhythm in phytosiderophore secretion, but the secretion time differed between species; the secretion peak time was about 2 h earlier in L. perenne than in P. pratensis under the same growth conditions. The secretion time was shifted by changing temperature during the collection of phytosiderophores in both L. perenne and P. pratensis. Increasing root-zone temperature resulted in earlier secretion, while lowering the temperature resulted in delayed secretion. Furthermore, this shift of secretion time was achieved by changing the temperature around the root-zone. Shading treatment during the secretion period did not affect the secretion time in either species. These results indicate that the secretion of phytosiderophore is triggered by the temperature around the roots, but not light, in these two perennial grasses.

DOI： 10.1007/s11104-009-9962-8

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A Transporter at the Node Responsible for Intervascular Transfer of Silicon in Rice

Naoki Yamaji, Jian Feng Ma

PLANT CELL   21 ( 9 )   2878 - 2883   2009.9

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The concentration of essential mineral nutrients in the edible portion of plants such as grains may affect the nutritional value of these foods, while concentrations of toxic minerals in the plant are matter of food safety. Minerals taken up by the roots from soils are normally redirected at plant nodes before they are finally transported into developing seeds. However, the molecular mechanisms involved in this process have not been identified so far. Herein, we report on a transporter (Lsi6) responsible for the redirection of a plant nutrient at the node. Lsi6 is a silicon transporter in rice (Oryza sativa), and its expression in node I below the panicles is greatly enhanced when the panicle is completely emerged. Lsi6 is mainly localized at the xylem transfer cells located at the outer boundary region of the enlarged large vascular bundles in node I. Knockout of Lsi6 decreased Si accumulation in the panicles but increased Si accumulation in the flag leaf. These results suggest that Lsi6 is a transporter involved in intervascular transfer (i.e., transfer of silicon from the large vascular bundles coming from the roots to the diffuse vascular bundles connected to the panicles). These findings will be useful for selectively enhancing the accumulation of essential nutrients and reducing toxic minerals in the edible portion of cereals.

DOI： 10.1105/tpc.109.069831

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The Rice Aquaporin Lsi1 Mediates Uptake of Methylated Arsenic Species

Ren-Ying Li, Yukiko Ago, Wen-Ju Liu, Namiki Mitani, Joerg Feldmann, Steve P. McGrath, Jian Feng Ma, Fang-Jie Zhao

PLANT PHYSIOLOGY   150 ( 4 )   2071 - 2080   2009.8

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Pentavalent methylated arsenic (As) species such as monomethylarsonic acid [MMA(V)] and dimethylarsinic acid [DMA(V)] are used as herbicides or pesticides, and can also be synthesized by soil microorganisms or algae through As methylation. The mechanism of MMA(V) and DMA(V) uptake remains unknown. Recent studies have shown that arsenite is taken up by rice (Oryza sativa) roots through two silicon transporters, Lsi1 (the aquaporin NIP2;1) and Lsi2 (an efflux carrier). Here we investigated whether these two transporters also mediate the uptake of MMA(V) and DMA(V). MMA(V) was partly reduced to trivalent MMA(III) in rice roots, but only MMA(V) was translocated to shoots. DMA(V) was stable in plants. The rice lsi1 mutant lost about 80% and 50% of the uptake capacity for MMA(V) and DMA(V), respectively, compared with the wild-type rice, whereas Lsi2 mutation had little effect. The short-term uptake kinetics of MMA(V) can be described by a Michaelis-Menten plus linear model, with the wild type having 3.5-fold higher V-max than the lsi1 mutant. The uptake kinetics of DMA(V) were linear with the slope being 2.8-fold higher in the wild type than the lsi1 mutant. Heterologous expression of Lsi1 in Xenopus laevis oocytes significantly increased the uptake of MMA(V) but not DMA(V), possibly because of a very limited uptake of the latter. Uptake of MMA(V) and DMA(V) by wild-type rice was increased as the pH of the medium decreased, consistent with an increasing proportion of the undissociated species. The results demonstrate that Lsi1 mediates the uptake of undissociated methylated As in rice roots.

DOI： 10.1104/pp.109.140350

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Effects of active silicon uptake by rice on Si-29 fractionation in various plant parts

Jan Reent Koester, Roland Bol, Melanie J. Leng, Adrian G. Parker, Hilary J. Sloane, Jian F. Ma

RAPID COMMUNICATIONS IN MASS SPECTROMETRY   23 ( 16 )   2398 - 2402   2009.8

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：WILEY-BLACKWELL  

Rice (Oryza sativa L.) accumulates large amounts of silicon which improves its growth and health due to enhanced resistance to biotic and abiotic stresses. Silicon uptake and loading to xylem in rice are predominantly active processes performed by transporters encoded by the recently identified genes Lsi1 (Si influx transporter gene) and Lsi2 (Si efflux transporter gene). Silicon deposition in rice during translocation to upper plant tissues is known to discriminate against the heavier isotopes Si-29 and Si-30, resulting in isotope fractionation within the plant. We analyzed straw and husk samples of rice mutants defective in Lsi1, Lsi2 or both for silicon content and delta Si-29 using isotope ratio mass spectrometry (IRMS) and compared these results with those for the corresponding wild-type varieties (WT). The silicon content was higher in husk than in straw. All the mutant rice lines showed clearly lower silicon content than the WT lines (4-23% Si of WT). The delta Si-29 was lower in straw and husk for the uptake defective mutant (lsi1) than for WT, albeit delta Si-29 was 0.3 parts per thousand higher in husk than in straw in both lines. The effect of defective efflux (lsi2) differed for straw and husk with higher delta Si-29 in straw, but lower delta Si-29 in husk while WT showed similar delta Si-29 in both fractions. These initial results show the potential of Si isotopes to enlighten the influence of active uptake on translocation and deposition processes in the plant. Copyright (C) 2009 John Wiley & Sons, Ltd.

DOI： 10.1002/rcm.3971

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Further characterization of ferric-phytosiderophore transporters ZmYS1 and HvYS1 in maize and barley

Daisei Ueno, Naoki Yamaji, Jian Feng Ma

JOURNAL OF EXPERIMENTAL BOTANY   60 ( 12 )   3513 - 3520   2009.8

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Roots of some gramineous plants secrete phytosiderophores in response to iron deficiency and take up Fe as a ferric-phytosiderophore complex through the transporter YS1 (Yellow Stripe 1). Here, this transporter in maize (ZmYS1) and barley (HvYS1) was further characterized and compared in terms of expression pattern, diurnal change, and tissue-type specificity of localization. The expression of HvYS1 was specifically induced by Fe deficiency only in barley roots, and increased with the progress of Fe deficiency, whereas ZmYS1 was expressed in maize in the leaf blades and sheaths, crown, and seminal roots, but not in the hypocotyl. HvYS1 expression was not induced by any other metal deficiency. Furthermore, in maize leaf blades, the expression was higher in the young leaf blades showing severe chlorosis than in the old leaf blades showing no chlorosis. The expression of HvYS1 showed a distinct diurnal rhythm, reaching a maximum before the onset of phytosiderophore secretion. In contrast, ZmYS1 did not show such a rhythm in expression. Immunostaining showed that ZmYS1 was localized in the epidermal cells of both crown and lateral roots, with a polar localization at the distal side of the epidermal cells. In maize leaves, ZmYS1 was localized in mesophyll cells, but not epidermal cells. These differences in gene expression pattern and tissue-type specificity of localization suggest that HvYS1 is only involved in primary Fe acquisition by barley roots, whereas ZmYS1 is involved in both primary Fe acquisition and intracellular transport of iron and other metals in maize.

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Identification and Characterization of Maize and Barley Lsi2-Like Silicon Efflux Transporters Reveals a Distinct Silicon Uptake System from That in Rice

Namiki Mitani, Yukako Chiba, Naoki Yamaji, Jian Feng Ma

PLANT CELL   21 ( 7 )   2133 - 2142   2009.7

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Silicon (Si) uptake has been extensively examined in rice (Oryza sativa), but it is poorly understood in other gramineous crops. We identified Low Silicon Rice 2 (Lsi2)-like Si efflux transporters from two important gramineous crops: maize (Zea mays) and barley (Hordeum vulgare). Both maize and barley Lsi2 expressed in Xenopus laevis oocytes showed Si efflux transport activity. Furthermore, barley Lsi2 was able to recover Si uptake in a rice mutant defective in Si efflux. Maize and barley Lsi2 were only expressed in the roots. Expression of maize and barley Lsi2 was downregulated in response to exogenously applied Si. Moreover, there was a significant positive correlation between the ability of roots to absorb Si and the expression levels of Lsi2 in eight barley cultivars, suggesting that Lsi2 is a key Si transporter in barley. Immunostaining showed that maize and barley Lsi2 localized only at the endodermis, with no polarity. Protein gel blot analysis indicated that maize and barley Lsi2 localized on the plasma membrane. The unique features of maize and barley Si influx and efflux transporters, including their cell-type specificity and the lack of polarity of their localization in Lsi2, indicate that these crops have a different Si uptake system from that in rice.

DOI： 10.1105/tpc.109.067884

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Arsenic transport in plants

Fangjie Zhao, Jian Feng Ma, Steve P. McGrath

COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY A-MOLECULAR & INTEGRATIVE PHYSIOLOGY   153A ( 2 )   S187 - S187   2009.6

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DOI： 10.1016/j.cbpa.2009.04.411

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Mitigation of Arsenic Accumulation in Rice with Water Management and Silicon Fertilization

R. Y. Li, J. L. Stroud, J. F. Ma, S. P. McGrath, F. J. Zhao

ENVIRONMENTAL SCIENCE & TECHNOLOGY   43 ( 10 )   3778 - 3783   2009.5

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Rice represents a major route of As exposure in populations that depend on a rice diet. Practical measures are needed to mitigate the problem of excessive As accumulation in paddy rice. Two potential mitigation methods, management of the water regime and Si fertilization, were investigated under greenhouse conditions. Growing rice aerobically during the entire rice growth duration resulted in the leastAS accumulation. Maintaining aerobic conditions during either vegetative or reproductive stage of rice growth also decreased As accumulation in rice straw and grain significantly compared with rice grown under flooded conditions. The effect of water management regimes was consistent with the observed effect of flooding-induced arsenite mobilization in the soil solution. Aerobic treatments increased the percentage of inorganic As in grain, but the concentrations of inorganic As remained lower than in the flooded rice. Silicon fertilization decreased the total As concentration in straw and grain by 78 and 16%, respectively, even though Si addition increased As concentration in the soil solution. Silicon also significantly influenced As speciation in rice grain and husk by enhancing methylation. Silicon decreased the inorganic As concentration in grain by 59% while increasing the concentration of dimethylarsinic acid (DMA) by 33%. There were also significant differences between two rice genotypes in grain As speciation. This study demonstrated that water management, Si fertilization, and selection of rice cultivars are effective measures that can be used to reduce As accumulation in rice.

DOI： 10.1021/es803643v

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A Rice Mutant Sensitive to Al Toxicity is Defective in the Specification of Root Outer Cell Layers

Chao-Feng Huang, Naoki Yamaji, Minoru Nishimura, Shigeyuki Tajima, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   50 ( 5 )   976 - 985   2009.5

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Outer cell layers of rice roots, which comprise epidermis, exodermis and sclerenchyma, have been proposed to protect the roots from various stresses in soil. Here, we report a mutant which is defective in the specification of outer cell layers, and examined the role of these layers in Al and other metal resistance. Morphological and histochemical observations revealed that the mutant isolated based on Al sensitivity frequently showed a disordered pattern of periclinal cell division in the epidermal layers at a region close to the root apical meristem. The lateral root caps in the mutant became difficult to peel off from the epidermis, and epidermal cells became smaller and irregular with far fewer root hairs. Furthermore, some exodermal cells were transformed into additional sclerenchyma cells. However, there was no difference in the inner cell layers between the wild-type rice and the mutant. The mutant showed similar root growth to the wild-type rice in the absence of Al, but greater inhibition of root elongation by Al was found in the mutant. Morin staining showed that Al penetrated into the inner cortical cells in the mutant. Furthermore, the mutant was also sensitive to other metals including Cd and La. Taken together, our results indicate that root outer cell layers protect the roots against the toxicity of Al and other metals by preventing metal penetration into the inner cells. Genetic analysis showed that the mutant phenotypes were controlled by a single recessive gene, which was located on the short arm of rice chromosome 2.

DOI： 10.1093/pcp/pcp050

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HvLsi1 is a silicon influx transporter in barley

Yukako Chiba, Namiki Mitani, Naoki Yamaji, Jian Feng Ma

PLANT JOURNAL   57 ( 5 )   810 - 818   2009.3

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Most plants accumulate silicon in their bodies, and this is thought to be important for resistance against biotic and abiotic stresses; however, the molecular mechanisms for Si uptake and accumulation are poorly understood. Here, we describe an Si influx transporter, HvLsi1, in barley. This protein is homologous to rice influx transporter OsLsi1 with 81% identity, and belongs to a Nod26-like major intrinsic protein sub-family of aquaporins. Heterologous expression in both Xenopus laevis oocytes and a rice mutant defective in Si uptake showed that HvLsi1 has transport activity for silicic acid. Expression of HvLsi1 was detected specifically in the basal root, and the expression level was not affected by Si supply. There was a weak correlation between Si uptake and the expression level of HvLsi1 in eight cultivars tested. In the seminal roots, HvLsi1 is localized on the plasma membrane on the distal side of epidermal and cortical cells. HvLsi1 is also located in lateral roots on the plasma membrane of hypodermal cells. These cell-type specificity of localization and expression patterns of HvLsi1 are different from those of OsLsi1. These observations indicate that HvLsi1 is a silicon influx transporter that is involved in radial transport of Si through the epidermal and cortical layers of the basal roots of barley.

DOI： 10.1111/j.1365-313X.2008.03728.x

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A Bacterial-Type ABC Transporter Is Involved in Aluminum Tolerance in Rice

Chao Feng Huang, Naoki Yamaji, Namiki Mitani, Masahiro Yano, Yoshiaki Nagamura, Jian Feng Ma

PLANT CELL   21 ( 2 )   655 - 667   2009.2

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Aluminum (Al) toxicity is a major factor limiting crop production in acidic soil, but the molecular mechanisms of Al tolerance are poorly understood. Here, we report that two genes, STAR1 (for sensitive to Al rhizotoxicity1) and STAR2, are responsible for Al tolerance in rice. STAR1 encodes a nucleotide binding domain, while STAR2 encodes a transmembrane domain, of a bacterial-type ATP binding cassette (ABC) transporter. Disruption of either gene resulted in hypersensitivity to aluminum toxicity. Both STAR1 and STAR2 are expressed mainly in the roots and are specifically induced by Al exposure. Expression in onion epidermal cells, rice protoplasts, and yeast showed that STAR1 interacts with STAR2 to form a complex that localizes to the vesicle membranes of all root cells, except for those in the epidermal layer of the mature zone. When expressed together in Xenopus laevis oocytes, STAR1/2 shows efflux transport activity specific for UDP-glucose. Furthermore, addition of exogenous UDP-glucose rescued root growth in the star1 mutant exposed to Al. These results indicate that STAR1 and STAR2 form a complex that functions as an ABC transporter, which is required for detoxification of Al in rice. The ABC transporter transports UDP-glucose, which may be used to modify the cell wall.

DOI： 10.1105/tpc.108.064543

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OsFRDL1 Is a Citrate Transporter Required for Efficient Translocation of Iron in Rice

Kengo Yokosho, Naoki Yamaji, Daisei Ueno, Namiki Mitani, Jian Feng Ma

PLANT PHYSIOLOGY   149 ( 1 )   297 - 305   2009.1

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Multidrug and toxic compound extrusion (MATE) transporters represent a large family in plants, but their functions are poorly understood. Here, we report the function of a rice (Oryza sativa) MATE gene (Os03g0216700, OsFRDL1), the closest homolog of barley (Hordeum vulgare) HvAACT1 (aluminum [Al]-activated citrate transporter 1), in terms of metal stress (iron [Fe] deficiency and Al toxicity). This gene was mainly expressed in the roots and the expression level was not affected by either Fe deficiency or Al toxicity. Knockout of this gene resulted in leaf chlorosis, lower leaf Fe concentration, higher accumulation of zinc and manganese concentration in the leaves, and precipitation of Fe in the root's stele. The concentration of citrate and ferric iron in the xylem sap was lower in the knockout line compared to the wild-type rice. Heterologous expression of OsFRDL1 in Xenopus oocytes showed transport activity for citrate. Immunostaining showed that OsFRDL1 was localized at the pericycle cells of the roots. On the other hand, there was no difference in the Al-induced secretion of citrate from the roots between the knockout line and the wild-type rice. Taken together, our results indicate that OsFRDL1 is a citrate transporter localized at the pericycle cells, which is necessary for efficient translocation of Fe to the shoot as a Fe-citrate complex.

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NIP1;1, an Aquaporin Homolog, Determines the Arsenite Sensitivity of Arabidopsis thaliana

Takehiro Kamiya, Mayuki Tanaka, Namiki Mitani, Jian Feng Ma, Masayoshi Maeshima, Toru Fujiwara

JOURNAL OF BIOLOGICAL CHEMISTRY   284 ( 4 )   2114 - 2120   2009.1

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Arsenite [As(III)] is highly toxic to organisms, including plants. Very recently, transporters in rice responsible for As(III) transport have been described (Ma, J. F., Yamaji, N., Mitani, N., Xu, X. Y., Su, Y. H., McGrath, S. P., and Zhao, F. J. (2008) Proc. Natl. Acad. Sci. U. S. A. 105, 9931-9935), but little is known about As(III) tolerance. In this study, three independent As(III)-tolerant mutants were isolated from ethyl methanesulfonate-mutagenized M2 seeds of Arabidopsis thaliana. All three mutants carried independent mutations in Nodulin 26-like intrinsic protein 1;1 (NIP1;1), a homolog of an aquaporin. Two independent transgenic lines carrying T-DNA in NIP1; 1 were highly tolerant to As(III), establishing that NIP1;1 is the causal gene of As(III) tolerance. Because an aquaglyceroporin is able to transport As(III), we measured As(III) transport activity. When expressed in Xenopus oocytes, NIP1; 1 was capable of transporting As(III). As content in the mutant plants was 30% lower than in wild-type plants. Promoter beta-glucuronidase and real-time PCR analysis showed that NIP1; 1 is highly expressed in roots, and GFP-NIP1;1 is localized to the plasma membrane. These data show that NIP1; 1 is involved in As(III) uptake into roots and that disruption of NIP1; 1 function confers As(III) tolerance to plants. NIP1;2 and NIP5;1, closely related homologs of NIP1;1, were also permeable to As(III). Although the disruption of these genes reduced the As content in plants, As(III) tolerance was not observed in nip1;2 and nip5;1 mutants. This indicates that As(III) tolerance cannot be simply explained by decreased As contents in plants.

DOI： 10.1074/jbc.M806881200

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Defective Active Silicon Uptake Affects Some Components of Rice Resistance to Brown Spot

Leandro J. Dallagnol, Fabricio A. Rodrigues, Mateus V. B. Mielli, Jian F. Ma, Lawrence E. Datnoff

PHYTOPATHOLOGY   99 ( 1 )   116 - 121   2009.1

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Rice is known to accumulate high amounts of silicon (Si) in plant tissue, which helps to decrease the intensity of many economically important rice diseases. Among these diseases, brown spot, caused by the fungus Bipolaris oryzae, is one of the most devastating because it negatively affects yield and grain quality. This study aimed to evaluate the importance of active root Si uptake in rice for controlling brown spot development. Some components of host resistance were evaluated in a rice mutant, low silicon 1 (lsi1), defective in active Si uptake, and its wild-type counterpart (cv. Oochikara). Plants were inoculated with B. oryzae after growing for 35 days in a hydroponic culture amended with 0 or 2 mMol Si. The components of host resistance evaluated were incubation period (IP), relative infection efficiency (RIE), area under brown spot progress curve (AUBSPC), final lesion size (FLS), rate of lesion expansion (r), and area under lesion expansion progress curve (AULEPC). Si content from both Oochikara and lsi1 in the +Si treatment increased in leaf tissue by 219 and 178%, respectively, over the nonamended controls. Plants from Oochikara had 112% more Si in leaf tissue than plants from lsi1. The IP of brown spot from Oochikara increased approximate to 6 h in the presence of Si and the RIE, AUBSPC, FLS, r, and AULEPC were significantly reduced by 65, 75, 33, 36, and 35%, respectively. In the presence of Si, the IP increased 3 h for lsi1 but the RIE, AUBSPC, FLS, r, and AULEPC were reduced by only 40, 50, 12, 21, and 12%, respectively. The correlation between Si leaf content and IP was significantly positive but Si content was negatively correlated with RIE, AUBSPC, FLS, r, and AULEPC. Single degree-of-freedom contrasts showed that Oochikara and lsi1 supplied with Si were significantly different from those not supplied with Si for all components of resistance evaluated. This result showed that a reduced Si content in tissues of plants from lsi1 dramatically affected its basal level of resistance to brown spot, suggesting that a minimum Si concentration is needed. Consequently, the results of this study emphasized the importance of an active root Si uptake system for an increase in rice resistance to brown spot.

DOI： 10.1094/PHYTO-99-1-0116

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Identification of Maize Silicon Influx Transporters

Namiki Mitani, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   50 ( 1 )   5 - 12   2009.1

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Maize (Zea mays L.) shows a high accumulation of silicon (Si), but transporters involved in the uptake and distribution have not been identified. In the present study, we isolated two genes (ZmLsi1 and ZmLsi6), which are homologous to rice influx Si transporter OsLsi1. Heterologous expression in Xenopus laevis oocytes showed that both ZmLsi1 and ZmLsi6 are permeable to silicic acid. ZmLsi1 was mainly expressed in the roots. By contrast, ZmLsi6 was expressed more in the leaf sheaths and blades. Different from OsLsi1, the expression level of both ZmLsi1 and ZmLsi6 was unaffected by Si supply. Immunostaining showed that ZmLsi1 was localized on the plasma membrane of the distal side of root epidermal and hypodermal cells in the seminal and crown roots, and also in cortex cells in lateral roots. In the shoots, ZmLsi6 was found in the xylem parenchyma cells that are adjacent to the vessels in both leaf sheaths and leaf blades. ZmLsi6 in the leaf sheaths and blades also exhibited polar localization on the side facing towards the vessel. Taken together, it can be concluded that ZmLsi1 is an influx transporter of Si, which is responsible for the transport of Si from the external solution to the root cells and that ZmLsi6 mainly functions as a Si transporter for xylem unloading.

DOI： 10.1093/pcp/pcn110

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Arsenic uptake and metabolism in plants

F. J. Zhao, J. F. Ma, A. A. Meharg, S. P. McGrath

NEW PHYTOLOGIST   181 ( 4 )   777 - 794   2009

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Arsenic (As) is an element that is nonessential for and toxic to plants. Arsenic contamination in the environment occurs in many regions, and, depending on environmental factors, its accumulation in food crops may pose a health risk to humans. Recent progress in understanding the mechanisms of As uptake and metabolism in plants is reviewed here. Arsenate is taken up by phosphate transporters. A number of the aquaporin nodulin26-like intrinsic proteins (NIPs) are able to transport arsenite, the predominant form of As in reducing environments. In rice (Oryza sativa), arsenite uptake shares the highly efficient silicon (Si) pathway of entry to root cells and efflux towards the xylem. In root cells arsenate is rapidly reduced to arsenite, which is effluxed to the external medium, complexed by thiol peptides or translocated to shoots. One type of arsenate reductase has been identified, but its in planta functions remain to be investigated. Some fern species in the Pteridaceae family are able to hyperaccumulate As in above-ground tissues. Hyperaccumulation appears to involve enhanced arsenate uptake, decreased arsenite-thiol complexation and arsenite efflux to the external medium, greatly enhanced xylem translocation of arsenite, and vacuolar sequestration of arsenite in fronds. Current knowledge gaps and future research directions are also identified.

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A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa)

D. Ueno, I. Kono, K. Yokosho, T. Ando, M. Yano, J. F. Ma

NEW PHYTOLOGIST   182 ( 3 )   644 - 653   2009

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：WILEY-BLACKWELL PUBLISHING, INC  

The trait of low cadmium (Cd) accumulation in brown rice (Oryza sativa) is important for food safety. An effective way to reduce Cd accumulation in the grain is to control Cd transfer from the roots to the shoots.
Here, we investigated genotypic variation in the shoot Cd concentration among 146 accessions from a rice core collection and performed a quantitative trait locus (QTL) analysis to determine the loci controlling shoot Cd accumulation. Furthermore, we physiologically characterized the two accessions used for QTL analysis.
Large genotypic variation (13-fold) in the shoot Cd concentration was found. A major QTL was detected on chromosome 11 using a F(2) population derived from Badari Dhan (a high-Cd accession) and Shwe War (a low-Cd accession). This QTL explained 16.1% of the phenotypic variation in Cd accumulation. Furthermore, this QTL was confirmed by analysis of advanced progeny. Physiological studies showed that Badari Dhan and Shwe War did not differ in uptake of Cd by the roots, but differed greatly in the translocation of Cd from the roots to the shoots.
Taken together, our findings suggest that the major QTL detected is responsible for the translocation of Cd from the roots to the shoots.
New Phytologist (2009) 182: 644-653doi: 10.1111/j.1469-8137.2009.02784.x.

DOI： 10.1111/j.1469-8137.2009.02784.x

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Differential gene expression of rice in response to silicon and rice blast fungus Magnaporthe oryzae

A. M. Brunings, L. E. Datnoff, J. F. Ma, N. Mitani, Y. Nagamura, B. Rathinasabapathi, M. Kirst

ANNALS OF APPLIED BIOLOGY   155 ( 2 )   161 - 170   2009

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Silicon increases the resistance of rice (Oryza sativa) to the rice blast pathogen Magnaporthe oryzae. This study described the relationship between silicon and M. oryzae in terms of whole-genome gene expression. By assessing gene expression patterns in the rice cultivar Monko-to using microarray technology, the physiological basis for silicon-induced resistance was investigated. Silicon amendment resulted in the differential regulation of 221 genes in rice without being challenged with the pathogen. This means that silicon had an observable effect on rice metabolism, as opposed to playing a simple passive role in the resistance response of rice. Compared with control plants, silicon-amended rice differentially regulated 60% less genes, implying that silicon affects the rice response to rice blast infection at a transcriptional level.

DOI： 10.1111/j.1744-7348.2009.00347.x

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Specific transporter for iron(III)-phytosiderophore complex involved in iron uptake by barley roots

Yoshiko Murata, Emiko Harada, Kenji Sugase, Kosuke Namba, Manabu Horikawa, Jian Feng Ma, Naoki Yamaji, Daisei Ueno, Kyosuke Nomoto, Takashi Iwashita, Shoichi Kusumoto

PURE AND APPLIED CHEMISTRY   80 ( 12 )   2689 - 2697   2008.12

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：INT UNION PURE APPLIED CHEMISTRY  

Iron (Fe) is an essential element for plant growth. Gramineous plants have generally developed a distinct strategy to efficiently acquire insoluble Fe, which is characterized by the synthesis and secretion of an Fe-chelating substance, phytosiderophore (PS) such as mugineic acid (MA), and by a specific uptake system for Fe(III)-PS complexes. In a previous study, we identified a gene specifically encoding an Fe(III)-PS transporter (HvYS1) in barley. This gene as well as the encoded protein is specifically expressed in the epidermal cells of the roots, and gene expression is greatly enhanced under Fe-deficient conditions. The localization and substrate specificity of HvYS1 indicate that it is a Fe(III)-PS specific transporter in barley roots. In contrast, ZmYS1, which has been reported as ail Fe-PS transporter from maize, possesses broad substrate specificity despite a high homology with HvYS1. By assessing the transport activity of a series of HvYS1-ZmYS1 chimeras, we revealed that the outer membrane loop between the 6(th) and 7(th) transmembrane regions is essential for the substrate specificity. We also achieved an efficient short-step synthesis of MA and 2'-deoxymugineic acid (DMA). Our new synthetic method enabled us to use them in a large quantity for biological studies.

DOI： 10.1351/pac200880122689

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Functions and transport of silicon in plants

J. F. Ma, N. Yamaji

CELLULAR AND MOLECULAR LIFE SCIENCES   65 ( 19 )   3049 - 3057   2008.10

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Silicon exerts beneficial effects on plant growth and production by alleviating both biotic and abiotic stresses including diseases, pests, lodging, drought, and nutrient imbalance. Recently, two genes (Lsi1 and Lsi2) encoding Si transporters have been identified from rice. Lsi1 (low silicon 1) belongs to a Nod26-like major intrinsic protein subfamily in aquaporin, while Lsi2 encodes a putative anion transporter. Lsi1 is localized on the distal side of both exodermis and endodermis in rice roots, while Lsi2 is localized on the proximal side of the same cells. Lsi1 shows influx transport activity for Si, while Lsi2 shows efflux transport activity. Therefore, Lsi1 is responsible for transport of Si from the external solution to the root cells, whereas Lsi2 is an efflux transporter responsible for the transport of Si from the root cells to the apoplast. Coupling of Lsi1 with Lsi2 is required for efficient uptake of Si in rice.

DOI： 10.1007/s00018-008-7580-x

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Transporters of arsenite in rice and their role in arsenic accumulation in rice grain

Jian Feng Ma, Naoki Yamaji, Namiki Mitani, Xiao-Yan Xu, Yu-Hong Su, Steve P. McGrath, Fang-Jie Zhao

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA   105 ( 29 )   9931 - 9935   2008.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATL ACAD SCIENCES  

Arsenic poisoning affects millions of people worldwide. Human arsenic intake from rice consumption can be substantial because rice is particularly efficient in assimilating arsenic from paddy soils, although the mechanism has not been elucidated. Here we report that two different types of transporters mediate transport of arsenite, the predominant form of arsenic in paddy soil, from the external medium to the xylem. Transporters belonging to the NIP subfamily of aquaporins in rice are permeable to arsenite but not to arsenate. Mutation in OsNIP2;1 (Lsi1, a silicon influx transporter) significantly decreases arsenite uptake. Furthermore, in the rice mutants defective in the silicon efflux transporter Lsi2, arsenite transport to the xylem and accumulation in shoots and grain decreased greatly. Mutation in Lsi2 had a much greater impact on arsenic accumulation in shoots and grain in field-grown rice than Lsi1. Arsenite transport in rice roots therefore shares the same highly efficient pathway as silicon, which explains why rice is efficient in arsenic accumulation. Our results provide insight into the uptake mechanism of arsenite in rice and strategies for reducing arsenic accumulation in grain for enhanced food safety.

DOI： 10.1073/pnas.0802361105

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Characterization of substrate specificity of a rice silicon transporter, Lsi1

Namiki Mitani, Naoki Yamaji, Jian Feng Ma

PFLUGERS ARCHIV-EUROPEAN JOURNAL OF PHYSIOLOGY   456 ( 4 )   679 - 686   2008.7

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Language：English   Publisher：SPRINGER HEIDELBERG  

Lsi1 (OsNIP2;1) is the first silicon (silicic acid) transporter identified in plant, which belongs to the nodulin 26-like intrinsic membrane protein (NIP) subfamily. In this study, we characterized the function of this transporter by using the Xenopus laevis oocyte expression system. The transport activity of Lsi1 for silicic acid was significantly inhibited by HgCl2 but not by low temperature. Lsi1 also showed an efflux transport activity for silicic acid. The substrate specificity study showed that Lsi1 was able to transport urea and boric acid; however, the transport activity for silicic acid was not affected by the presence of equimolar urea and was decreased only slightly by boric acid. Furthermore, among the NIPs subgroup, OsNIP2;2 showed transport activity for silicic acid, whereas OsNIP1;1 and OsNIP3;1 did not. We propose that Lsi1 and its close homologues form a unique subgroup of NIP with a distinct ar/R selectivity filter, which is located in the narrowest region on the extra-membrane mouth and govern the substrate specificity of the pore.

DOI： 10.1007/s00424-007-0408-y

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Transcriptome analysis of the silicon-Magnaporthe grisea interaction

A. M. Brunings, L. E. Datnoff, J. F. Ma, N. Mitani, Y. Nagamura, B. Rathinasabapathi

PHYTOPATHOLOGY   98 ( 6 )   S28 - S28   2008.6

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Reexamination of silicon effects on rice growth and production under field conditions using a low silicon mutant

Kazunori Tamai, Jian Feng Ma

PLANT AND SOIL   307 ( 1-2 )   21 - 27   2008.6

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Silicon (Si) is a beneficial element for healthy growth and high and sustainable production of rice, but the mode of action of the beneficial effects has not been well understood. We carried out field trials for four years at two different locations to re-examine the effects of Si on the growth and production of rice using a low silicon rice (lsi1) mutant. The mutant accumulated much lower Si at each growth stage compared with the wild-type rice (Oryza sativa L. cv Oochikara), but there was no difference in the accumulation of other nutrients including N, P, and K. Measurements at different growth stages showed that low Si in the mutant hardly affected the tiller number, chlorophyll content (SPAD value), and root growth. The plant height and shoot dry weight of the wild-type rice were slightly higher than those of the mutant at a later growth stage, but the difference was not significant between the two lines. However, grain yield was reduced by 79-98%, depending on year, due to a low Si accumulation in the mutant, which showed the largest effect of Si on rice production among all studies reported so far. Among the yield components, the percentage of filled spikelets was mostly affected, being only 13.9% of the wild-type rice in the mutant. The grain color of the mutant became brown because of excessive transpiration and infection of pathogens. These results indicate that Si increases rice yield mainly by enhancing the fertility of spikelets.

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A transporter regulating silicon distribution in rice shoots

Naoki Yamaji, Namiki Mitatni, Jian Feng Ma

PLANT CELL   20 ( 5 )   1381 - 1389   2008.5

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Rice (Oryza sativa) accumulates very high concentrations of silicon (Si) in the shoots, and the deposition of Si as amorphous silica helps plants to overcome biotic and abiotic stresses. Here, we describe a transporter, Lsi6, which is involved in the distribution of Si in the shoots. Lsi6 belongs to the nodulin-26 intrinsic protein III subgroup of aquaporins and is permeable to silicic acid. Lsi6 is expressed in the leaf sheath and leaf blades as well as in the root tips. Cellular localization studies revealed that Lsi6 is found in the xylem parenchyma cells of the leaf sheath and leaf blades. Moreover, Lsi6 showed polar localization at the side facing toward the vessel. Knockdown of Lsi6 did not affect the uptake of Si by the roots but resulted in disordered deposition of silica in the shoots and increased excretion of Si in the guttation fluid. These results indicate that Lsi6 is a transporter responsible for the transport of Si out of the xylem and subsequently affects the distribution of Si in the leaf.

DOI： 10.1105/tpc.108.059311

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Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri

Daisei Ueno, Takashi Iwashita, Fang-Jie Zhao, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   49 ( 4 )   540 - 548   2008.4

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Arabidopsis halleriis a Cd hyperaccumulator; however, the mechanisms involved in the root to shoot translocation of Cd are not well understood. In this study, we characterized Cd transfer from the root medium to xylem in this species. Arabidopsis halleri accumulated 1,500 mg kg(1) Cd in the shoot without growth inhibition. A time-course experiment showed that the release of Cd into the xylem was very rapid; by 2 h exposure to Cd, Cd concentration in the xylem sap was 5-fold higher than that in the external solution. The concentration of Cd in the xylem sap increased linearly with increasing Cd concentration in the external solution. Cd transfer to the xylem was completely inhibited by the metabolic inhibitor carbonyl cyanide 3-chlorophenylhydrazone (CCCP). Cd concentration in the xylem sap was decreased by increasing the concentration of external Zn, but enhanced by Fe deficiency treatment. Analysis with (113)Cd-nuclear magnetic resonance (NMR) showed that the chemical shift of (113)Cd in the xylem sap was the same as that of Cd(NO(3))(2). Metal speciation with Geochem-PC also showed that Cd occurred mainly in the free ionic form in the xylem sap. These results suggest that Cd transfer from the root medium to the xylem in A. halleri is an energy-dependent process that is partly shared with Zn and/or Fe transport. Furthermore, Cd is translocated from roots to shoots in inorganic forms.

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Secretion of malate and citrate from roots is related to high Al-resistance in Lespedeza bicolor

Xiao Ying Dong, Ren Fang Shen, Rong Fu Chen, Zhao Liang Zhu, Jian Feng Ma

PLANT AND SOIL   306 ( 1-2 )   139 - 147   2008.4

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：SPRINGER  

Lespedeza bicolor (Lespedeza bicolor Turcz. cv. Jiangxi) is a leguminous shrub that is well adapted to acid infertile soils. However, the mechanisms of aluminum resistance in this species have not been established. This study aimed to assess the possible resistance mechanisms of this plant to Al. An Al-sensitive species of Lespedeza, sericea lespedeza [Lespedeza cuneata (Dum.-Cours.) G. Don cv. Zhejiang], was used as a reference. The roots of L. bicolor secreted both malate and citrate after exposure to Al, but roots of L. cuneata did not. The secretion of organic acids from L. bicolor was specific to Al; neither 15-day P starvation nor 50 mu M lanthanum induced the secretion of these organic acid anions. Secretion of organic acid anions in L. bicolor was detected after 3-6 h exposure to Al, and the amount increased significantly after 6 h exposure, suggesting that this plant shows a pattern II-type organic acid secretion. This is supported by the finding that the secretion was significantly inhibited by a protein-synthesis inhibitor, cycloheximide. Two kinds of anion-channel inhibitors had different effects on Al-induced secretion of organic acids: 9-anthracene carboxylic acid completely inhibited secretion, phenylglyoxal had no effect. Root elongation in L. bicolor was more severely inhibited by Al in the presence of 9-anthracene carboxylic acid. All these results indicated that the secretion of malate and citrate is a specialized response to Al stress in L. bicolor roots, which might be one of the Al-resistance mechanisms in this species.

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Uptake of Silicon in Different Plant Species

Jian Feng Ma

Handbook of Biomineralization: Biological Aspects and Structure Formation   1   113 - 124   2008.3

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Silicon (Si) is the second most abundant element in soil, and has a wide array of functions in the growth and development of plants. Silicon is able to alleviate various stresses including diseases, pests, lodging, drought, and nutrient imbalance. Although all plants contain some Si in their tissues, the concentrations of Si in the shoots differ greatly with plant species, and this difference is attributed to the capacity of the roots to take up Si. At least two steps are involved in Si uptake, including radial transport from external solution to the root cells, and subsequent release from the root cells to the xylem. Currently, the latter process seems more important for high Si accumulation. The first gene encoding Si transporter has recently been identified in rice, a typical Si-accumulating plant. The transporter encoded by this gene shows a high specificity for Si, and is localized at the distal side of both exodermis and endodermis. The future cloning of more genes will help in our understanding of the molecular mechanisms of Si uptake in different plant species. © 2007 WILEY-VCH Verlag GmbH & Co. KGaA.

DOI： 10.1002/9783527619443.ch7

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Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox

J. P. Xing, R. F. Jiang, D. Ueno, J. F. Ma, H. Schat, S. P. McGrath, F. J. Zhao

NEW PHYTOLOGIST   178 ( 2 )   315 - 325   2008

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：BLACKWELL PUBLISHING  

Efficient root-to-shoot translocation is a key trait of the zinc/cadmium hyperaccumulators Thlaspi caerulescens and Thlaspi praecox, but the extent of variation among different accessions and the underlying mechanisms remain unclear.
Root-to-shoot translocation of Cd and Zn and apoplastic bypass flow were determined in 10 accessions of T. caerulescens and one of T. praecox, using radiolabels Cd-109 and Zn-65. Two contrasting accessions (Pr and Ga) of T. caerulescens were further characterized for TcHMA4 expression and metal compartmentation in roots.
Root-to-shoot translocation of Cd-109 and Zn-65 after 1 d exposure varied 4.4 to 5-fold among the 11 accessions, with a significant correlation between the two metals, but no significant correlation with uptake or the apoplastic bypass flow. The F-2 progeny from a cross between accessions from Prayon, Belgium (Pr) and Ganges, France (Ga) showed a continuous phenotype pattern and transgression. There was no significant difference in the TcHMA4 expression in roots between Pr and Ga. Compartmentation analysis showed a higher percentage of Cd-109 sequestered in the root vacuoles of Ga than Pr, the former being less efficient in translocation than the latter.
Substantial natural variation exists in the root-to-shoot translocation of Cd and Zn, and root vacuolar sequestration may be an important factor related to this variation.

DOI： 10.1111/j.1469-8137.2008.02376.x

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The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminium tolerance in rice

Y. Xue, L. Jiang, N. Su, J. K. Wang, P. Deng, J. F. Ma, H. Q. Zhai, J. M. Wan

PLANTA   227 ( 1 )   255 - 262   2007.12

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Aluminium (Al) toxicity is a primary cause of low rice productivity in acid soils. We have mapped a number of quantitative-trait loci (QTL) controlling Al tolerance in a recombinant inbred line population derived from a cross between the tolerant japonica cultivar Asominori and the sensitive indica cultivar IR24. Tolerance was assessed on the basis of relative root elongation. QTL were detected on chromosomes 1, 9, and 11, with the percentages of phenotypic variance explained ranging from 13.5 to 17.7%. Alleles from Asominori at all three QTL were associated with increased Al tolerance. qRRE-9 is expressed both in the genetic background of IR24 and in an Asominori/IR24-mixed background. qRRE-9 was reduced to the single recessive Mendelian factor Alt-9. High-resolution genetic and physical maps were constructed for Alt-9 in a BC3F2 population of 1,043 individuals. Alt-9 maps between RM24702 and ID47-2 on chromosome 9, and co-segregates with RM5765.

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Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in Rice

Longjun Cheng, Fang Wang, Huixia Shou, Fangliang Huang, Luqing Zheng, Fei He, Jinhui Li, Fang-Jie Zhao, Daisei Ueno, Jian Feng Ma, Ping Wu

PLANT PHYSIOLOGY   145 ( 4 )   1647 - 1657   2007.12

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Higher plants acquire iron (Fe) from the rhizosphere through two strategies. Strategy II, employed by graminaceous plants, involves secretion of phytosiderophores (eg. deoxymugineic acid in rice [Oryza sativa]) by roots to solubilize Fe(III) in soil. In addition to taking up Fe in the form of Fe(III)-phytosiderophore, rice also possesses the strategy I-like system that may absorb Fe(II) directly. Through mutant screening, we isolated a rice mutant that could not grow with Fe(III)-citrate as the sole Fe source, but was able to grow when Fe(II)-EDTA was supplied. Surprisingly, the mutant accumulated more Fe and other divalent metals in roots and shoots than the wild type when both were supplied with EDTA-Fe(II) or grown under waterlogged field conditions. Furthermore, the mutant had a significantly higher concentration of Fe in both unpolished and polished grains than the wild type. Using the map-based cloning method, we identified a point mutation in a gene encoding nicotianamine aminotransferase (NAAT1), which was responsible for the mutant phenotype. Because of the loss of function of NAAT1, the mutant failed to produce deoxymugineic acid and could not absorb Fe(III) efficiently. In contrast, nicotianamine, the substrate for NAAT1, accumulated markedly in roots and shoots of the mutant. Microarray analysis showed that the expression of a number of the genes involved in Fe(II) acquisition was greatly stimulated in the naat1 mutant. Our results demonstrate that disruption of deoxymugineic acid biosynthesis can stimulate Fe(II) acquisition and increase iron accumulation in rice.

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Silicon transporters in rice

Jian Feng Ma, Naoki Yamaji, Namiki Mitani

Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme   52 ( 14 )   1849 - 1856   2007.11

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Genotypic difference in silicon uptake and expression of silicon transporter genes in rice

Jian Feng Ma, Naoki Yamaji, Kazunori Tamai, Namiki Mitani

PLANT PHYSIOLOGY   145 ( 3 )   919 - 924   2007.11

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Rice (Oryza sativa) is a highly silicon (Si)-accumulating species that shows genotypic differences in Si accumulation. We investigated the physiological and molecular mechanisms involved in the genotypic difference in Si uptake between the japonica var. Nipponbare and the indica var. Kasalath. Both the Si concentration in the shoot and the Si uptake per root dry weight were higher in Nipponbare than in Kasalath grown in either soil or nutrient solution. The Si uptake by a single root was also higher in Nipponbare than in Kasalath. A kinetics study showed that Nipponbare and Kasalath had a similar K-m value, whereas the V-max was higher in Nipponbare. The expression of two Si transporter genes (Low silicon rice 1 [Lsi1] and Lsi2) investigated using real-time reverse transcription polymerase chain reaction revealed higher expression of both genes in Nipponbare than in Kasalath. Immunostaining with Lsi1 and Lsi2 antibodies revealed a similar pattern of subcellular localization of these two Si transporters in both varieties; Lsi1 and Lsi2 were localized at the distal and proximal sides, respectively, of both exodermis and endodermis of the roots. These results revealed that the genotypic difference in the Si accumulation results from the difference in abundance of Si transporters in rice roots.

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An aluminum-activated citrate transporter in barley

Jun Furukawa, Naoki Yamaji, Hua Wang, Namiki Mitani, Yoshiko Murata, Kazuhiro Sato, Maki Katsuhara, Kazuyoshi Takeda, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   48 ( 8 )   1081 - 1091   2007.8

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Soluble ionic aluminum (Al) inhibits root growth and reduces crop production on acid soils. Al-resistant cultivars of barley (Hordeum vulgare L.) detoxify Al by secreting citrate from the roots, but the responsible gene has not been identified yet. Here, we identified a gene (HvAACT1) responsible for the Al-activated citrate secretion by fine mapping combined with microarray analysis, using an Al-resistant cultivar, Murasakimochi, and an Al-sensitive cultivar, Morex. This gene belongs to the multidrug and toxic compound extrusion (MATE) family and was constitutively expressed mainly in the roots of the Al-resistant barley cultivar. Heterologous expression of HvAACTI in Xenopus oocytes showed efflux activity for 14 C-labeled citrate, but not for malate. Twoelectrode voltage clamp analysis also showed transport activity of citrate in the HvAACT1-expressing oocytes in the presence of Al. Overexpression of this gene in tobacco enhanced citrate secretion and Al resistance compared with the wild-type plants. Transiently expressed green fluorescent protein-tagged HvAACT1 was localized at the plasma membrane of the onion epidermal cells, and immunostaining showed that HvAACT1 was localized in the epidermal cells of the barley root tips. A good correlation was found between the expression of HvAACT1 and citrate secretion in 10 barley cultivars differing in Al resistance. Taken together, our results demonstrate that HvAACT1 is an Al-activated citrate transporter responsible for Al resistance in barley.

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An efflux transporter of silicon in rice

Jian Feng Ma, Naoki Yamaji, Namiki Mitani, Kazunori Tamai, Saeko Konishi, Toru Fujiwara, Maki Katsuhara, Masahiro Yano

NATURE   448 ( 7150 )   209 - U12   2007.7

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Silicon is an important nutrient for the optimal growth and sustainable production of rice(1-4). Rice accumulates up to 10% silicon in the shoot, and this high accumulation is required to protect the plant from multiple abiotic and biotic stresses(1-5). A gene, Lsi1, that encodes a silicon influx transporter has been identified in rice(6). Here we describe a previously uncharacterized gene, low silicon rice 2 (Lsi2), which has no similarity to Lsi1. This gene is constitutively expressed in the roots. The protein encoded by this gene is localized, like Lsi1, on the plasma membrane of cells in both the exodermis and the endodermis, but in contrast to Lsi1, which is localized on the distal side, Lsi2 is localized on the proximal side of the same cells. Expression of Lsi2 in Xenopus oocytes did not result in influx transport activity for silicon, but preloading of the oocytes with silicon resulted in a release of silicon, indicating that Lsi2 is a silicon efflux transporter. The identification of this silicon transporter revealed a unique mechanism of nutrient transport in plants: having an influx transporter on one side and an efflux transporter on the other side of the cell to permit the effective transcellular transport of the nutrients.

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Sorghum roots are inefficient in uptake of EDTA-chelated lead

Yong Xu, Naoki Yamaji, Renfang Shen, Jian Feng Ma

ANNALS OF BOTANY   99 ( 5 )   869 - 875   2007.5

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Background and Aims Ethylene diamine tetraacetic acid (EDTA)-assisted phytoremediation has been developed to clean up lead (Pb)-contaminated soil; however, the mechanism responsible for the uptake of EDTA-Pb complex is not well understood. In this study, the accumulation process of Pb from EDTA-Pb is characterized in comparison to ionic Pb [Pb(NO3)(2)] in sorghum (Sorghum bicolor).Methods Sorghum seedlings were exposed to a 0.5 mm CaCl2 (pH 5.0) solution containing 0, 1 mm Pb(NO3)(2) or EDTA-Pb complexes at a molar ratio of 1:0.5, 1:1, 1:2 and 1:4 (Pb:EDTA). The root elongation of sorghum at different ratios of Pb:EDTA was measured. Xylem sap was collected after the stem was severed at different times. The concentration of Pb in the shoots and roots were determined by an atomic absorption spectrometer. In addition, the roots were stained with Fluostain I for observation of the root structure.Key Results Lead accumulation in the shoots of the plants exposed to EDTA-Pb at 1:1 ratio was only one-fifth of that exposed to ionic Pb at the same concentration. Lead accumulation decreased when transpiration was suppressed. The concentration of Pb in the xylem sap from the EDTA-Pb-treated plants was about 1/25 000 of that in the external solution. Root elongation was severely inhibited by ionic Pb, but not by EDTA-Pb at a 1:1 ratio. Root staining showed that a physiological barrier was damaged in the roots exposed to ionic Pb, but not in the roots exposed to EDTA-Pb.Conclusions All these results suggest that sorghum roots are inefficient in uptake of EDTA-chelated Pb and that enhanced Pb accumulation from ionic Pb was attributed to the damaged structure of the roots.

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Spatial distribution and temporal variation of the rice silicon transporter Lsi1

Naoki Yamaji, Jian Feng Ma

PLANT PHYSIOLOGY   143 ( 3 )   1306 - 1313   2007.3

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Rice (Oryza sativa) is a typical silicon (Si) accumulator and requires a large amount of Si for high-yield production. Recently, a gene (Low silicon rice1 [Lsi1]) encoding a Si transporter was identified in rice roots. Here, we characterized Lsi1 in terms of spatial distribution and temporal variation using both physiological and molecular approaches. Results from a multicompartment transport box experiment showed that the major site for Si uptake was located at the basal zone (> 10 mm from the root tip) of the roots rather than at the root tips (< 10 mm from the root tip). Consistent with the Si uptake pattern, Lsi1 expression and distribution of the Lsi1 protein were found only in the basal zone of roots. In the basal zones of the seminal, crown, and lateral roots, the Lsi1 protein showed a polar localization at the distal side of both the exodermis and endodermis, where the Casparian bands are formed. This indicates that Lsi1 is required for the transport of Si through the cells of the exodermis and endodermis. Expression of Lsi1 displayed a distinct diurnal pattern. Furthermore, expression was transiently enhanced around the heading stage, which coincides with a high Si requirement during this growth stage. Expression was down-regulated by dehydration stress and abscisic acid, suggesting that expression of Lsi1 may be regulated by abscisic acid.

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Phytoremediation of Pb contaminated soil with polymer-coated EDTA

Masaru Shibata, Takayuki Konno, Ryo Akaike, Yong Xu, Renfang Shen, Jian Feng Ma

PLANT AND SOIL   290 ( 1-2 )   201 - 208   2007.1

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EDTA-assisted phytoextraction of lead (Pb) has been developed, but concerns have arisen due to the possibility of leaching of both Pb and EDTA to ground water caused by uncontrolled release. We developed five types of controlled-release EDTA (polymer-coated EDTA) by coating the EDTA with a polyolefin polymer. A test of the release rate showed that the duration for the release of 75% of total EDTA ranged from 3 to 210 days. A pot experiment was conducted to compare the effect of these polymer-coated EDTA and non-coated EDTA on the concentrations of Pb and EDTA in soil solution, and Pb accumulation in sorghum (Sorghum bicolor L. cv. EARLY SUMAC) in a Pb-contaminated soil. One of the polymer-coated EDTAs, C-EDTA-4, with a release period of 80 days proved to be the best in decreasing Pb and EDTA concentrations in soil solution, and increasing Pb accumulation in sorghum shoots compared to the direct application of EDTA. Our results suggest that polymer-coated EDTA has a potential for phytoextraction of Pb with a reduced environmental risk.

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Functional analysis of a rice Al-tolerant gene Als1 Reviewed

Chaofeng Huang, Naoki Yamaji, Masahiro Yano, Jianfeng Ma

PLANT AND CELL PHYSIOLOGY   48   S45 - S45   2007

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DOI： 10.14841/jspp.2007.0.113.0

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Characterization of silicon permeability of NIP in gramineous plants Reviewed

Namiki Mitani, Naoki Yamaji, Maki Katsuhara, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   48   S30 - S30   2007

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Gene expression and functional analysis of a candidate gene related to Al-activated citrate transporter in barley Reviewed

Jun Furukawa, Naoki Yamaji, Hua Wang, Maki Katsuhara, Kazuhiro Sato, Kazuyoshi Takeda, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   48   S44 - S44   2007

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Functional analysis of a rice Si transporter homolog Lsi6. Reviewed

Naoki Yamaji, Namiki Mitani, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   48   S30 - S30   2007

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DOI： 10.14841/jspp.2007.0.054.0

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Further characterization of an Fe-phytosiderophore transporter gene ZmYS 1 in maize Reviewed

Daisei Ueno, Naoki Yamaji, Jian Feng Ma

PLANT AND CELL PHYSIOLOGY   48   S29 - S29   2007

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Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants

Jian Feng Ma

SURVEY OF CELL BIOLOGY   264   225 - +   2007

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Aluminum (Al) is the most abundant metal in the earth's crust, while its soluble ionic form (Al3+) shows phytotoxicity, which is characterized by a rapid inhibition of root elongation. Aluminum targets multiple cellular sites by binding, resulting in disrupted structure and/or functions of the cell wait, plasma membrane, signal transduction pathway, and Ca homeostasis. On the other hand, some plant species have evolved mechanisms to cope with At toxicity both externally and internally. The well-documented mechanisms for external detoxification of At include the release of organic acid anions from roots and alkalination of the rhizosphere. Genes encoding transporters for Al-induced secretion of organic acid anions have been identified and characterized. Recent studies show that ABC transporters are involved in At resistance. The internal detoxification of Al in Al-accumulating plants is achieved by the formation of nontoxic Al complexes with organic acids or other chelators and sequestration of these complexes in the vacuoles. In some plant species, Al shows beneficial effects on plant growth under particular conditions, although the exact mechanisms for these effects are unknown.

DOI： 10.1016/S0074-7696(07)64005-4

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Identification of two novel phytosiderophores secreted by perennial grasses

D. Ueno, A. D. Rombola, T. Iwashita, K. Nomoto, J. F. Ma

NEW PHYTOLOGIST   174 ( 2 )   304 - 310   2007

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It has been suggested that some perennial grasses secrete phytosiderophores in response to iron (Fe) deficiency, but the compounds have not been identified. Here, we identified and characterized the phytosiderophores secreted by two perennial grasses, Lolium perenne cv. Tove and Poa pratensis cv. Baron.
Root exudates were collected from the roots of Fe-deficient grasses and then purified with various chromatographies. The structure of the purified compounds was determined using both nuclear magnetic resonance and fast atom bombardment mass spectrometry.
Both species secreted phytosiderophores in response to Fe deficiency, and the amount of phytosiderophores secreted increased with the development of Fe deficiency. The type of phytosiderophores secreted differed with plant species; L. perenne cv. Tove secreted 3-epihydroxy-2'-deoxymugineic acid (epiHDMA), 2'-deoxymugineic acid (DMA) and an unknown compound, whereas P. pratensis cv. Baron secreted DMA, avenic acid A (AVA) and an unknown compound.
Purification and subsequent analysis with nuclear magnetic resonance and mass led to identification of the two novel phytosiderophores; 3-hydroxy-2'-deoxymugineic acid (HDMA) from L. perenne, and 2'-hydroxyavenic acid A (HAVA) from P. pratensis. Both novel phytosiderophores have similar chelating activity to known phytosiderophores.

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Strategies of plants to adapt to mineral stresses in problem soils

Syuntaro Hiradate, Jian Feng Ma, Hideaki Matsumoto

ADVANCES IN AGRONOMY, VOL 96   96   65 - 132   2007

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Mineral imbalance in high-input agricultural ecosystems has become an acute concern in many developed countries. Relapse into low-input agricultural ecosystems, however, will cause mineral stresses to crops, resulting in reduced food productions. Under such natural soil conditions, some endemic plants can tolerate the mineral stresses because they have evolved to adapt to the stresses. Numerous studies have been conducted to clarify the chemistry of the mineral elements of interest in rhizosphere and to utilize the tolerant mechanisms in plants. In this chapter, the authors reviewed the research progress on molecular scale mechanisms of Fe-deficiency, Al-toxicity, and P-deficiency stresses in soils and their tolerances by plants. In low Fe-availability conditions, two Fe-acquisition mechanisms of plants have been clarified: enhanced Fe dissolution in rhizosphere by secreted proton/reductants/chelators followed by reduction of Fe3+ to Fe2+ and specific uptake of Fe2+ (Strategy I) and Fe dissolution by secreted hexadentate Fe3+-transporting molecule (phytosiderophore) by forming Fe3+-phytosiderophore complex followed by specific uptake of the complex (Strategy II). Two tolerant mechanisms against high Al-toxicity of soils have been reported: exclusion of Al from cytoplasm (exclusion mechanism) and detoxification of Al in plants (internal detoxification mechanism). Phosphorous acquisition mechanisms of plants from low P-availability soils would be (1) alteration of root architecture, (2) secretion of organic acids, (3) secretion of phosphatase, and (4) enhanced expression of P transporter on roots. Some of the molecular mechanisms for the expression of the tolerances and their application to the genetic improvement are also reviewed. © 2007 Elsevier Inc. All rights reserved.

DOI： 10.1016/S0065-2113(07)96004-6

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Studies on Beneficial Effects and Uptake System of Silicon in Rice(JSSSPN Awards)

Ma Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   78 ( 5 )   431 - 434   2007

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DOI： 10.20710/dojo.78.5_431

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Genetic dissection of silicon uptake ability in rice (Oryza sativa L.)

Q. -S. Wu, X. -Y. Wan, N. Su, Z. -J. Cheng, J. -K. Wang, C. -L. Lei, X. Zhang, L. Jiang, J. -F. Ma, J. -M. Wan

PLANT SCIENCE   171 ( 4 )   441 - 448   2006.10

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The adequate presence of silicon (Si) in rice plants can enhance their yield and improve their tolerance to various biotic and abiotic stresses. In this study Si uptake abilities were compared between the japonica rice cultivar (cv.) Kinmaze and the indica rice cv. DV85 under three Si concentrations (0.16, 0.4, and 1.6 mM) at different time points from 1 to 12 h. The results showed that the phenotypic values of two traits-Si uptake by individual plants (SP, Si uptake by all roots of a plant) and Si uptake per unit root dry weight (SR = SP/root dry weight)-of Kinmaze were significantly higher than those of DV85 (P &lt; 0.01). Meanwhile, a kinetic study indicated that the Si transporters in Kinmaze and DV85 had the same affinity for silicic acid, but with different V-max values, indicating that Kinmaze had more Si transporters in the roots than DV85. This may be the main reason for the difference in Si uptake ability between Kinmaze and DV85. In addition, a mapping population consisting of 81 recombinant inbred lines (RILs) derived from the cross between Kinmaze and DV85 was used to detect quantitative trait loci (QTLs) underlying SP and SR. The RILs follow a continuous one-peak distribution and show transgressive segregation in both directions for SP, SR, and root dry weight (RDW). Three QTLs for SP, four for SR, and three for RDW were detected. This can explain 7.16-17.15% of the phenotypic variation (PVE). Thus, the results obtained in this study provide a better understanding of the mechanism of rice Si uptake ability and the basis for fine-mapping the genes involved. (c) 2006 Elsevier Ireland Ltd. All rights reserved.

DOI： 10.1016/j.plantsci.2006.05.001

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QTL analysis of aluminum resistance in rice (Oryza sativa L.)

Y. Xue, J. M. Wan, L. Jiang, L. L. Liu, N. Su, H. Q. Zhai, J. F. Ma

PLANT AND SOIL   287 ( 1-2 )   375 - 383   2006.9

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Aluminum (Al) toxicity is considered as one of the primary causes of low-rice productivity in acid soils. In the present study, quantitative trait loci (QTLs) controlling Al resistance based on relative root elongation (RRE) were dissected using a complete linkage map and a recombinant inbred lines (RILs) derived from a cross of Al-tolerant japonica cultivar Asominori (Oryza sativa L.) and Al sensitive indica cultivar IR24 (O. sativa L.). A total of three QTLs (qRRE-1, qRRE-9, and qRRE-11) were detected on chromosomes 1, 9, and 11 with LOD score ranging from 2.64 to 3.60 and the phenotypic variance explained from 13.5 to 17.7%. The Asominori alleles were all associated with Al resistance at all the three QTLs. The existence of these QTLs was confirmed using Asominori chromosome segment substitution lines (CSSLs) in IR24 genetic background (IAS). By QTL comparative analysis, the two QTLs (qRRE-1 and qRRE-9) on chromosomes 1 and 9 appeared to be consistent among different rice populations while qRRE-11 was newly detected and syntenic with a major Al resistance gene on chromosome 10 of maize. This region may provide an important case for isolating genes responsible for different mechanisms of Al resistance among different cereals. These results also provide the possibilities of enhancing Al resistance in rice breeding program by marker-assisted selection (MAS) and pyramiding QTLs.

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Silicon uptake and accumulation in higher plants

Jian Feng Ma, Naoki Yamaji

TRENDS IN PLANT SCIENCE   11 ( 8 )   392 - 397   2006.8

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Silicon (Si) accumulation differs greatly between plant species because of differences in Si uptake by the roots. Recently, a gene encoding a Si uptake transporter in rice, a typical Si-accumulating plant, was isolated. The beneficial effects of Si are mainly associated with its high deposition in plant tissues, enhancing their strength and rigidity. However, Si might play an active role in enhancing host resistance to plant diseases by stimulating defense reaction mechanisms. Because many plants are not able to accumulate Si at high enough levels to be beneficial, genetically manipulating the Si uptake capacity of the root might help plants to accumulate more Si and, hence, improve their ability to overcome biotic and abiotic stresses.

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Response of rice (Oryza sativa) with root surface iron plaque under aluminium stress

Rong Fu Chen, Ren Fang Shen, Pei Gu, Xiao Ying Dong, Chang Wen Du, Jian Feng Ma

ANNALS OF BOTANY   98 ( 2 )   389 - 395   2006.8

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Background and Aims Rice (Oryza sativa) is an aquatic plant with a characteristic of forming iron plaque on its root surfaces. It is considered to be the most Al-tolerant species among the cereal crops. The objective of this study was to determine the effects of root surface iron plaque on Al translocation, accumulation and the change of physiological responses under Al stress in rice in the presence of iron plaque. 9Methods The japonica variety rice, Koshihikari, was used in this study and was grown hydroponically in a growth chamber. Iron plaque was induced by exposing the rice roots to 30 mg L-1 ferrous iron either as Fe(II)-EDTA in nutrient solution (6 d, Method I) or as FeSO4 in water solution (12 h, Method II). Organic acid in root exudates was retained in the anion-exchange resin and eluted with 2M HCl, then analysed by high-performance liquid chromatography (HPLC) after proper pre-treatment. Fe and Al in iron plaque were extracted with DCB (dithionite-citrate-bicarbonate) solution.Key Results and Conclusions Both methods (I and II) could induce the formation of iron plaque on rice root surfaces. The amounts of DCB-extractable Fe and Al on root surfaces were much higher in the presence of iron plaque than in the absence of iron plaque. Al contents in root tips were significantly decreased with iron plaque; translocation of At from roots to shoots was significantly reduced with iron plaque. Al-induced secretion of citrate was observed and iron plaque could greatly depress this citrate secretion. These results suggested that iron plaque on rice root surfaces can be a sink to sequester Al onto the root surfaces and Fe ions can pre-saturate Al-binding sites in root tips, which protects the rice root tips from suffering Al stress to a certain extent.

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P-157 A SPECIFIC TRANSPORTER OF IRON (III)-PHYTOSIDEROPHORE, MUGINEIC ACID IN BARLEY ROOTS

Murata Yoshiko, Ma Jian Feng, Yamaji Naoki, Ueno Daisei, Nomoto Kyosuke, Iwashita Takashi

International Symposium on the Chemistry of Natural Products   2006   "P - 157"   2006.7

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DOI： 10.24496/intnaturalprod.2006.0__P-157_

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Buckwheat accumulates aluminum in leaves but not in seeds

Ren Fang Shen, Rong Fu Chen, Jian Feng Ma

PLANT AND SOIL   284 ( 1-2 )   265 - 271   2006.6

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Buckwheat (Fagopyrum esculentum Moench. cv Jianxi) is highly resistant to Al stress and is known to be an Al-accumulator. Pot experiments were carried out in a greenhouse to investigate the accumulation of Al in leaves and seeds of buckwheat. Plants were grown for 12 weeks in a strong acid soil amended with or without CaCO3 at a rate of 1 g kg(-1) soil. Old leaves accumulated as much as 10 g kg(-1) Al of dry weight when the plants were grown in the acid soil, while the Al concentrations in leaves immediately adjacent to seeds, seed coats, and embryos were, on average, 4516, 41.2 and 7.7 mg kg(-1) stop, respectively. The Al concentration significantly decreased in leaves when the plants were grown in the limed soil, and the Al concentrations in leaves immediately adjacent to seeds, seed coats, and embryos were, on average, 1586, 21.3 and 3.1 mg kg(-1), respectively. These results show that seeds accumulate much less Al than buckwheat leaves. The underlying mechanisms are discussed.

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A specific transporter for iron(III)-phytosiderophore in barley roots

Y Murata, JF Ma, N Yamaji, D Ueno, K Nomoto, T Iwashita

PLANT JOURNAL   46 ( 4 )   563 - 572   2006.5

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Iron acquisition of graminaceous plants is characterized by the synthesis and secretion of the iron-chelating phytosiderophore, mugineic acid (MA), and by a specific uptake system for iron(III)-phytosiderophore complexes. We identified a gene specifically encoding an iron-phytosiderophore transporter (HvYS1) in barley, which is the most tolerant species to iron deficiency among graminaceous plants. HvYS1 was predicted to encode a polypeptide of 678 amino acids and to have 72.7% identity with ZmYS1, a first protein identified as an iron(III)-phytosiderophore transporter in maize. Real-time RT-PCR analysis showed that the HvYS1 gene was mainly expressed in the roots, and its expression was enhanced under iron deficiency. In situ hybridization analysis of iron-deficient barley roots revealed that the mRNA of HvYS1 was localized in epidermal root cells. Furthermore, immunohistological staining with anti-HvYS1 polyclonal antibody showed the same localization as the mRNA. HvYS1 functionally complemented yeast strains defective in iron uptake on media containing iron(III)-MA, but not iron-nicotianamine (NA). Expression of HvYS1 in Xenopus oocytes showed strict specificity for both metals and ligands: HvYS1 transports only iron(III) chelated with phytosiderophore. The localization and substrate specificity of HvYS1 is different from those of ZmYS1, indicating that HvYS1 is a specific transporter for iron(III)-phytosiderophore involved in primary iron acquisition from soil in barley roots.

DOI： 10.1111/j.1365-313X.2006.02714.x

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Transcriptiomic analysis of gene expression pattern in the root tips of Al-tolerant and -sensitive cultivars of barley Reviewed

J Furukawa, JF Ma, K Sato, K Takeda

PLANT AND CELL PHYSIOLOGY   47   S121 - S121   2006

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Functional analysis of rice gene Lsi2 related to Si uptake Reviewed

N Yamaji, JF Ma

PLANT AND CELL PHYSIOLOGY   47   S61 - S61   2006

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DOI： 10.14841/jspp.2006.0.149.0

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Awarding of the 2nd JSPS Prize and Japan Academy Medal

Ma Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   77 ( 4 )   463 - 464   2006

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DOI： 10.20710/dojo.77.4_463

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Introduction of Third Silicon in Agriculture Conference

Ma Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   77 ( 2 )   243 - 243   2006

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DOI： 10.20710/dojo.77.2_243

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3. Application of Proteomics to the Study of Plant Mineral Stress(Impact of Genomics on the Study of Plant Nutrition)

Furukawa Jun, Ma Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   77 ( 1 )   109 - 114   2006

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Language：Japanese   Publisher：Japanese Society of Soil Science and Plant Nutrition  

DOI： 10.20710/dojo.77.1_109

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Physiological mechanisms of at resistance in higher plants

JF Ma

SOIL SCIENCE AND PLANT NUTRITION   51 ( 5 )   609 - 612   2005.9

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：JAPANESE SOC SOIL SCIENCE PLANT NUTRITION  

Aluminum (Al) ion is toxic to plant growth, while the resistance to Al toxicity varies widely among plant species. Accumulating evidence has shown that organic acids play an important role in both internal and external detoxification of Al. Two patterns of Al-induced secretion of organic acid anions have been characterized in the external detoxification. Involvement of ABA or protein phosphorylation in the activation of anion channel in Pattern I and less contribution of organic acid metabolism in Pattern 11 have been reported. Recently, gene or quantitative trait locus (QTL) for Al-activated secretion of organic acid anions has been identified. Other mechanisms of Al resistance are also reported such as pH increase in the rhizosphere. The formation of a non-toxic Al complex with organic acids or other chelators and sequestering these complexes in the vacuoles play an important role in internal detoxification of Al in Al-accumulating plants.

DOI： 10.1111/j.1747-0765.2005.tb00074.x

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Identification of the form of Cd in the leaves of a superior Cd-accumulating ecotype of Thlaspi caerulescens using Cd-113-NMR

D Ueno, JF Ma, T Iwashita, FJ Zhao, SP McGrath

PLANTA   221 ( 6 )   928 - 936   2005.8

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：SPRINGER  

Thlaspi caerulescens (Ganges ecotype) is a known Cd hyperaccumulator, however, the ligands which coordinate to Cd ions in the leaves have not been identified. In the present study, the chemical form of Cd was investigated by using (113)supercript stopCd-nuclear magnetic resonance (NMR) spectroscopy. Plants were grown hydroponically with a highly enriched (113)supercript stopCd stable isotope. Measurements of (113)supercript stopCd-NMR with intact leaves showed a signal at the chemical shift of around -16 ppm. Crude leaf sap also gave a similar chemical shift. Purification by gel filtration (Sephadex G-10), followed by cationic and anionic exchange chromatography, showed that Cd occurred only in the anionic fraction, which gave the same chemical shift as intact leaves. Further purification of the anionic fraction, combined with (113)supercript stopCd- and (1)supercript stopH-NMR studies, revealed that only the fraction containing malate showed a chemical shift similar to the intact leaves. These results indicate that Cd was coordinated mainly with malate in the leaves of T. caerulescens. The malate concentration in the leaves was not affected by increasing Cd concentration in the solution, suggesting that malate synthesis is not induced by Cd. Because the Cd-malate complex is relatively weak, we suggest that the complex forms inside the vacuoles as a result of an efficient tonoplast transport of Cd and a constitutively high concentration of malate in the vacuoles, and that the formation of the Cd-malate complex may lead to a decrease of subsequent Cd efflux to the cytoplasm.

DOI： 10.1007/s00425-005-1491-y

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Isolation and characterization of a rice mutant hypersensitive to Al

JF Ma, S Nagao, CF Huang, M Nishimura

PLANT AND CELL PHYSIOLOGY   46 ( 7 )   1054 - 1061   2005.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Rice (Oryza sativa L.) is a highly Al-resistant species among small grain crops, but the mechanism responsible for the high Al resistance has not been elucidated. In this study, rice mutants sensitive to Al were isolated from M-3 lines derived from an Al-resistant cultivar, Koshihikari, irradiated with gamma-rays. Relative root elongation was used as a parameter for evaluating Al resistance. After initial screening plus two rounds of confirmatory testing, a mutant (als1) was isolated from a total of 560 lines. This mutant showed a phenotype similar to the wild-type plant in the absence of Al. However, in the presence of 10 mu M Al, root elongation was inhibited 70% in the mutant, but only 8% in the wild-type plant. The mutant also showed poorer root growth in acid soil. The Al content of root apices (0-1 cm) was much lower in the wild-type plant. The sensitivity to other metals including Cd and La did not differ between the mutant and the wild-type plants. A small amount of citrate was secreted from the roots of the mutant in response to Al stress, but there was no difference from that secreted by the wild-type plant. Genetic analysis of F-2 populations between als1 and wild-type plants showed that the Al-resistant seedlings and Al-sensitive seedlings segregated at a 3 : 1 ratio, indicating that the high sensitivity to Al in als1 is controlled by a single recessive gene. The gene was mapped to the long arm of chromosome 6, flanked by InDel markers MaOs0619 and MaOs0615.

DOI： 10.1093/pcp/pci116

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Uptake system of silicon in different plant species

N Mitani, JF Ma

JOURNAL OF EXPERIMENTAL BOTANY   56 ( 414 )   1255 - 1261   2005.4

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

The accumulation of silicon (Si) in the shoots varies considerably among plant species, but the mechanism responsible for this variation is poorly understood. The uptake system of Si was investigated in terms of the radial transport from the external solution to the root cortical cells and the release of Si from the cortical cells to the xylem in rice, cucumber, and tomato, which differ greatly in shoot Si concentration. Symplasmic solutions of the root tips were extracted by centrifugation. The concentrations of Si in the root-cell symplast in all species were higher than that in the external solution, although the concentration in rice was 3- and 5-fold higher than that in cucumber and tomato, respectively. A kinetic study showed that the radial transport of Si was mediated by a transporter with a K-m value of 0.15 mM in all species, but with different V-max values in the order of rice &gt; cucumber &gt; tomato. In the presence of the metabolic inhibitor 2,4-dinitrophenol, and at low temperature, the Si concentration in the root-cell symplast decreased to a level similar to that of the apoplasmic solution. These results suggest that both transporter-mediated transport and passive diffusion of Si are involved in the radial transport of Si and that the transporter-mediated transport is an energy-dependent process. The Si concentration of xylem sap in rice was 20- and 100-fold higher than that in cucumber and tomato, respectively. In contrast to rice, the Si concentration in the xylem sap was lower than that in the external solution in cucumber and tomato. A kinetic study showed that xylem loading of Si was also mediated by a kind of transporter in rice, but by passive diffusion in cucumber and tomato. These results indicate that a higher density of transporter for radial transport and the presence of a transporter for xylem loading are responsible for the high Si accumulation in rice.

DOI： 10.1093/jxb/eri121

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Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens

JF Ma, D Ueno, FJ Zhao, SP McGrath

PLANTA   220 ( 5 )   731 - 736   2005.3

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Thlaspi caerulescens (Ganges ecotype) is able to accumulate large concentrations of cadmium (Cd) and zinc (Zn) in the leaves without showing any toxicity, suggesting a strong internal detoxification. The distribution of Cd and Zn in the leaves was investigated in the present study. Although the Cd and Zn concentrations in the epidermal tissues were 2-fold higher than those of mesophyll tissues, 65-70% of total leaf Cd and Zn were distributed in the mesophyll tissues, suggesting that mesophyll is a major storage site of the two metals in the leaves. To examine the subcellular localisation of Cd and Zn in mesophyll tissues, protoplasts and vacuoles were isolated from plants exposed to 50 muM Cd and Zn hydroponically. Pure protoplasts and vacuoles were obtained based on light-microscopic observation and the activities of marker enzymes of cytosol and vacuoles. Of the total Cd and Zn in the mesophyll tissues, 91% and 77%, respectively, were present in the protoplast, and all Cd and 91% Zn in the protoplast were localised in the vacuoles. Furthermore, about 70% and 86% of total Cd and Zn, respectively, in the leaves were extracted in the cell sap, suggesting that most Cd and Zn in the leaves is present in soluble form. These results indicate that internal detoxification of Cd and Zn in Thlaspi caerulescens leaves is achieved by vacuolar compartmentalisation.

DOI： 10.1007/s00425-004-1392-5

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Identification of the silicon form in xylem sap of rice (Oryza sativa L.)

N Mitani, JF Ma, T Iwashita

PLANT AND CELL PHYSIOLOGY   46 ( 2 )   279 - 283   2005.2

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Rice (Oryza sativa L.) is a typical silicon (Si)-accumulating plant, but the mechanism responsible for the translocation from the root to the shoot is poorly understood. In this study, the form of Si in xylem sap was identified by 2 Si-29-nuclear magnetic resonance (NMR) spectroscopy. In rice (cv. Oochikara) cultured in a monosilicic acid solution containing 0.5 mM Si, the Si concentration in the xylem reached 6 mM,l within 30 min. In the Si-29-NMR spectra of the xylem sap, only one signal was observed at a chemical shift of -72.6 ppm, which is consistent with that of monosilicic acid. A H-1-NMR study of xylem sap did not show any significant difference between the wild-type rice and mutant rice defective in Si uptake, and the components of the xylem sap were not affected by the Si supply. The Si concentration in the xylem sap in vitro decreased from an initial 18 mM to 2.6 mM with time. Addition of xylem sap to a solution containing 8 mM Si did not prevent the polymerization of silicic acid. All these results indicate that Si is translocated in the form of monosilicic acid through the xylem and that the concentration of monosilicic acid is high in the xylem only transiently.

DOI： 10.1093/pcp/pci018

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Isolation and characterization of Lsi1 Reviewed

N Mitani, K Tamai, S Konishi, M Yano, N Yamaji, M Kyo, JF Ma

PLANT AND CELL PHYSIOLOGY   46   S82 - S82   2005

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Language：English   Publisher：OXFORD UNIV PRESS  

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Plant root responses to three abundant soil minerals: Silicon, aluminum and iron

JF Ma

CRITICAL REVIEWS IN PLANT SCIENCES   24 ( 4 )   267 - 281   2005

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Language：English   Publisher：TAYLOR & FRANCIS INC  

Silicon (Si), aluminum (Al), and iron (Fe) are the three most abundant minerals in soil; however, their effects on plants differ because they are beneficial, toxic, and essential to plant growth, respectively. High accumulation of silicon in the shoots helps some plants to overcome a range of biotic and abiotic stresses. However, plants vary in their ability to take up Si from the soil and load it into the xylem and so the accumulation of silicon varies greatly between plant species. Aluminum toxicity is characterized by a rapid inhibition of root elongation but some species and even genotypes within species can tolerate Al toxicity better than others. While the mechanisms controlling this tolerance in most of the more resistant species are poorly understood, some plants are able to detoxify Al externally and/or internally by complexation with ligands or by pH changes in the rhizosphere. Iron is taken up from the soil by two efficient mechanisms called Strategy I and Strategy II, which operate in distinct phylogenic groups. Strategy I plants increase soil Fe solubility by releasing protons and reductants/chelators, such as organic acids and phenolics, into the rhizosphere, while Strategy II plants are characterized by the secretion of ferric chelating substances (phytosiderophores) coupled with a specific Fe3+ :chelate uptake system. In this review, the molecular mechanisms underlying root response to Si, Al, and Fe are described.

DOI： 10.1080/07352680500196017

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Genotypic variation in Fe concentration of barley grain

JF Ma, A Higashitani, K Sato, K Takeda

SOIL SCIENCE AND PLANT NUTRITION   50 ( 7 )   1115 - 1117   2004.12

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：TAYLOR & FRANCIS LTD  

Iron deficiency in humans is the most prevalent micronutrient deficiency worldwide. To screen for high Fe cultivar, genotypic variation in Fe concentration of barley grain was investigated in two collections of barley: 274 standard varieties selected at the Barley Germplasm Center of the Research Institute for Bioresources, Okayama University (SV) and 135 varieties from the Barley Core Collection of Americas (BCCAM). The Fe concentration of barley grain showed large variation, ranging from 24.6 to 63.3 mg kg(-1) in SV, from 21.0 to 83.0 mg kg(-1) in BCCAM barleys. The Fe concentration was not affected by the key characters of barley varieties, kernel row types, and hulled or hull-less. The Fe concentration was also not related to the place of origin of the barley variety. About 90% of total Fe was localized in the grain without hull. These results provide fundamental data for breeding Fe-rich cultivars and for studying the mechanisms involved in genotypic variation in Fe concentration.

DOI： 10.1080/00380768.2004.10408583

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Characterization of the silicon uptake system and molecular mapping of the silicon transporter gene in rice

JF Ma, N Mitani, S Nagao, S Konishi, K Tamai, T Iwashita, M Yano

PLANT PHYSIOLOGY   136 ( 2 )   3284 - 3289   2004.10

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER SOC PLANT BIOLOGISTS  

Rice (Oryza sativa L. cv Oochikara) is a typical silicon-accumulating plant, but the mechanism responsible for the high silicon uptake by the roots is poorly understood. We characterized the silicon uptake system in rice roots by using a low-silicon rice mutant (Isi1) and wild-type rice. A kinetic study showed that the concentration of silicon in the root symplastic solution increased with increasing silicon concentrations in the external solution but saturated at a higher concentration in both lines. There were no differences in the silicon concentration of the symplastic solution between the wild-type rice and the mutant. The form of soluble silicon in the root, xylem, and leaf identified by Si-29-NMR was also the same in the two lines. However, the concentration of silicon in the xylem sap was much higher in the wild type than in the mutant. These results indicate that at least two transporters are involved in silicon transport from the external solution to the xylem and that the low-silicon rice mutant is defective in loading silicon into xylem rather than silicon uptake from external solution to cortical cells. To map the responsible gene, we performed a bulked segregant analysis by using both microsatellite and expressed sequence tag-based PCR markers. As a result, the gene was mapped to chromosome 2, flanked by microsatellite marker RM5303 and expressed sequence tag-based PCR marker E60168.

DOI： 10.1104/pp.104.047365

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Cadmium and zinc accumulation by the hyperaccumulator Thlaspi caerulescens from soils enriched with insoluble metal compounds

D Ueno, FJ Zhao, RF Shen, JF Ma

SOIL SCIENCE AND PLANT NUTRITION   50 ( 4 )   511 - 515   2004.8

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：JAPANESE SOC SOIL SCIENCE PLANT NUTRITION  

Thlaspi caerulescens J. & C. Presl is a hyperaccumulator of both Zn and Cd. A pot experiment was carried out to investigate whether T caerulescens (the Ganges ecotype) could utilize Cd and Zn from insoluble sources. An uncontaminated soil was enriched with either insoluble Cd compounds (CdS or CdCO3), or soluble Cd (CdSO4) at a rate of 56 mg Cd kg(-1) soil. In a separate experiment, soil was enriched with either ZnSO4, Zn-3(PO4)(2), or ZnS at a rate of 100 mg Zn kg(-1). Neither soluble nor insoluble forms of Cd or Zn affected the growth of T caerulescens. The Cd concentration of the shoots of the plants grown on the unenriched soil was 40 mg kg(-1) dry wt., whereas the concentration in the case of the enriched soil reached 2,050 to 2,900 mg kg(-1) dry wt. However, there were no significant differences in the shoot Cd concentration between the treatments with soluble or insoluble Cd compounds, even though the Cd concentration in the soil solution was in the order of CdSO4 much greater thanCdC03 &gt; CdS. T caerulescens grown on the ZnS-enriched soil accumulated up to 6,900 mg kg(-1) Zn in the shoots, although Zn accumulation was 1.5-fold higher with the addition of the more soluble compounds Zn-3(PO4)(2) or ZnSO4. These results indicate that the Ganges ecotype of T caerulescens is able to utilize both insoluble Cd and Zn compounds.

DOI： 10.1080/00380768.2004.10408507

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Interactions between Cd and Zn in relation to their hyperaccumulation in Thlaspi caerulescens

D Ueno, FJ Zhao, JF Ma

SOIL SCIENCE AND PLANT NUTRITION   50 ( 4 )   591 - 597   2004.8

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：JAPANESE SOC SOIL SCIENCE PLANT NUTRITION  

Ganges, an ecotype of Thlaspi caerulescens from southern France accumulates both Zn and Cd to extraordinary levels in the shoots. The interactions between Zn and Cd in this ecotype were investigated using solution culture and pot experiments with soil. Results from both relatively long-term (4 weeks) and short-term (1 week) solution culture experiments indicated that Cd accumulation in the shoots was not affected by the supply of a 4 to 10-fold excess of Zn, whereas the Cd concentration of the roots decreased with increasing Zn concentration in the solution. By contrast, the supply of an equimolar concentration of Cd significantly reduced the Zn concentration in both roots and shoots. However, when 4-fold more Zn than Cd was supplied, Cd-induced decrease in Zn accumulation was not observed. In soil treated with Cd or Zn, addition of one metal increased the metal concentration of the other in the soil solution. However, Zn accumulation by T caerulescens decreased by Cd addition, whereas Cd accumulation was not affected by Zn addition. These results suggested that the Ganges ecotype of T. caerulescens displayed different uptake systems for Cd and Zn, and that Cd competed with Zn uptake while Zn did not compete with Cd uptake.

DOI： 10.1080/00380768.2004.10408516

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Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. International journal

Jian Feng Ma, Sakiko Nagao, Kazuhiro Sato, Hiroyuki Ito, Jun Furukawa, Kazuyoshi Takeda

Journal of experimental botany   55 ( 401 )   1335 - 41   2004.6

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Aluminium (Al) toxicity is an important limitation to barley (Hordeum vulgare L.) on acid soil. Al-resistant cultivars of barley detoxify Al externally by secreting citrate from the roots. To link the genetics and physiology of Al resistance in barley, genes controlling Al resistance and Al-activated secretion of citrate were mapped. An analysis of Al-induced root growth inhibition from 100 F2 seedlings derived from an Al-resistant cultivar (Murasakimochi) and an Al-sensitive cultivar (Morex) showed that a gene associated with Al resistance is localized on chromosome 4H, tightly linked to microsatellite marker Bmag353. Quantitative trait locus (QTL) analysis from 59 F4 seedlings derived from an F3 plant heterozygous at the region of Al resistance on chromosome 4H showed that a gene responsible for the Al-activated secretion of citrate was also tightly linked to microsatellite marker Bmag353. This QTL explained more than 50% of the phenotypic variation in citrate secretion in this population. These results indicate that the gene controlling Al resistance on barley chromosome 4H is identical to that for Al-activated secretion of citrate and that the secretion of citrate is one of the mechanisms of Al resistance in barley. The identification of the microsatellite marker associated with both Al resistance and citrate secretion provides a valuable tool for marker-assisted selection of Al-resistant lines.

DOI： 10.1093/jxb/erh152

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Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses

JF Ma

SOIL SCIENCE AND PLANT NUTRITION   50 ( 1 )   11 - 18   2004.2

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：JAPANESE SOC SOIL SCIENCE PLANT NUTRITION  

Although silicon (Si) has not been recognized as an essential element for plant growth, the beneficial effects of Si have been observed in a wide variety of plant species. The beneficial effects of Si are usually expressed more clearly in Si-accumulating plants under various abiotic and biotic stress conditions. Silicon is effective in controlling various pests and diseases caused by both fungi and bacteria in different plant species. Silicon also exerts alleviative effects on various abiotic stresses including salt stress, metal toxicity, drought stress, radiation damage, nutrient imbalance, high temperature, freezing and so on. These beneficial effects are mainly attributed to the high accumulation of silica on the tissue surface although other mechanisms have also been proposed. To obtain plants resistant to multiple stresses, genetic modification of the root ability to take up Si has been proposed. In this review, the role of Si in conferring resistance to mutiple stresses is described.

DOI： 10.1080/00380768.2004.10408447

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Form of Al changes with Al concentration in leaves of buckwheat

RF Shen, T Iwashita, JF Ma

JOURNAL OF EXPERIMENTAL BOTANY   55 ( 394 )   131 - 136   2004.1

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Buckwheat (Fagopyrum esculentum Moench. cv. Jianxi) is known as an Al-accumulating plant. The process leading to the accumulation of Al in the leaves was investigated, focusing on the chemical form of Al using Al-27-nuclear magnetic resonance. Leaves with different Al concentrations were prepared by growing buckwheat on a very acidic soil (Andosol) amended with or without CaCO3 (1 or 3 g kg(-1) soil). When the Al concentration of the leaves was lower, only one major signal was observed at a chemical shift of 16.1 ppm, which was assigned to an Al-oxalate complex at a 1:3 ratio. However, when the Al concentration of the leaves increased to a high level (e.g. 12 g Al kg(-1)), an additional signal at a chemical shift of 11.2 ppm was observed. This signal was assigned to an Al-citrate complex at a 1:1 ratio. In the leaf with a high Al concentration, both Al-oxalate (1:3) and Al-citrate (1:1) were detected in marginal and middle parts, while only Al-oxalate was detected in the basal part. The oxalate concentration did not differ very much between leaves with low and high Al concentrations at the same position, while citrate concentration significantly increased with increasing Al concentration when the oxalate/Al ratio became lower than 3.0. As the Al-citrate complex has been demonstrated to be the form of transport in the xylem, the results suggest that when internal oxalate is enough to form a complex with Al at a 3:1 ratio in the leaves with a low Al concentration, Al-citrate converts to Al-oxalate. However, this conversion does not occur in the leaves with a very high Al concentration, resulting in the coexistence of both Al-oxalate and Al-citrate complexes.

DOI： 10.1093/jxb/erh016

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Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots

JF Ma, RF Shen, S Nagao, E Tanimoto

PLANT AND CELL PHYSIOLOGY   45 ( 5 )   583 - 589   2004

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

Phytotoxicity of aluminum is characterized by a rapid inhibition of root elongation at micromolar concentrations, however, the mechanisms primarily responsible for this response are not well understood. We investigated the effect of Al on the viscosity and elasticity parameters of root cell wall by a creep-extension analysis in two cultivars of wheat (Triticum aestivum L.) differing in Al resistance. The root elongation and both viscous and elastic extensibility of cell wall of the root apices were hardly affected by the exposure to 10 muM Al in an Al-resistant cultivar, Atlas 66. However, similar exposure rapidly inhibited root elongation in an Al-sensitive cultivar, Scout 66 and this was associated with a time-dependent accumulation of Al in the root tissues with more than 77% residing in the cell wall. Al caused a significant decrease in both the viscous and elastic extensibility of cell wall of the root apices of Scout 66. The "break load" of the root apex of Scout 66 was also decreased by Al. However, neither the viscosity nor elasticity of the cell wall was affected by in vitro Al treatment. Furthermore, pre-treatment of seedlings with Al in conditions where root elongation was slow (i.e. low temperature) did not affect the subsequent elongation of roots in a 0 Al treatment at room temperature. These results suggest that the Al-dependent changes in the cell wall viscosity and elasticity are involved in the inhibition of root growth. Furthermore, for Al to reduce cell wall extensibility it must interact with the cell walls of actively elongating cells.

DOI： 10.1093/pcp/pch060

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Announcement of XV International Plant Nutrition Colloquium

Ma Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   75 ( 4 )   535 - 535   2004

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Language：Japanese   Publisher：Japanese Society of Soil Science and Plant Nutrition  

DOI： 10.20710/dojo.75.4_535

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Recent progress in the research of external Al detoxification in higher plants: a minireview

JF Ma, J Furukawa

JOURNAL OF INORGANIC BIOCHEMISTRY   97 ( 1 )   46 - 51   2003.9

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：ELSEVIER SCIENCE INC  

Aluminum (Al) is highly toxic to plant growth. The toxicity is characterized by rapid inhibition of root elongation. However, some plant species and cultivars have evolved some mechanisms for detoxifying Al both internally and externally. In this review, the recent progress made in the research of external detoxification of Al is described. Accumulating evidence has shown that organic acids play an important role in the detoxification of Al. Some plant species and cultivars respond to Al by secreting citrate, malate or oxalate from the roots. Recently, the anion channel of malate and citrate in the plasma membrane has been characterized and a gene encoding the malate channel has been cloned. The metabolism of organic acids seems to be poorly correlated with the Al-induced secretion of organic acid anions. A number of QTLs (quantitative trait loci) for Al resistance have been identified in rice, Arabidopsis, and other species. Transgenic plants with enhanced resistance to Al have also been reported, but introduction of multiple genes may be required to gain high Al resistance in future. (C) 2003 Published by Elsevier Inc.

DOI： 10.1016/S0162-0134(03)00245-9

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Characterization of phytosiderophore secretion under Fe deficiency stress in Festuca rubra

JF Ma, H Ueno, D Ueno, AD Rombola, T Iwashita

PLANT AND SOIL   256 ( 1 )   131 - 137   2003.9

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：KLUWER ACADEMIC PUBL  

In the present study we investigated the response to iron (Fe) deficiency in two cultivars of Festuca rubra L. (Rubina and Barnica) used in correction of chlorosis of fruit trees cultivated on calcareous soils. We found that a Fe-chelating compound, identified as 2'-deoxymugineic acid (DMA), was secreted from the roots in response to Fe-deficiency in both cultivars. The amount of DMA secreted into solution increased with the development of Fe-deficiency. The secretion showed a distinct diurnal rhythm characterized by a secretion peak at between 2 and 5 hours after sunrise at 20degreesC. However, this secretion peak was delayed by 3 hour at low temperature (&lt; 10&DEG;C) and occurred 3 h earlier at high temperature (30&DEG;C). When water used for the collection of root exudates was pre-warmed (25&DEG;C) or pre-cooled (10&DEG;C), this led to an earlier or a delayed secretion compared to control (15&DEG;C) under the same air temperature, respectively. Short-term shading treatment did not affect the secretion pattern of DMA. These results demonstrate that the secretion time of DMA from the roots is, at least partly controlled by the temperature in the root environment. Overall, these findings suggest that the ability of Festuca rubra to prevent Fe chlorosis symptoms('re-greening effect') of associated fruit trees is partially related to the secretion of DMA which increase Fe availability in calcareous soils.

DOI： 10.1023/A:1026285813248

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Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). International journal

Zhuqing Zhao, Jian Feng Ma, Kazuhiro Sato, Kazuyoshi Takeda

Planta   217 ( 5 )   794 - 800   2003.9

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While barley ( Hordeum vulgare L.) is the most sensitive species to Al toxicity among small-grain crops, variation in Al resistance between cultivars does exist. We examined the mechanism responsible for differential Al resistance in 21 barley varieties. Citrate was secreted from the roots in response to Al stress. A positive correlation between citrate secretion and Al resistance [(root elongation with Al)/(root elongation without Al)] and a negative correlation between citrate secretion and Al content of root apices, were obtained, suggesting that citrate secretion from the root apices plays an important role in excluding Al and thereby detoxifying Al. The Al-induced secretion of citrate was characterized using an Al-resistant variety (Sigurdkorn) and an Al-sensitive variety (Kearney). In Sigurdkorn, Al-induced secretion of citrate occurred within 20 min, and the secretion did not increase with increasing external Al concentration. The Al-induced citrate secretion ceased at low temperature (6 degrees C) and was inhibited by anion-channel inhibitors. Internal citrate content of root apices was increased by Al exposure in Sigurdkorn, but was not affected in Kearney. The activity of citrate synthase was unaffected by Al in both Al-resistant and Al-sensitive varieties. The secretion rate of organic acid anions from barley was the lowest among wheat, rye and triticale.

DOI： 10.1007/s00425-003-1043-2

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Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots

JE Hayes, JF Ma

JOURNAL OF EXPERIMENTAL BOTANY   54 ( 388 )   1753 - 1759   2003.7

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS  

The secretion of organic acid anions from roots has been identified as a mechanism of resistance to Al. However, the process leading to the secretion of organic acid anions is poorly understood. The effect of Al on organic acid metabolism was investigated in two lines of triticale (xTriticosecale Wittmark) differing in Al-induced secretion of malate and citrate and in Al resistance. The site of Al-induced secretion of citrate and malate from a resistant line was localized to the root apices (terminal 5 mm). The levels of citrate (root apices and mature root segments) and malate (mature segments only) in roots increased during exposure to Al, but similar changes were observed in both triticale genotypes. The in vitro activities of four enzymes involved in malate and citrate metabolism (citrate synthase, phosphoenolpyruvate carboxylase, malate dehydrogenase, and NADP-isocitrate dehydrogenase) were similar for sensitive and resistant lines in both root apices and mature root segments. The response of these enzymes to pH did not differ between tolerant and sensitive lines or in the presence and absence of Al. Moreover, cytoplasmic and vacuolar pH were not affected by exposure to Al in either line. Together, these results indicate that the Al-dependent efflux of organic acid anions from the roots of triticale is not regulated by their internal levels in the roots or by the capacity of the root cells to synthesize malate and citrate.

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Characterization of silicon uptake by rice roots

K Tamai, JF Ma

NEW PHYTOLOGIST   158 ( 3 )   431 - 436   2003.6

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Rice (Oryza sativa) is a typical Si-accumulating plant and it has been suggested that it has a specific uptake system for silicic acid in the roots.
Here, we characterized this specific system in rice roots. The ability of rice roots to take up Si was much higher than that of other gramineous species.
A kinetic study indicated that Si uptake was mediated by a type of proteinaceous transporter; the K-m value was estimated to be 0.32 mm, suggesting that the transporter had a low affinity for silicic acid. Si uptake increased linearly with time, but pretreatment with Si did not affect the uptake of Si, suggesting that the system for Si uptake was not inducible. Mercuric chloride and phloretin, significantly inhibited Si uptake, but 4,4'-diisothiocyanato-stilbene-2,2'-disulfonic acid (DIDS) did not. Mercuric chloride and phloretin also inhibited water uptake, but to a lesser extent. Si uptake was unaffected by the presence of boric acid.
Taken together, the data indicate that the uptake of Si by rice roots is a transporter-mediated process and this transporter contains Cys residues but not Lys residues.

DOI： 10.1046/j.1469-8137.2003.00773.x

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Genotypic variation in silicon concentration of barley grain

JF Ma, A Higashitani, K Sato, K Takeda

PLANT AND SOIL   249 ( 2 )   383 - 387   2003.2

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Soluble silicon (Si) in foods and drinks has been suggested to have a protective effect against neurotoxicity of Al. We investigated the genotypic variation in Si concentration of barley grain, which has many uses including in livestock feeds, malts for beer and whisky, and some foods for human consumption. Two collections of barley, grown in the same field, were subjected to analysis; 274 standard varieties selected at the Barley Germplasm Center of the Research Institute for Bioresources, Okayama University (SV), and 135 varieties from the Barley Core Collection of Americans (BCCAM). The Si concentration of barley grain showed large variation, ranging from 0 (under detection) to 3600 mg kg(-1) in SV and from 0 to 3800 mg kg(-1) in BCCAM barleys. The Si concentration was much lower in hull-less barley than in hulled barley. The Si concentration of two-row barley was similar to that of six-row barley, suggesting that Si concentration is not affected by the number of spike rows. Si concentration also did not differ with the origin of the barley variety. More than 80% of total Si was localized in the hull. The Si concentration of the hull was between 15 343 and 27 089 mg kg(-1) in the varieties tested. A close correlation was obtained between the Si concentrations of barley grains harvested in different years, suggesting that the variation in Si concentration of barley grain is controlled genetically. These results provide fundamental data for breeding Si-rich cultivars.

DOI： 10.1023/A:1022842421926

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A rice mutant defective in Si uptake

JF Ma, K Tamai, M Ichii, GF Wu

PLANT PHYSIOLOGY   130 ( 4 )   2111 - 2117   2002.12

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Rice (Oryza sativa) accumulates silicon (Si) in the tops to levels up to 10.0% of shoot dry weight, but the mechanism responsible for high Si uptake by rice roots is not understood. We isolated a rice mutant (GR1) that is defective in active Si uptake by screening M-2 seeds (64,000) of rice cv Oochikara that were treated with 10(-3) M sodium azide for 6 h at 25degreesC. There were no phenotypic differences between wild type (WT) and GR1 except that the leaf blade of GR1 remained droopy when Si was supplied. Uptake experiments showed that Si uptake by GR1 was significantly lower than that by WT at both low and high Si concentrations. However, there was no difference in the uptake of other nutrients such as phosphorus and potassium. Si concentration in the xylem sap of WT was 33-fold that of the external solution, but that of GR1 was 3-fold higher than the external solution at 0.15 mm Si. Si uptake by WT was inhibited by metabolic inhibitors including NaCN and 2,4-dinitrophenol and by low temperature, whereas Si uptake by GR1 was not inhibited by these agents. These results suggest that an active transport system for Si uptake is disrupted in GR1. Analysis of F-2 populations between GR1 and WT showed that roots with high Si uptake and roots with low Si uptake segregated at a 3:1 ratio, suggesting that GR1 is a recessive mutant of Si uptake.

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Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench.

RF Shen, JF Ma, M Kyo, T Iwashita

PLANTA   215 ( 3 )   394 - 398   2002.7

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Buckwheat (Fagopyrum esculentum Moench.) is an Al-accumulating plant, but the internal mechanism(s) of detoxification of Al is not fully understood. We investigated the subcellular localization of Al in the leaves of this plant (cv. Jianxi) by directly isolating protoplasts and vacuoles. Pure protoplasts and vacuoles from the leaves of buckwheat, grown hydroponically in Al solution, were obtained based oil light-microscopic observation and the activities of marker enzymes of cytosol and vacuoles. More than 80% of total Al in the leaves was present in the protoplasts. and was identified as an Al-oxalate complex (1:3 ratio) by 27 Al-nuclear magnetic resonance. Oxalate and Al in the protoplasts was localized in the vacuoles. These results suggest that internal detoxification of Al in the buckwheat leaves is achieved by both complexation with oxalate and sequestration into vacuoles.

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Response of rice to Al stress and identification of quantitative trait loci for Al tolerance

JF Ma, RF Shen, ZQ Zhao, M Wissuwa, Y Takeuchi, T Ebitani, M Yano

PLANT AND CELL PHYSIOLOGY   43 ( 6 )   652 - 659   2002.6

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Rice (Oryza sativa L.) shows the highest tolerance to Al toxicity among small-grain cereal crops, however, the mechanisms and genetics responsible for its high Al tolerance are not yet well understood. We investigated the response of rice to Al stress using the japonica variety Koshihikari in comparison to the indica variety Kasalath. Koshihikari showed higher tolerance at various Al concentrations than Kasalath. The Al content in root apexes was less in Koshihikari than in Kasalath, suggesting that exclusion mechanisms rather than internal detoxification are acting in Koshihikari. Al-induced secretion of citrate was observed in both Koshihikari and Kasalath, however, it is unlikely to be the mechanism for Al tolerance because there was no significant difference in the amount of citrate secreted between Koshihikari and Kasalath. Quantitative trait loci (QTLs) for Al tolerance were mapped in a population of 183 backcross inbred lines (BILs) derived from a cross of Koshihikari and Kasalath. Three putative QTLs controlling Al tolerance were detected on chromosomes 1, 2 and 6. Kasalath QTL alleles on chromosome 1 and 2 reduced Al tolerance but increased tolerance on chromosome 6. The three QTLs explained about 27% of the phenotypic variation in Al tolerance. The existence of QTLs for Al tolerance was confirmed in substitution lines for corresponding chromosomal segments.

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Role of root hairs and lateral roots in silicon uptake by rice

JF Ma, S Goto, K Tamai, M Ichii

PLANT PHYSIOLOGY   127 ( 4 )   1773 - 1780   2001.12

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The rice plant (Oryza sativa L. cv Oochikara) is known to be a Si accumulator, but the mechanism responsible for the high uptake of Si by the roots is not well understood. We investigated the role of root hairs and lateral roots in the Si uptake using two mutants of rice, one defective in the formation of root hairs (RH2) and another in that of lateral roots (RM109). Uptake experiments with nutrient solution during both a short term (up to 12 h) and relatively long term (26 d) showed that there was no significant difference in Si uptake between RH2 and the wild type (WT), whereas the Si uptake of RM109 was much less than that of WT. The number of silica bodies formed on the third leaf in RH2 was similar to that in WT, but the number of silica bodies in RM109 was only 40% of that in WT, when grown in soil amended with Si under flooded conditions. There was also no difference in the shoot Si concentration between WT and RH2 when grown in soil under upland conditions. Using a multi-compartment transport box, the Si uptake at the root tip (0-1 cm, without lateral roots and root hairs) was found to be similar in WT, RH2, and RM109. However, the Si uptake in the mature zone (1-4 cm from root tip) was significantly lower in RM109 than in WT, whereas no difference was found in Si uptake between WT and RH2. All these results clearly indicate that lateral roots contribute to the Si uptake in rice plant, whereas root hairs do not. Analysis of F-2 populations between RM109 and WT showed that Si uptake was correlated with the presence of lateral roots and that the gene controlling formation of lateral roots and Si uptake is a dominant gene.

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Distribution and mobility of aluminium in an Al-accumulating plant, Fagopyrum esculentum Moench.

RF Shen, JF Ma

JOURNAL OF EXPERIMENTAL BOTANY   52 ( 361 )   1683 - 1687   2001.8

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Buckwheat (Fagopyrum esculentum Moench. cv. Jianxi) accumulates high concentrations of Al in the leaves without showing any toxicity. To understand the accumulation mechanism of All in buckwheat, the distribution and mobility of Al in buckwheat were investigated. Relatively long-term treatment (28 d) with Al led to a decrease in Al concentration from old to young leaves, while a short-term (1 d) exposure to Al resulted in a uniform distribution of All in the leaves. When the fourth leaf was wrapped inside a transparent plastic bag to suppress transpiration, the Al concentration of this leaf was only one-quarter of that in the corresponding leaf without wrappng. Wit in a leaf, the Al concentration at the margins was much higher than that in the centre. These results indicate that Al distribution in the leaves is controlled by both rate and duration of transpiration. The mobility of Al between old and new leaves was studied by first growing plants in a solution with Al, followed by culture in a solution without Al. The Al content in the two new leaves appeared after removal of external Al was very low, whereas that in the old leaves did not decrease but continued to increase. The increased Al content was found to be translocated from Al remaining in the roots. It is concluded that Al is not mobile once it is accumulated in the leaf.

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Aluminium tolerance in plants and the complexing role of organic acids

JF Ma, PR Ryan, E Delhaize

TRENDS IN PLANT SCIENCE   6 ( 6 )   273 - 278   2001.6

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The aluminium cation Al3+ is toxic to many plants at micromolar concentrations. A range of plant species has evolved mechanisms that enable them to grow on acid soils where toxic concentrations of Al3+ can limit plant growth, Organ ic acids play a central role in these aluminium tolerance mechanisms. Some plants detoxify aluminium in the rhizosphere by releasing organic acids that chelate aluminium. In at least two species, wheat and maize, the transport of organic acid anions out of the root cells is mediated by aluminium-activated anion channels in the plasma membrane. Other plants, including species that accumulate aluminium in their leaves, detoxify aluminium internally by forming complexes with organic acids.

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Regulatory mechanisms of Al-induced secretion of organic acids anions-Involvement of ABA in the Al-induced secretion of oxalate in buckwheat

Ma, J. F, Zhang, W, Zhao, Z

Plant Nutrition-Food security and sustainability of agro-ecosystems through basic and applied Research.   2001

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Pattern of aluminum-induced secretion of organic acids differs between rye and wheat

XF Li, JF Ma, H Matsumoto

PLANT PHYSIOLOGY   123 ( 4 )   1537 - 1543   2000.8

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Al-Induced secretion of organic acids from the roots has been considered as a mechanism of Al tolerance, but the processes leading to the secretion of organic acids are still unknown. In this study, the secretion pattern and alteration in the metabolism of organic acids under Al stress were examined in rye (Secale cereale L. cv King) and wheat (Triticum aestivum L. cv Atlas 66). Al induced rapid secretion of malate in the wheat, but a lag (6 and 10 h for melic and citric acids, respectively) between the exposure to Al and the secretion of organic acids was observed in the rye. The activities of isocitrate dehydrogenase, phosphoenolpyruvate carboxylase, and malate dehydrogenase were not affected by Al in either plant. The activity of citrate synthase was increased by the exposure to Al in the rye, but not in the wheat. The secretion of malate was not suppressed at low temperature in the wheat, but that of citrate was stopped in the rye. The Al-induced secretion of citrate from roots of the rye was inhibited by the inhibitors of a citrate carrier, which transports citrate from the mitochondria to the cytoplasm. All of these results suggest that alteration in the metabolism of organic acids is involved in the Al-induced secretion of organic acids in rye, but only activation of an anion channel seems to be responsible for the rapid secretion of malate in the wheat.

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Role of organic acids in detoxification of aluminum in higher plants

JF Ma

PLANT AND CELL PHYSIOLOGY   41 ( 4 )   383 - 390   2000.4

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Phytotoxicity of aluminum ion (Al3+) is a serious problem limiting crop production on acid soils. Organic acids with Al-chelating ability play an important role in the detoxification of Al both externally and internally. Al is detoxified externally by the secretion of organic acids such as citric, oxalic, and /or malic acids from the roots. The secretion of organic acids is highly specific to Al and the site of secretion is localized to the root apex. The kind of organic acids secreted as well as secretion pattern differ among plant species. There are two patterns of Al-induced secretion of organic acids: In pattern I, there is no discernible delay between the addition of Al and the onset of the release of organic acids. Activation of the anion channel seems to be involved in this pattern; In pattern II, there is a marked lag phase between the addition of Al and the onset of organic acid release. The action of genes related to the metabolism and secretion of organic acids seems to be involved in this pattern. Internal detoxification of Al in Al-accumulating plants is achieved by the formation of Al-organic acid complex. For instance, the complex of Al-citrate (1:1) in hydrangea and Al-oxalate (1:3) in buckwheat has been identified.

DOI： 10.1093/pcp/41.4.383

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IDENTIFICATION OF CHROMOSOMAL ARM LOCATION OF AL-TOLERANT GENES IN RYE

MA Jian Feng, TAKETA Shin, YANG Zhen Ming, TAKEDA Kazuyoshi, MATSUMOTO Hideaki

40   s101 - s101   1999.3

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IDENTIFICATION OF CHROMOSOMAL ARM LOCATION OF GENES CONTROLLING HYDROXYLATION OF PHYTOSIDEROPHORES IN BARLEY

MA Jian Feng, TAKETA Shin, CHANG Yi-Chieh, NOMOTO Kyosuke, IWASHITA Takashi, TAKEDA Kazuyoshi, MATSUMOTO Hideaki

40   s96 - s96   1999.3

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Role of metal-chelating substances in root exudates

MA Jian Feng

Root Research   7 ( 4 )   105 - 108   1998.12

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DOI： 10.3117/rootres.7.105

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9-21 ソバにおけるアルミニウムストレスの抵抗性機構 : アルミニウム存在形態の同定(9.植物の無機栄養)

馬 建鋒, 平舘 俊太郎, 松本 英明

日本土壌肥料学会講演要旨集   44   75 - 75   1998

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DOI： 10.20710/dohikouen.44.0_75_1

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Early events induced by aluminum stress in elongating cells of wheat root

Masao Sasaki, Yoko Yamamoto, Jian Feng Ma, Hideaki Matsumoto

Soil Science and Plant Nutrition   43 ( SPEC. ISS. )   1009 - 1014   1997.12

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The relation between the toxic effects of alminum (Al) on growth and cell viability in roots of wheat (Triticum aestivum L. cv Atlas 66) was investigated. Root elongation of wheat was reduced after 3 h of treatment with 50 pM AlCl3 at pH 4.7. Only the apical region of the root treated with Al was stained with hematoxylin. Al treatment decreased the length and increased the diameter of the cells at the elongation zone of the root. Staining with propidium iodide which can permeate through only a damaged plasma membrane showed that treatment with Al for longer than 3 h decreased cell viability. These findings suggest that inhibition of cell elongation by Al is partially accompanied by cell death. Lignin was deposited in the cell wall of the second and third layers of the cortex in the elongation zone of the root. Also the disruption of microtubules ocurred in elongating cells treated with 50 μM Al for 3 h. The effects of Al stress on root elongation and cell viability in the elongation zone were inhibited by 1 mM Ca. In conclusion, inhibition of root elongation by Al is strongly related to the inhibition of cell elongation, accompanied by decreased cell viability, lignin deposition and the disruption of microtubules.

DOI： 10.1080/00380768.1997.11863708

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A rapid hydroponic screening for aluminium tolerance in barley

JF Ma, SJ Zheng, XF Li, K Takeda, H Matsumoto

PLANT AND SOIL   191 ( 1 )   133 - 137   1997.4

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Selection and breeding of crops for aluminium (Al) tolerance is a useful approach to increase production on acid soils. This requires a rapid and reliable system to discriminate between Al-tolerant and Al-sensitive genotypes. A hydroponic system was developed to screen for Al tolerance in barley (Hordeum vulgare L.) to overcome several problems encountered in previous screening methods. Four levels of Al (5, 10, 20, and 40 mu M) in 1 mM CaCl2 solution at pH 4.5 were used to rank lines for Al-tolerance. Each line was cultured in a different compartment to eliminate chemical and pH interactions among lines. To avoid changes in Al tolerance due to other factors such as the calcium (Ca) concentration of the solution, Al-tolerant (Atlas 66) and Al-sensitive (Scout 66) cultivars of wheat (Triticum aestivum L.) were used as reference cultivars. Five ranks of Al tolerance from highly tolerant to highly sensitive were established by comparison with each reference. Eriochrome cyanine R staining was used for the rapid evaluation of Al tolerance. This screening system allowed classification of about 50 barley lines into five different Al tolerance groups within one week. Using this system, screening of ca. 600 barley lines from various regions of the world was conducted. Most lines were sensitive to Al, but ninety lines showed intermediate Al-tolerance. Thirty nine lines were highly sensitive to Al in solution.

DOI： 10.1023/A:1004257711952

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Internal detoxification mechanism of Al in hydrangea - Identification of Al form in the leaves

JF Ma, S Hiradate, K Nomoto, T Iwashita, H Matsumoto

PLANT PHYSIOLOGY   113 ( 4 )   1033 - 1039   1997.4

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An internal detoxification mechanism for Al was investigated in an Al-accumulating plant, hydrangea (Hydrangea macrophylla), focusing on Al forms present in the cells. The leaves of hydrangea contained as much as 15.7 mmol Al kg(-1) fresh weight, and more than two-thirds of the Al was found in the cell sap. Using Al-27-nuclear magnetic resonance, the dominant peak of Al was observed at a chemical shift of 11 to 12 parts per million in both intact leaves and the extracted cell sap, which is in good accordance with the chemical shift for the 1:1 Al-citrate complex. Purification of cell sap by molecular sieve chromatography (Sephadex G-10) combined with ion-exclusion chromatography indicated that Al in fractions with the same retention time as citric acid contributed to the observed Al-27 peak in the intact leaves. The molar ratio of Al to citric acid in the crude and purified cell sap approximated 1. The structure of the ligand chelated with Al was identified to be citric acid. Bioassay experiments showed that the purified Al complex from the cell sap did not inhibit root elongation of corn (Zea mays L.) and the viability of cells on the root tip surface was also not affected. These observations indicate that Al is bound to citric acid in the cells of hydrangea leaves.

DOI： 10.1104/pp.113.4.1033

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MOLECULAR MECHANISMS FOR IRON ACQUISITION IN HIGHER PLANTS

MA Jian Feng, NOMOTO Kyosuke

38   s5   1997.3

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IDENTIFICATION OF AL FORM IN LEAVES OF Hydrangea macrophylla

MA Jian Feng, HIRADATE Syuntaro, NOMOTO Kyosuke, MATSUMOTO Hideaki

38   s103   1997.3

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Early events induced by aluminum stress in elongating cells of wheat root.T.ANDO et al.(eds.)

Plant Nutrition-for Sustainable Food Production and Environment.   439 - 444   1997

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Secretion of citric acid as an aluminum-resistant mechanism in Cassia tora L.T.ANDO et al.(eds.)

馬建鋒, 鄭紹建, 松本英明

Plant Nutrition-for Sustainable Food Production and Environment.   37th(1997)   449 - 450   1997

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19 Secretion of organic acids by different plant species in response to Al stress

Zheng S.J., Ma J.F., Matsumoto H.

Abstracts of the Annual Meetings, Japanese Society of Soil Science and Plant Nutrition   43   401 - 401   1997

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DOI： 10.20710/dohikouen.43.0_401_1

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Comparison of Two Inbreds of Corn Differing in Tolerance to Potassium Deficiency

CAO Min Jian, MATSUMOTO Hideaki, MA Jian Feng

Japanese Journal of Soil Science and Plant Nutrition   68 ( 6 )   607 - 613   1997

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Two inbreds of Zea mays, tolerant to K^+ deficiency and control, were grown in the presence of different concentrations of K^+. Several parameters were compared between the two inbreds and characteristic differences in terms of K^+ utilization were observed. 1. The dry weight of both inbreds was nearly the same in the presence of a sufficient concentration of K^+, but was apparently higher in the tolerant inbred than the control inbred according to the decreasing amount of K^+ supply. 2. Symptoms of K^+ deficiency in the tolerant inbred appeared only with complete absence of K^+, but those in the control inbred could be observed even at a decreased level of K^+ supply. 3. The increased length of the main root and top to root ratio in the control inbred were conspicuously lower than those of the tolerant inbred due to K^+ deficiency. Furthermore, the amout of lateral roots of the cotrol inbred was approximately one-half to one-fourth of that of the tolerant inbred. 4. The capability of K^+ absorption by the roots treated for K^+ deficiency was higher in the tolerant inbred than in the controel inbred. The difference in the capability became larger when assayed with decreasing concentrations of K^+. 5. K^+-dependent H^+ extrusion from roots treated for K^+ deficiency was larger in the tolerant inbred than in the control inbred.

DOI： 10.20710/dojo.68.6_607

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Effective regulation of iron acquisition in graminaceous plants. The role of mugineic acids as phytosiderophores

JF Ma, K Nomoto

PHYSIOLOGIA PLANTARUM   97 ( 3 )   609 - 617   1996.7

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Discovery of mugineic acids as phytosiderophores has shown that some graminaceous monocotyledonous plants have a different iron acquisition strategy (strategy II) from dicotyledonous and nongraminaceous monocotyledonous plants (strategy I). The process of iron acquisition by strategy II plants can be divided into four main steps: biosynthesis, secretion, solubilization, and uptake, all of which are effectively regulated by different systems. The biosynthesis of mugineic acids is controlled by an on-off system which is operated under the control of iron demand in the plant. All mugineic acids share the same biosynthetic pathway from L-methionine to 2'-deoxymugineic acid, but the subsequent steps differ among plant species and even cultivars. The biosynthesis of mugineic acids is associated with the methionine recycling pathway. The secretion of mugineic acids shows a distinct diurnal rhythm. Mugineic acids solubilize sparingly soluble inorganic iron by chelation and possess a high chelation affinity for iron, but not for other polyvalent ions such as Ca2+, Mg2+ and Al3+. The iron uptake process is regulated by a specific uptake system that transports the mugineic acid-Fe(III) complex as an intact molecule. This system specifically recognizes the mugineic acid-Fe(III) complexes, but not other mugineic acid-metal or synthetic chelator-Fe(III) complexes, suggesting that binding sites with strict recognition for stereostructure of the complex are located on the plasma membrane. All these regulatory systems are considered to represent an efficient strategy to acquire adequate amounts of iron and to avoid factors unfavorable for iron acquisition such as high pH, high concentrations of bicarbonate, Ca2+ and Mg2+, microbial degradation, and uptake of other metals that are common in calcareous soils.

DOI： 10.1034/j.1399-3054.1996.970325.x

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25 STUDIES ON THE BIOSYNTHESIS OF PHYTOSIDEROPHORES : MUGINEIC ACIDS

Ma J. F., Nomoto K.

Symposium on the Chemistry of Natural Products, symposium papers   ( 36 )   188 - 195   1994.9

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Mugineic acids are a group of compounds having ferric chelating activity. They are secreted from the roots of some gramineous plants under iron deficiency. These compounds play an important role in the acquisition of insoluble iron from soils by the gramineous plants. In the present study, the biosynthetic pathways of five mugineic acids were investigated in different gramineous plants using feeding experiments with ^<13>-and/or ^2H-labeled compounds and by NMR techniques. The results revealed that L-Met serves as a precursor for all mugineic acids tested. All mugineic acids share the pathway from L-Met to 2'-deoxymugineic acid although subsequent steps differ and are dependent on the plant species and cultivars. In oats, avenic acid A is biosynthesized from 2'-deoxymugineic acid by cleavage of the azetidine ring. In barley, hydroxylation at the C-2' position in 2'-deoxymugineic acid yields mugineic acid. Further hydroxylation at the C-3 position in mugineic acid produces 3-epihydroxymugineic acid and hydroxymugineic acid in beer barley and rye, respectively. All mugineic acids were found to have similar effect on iron uptake, suggesting that 2'-deoxymugineic acid is a key phytosiderophore. The biosynthetic pathway between L-methionine and 2'-deoxymugineic acid was investigated by observing the incorporation of label from ^<13>C, ^2H, and ^<15>N-labeled methionine in wheat roots (Triticum aestivum L. cv Minori). As a result, only the deuterium atom from the C-2 position of L-methionine was lost, while other atoms were completely incorporated when three molecules of methionine were converted to 2'-deoxymugineic acid. These observations are consistent with the conversion of L-methionine to azetidine-2-carboxylic acid, suggesting that L-methionine is first converted to azetidine-2-carboxylic acid during biosynthesis leading to 2'-deoxymugineic acid. Based on these results, a hypothetical pathway from L-methionine to 2'-deoxymugineic acid was postulated.

DOI： 10.24496/tennenyuki.36.0_188

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Incorporation of label from ¹³C-, ²H-, and ¹⁵N-labeled methionine molecules during the biosynthesis of 2′-deoxymugineic acid in roots of wheat

Jian Feng Ma, Kyosuke Nomoto

Plant Physiology   105 ( 2 )   607 - 610   1994.6

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The biosynthetic pathway of 2′-deoxymugineic acid, a key phytosiderophore, was investigated by feeding 13C-, 2H-, and 15N-labeled methionine, the first precursor, to the roots of hydroponically cultured wheat (Triticum aestivum L. cv Minori). The incorporation of label from each methionine species was observed during their conversion to 2′-deoxymugineic acid, using 2H-, 15N-, and 13C-nuclear magnetic resonance (NMR). L-[1-13C]Methionine (99% 13C) was efficiently incorporated, resulting in 13C enrichment of the three carboxyl groups of 2′-deoxymugineic acid. Use of D,L-[15N]methionine (95% 15N) resulted in 15N enrichment of 2′-deoxymugineic acid at the azetidine ring nitrogen and the secondary amino nitrogen. When D,L-[2,3,3-2H3-S-methyl-2H 3]methionine (98.2% 2H) was fed to the roots, 2H-NMR results indicated that only six deuterium atoms were incorporated, and that the deuterium atom from the C-2 position of each methionine was almost completely lost. [2,2,3,3-2H4]1-Aminocyclopropane-1-carboxylic acid (98% 2H) was not incorporated into 2′-deoxymugineic acid. These data and our previous findings demonstrated that only the deuterium atom from the C-2 position of L-methionine was lost, and that other atoms were completely incorporated when three molecules of methionine were converted to 2′-deoxymugineic acid. These observations are consistent with the conversion of L-methionine to azetidine-2-carboxylic acid, suggesting that L-methionine is first converted to azetidine-2-carboxylic acid during biosynthesis leading to 2′-deoxymugineic acid. Based on these results, a hypothetical pathway from L-methionine to 2′-deoxymugineic acid was postulated.

DOI： 10.1104/pp.105.2.607

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Biosynthetic pathways of 3-epihydroxymugineic acid and 3-hydroxymugineic acid in gramineous plants

Jian Feng Ma, Kyosuke Nomoto

Soil Science and Plant Nutrition   40 ( 2 )   311 - 317   1994.6

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To elucidate the biosynthetic pathways of 3-epihydroxymugineic acid and 3-hydroxymugineic acid, feeding experiments using 2H- and/or 13C-labeled compounds were conducted with barley (Hordeum vulgare L. cv Ehimehadaka) and rye (Secale cereale L. cv Elubon), respectively. Feeding of [1, 4′, 4″13C3]2′-deoxymugineic acid (25 atom% 13C) to iron-deficient barley yielded mugineic acid and 3-epihydroxymugineic acid enriched with 13C at their corresponding positions. These results enabled us to demonstrate that 2′-deoxymugineic acid acts as a precursor for mugineic acid and 3-epihydroxymugineic acid. The 2H-labeled 3-hydroxymugineic acid was obtained by feeding d, l- [3, 3, 4, 42H4] methionine (98.6 atom% 2H) to iron-deficient rye plants. The 2H-NMR study revealed that two deuterium atoms (one each at the C-2′ and C-3 positions) from the three 2H-labeled methionine molecules were lost in 3-hydroxymugineic acid, whereas the other 10 deuterium atoms were incorporated in a manner similar to that of 2′-deoxymugineic acid and mugineic acid. These findings suggested that 3-hydroxymugineic acid, instead of being biosynthesized from 3-epihydroxymugineic acid by epimerization, was in fact derived from mugineic acid by hydroxylation at the C-3 position. This assumption was further confirmed by the results of the incorporation of 13C-labeled 2’-deoxymugineic acid into 3-hydroxymugineic acid. These results revealed that the biosynthetic pathways of both 3-epihydroxymugineic acid and 3-hydroxymugineic acid are as follows: L-methionineℲ2′-deoxymugineic acid→mugineic acid→3-epihydroxymugineic acid in barley and→hydroxymugineic acid in rye. © Taylor & Francis Group, LLC.

DOI： 10.1080/00380768.1994.10413305

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Inhibition of mugineic acid‐ferric complex uptake in barley by copper, zinc and cobalt

Jian Feng Ma, Kyosuke Nomoto

Physiologia Plantarum   89 ( 2 )   331 - 334   1993.10

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The interfering effects of copper, zinc, and cobalt on the uptake of mugineic acid‐ferric complex were studied in barley (Hordeum vulgare, cv. Minorimugi) grown in nutrient solution. Short‐term uptake experiments of 3 h were performed utilizing both ionic and mugineic acid‐complex forms of each metal at two different concentrations. Copper was most effective in decreasing iron uptake when added in an ionic form at either concentration. The inhibition order at higher concentrations followed Cu(II) > Zn(II) ≥ Co(II), Co(III), which is consistent with the stability constants of these metal complexes with mugineic acid. The displacement of iron from its mugineic acid complex by these metals is suggested as a probable explanation for the decreased iron uptake. The inhibitory effect of metal complexes with mugineic acid on iron uptake was only found in cases with higher concentrations of Cu(II) and Zn(II) complexes. Deformation of the specific iron transport system in the plasma membrane due to their adsorption may be responsible for this effect. Copyright © 1993, Wiley Blackwell. All rights reserved

DOI： 10.1111/j.1399-3054.1993.tb00162.x

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Specific recognition of mugineic acid-ferric complex by barley roots

Jian Feng Ma, Genjiro Kusano, Syojiro Kimura, Kyosuke Nomoto

Phytochemistry   34 ( 3 )   599 - 603   1993.10

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The uptake rate by iron-deficient barley roots (Hordeum vulgare, cv Minorimugi) from mugineic acid complexed with Fe(III) was much higher than corr. © 1993.

DOI： 10.1016/0031-9422(93)85323-J

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Two related biosynthetic pathways of mugineic acids in gramineous plants

Jian Feng Ma, Kyosuke Nomoto

Plant Physiology   102 ( 2 )   373 - 378   1993.6

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The biosynthesis of mugineic acids was studied by feeding 2H- or 13C-labeled compounds to water-cultured roots in several gramineous plants. The fate of labeled compounds was monitored by using 2H- and 13C-nuclear magnetic resonance. On investigating the proton changes during biosynthesis by feeding D,L-[3,3,4,4-d4]- methionine (98.6% 2H), 2H-labeled 2′-deoxymugineic, mugineic, and 3-epihydroxymugineic acids were isolated from root washings of wheat (Triticum aestivum L. cv Minori), barley (Hordeum vulgare L. cv Minorimugi), and beer barley (Hordeum vulgare L. cv AM Nijo Tochigi), respectively. The 2H-nuclear magnetic resonance study indicated that 12 deuteriums were incorporated into the labeled 2′-deoxymugineic acid, suggesting that three molecules of L-[3,3,4,4-d4]methionme were combined. In comparison, one of the deuteriums at C-2′ position in the mugineic acid, and one each of the deuteriums at C-2′ and C-3 positions in the 3-epihydroxymugineic acid, were lost. However, all other deuteriums were incorporated in a manner similar to that of the labeled 2′-deoxymugineic acid. When [1,4′,4″-13C3]2′-deoxymugineicacid (20% 13C) was fed to oat roots (Avena saliva L. cv Amuri II), avenic acid A, which was 13C enriched at the corresponding positions, was obtained. These results revealed that L-methionine was the precursor for all these mugineic acids and that cleavage of the azetidine ring or hydroxylation of the 2′-deoxymugineic acid produced two related biosynthetic pathways in different gramineous plant species: L-methionine → 2′-deoxymugineic acid → avenic acid A in oat; and L-methionine → 2′-deoxymugineic acid → mugineic acid → 3-epihydroxymugineic acid in barley and beer barley.

DOI： 10.1104/pp.102.2.373

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Interaction between calcium and silicon in water-cultured rice plants

Jian Feng Ma, Eiichi Takahashi

Plant and Soil   148 ( 1 )   107 - 113   1993.1

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The interaction between Ca and Si in water-cultured rice plants (Oryza sativa L. cv. Akebono) was investigated in terms of uptake. The effect of Ca levels in the solution on Si chemical forms and on the formation of silica bodies in the leaf blades was also examined using soft X-ray irradiation for detection of silica bodies. Si addition (1.66 m M Si) decreased both Ca content of the shoot and uptake at each Ca level. This might mainly result from a decreased transpiration rate caused by Si. Si uptake was not affected when the Ca levels were increased. The results of Si forms showed that silica sol constituted more than 90% of the total Si in the leaf blades regardless of Si and Ca levels, and soluble silica and/or polysilicic acid seems to gel physically over 8.0 m M Si within the plants. Significant difference in the numbers of silica bodies on the third leaf blade was not found between different Ca levels at the same Si level. The content of Si in the leaf blade seems to be a determining factor for the formation of silica bodies. ei]H. Marschner © 1993 Kluwer Academic Publishers.

DOI： 10.1007/BF02185390

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5-9 イネ科植物におけるムギネ酸類の生合成研究(5. 植物の無機栄養および養分吸収)

馬 建鋒, 野本 享資

日本土壌肥料学会講演要旨集   39   57 - 57   1993

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Language：Japanese   Publisher：一般社団法人日本土壌肥料学会  

DOI： 10.20710/dohikouen.39.0_57_1

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Biosynthesis of avenic acid a, a ferric chelating substance secreted from avena sativa l

Jian Feng Ma

Chemical and Pharmaceutical Bulletin   40 ( 10 )   2888 - 2890   1992

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The biosynthesis of avenic acid A was studied by feeding L-methionine-l-13C or D,L-methionine-3, 3, 4, 4-d4 to iron-deficient oat roots (Avena sativa L. cv Amuri II). Both avenic acid A and 2’-deoxymugineic acid labeled with 13C or 2H were isolated from root-washings of the same plants. The 13C-NMR elucidated that three molecules of L-methionine were incorporated into avenic acid A in the same way as 2’-deoxymugineic acid. The 2H-NMR spectra indicated that all deuteriums from the methionine were incorporated into 2’-deoxymugineic acid, but one of the deuteriums at C-4 was lost in avenic acid A. A possible biosynthetic pathway is L-methionine-> — 2’-deoxymugineic acid-»avenic acid A. © 1992, The Pharmaceutical Society of Japan. All rights reserved.

DOI： 10.1248/cpb.40.2888

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Effect of silicate on phosphate availability for rice in a P-deficient soil

M. A. Jianfeng, Eiichi Takahashi

Plant and Soil   133 ( 2 )   151 - 155   1991.6

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In a pot experiment the effect of silicate on P availability for rice grown in a P-deficient soil with and without flooding was analyzed. Treatments were designed as follows: C (control: Yakuno soil), SS (sodium silicate application, at 0.47 mg Si g-1 soil) and SC (sodium carbonate application). In order to separate pH effect from Si effect, SC was adjusted to the same pH as SS. Soil pH of SS and SC increased by 1.0 unit. Shoot dry weight of SC plants, and more so of SS plants, increased under both nonflooded and flooded conditions. P concentrations in the shoots were not increased under either condition of SS and SC. With SS, Si concentration in the shoots significantly increased, Mn concentration significantly decreased, resulting in a higher P/Mn ratio in the shoot, but not with SC. Both SS and SC increased N concentration in the shoots nearly two times compared with control under both conditions. Adsorption experiments showed that neither SS nor SC decreased P adsorption by soil. SS also could not displace the adsorbed P in soil samples which had previously either received P or not. These results suggest that the beneficial effects of silicate on rice growth do not result from increasing P availability in soil. The Si effect may be attributed to decreasing Mn uptake, thus indirectly improving P utilization in the plant. © 1991 Kluwer Academic Publishers.

DOI： 10.1007/BF00009187

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Availability of rice straw Si to rice plants

Jianfeng Ma, Eiichi Takahashi

Soil Science and Plant Nutrition   37 ( 1 )   111 - 116   1991.3

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A pot experiment was conducted to estimate the availability to rice plants of Si contained in rice straw. To separate the effect of straw application on Si availability in soil, two kinds of rice straws, which contained 15.5% (+ Si straw) and 0.2% SiO2 (−Si straw), were used at a rate of 1% of air-dry soil, respectively. Rice plants were cultivated twice during a period of 2 months each. Results of the two harvests indicated that +Si straw application increased the Si concentration in the percolating water, the Si content of rice shoots, and soil-available silicate. However, compared to the Si contained in the added straw, the release of Si from the +Si straw was only about 6% in the first cultivation, and 3% in the second cultivation, respectively. The −Si straw application was not associated with any of the effects observed in the +Si straw application. Successive water extractions showed that the solubility of Si in the +Si straw was lower than that of silica gel, but much higher than that of opal. These facts suggest that the short term availability of Si in the straw applied to the soil is low and the application of materials with a higher availability of Si such as slags may be desirable for satisfactory growth of rice plant. © 1991 Taylor & Francis Group, LLC.

DOI： 10.1080/00380768.1991.10415016

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The effect of silicic acid on rice in a P-deficient soil

Jianfeng Ma, Eiichi Takahashi

Plant and Soil   126 ( 1 )   121 - 125   1990.8

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A pot experiment was conducted to analyze the effect of silicon on the growth of rice grown in a P-deficient soil and on P availability in the soil. Silicic acid was used, rather than a silicate salt, to avoid the complication of changes in soil pH. Shoot dry weight on silicic acid treated soil (0.47 mg Si g-1 soil) increased significantly under both nonflooded and flooded conditions. Shoot Si concentration also increased although P concentration did not. Mn concentration decreased with silicic acid, resulting in a higher P/Mn ratio in shoots. An adsorption and desorption experiment showed that silicic acid did not displace P nor decrease the ability of the soil to adsorb P. In contrast, Si desorption increased with increasing P concentration in the solution, and Si adsorption was reduced when P was applied first. These results suggest that silicic acid does not increase P availability in soil. Increased dry weight may be attributed to a higher P/Mn ratio in the shoot, which may improve P utilization in the plant. © 1990 Kluwer Academic Publishers.

DOI： 10.1007/BF00041377

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Effect of silicon on the growth and phosphorus uptake of rice

Jianfeng Ma, Eiichi Takahashi

Plant and Soil   126 ( 1 )   115 - 119   1990.8

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A pot experiment was conducted to measure the effect of silicon on phosphorus uptake and on the growth of rice at different P levels. Rice (Oryza sativa L. cv. Akebono) was cultured in Kimura B nutrient solution without and with silicon (1.66 m M Si) and with three phosphorus levels (0.014 m M P, low; 0.21 m M, medium; and 0.70 m M, high). Shoot dry weight with Si (+Si) in solution increased with increasing P level, while shoot weight without Si (-Si) was maximum at 0.21 m M P, suggesting that +Si raised the optimum P level for rice. +Si increased shoot weight more when P was low or high than when P was medium. The concentration and amount of inorganic P in shoots increased with increasing P level. +Si did not significantly decrease P uptake by rice at 0.014 m M P, however, uptake at 0.21 and 0.70 m M P was 27 and 30 percent less than uptake with -Si, respectively. In -Si with 0.21 and 0.70 m M P, inorganic P in shoots was more than double the concentration in shoots grown in +Si solutions. The Si concentration in shoots decreased slightly with increasing P level, although Si uptake was not significantly affected by P. +Si decreased the uptake of Fe and Mn by an average of 20 and 50 percent, respectively, thus P/Mn and P/Fe ratios increased in the shoot when P was low. From the results above, the beneficial effect of Si on the growth of rice was clearly shown when P was low or high. This effect may have resulted from decreased Mn and Fe uptake, and thus increased P availability within P deficient plants, or from reduced P uptake when P was high. © 1990 Kluwer Academic Publishers.

DOI： 10.1007/BF00041376

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Release of silicon from rice straw under flooded conditions

Jianfeng Ma, Eiichi Takahashi

Soil Science and Plant Nutrition   35 ( 4 )   663 - 667   1989.12

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It is estimated that nearly 20 kg of SiO2is removed from the soil by rice plants for producing 100 kg brown rice (Takahashi 1987). Although there is a large amount of silicon in soil, little is available to the rice plant. To supply a sufficient amount of silicon to the rice plant for healthy growth, therefore, it is nccessary to supply various silicon materials to the soil. Rice straw application to the soil is one of the means. © 1989 Taylor & Francis Group, LLC.

DOI： 10.1080/00380768.1989.10434802

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Effect of silicon on the growth of rice plant at different growth stages

Jianfeng Ma, Kazuo Nishimura, Eiichi Takahashi

Soil Science and Plant Nutrition   35 ( 3 )   347 - 356   1989.9

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Rice plants (Oryza sativa L. cv. Akebono) were cultured in Kimura B solution. The effect of silicon on plant growth and the characteristics of the uptake and distribution of silicon at different growth stages were studied from both aspects: The addition and removal of silicon during the vegetative, reproductive and ripening stages. When silicon was removed during the reproductive stage, the dry weights of straw (stem+leaf blade) and grain decreased by 20 and 50% respectively, compared with those of the plants cultured in the solution with silicon throughout the growth period. Conversely, when silicon was added during the reproductive stage, the dry weights of straw and grain increased by 243 and 30%, respectively, over those of the plants cultured in a solution devoid of silicon throughout the growth period. The effect of silicon on the dry weights of straw and grain was small when silicon was either added or removed during the vegetative and ripening stages. The percentage of filled spikelets remarkably increased or decreased when silicon was added or removed during the reproductive stage. The 1, 000-grain weight was hardly influenced by the addition or removal of silicon regardless of the growth stage. About 66% of silicon in the whole plant and 70 to 75% of silicon in the leaf blades were absorbed during the reproductive stage. About 75% of silicon in the panicle was absorbed during the ripening stage although no beneficial effect was detected in this experiment. Forty to 50% of the silicon absorbed during the vegetative and reproductive stages was present in the leaf blades, whereas only 20 to 30% of silicon absorbed during the ripening stage was present in the leaf blades. Based on these results, it is concluded that the supply of silicon during the reproductive stage is most important for plant growth. © Taylor & Francis Group, LLC.

DOI： 10.1080/00380768.1989.10434768

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Effect of silicic acid on phosphorus uptake by rice plant

Jianfeng Ma, Eiichi Takahashi

Soil Science and Plant Nutrition   35 ( 2 )   227 - 234   1989.6

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The Effect of silicic acid on the phosphorus uptake by rice plants (Oryza sativa L. cv. Akebono) grown in a culture solution was studied by several experiments. In long-term experiments, both the content and the uptake of phosphorus were decreased by the addition of silicic acid, and the effect was more pronounced at the vegetative stage than at the reproductive stage. Under the different phosphorus supply levels ranging from deficient to excess (from 0.1 to 50 ppm as P2O5), we found that, when the phosphorus level in the medium was low, the retardation effect of silicic acid on the phosphorus uptake was hardly observed, but with the rise of the phosphorus level in the medium, the effect became severe, especially at excess level. The rice plants which received silicic acid in advance (pretreatment) absorbed less phosphorus compared with those which were not pretreated with silicic acid, suggesting that the phosphorus uptake was also influenced by the silicon already present in the rice plants. There was no significant difference in the organic-P content between the —Si plants and + Si plants, but the inorganic-P content in the —Si plants was higher than that in the + Si plants. This fact suggests that the excess phosphorus absorbed by the —Si plants was almost completely in the inorganic-P form. In the inorganic-P form, the content of cations such as Ca, Mg, Fe, Mn, was also higher in the —Si plants than in the +Si plants, suggesting that these excess cations probably combine with the excess phosphorus in the —Si plants. © Taylor & Francis Group, LLC.

DOI： 10.1080/00380768.1989.10434755

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