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Plastids are essential organelles in angiosperms and show non-Mendelian inheritance due to their evolution as endosymbionts. In approximately 80% of angiosperms, plastids are thought to be inherited from the maternal parent, whereas other species transmit plastids biparentally. Maternal inheritance can be generally explained by the stochastic segregation of maternal plastids after fertilization because the zygote is overwhelmed by the maternal cytoplasm. In contrast, biparental inheritance shows transmission of organelles from both parents. In some species, maternal inheritance is not absolute and paternal leakage occurs at a very low frequency (~10-5). A key process controlling the inheritance mode lies in the behavior of plastids during male gametophyte (pollen) development, with accumulating evidence indicating that the plastids themselves or their DNAs are eliminated during pollen maturation or at fertilization. Cytological observations in numerous angiosperm species have revealed several critical steps that mutually influence the degree of plastid transmission quantitatively among different species. This review revisits plastid inheritance and focuses on the mechanistic viewpoint. Particularly, we focus on a recent finding demonstrating that both low temperature and plastid DNA degradation mediated by the organelle exonuclease DPD1 influence the degree of paternal leakage significantly in tobacco. Given these findings, we also highlight the emerging role of DPD1 in organelle DNA degradation.

DOI： 10.1093/pcp/pcad104

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Plants cope with sudden increases in light intensity through various photoprotective mechanisms. Redox regulation by thioredoxin (Trx) systems also contributes to this process. Whereas the functions of f- and m-type Trxs in response to such fluctuating light conditions have been extensively investigated, those of x- and y-type Trxs are largely unknown. Here, we analyzed the trx x single, trx y1 trx y2 double, and trx x trx y1 trx y2 triple mutants in Arabidopsis (Arabidopsis thaliana). A detailed analysis of photosynthesis revealed changes in photosystem I (PSI) parameters under low light in trx x and trx x trx y1 trx y2. The electron acceptor side of PSI was more reduced in these mutants than in the wild type. This mutant phenotype was more pronounced under fluctuating light conditions. During both low- and high-light phases, the PSI acceptor side was largely limited in trx x and trx x trx y1 trx y2. After fluctuating light treatment, we observed more severe PSI photoinhibition in trx x and trx x trx y1 trx y2 than in the wild type. Furthermore, when grown under fluctuating light conditions, trx x and trx x trx y1 trx y2 plants showed impaired growth and decreased level of PSI subunits. These results suggest that Trx x and Trx y prevent redox imbalance on the PSI acceptor side, which is required to protect PSI from photoinhibition, especially under fluctuating light. We also propose that Trx x and Trx y contribute to maintaining the redox balance even under constant low-light conditions to prepare for sudden increases in light intensity.

DOI： 10.1093/plphys/kiad466

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DOI： 10.1093/pcp/pcad061

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Organelle DNAs (orgDNAs) in mitochondria and plastids are generally inherited from the maternal parent; however, it is unclear how their inheritance mode is controlled, particularly in the plastids of seed plants. Chung et al. identify two factors that affect maternal inheritance in tobacco plastids: cold temperature and DNA amount in pollen.

DOI： 10.1016/j.tig.2023.03.002

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DOI： 10.1080/17429145.2022.2153182

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Photosynthetic electron transfer and its regulation processes take place on thylakoid membranes, and the thylakoid of vascular plants exhibits particularly intricate structure consisting of stacked grana and flat stroma lamellae. It is known that several membrane remodeling proteins contribute to maintain the thylakoid structure, and one putative example is FUZZY ONION LIKE (FZL). In this study, we re-evaluated the controversial function of FZL in thylakoid membrane remodeling and in photosynthesis. We investigated the sub-membrane localization of FZL and found that it is enriched on curved grana edges of thylakoid membranes, consistent with the previously proposed model that FZL mediates fusion of grana and stroma lamellae at the interfaces. The mature fzl thylakoid morphology characterized with the staggered and less connected grana seems to agree with this model as well. In the photosynthetic analysis, the fzl knockout mutants in Arabidopsis displayed reduced electron flow, likely resulting in higher oxidative levels of Photosystem I (PSI) and smaller proton motive force (pmf). However, nonphotochemical quenching (NPQ) of chlorophyll fluorescence was excessively enhanced considering the pmf levels in fzl, and we found that introducing kea3-1 mutation, lowering pH in thylakoid lumen, synergistically reinforced the photosynthetic disorder in the fzl mutant background. We also showed that state transitions normally occurred in fzl, and that they were not involved in the photosynthetic disorders in fzl. We discuss the possible mechanisms by which the altered thylakoid morphology in fzl leads to the photosynthetic modifications.

DOI： 10.3389/fpls.2023.1279699

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The awn, a needle-like structure extending from the tip of the lemma in grass species, plays a role in environmental adaptation and fitness. In some crops, awns appear to have been eliminated during domestication. Although numerous genes involved in awn development have been identified, several dominant genes that eliminate awns are also known to exist. For example, in sorghum (Sorghum bicolor), the dominant awn-inhibiting gene has been known since 1921; however, its molecular features remain uncharacterized. In this study, we conducted quantitative trait locus analysis and a genome-wide association study of awn-related traits in sorghum and identified DOMINANT AWN INHIBITOR (DAI), which encodes the ALOG family protein on chromosome 3. DAI appeared to be present in most awnless sorghum cultivars, likely because of its effectiveness. Detailed analysis of the ALOG protein family in cereals revealed that DAI originated from a duplication of its twin paralog (DAIori) on chromosome 10. Observations of immature awns in near-isogenic lines revealed that DAI inhibits awn elongation by suppressing both cell proliferation and elongation. We also found that only DAI gained a novel function to inhibit awn elongation through an awn-specific expression pattern distinct from that of DAIori. Interestingly, heterologous expression of DAI with its own promoter in rice inhibited awn elongation in the awned cultivar Kasalath. We found that DAI originated from gene duplication, providing an interesting example of gain-of-function that occurs only in sorghum but shares its functionality with rice and sorghum.

DOI： 10.1093/pcp/pcac057

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Understanding uptake and redistribution of essential minerals or sequestering of toxic elements is important for optimized crop production. Although the mechanisms controlling mineral transport have been elucidated in rice and other species, little is understood in sorghum-an important C4 cereal crop. Here, we assessed the genetic factors that govern grain ionome profiles in sorghum using recombinant inbred lines (RILs) derived from a cross between BTx623 and NOG (Takakibi). Pairwise correlation and clustering analysis of 22 elements, measured in sorghum grains harvested under greenhouse conditions, indicated that the parental lines, as well as the RILs, show different ionomes. In particular, BTx623 accumulated significantly higher levels of cadmium (Cd) than NOG, because of differential root-to-shoot translocation factors between the two lines. Quantitative trait locus (QTL) analysis revealed a prominent QTL for grain Cd concentration on chromosome 2. Detailed analysis identified SbHMA3a, encoding a P1B-type ATPase heavy metal transporter, as responsible for low Cd accumulation in grains; the NOG allele encoded a functional HMA3 transporter (SbHMA3a-NOG) whose Cd-transporting activity was confirmed by heterologous expression in yeast. BTx623 possessed a truncated, loss-of-function SbHMA3a allele. The functionality of SbHMA3a in NOG was confirmed by Cd concentrations of F2 grains derived from the reciprocal cross, in which the NOG allele behaved in a dominant manner. We concluded that SbHMA3a-NOG is a Cd transporter that sequesters excess Cd in root tissues, as shown in other HMA3s. Our findings will facilitate the isolation of breeding cultivars with low Cd in grains or in exploiting high-Cd cultivars for phytoremediation.

DOI： 10.1093/pcp/pcac035

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Chlorophyll (Chl) serves a number of essential functions, capturing and converting light energy as a component of photosystem supercomplexes. Chl degradation during leaf senescence is also required for adequate degeneration of chloroplasts and salvaging of nutrients from senescent leaves. In this study, we performed genetic analysis to determine the functions of BALANCE of CHLOROPHYLL METABOLISM1 (BCM1) and BCM2, which control Chl levels by regulating synthesis and degradation, and STAY-GREEN (SGR)1 (also known as NON-YELLOWING1 [NYE1]) and SGR2, which encode Mg-dechelatase and catalyze Chl a degradation in Arabidopsis (Arabidopsis thaliana). Analysis of bcm1 bcm2 revealed that both BCM1 and BCM2 are involved in the regulation of Chl levels in presenescent leaves and Chl degradation in senescing leaves. Analysis of bcm1 bcm2 nye1 nye2 suggested that BCMs repress Chl-degrading activity in both presenescent and senescing leaves by regulating SGR activity. Furthermore, transactivation analysis and chromatin immunoprecipitation (ChIP) assay revealed that GOLDEN2-LIKE1 (GLK1), a central transcription factor regulating the expression of genes encoding photosystem-related proteins, such as light-harvesting Chl a/b-binding proteins (LHCPs), directly regulates the transcription of BCM1. LHCPs are stabilized by Chl binding, suggesting that GLKs control the amount of LHCP through transcriptional and post-translational regulation via BCM-mediated Chl-level regulation. Meanwhile, we generated a mutant of the BCM ortholog in lettuce (Lactuca sativa) by genome editing and found that it showed an early yellowing phenotype, but only a slight reduction in Chl in presenescent leaves. Thus, this study revealed a conserved but slightly diversified regulation of Chl and LHCP levels via the GLK-BCM pathway in eudicots.

DOI： 10.1093/plphys/kiac059

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Redox regulation of chloroplast proteins is necessary to adjust photosynthetic performance with changes in light. The thioredoxin (Trx) system plays a central role in this process. Chloroplast-localized classical Trx is a small redox-active protein that regulates many target proteins by reducing their disulfide bonds in a light-dependent manner. Arabidopsis thaliana mutants lacking f-type Trx (trx f1f2) or m-type Trx (trx m124-2) have been reported to show delayed reduction of Calvin cycle enzymes. As a result, the trx m124-2 mutant exhibits growth defects. Here, we characterized a quintuple mutant lacking both Trx f and Trx m to investigate the functional complementarity of Trx f and Trx m. The trx f1f2 m124-2 quintuple mutant was newly obtained by crossing, and is analyzed here for the first time. The growth defects of the trx m124-2 mutant were not enhanced by the lack of Trx f. In contrast, deficiencies of both Trxs additively suppressed the reduction of Calvin cycle enzymes, resulting in a further delay in the initiation of photosynthesis. Trx f appeared to be necessary for the rapid activation of the Calvin cycle during the early induction of photosynthesis. To perform effective photosynthesis, plants seem to use both Trxs in a coordinated manner to activate carbon fixation reactions. In contrast, the PROTON GRADIENT REGULATION 5 (PGR5)-dependent cyclic electron transport around photosystem I was regulated by Trx m, but not by Trx f. Lack of Trx f did not affect the activity and regulation of the PGR5-dependent pathway. Trx f may have a higher specificity for target proteins, whereas Trx m has a variety of target proteins to regulate overall photosynthesis and other metabolic reactions in the chloroplasts.

DOI： 10.1007/s10265-022-01388-7

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Vesicle-inducing protein in plastid 1 (VIPP1), characteristic to oxygenic photosynthetic organisms, is a membrane-remodeling factor that forms homo-oligomers and functions in thylakoid membrane formation and maintenance. The cyanobacterial VIPP1 structure revealed a monomeric folding pattern similar to that of endosomal sorting complex required for transport (ESCRT) III. Characteristic to VIPP1, however, is its own GTP and ATP hydrolytic activity without canonical domains. In this study, we found that histidine-tagged Arabidopsis VIPP1 (AtVIPP1) hydrolyzed GTP and ATP to produce GDP and ADP in vitro, respectively. Unexpectedly, the observed GTPase and ATPase activities were biochemically distinguishable, because the ATPase was optimized for alkaline conditions and dependent on Ca2+ as well as Mg2+, with a higher affinity for ATP than GTP. We found that a version of AtVIPP1 protein with a mutation in its nucleotide-binding site, as deduced from the cyanobacterial structure, retained its hydrolytic activity, suggesting that Arabidopsis and cyanobacterial VIPP1s have different properties. Negative staining particle analysis showed that AtVIPP1 formed particle or rod structures that differed from those of cyanobacteria and Chlamydomonas. These results suggested that the nucleotide hydrolytic activity and oligomer formation of VIPP1 are common in photosynthetic organisms, whereas their properties differ among species.

DOI： 10.3389/fpls.2022.949578

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

<title>Abstract</title>Organophosphate is the commonly used pesticide to control pest outbreak, such as those by aphids in many crops. Despite its wide use, however, necrotic lesion and/or cell death following the application of organophosphate pesticides has been reported to occur in several species. To understand this phenomenon, called organophosphate pesticide sensitivity (OPS) in sorghum, we conducted QTL analysis in a recombinant inbred line derived from the Japanese cultivar NOG, which exhibits OPS. Mapping OPS in this population identified a prominent QTL on chromosome 5, which corresponded to <italic>Organophosphate-Sensitive Reaction</italic> (<italic>OSR</italic>) reported previously in other mapping populations. The <italic>OSR</italic> locus included a cluster of three genes potentially encoding nucleotide-binding leucine-rich repeat (NB-LRR, NLR) proteins, among which <italic>NLR-C</italic> was considered to be responsible for OPS in a dominant fashion. <italic>NLR-C</italic> was functional in NOG, whereas the other resistant parent, BTx623, had a null mutation caused by the deletion of promoter sequences. Our finding of <italic>OSR</italic> as a dominant trait is important not only in understanding the diversified role of NB-LRR proteins in cereals but also in securing sorghum breeding free from OPS.

DOI： 10.1038/s41598-021-98908-7

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Other Link： https://www.nature.com/articles/s41598-021-98908-7

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

Light-dependent activation of chloroplast enzymes is required for the rapid induction of photosynthesis after a shift from dark to light. The thioredoxin (Trx) system plays a central role in this process. In chloroplasts, the Trx system consists of two pathways: the ferredoxin (Fd)/Trx pathway and the NADPH-Trx reductase C (NTRC) pathway. In Arabidopsis (Arabidopsis thaliana) mutants defective in either pathway, photoreduction of thiol enzymes was impaired, resulting in decreased carbon fixation. The close relationship between the Fd/Trx pathway and PROTON GRADIENT REGULATION 5 (PGR5)-dependent photosystem I cyclic electron transport (PSI CET) in the induction of photosynthesis was recently elucidated. However, how the PGR5-dependent pathway is involved in the NTRC pathway is unclear, although NTRC has been suggested to physically interact with PGR5. In this study, we analyzed Arabidopsis mutants lacking either the PGR5 or the NADH dehydrogenase-like (NDH)-dependent PSI CET pathway in the ntrc mutant background. The ntrc pgr5 double mutant suppressed both the growth defects and the high non-photochemical quenching (NPQ) phenotype of the ntrc mutant when grown under long-day conditions. By contrast, inactivation of NDH activity with the chlororespiratory reduction 2-2 (crr2-2) mutant failed to suppress either phenotype. We discovered that the phenotypic rescue of ntrc by pgr5 is caused by the partial restoration of Trx-dependent reduction of thiol enzymes during the induction of photosynthesis. These results suggest that electron partitioning to the PGR5-dependent pathway and the Trx system needs to be properly regulated for activation of the Calvin-Benson-Bassham cycle enzymes during the induction of photosynthesis.

DOI： 10.1093/pcp/pcab148

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

The albino lemma 1 (alm1) mutants of barley (Hordeum vulgare L.) exhibit obvious chlorophyll-deficient hulls. Hulls are seed-enclosing tissues on the spike, consisting of the lemma and palea. The alm1 phenotype is also expressed in the pericarp, culm nodes and basal leaf sheaths, but leaf blades and awns are normal green. A single recessive nuclear gene controls tissue-specific alm1 phenotypic expression. Positional cloning revealed that the ALM1 gene encodes a Golden 2-like (GLK) transcription factor, HvGLK2, belonging to the GARP subfamily of Myb transcription factors. This finding was validated by genetic evidence indicating that all 10 alm1 mutants studied had a lesion in functionally important regions of HvGLK2, including the three alpha-helix domains, an AREAEAA motif and the GCT box. Transmission electron microscopy revealed that, in lemmas of the alm1.g mutant, the chloroplasts lacked thylakoid membranes, instead of stacked thylakoid grana in wild-type chloroplasts. Compared with wild type, alm1.g plants showed similar levels of leaf photosynthesis but reduced spike photosynthesis by 34%. The alm1.g mutant and the alm1.a mutant showed a reduction in 100-grain weight by 15.8% and 23.1%, respectively. As in other plants, barley has HvGLK2 and a paralog, HvGLK1. In flag leaves and awns, HvGLK2 and HvGLK1 are expressed at moderate levels, but in hulls, HvGLK1 expression was barely detectable compared with HvGLK2. Barley alm1/Hvglk2 mutants exhibit more severe phenotypes than glk2 mutants of other plant species reported to date. The severe alm1 phenotypic expression in multiple tissues indicates that HvGLK2 plays some roles that are nonredundant with HvGLK1.

DOI： 10.1093/pcp/pcab001

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Vesicle-inducing protein in plastids 1 (VIPP1) is essential for the biogenesis and maintenance of thylakoid membranes, which transform light into life. However, it is unknown how VIPP1 performs its vital membrane-remodeling functions. Here, we use cryo-electron microscopy to determine structures of cyanobacterial VIPP1 rings, revealing how VIPP1 monomers flex and interweave to form basket-like assemblies of different symmetries. Three VIPP1 monomers together coordinate a non-canonical nucleotide binding pocket on one end of the ring. Inside the ring's lumen, amphipathic helices from each monomer align to form large hydrophobic columns, enabling VIPP1 to bind and curve membranes. In vivo mutations in these hydrophobic surfaces cause extreme thylakoid swelling under high light, indicating an essential role of VIPP1 lipid binding in resisting stress-induced damage. Using cryo-correlative light and electron microscopy (cryo-CLEM), we observe oligomeric VIPP1 coats encapsulating membrane tubules within the Chlamydomonas chloroplast. Our work provides a structural foundation for understanding how VIPP1 directs thylakoid biogenesis and maintenance.

DOI： 10.1016/j.cell.2021.05.011

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

DOI： 10.1093/pcp/pcab005

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

DOI： 10.1093/pcp/pcab003

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Although spikelet-related traits such as size of anther, spikelet, style, and stigma are associated with sexual reproduction in grasses, no QTLs have been reported in sorghum. Additionally, there are only a few reports on sorghum QTLs related to grain size, such as grain length, width, and thickness. In this study, we performed QTL analyses of nine spikelet-related traits (length of sessile spikelet, pedicellate spikelet, pedicel, anther, style, and stigma; width of sessile spikelet and stigma; and stigma pigmentation) and six grain-related traits (length, width, thickness, length/width ratio, length/thickness ratio, and width/thickness ratio) using sorghum recombinant inbred lines. We identified 36 and 7 QTLs for spikelet-related traits and grain-related traits, respectively, and found that most sorghum spikelet organ length- and width-related traits were partially controlled by the dwarf genes Dw1 and Dw3. Conversely, we found that these Dw genes were not strongly involved in the regulation of grain size. The QTLs identified in this study aid in understanding the genetic basis of spikelet- and grain-related traits in sorghum.

DOI： 10.1038/s41598-021-88917-x

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Protein phosphorylation is a fundamental post-translational modification in all organisms. In photoautotrophic organisms, protein phosphorylation is essential for the fine-tuning of photosynthesis. The reversible phosphorylation of the photosystem II (PSII) core and the light-harvesting complex of PSII (LHCII) contribute to the regulation of photosynthetic activities. Besides the phosphorylation of these major proteins, recent phosphoproteomic analyses have revealed that several proteins are phosphorylated in the thylakoid membrane. In this study, we utilized the Phos-tag technology for a comprehensive assessment of protein phosphorylation in the thylakoid membrane of Arabidopsis. Phos-tag SDS-PAGE enables the mobility shift of phosphorylated proteins compared with their non-phosphorylated isoform, thus differentiating phosphorylated proteins from their non-phosphorylated isoforms. We extrapolated this technique to two-dimensional (2D) SDS-PAGE for detecting protein phosphorylation in the thylakoid membrane. Thylakoid proteins were separated in the first dimension by conventional SDS-PAGE and in the second dimension by Phos-tag SDS-PAGE. In addition to the isolation of major phosphorylated photosynthesis-related proteins, 2D Phos-tag SDS-PAGE enabled the detection of several minor phosphorylated proteins in the thylakoid membrane. The analysis of the thylakoid kinase mutants demonstrated that light-dependent protein phosphorylation was mainly restricted to the phosphorylation of the PSII core and LHCII proteins. Furthermore, we assessed the phosphorylation states of the structural domains of the thylakoid membrane, grana core, grana margin, and stroma lamella. Overall, these results demonstrated that Phos-tag SDS-PAGE is a useful biochemical tool for studying in vivo protein phosphorylation in the thylakoid membrane protein.

DOI： 10.1007/s11120-020-00803-1

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Mitochondria are frequently observed in the vicinity of chloroplasts in photosynthesizing cells, and this association is considered necessary for their metabolic interactions. We previously reported that, in leaf palisade cells of Arabidopsis thaliana, mitochondria exhibit blue-light-dependent redistribution together with chloroplasts, which conduct accumulation and avoidance responses under the control of blue-light receptor phototropins. In this study, precise motility analyses by fluorescent microscopy revealed that the individual mitochondria in palisade cells, labeled with green fluorescent protein, exhibit typical stop-and-go movement. When exposed to blue light, the velocity of moving mitochondria increased in 30 min, whereas after 4 h, the frequency of stoppage of mitochondrial movement markedly increased. Using different mutant plants, we concluded that the presence of both phototropin1 and phototropin2 is necessary for the early acceleration of mitochondrial movement. On the contrary, the late enhancement of stoppage of mitochondrial movement occurs only in the presence of phototropin2 and only when intact photosynthesis takes place. A plasma-membrane ghost assay suggested that the stopped mitochondria are firmly adhered to chloroplasts. These results indicate that the physical interaction between mitochondria and chloroplasts is cooperatively mediated by phototropin2- and photosynthesis-dependent signals. The present study might add novel regulatory mechanism for light-dependent plant organelle interactions.

DOI： 10.1111/jipb.12910

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Sorghum [Sorghum bicolor (L.) Moench] grown locally by Japanese farmers is generically termed Takakibi, although its genetic diversity compared with geographically distant varieties or even within Takakibi lines remains unclear. To explore the genomic diversity and genetic traits controlling biomass and other physiological traits in Takakibi, we focused on a landrace, NOG, in this study. Admixture analysis of 460 sorghum accessions revealed that NOG belonged to the subgroup that represented Asian sorghums, and it was only distantly related to American/African accessions including BTx623. In an attempt to dissect major traits related to biomass, we generated a recombinant inbred line (RIL) from a cross between BTx623 and NOG, and we constructed a high-density linkage map based on 3,710 single-nucleotide polymorphisms obtained by restriction-site-associated DNA sequencing of 213 RIL individuals. Consequently, 13 fine quantitative trait loci (QTLs) were detected on chromosomes 2, 3, 6, 7, 8 and 9, which included five QTLs for days to heading, three for plant height (PH) and total shoot fresh weight and two for Brix. Furthermore, we identified two dominant loci for PH as being identical to the previously reported dw1 and dw3. Together, these results corroborate the diversified genome of Japanese Takakibi, while the RIL population and high-density linkage map generated in this study will be useful for dissecting other important traits in sorghum.

DOI： 10.1093/pcp/pcaa056

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DOI： 10.1093/pcp/pcaa032

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Bundle Sheath Defective 2, BSD2, is a stroma-targeted protein initially identified as a factor required for the biogenesis of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) in maize. Plants and algae universally have a homologous gene for BSD2 and its deficiency causes a RuBisCO-less phenotype. As RuBisCO can be the rate-limiting step in CO2 assimilation, the overexpression of BSD2 might improve photosynthesis and productivity through the accumulation of RuBisCO. To examine this hypothesis, we produced BSD2 overexpression lines in Arabidopsis. Compared with wild type, the BSD2 overexpression lines BSD2ox-2 and BSD2ox-3 expressed 4.8-fold and 8.8-fold higher BSD2 mRNA, respectively, whereas the empty-vector (EV) harbouring plants had a comparable expression level. The overexpression lines showed a significantly higher CO2 assimilation rate per available CO2 and productivity than EV plants. The maximum carboxylation rate per total catalytic site was accelerated in the overexpression lines, while the number of total catalytic sites and RuBisCO content were unaffected. We then isolated recombinant BSD2 (rBSD2) from E. coli and found that rBSD2 reduces disulfide bonds using reductants present in vivo, for example glutathione, and that rBSD2 has the ability to reactivate RuBisCO that has been inactivated by oxidants. Furthermore, 15% of RuBisCO freshly isolated from leaves of EV was oxidatively inactivated, as compared with 0% in BSD2-overexpression lines, suggesting that the overexpression of BSD2 maintains RuBisCO to be in the reduced active form in vivo. Our results demonstrated that the overexpression of BSD2 improves photosynthetic efficiency in Arabidopsis and we conclude that it is involved in mediating RuBisCO activation.

DOI： 10.1111/tpj.14617

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Language：Japanese   Publisher：Japanese Society of Breeding  

DOI： 10.1270/jsbbr.22.W05

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Commercial seeds of Brassicaceae vegetable crops are mostly F1 hybrids, the production of which depends on self-incompatibility during pollination. Self-incompatibility is known to be weakened by exposure to elevated temperatures, which may compromise future breeding and seed production. In the Brassicaceae, self-incompatibility is controlled by two genes, SRK and SCR, which function as female and male determinants of recognition specificity, respectively. However, the molecular mechanisms underlying the breakdown of self-incompatibility under high temperature are poorly understood. In this study, we examined the self-incompatibility phenotypes of self-incompatible Arabidopsis thaliana SRK-SCR transformants under normal (23 °C) and elevated (29 °C) temperatures. Exposure to elevated temperature caused defects in the stigmatic, but not the pollen, self-incompatibility response. In addition, differences in the response to elevated temperature were observed among different S haplotypes. Subcellular localization revealed that high temperature disrupted the targeting of SRK to the plasma membrane. SRK localization in plants transformed with different S haplotypes corresponded to their self-incompatibility phenotypes, further indicating that defects in SRK localization were responsible for the breakdown in the self-incompatibility response at high temperature. Our results provide new insights into the causes of instability in self-incompatibility phenotypes.

DOI： 10.1093/jxb/erz343

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Sorghum [Sorghum bicolor (L.) Moench] is a C4 crop known to be adaptable to harsh environments such as those under high temperature and water deficit. In this study, we focused on a Japanese sorghum landrace Takakibi (NOG) and employed chlorophyll fluorescence measurements to assess its response to environmental stress. Comparison of photosynthetic rate evaluated using two parameters (effective quantum yield and electron transfer rate) indicated that NOG showed less activity than BTx623 in the pre-flowering stage, which was consistent with the higher susceptibility of NOG seedlings to drought than BTx623. The observed differences in photosynthetic activity between the two cultivars were detectable without drought conditions on days with high temperature and strong light. Interestingly, the photosynthetic activity of NOG leaves in stress conditions increased soon after heading, and the trend was similar to that in BTx642, a well-characterized post-flowering drought-tolerant cultivar. In contrast, BTx623 showed a gradual decline in photosynthetic rate. Thus, we inferred that Japanese Takakibi has the potential to show pre-flowering drought susceptibility and post-flowering drought tolerance, through which it adapts to local climates with high temperature and strong light at harvest.

DOI： 10.1093/pcp/pcz107

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：American Society of Plant Biologists ({ASPB})  

Photodamage of the PSII reaction center (RC) is an inevitable process in an oxygen-rich environment. The damaged PSII RC proteins (Dam-PSII) undergo degradation via the thylakoid membrane-bound FtsH metalloprotease, followed by posttranslational assembly of PSII. While the effect of Dam-PSII on gene regulation is described for cyanobacteria, its role in land plants is largely unknown. In this study, we reveal an intriguing retrograde signaling pathway by using the Arabidopsis (Arabidopsis thaliana) yellow variegated2-9 mutant, which expresses a mutated FtsH2 (FtsH2G267D) metalloprotease, specifically impairing its substrate-unfolding activity. This lesion leads to the perturbation of PSII protein homeostasis (proteostasis) and the accumulation of Dam-PSII. Subsequently, this results in an up-regulation of salicylic acid (SA)-responsive genes, which is abrogated by inactivation of either an SA transporter in the chloroplast envelope membrane or extraplastidic SA signaling components as well as by removal of SA. These results suggest that the stress hormone SA, which is mainly synthesized via the chloroplast isochorismate pathway in response to the impaired PSII proteostasis, mediates the retrograde signaling. These findings reinforce the emerging view of chloroplast function toward plant stress responses and suggest SA as a potential plastid factor mediating retrograde signaling.

DOI： 10.1104/pp.19.00483

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

Cell disruption and protein solubilization protocols for the relative quantification of individual subunits in photosystems were developed for photosynthetic organisms including cyanobacterium Synechocystis sp. PCC 6803, green-algae Chlamydomonas reinhardtii, and seed plant Arabidopsis thaliana. The optimal methods for the disruption of Chlamydomonas, Synechocystis, and Arabidopsis cells were sonication, microbeads (Φ approximately 0.1 mm), and large beads (Φ = 5.0 mm), respectively. Extraction of the total proteins exceeded 90% using each optimal cell disruption method. Solubilization efficiency of membrane proteins was improved by the phase transfer surfactant (PTS) method. Ninety seven and 114 proteins from Chlamydomonas and Synechocystis, respectively, including membrane proteins such as photosystem proteins, ATP synthase, and NADH dehydrogenase, were successfully analyzed by nano-liquid chromatography tandem mass spectrometry. These results also indicated the improved efficiency of solubilization and trypsin digestion using PTS buffer. The results of the relative quantitative evaluation of photosystem subunits in Chlamydomonas and Synechocystis grown under high-light conditions were consistent with those of previous studies. Thus, the optimal cell disruption and PTS methods allow for comprehensive relative quantitative proteome analysis of photosynthetic organisms. Additionally, NdhD1 and NdhF1, which are NDH-1 subunit homologs, were increased under high-light conditions, suggesting that the NDH-1L complex, including NdhD1 and NdhF1, is increased under high-light conditions. The relative quantitative proteome analysis of individual subunits indicates the diverse functions of NDH-1 protein.

DOI： 10.1016/j.jbiosc.2018.09.001

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FtsH is an essential ATP-dependent metalloprotease for protein quality control in the thylakoid membrane of Arabidopsis thaliana chloroplasts. It is required for chloroplast development during leaf growth, and particularly for the specific degradation of photo-damaged D1 protein in the photosystem II (PSII) complex to maintain photosynthesis activity. In the thylakoid membrane, the reversible phosphorylation of proteins is known to control the activity and remodeling of photosynthetic complexes, and previous studies implicate that FtsH is also phosphorylated. We therefore assessed the phosphorylation status of FtsH and its possible role in the regulatory mechanism in this study. The phosphorylation level of FtsHs that compose the FtsH heterohexameric complex was investigated by phosphate-affinity gel electrophoresis using a Phos-Tag molecule. Phos-tag SDS-PAGE of thylakoid proteins and subsequent immunoblot analysis showed that both type A (FtsH1/5) and type B (FtsH2/8) subunits were separable into phosphorylated and non-phosphorylated forms. Neither different light conditions nor the lack of two major thylakoid kinases, STN7 and STN8, resulted in any clear difference in FtsH phosphorylation, suggesting that this process is independent of the light-dependent regulation of photosynthesis-related proteins. Site-directed mutagenesis of putatively phosphorylated Ser or Thr residues into Ala demonstrated that Ser-212 may play a role in FtsH stability in the thylakoid membranes. Different phosphorylation status of FtsH oligomers analyzed by two-dimensional clear-native/Phos-tag SDS-PAGE implied that phosphorylation partially affects FtsH complex formation or its stability.

DOI： 10.3389/fpls.2019.01080

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

Mitochondria and chloroplasts (plastids) both harbour extranuclear DNA that originates from the ancestral endosymbiotic bacteria. These organelle DNAs (orgDNAs) encode limited genetic information but are highly abundant, with multiple copies in vegetative tissues, such as mature leaves. Abundant orgDNA constitutes a substantial pool of organic phosphate along with RNA in chloroplasts, which could potentially contribute to phosphate recycling when it is degraded and relocated. However, whether orgDNA is degraded nucleolytically in leaves remains unclear. In this study, we revealed the prevailing mechanism in which organelle exonuclease DPD1 degrades abundant orgDNA during leaf senescence. The DPD1 degradation system is conserved in seed plants and, more remarkably, we found that it was correlated with the efficient use of phosphate when plants were exposed to nutrient-deficient conditions. The loss of DPD1 compromised both the relocation of phosphorus to upper tissues and the response to phosphate starvation, resulting in reduced plant fitness. Our findings highlighted that DNA is also an internal phosphate-rich reservoir retained in organelles since their endosymbiotic origin.

DOI： 10.1038/s41477-018-0291-x

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：American Society of Plant Biologists ({ASPB})  

Specific degradation of photodamaged D1, the photosystem II (PSII) reaction center protein, is a crucial step in the PSII repair cycle to maintain photosynthesis activity. Processive proteolysis by the FtsH protease is fundamental to cooperative D1 degradation. Here, we attempted to purify the FtsH complex to elucidate its regulation mechanisms and substrate recognition in Arabidopsis (Arabidopsis thaliana). Unlike previously reported prokaryotic and mitochondrial FtsHs, the Arabidopsis chloroplastic FtsH does not appear to form a megacomplex with prohibition-like proteins but instead accumulates as smaller complexes. The copurified fraction was enriched with a partial PSII intermediate presumably undergoing repair, although its precise properties were not fully clarified. In addition, we copurified a bacteria-type GTPase localized in chloroplasts, EngA, and confirmed its interaction with FtsH by subsequent pull-down and bimolecular fluorescence complementation assays. While the engA mutation is embryo lethal, the transgenic lines overexpressing EngA (EngA-OX) showed leaf variegation reminiscent of the variegated mutant lacking FtsH2. EngA-OX was revealed to accumulate more cleaved D1 fragments and reactive oxygen species than the wild type, indicative of compromised PSII repair. Based on these results and the fact that FtsH becomes more stable in EngA-OX, we propose that EngA negatively regulates FtsH stability. We demonstrate that proper FtsH turnover is crucial for PSII repair in the chloroplasts of Arabidopsis. Consistent with the increased turnover of FtsH under high-light conditions in Chlamydomonas reinhardtii, our findings underline the rapid turnover of not only D1 but also FtsH proteases in the PSII repair cycle.

DOI： 10.1104/pp.18.00652

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DOI： 10.1186/s12870-018-1294-5

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DOI： 10.1104/pp.18.00444

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Protein homeostasis in the thylakoid membranes is dependent on protein quality control mechanisms, which are necessary to remove photodamaged and misfolded proteins. An ATP-dependent zinc metalloprotease, FtsH, is the major thylakoid membrane protease. FtsH proteases in the thylakoid membranes of Arabidopsis thaliana form a hetero-hexameric complex consisting of four FtsH subunits, which are divided into two types: type A (FtsH1 and FtsH5) and type B (FtsH2 and FtsH8). An increasing number of studies have identified the critical roles of FtsH in the biogenesis of thylakoid membranes and quality control in the photosystem II repair cycle. Furthermore, the involvement of FtsH proteolysis in a singlet oxygen- and EXECUTER1-dependent retrograde signaling mechanism has been suggested recently. FtsH is also involved in the degradation and assembly of several protein complexes in the photosynthetic electron-transport pathways. In this minireview, we provide an update on the functions of FtsH in thylakoid biogenesis and describe our current understanding of the D1 degradation processes in the photosystem II repair cycle. We also discuss the regulation mechanisms of FtsH protease activity, which suggest the flexible oligomerization capability of FtsH in the chloroplasts of seed plants.

DOI： 10.3389/fpls.2018.00855

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DOI： 10.4172/2329-9029.1000220

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DOI： 10.1038/NPLANTS2015.57

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DOI： 10.4161/auto.28529

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The reaction center protein D1 of photosystem II (PSII), known as a primary target of photodamage, is repaired efficiently by the PSII repair cycle, to cope with constant photooxidative damage. Recent studies of Arabidopsis show that the endo-type Deg protease and the exo-type FtsH proteases cooperatively degrade D1 in the PSII repair in vivo. It is particularly interesting that we observed upregulation of Clp and SppA proteases when FtsH was limited in the mutant lacking FtsH2. To examine how the complementary functions of chloroplastic proteases are commonly regulated, we undertook a high-light stress on wild-type Arabidopsis leaves. The result that wild type leaves also showed increased levels of these proteases upon exposure to excessively strong illumination not only revealed the importance of FtsH and Deg in the PSII repair, but also implied cooperation among chloroplastic proteases under chronic stress conditions.

DOI： 10.4161/psb.23198

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VIPP1 protein in photosynthetic organisms is homologous to bacterial PspA, which protects plasma membrane integrity upon stresses. Despite the proposed role of VIPP1 in thylakoid biogenesis, its precise function remains unclear. Recently, our in-depth analysis of Arabidopsis vipp1 mutants revealed VIPP1's involvement in the maintenance of chloroplast envelopes. Chloroplasts in intact vipp1 leaves exhibited spherical balloon-like morphology, which resulted from osmotic stress across envelopes. In fact, observation of VIPP1 fused to green fluorescence protein in vivo revealed that most VIPP1 is localized as a lattice-like macro complex attached along with the envelope. Because of the proposed function in thylakoids, we examined whether vipp1 also exhibited altered morphologies in thylakoids. Results show that thylakoid morphologies were detected irregularly, but vipp1 chloroplasts retained normal-appearing grana stacks. We infer that VIPP1 might influence thylakoids as well as envelopes, but that it is not involved directly in thylakoid membrane formation.

DOI： 10.4161/psb.22860

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DOI： 10.1111/pce.12090

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DOI： 10.1111/tpj.12154

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DOI： 10.1105/tpc.113.116947

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：The Japanese Society of Applied Glycoscience  

DOI： 10.5458/jag.jag.jag-2012_006

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DOI： 10.1007/978-3-642-32034-7_82

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DOI： 10.1007/978-3-642-32034-7_145

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DOI： 10.1093/pcp/pcr189

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DOI： 10.1105/tpc.112.103606

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DOI： 10.1111/j.1365-313X.2012.04904.x

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DOI： 10.1104/pp.112.199042

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Organelle DNA in plastids and mitochondria is present in multiple copies and undergoes degradation developmentally. For example, organelle DNA that is detectable cytologically using DNA-fluorescent dye disappears during pollen development. Nevertheless, nucleases involved in this degradation process remain unknown. Our recent study identified the organelle nuclease, DPD1, which has Mg2+ -dependent exonuclease activity in vitro. The discovery of DPD1 emerged from Arabidopsis mutant screening and concomitant isolation of dpd1 mutants that retain organelle DNA in mature pollen. DPD1 is conserved only in angiosperms: not in other photosynthetic organisms. Despite these findings, the physiological significance of organelle DNA degradation during pollen development remains unclear because dpd1 exhibits no apparent defects in pollen viability or in the maternal inheritance of organelle DNA. We discuss a possible role of organelle DNA degradation mediated by DPD1, based on a DPD1 expression profile studied using in silico analyses.

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DOI： 10.1371/journal.ppat.1002146

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DOI： 10.1105/tpc.111.084012

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DOI： 10.5511/plantbiotechnology.10.1104a

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Protein quality control plays an important role in the photosynthetic apparatus because its components receive excess light energy and are susceptible to photooxidative damage. In chloroplasts, photodamage is targeted to the D1 protein of Photosystem II (PSII). The coordinated PSII repair cycle (PSII disassembly, D1 degradation and synthesis, and PSII reassembly) is necessary to mitigate photoinhibition. A thylakoid protease FtsH, which is formed predominantly as a heteromeric complex with two isoforms of FtsH2 and FtsH5 in Arabidopsis, is the major protease involved in PSII repair. A mutant lacking FtsH2 (termed var2) shows compromised D1 degradation. Furthermore, var2 accumulates high levels of chloroplastic reactive oxygen species (cpROS), reflecting photooxidative stress without functional PSII repair. To examine if the cpROS produced in var2 are connected to a ROS signaling pathway mediated by plasma membrane NADPH oxidase (encoded by AtRbohD or AtRbohF), we generated mutants in which either Rboh gene was inactivated under var2 background. Lack of NADPH oxidases had little or no impact on cpROS accumulation. It seems unlikely that cpROS in var2 activate plasma membrane NADPH oxidases to enhance ROS production and the signaling pathway. Mutants that are defective in PSII repair might be valuable for investigating cpROS and their physiological roles.

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DOI： 10.1111/j.1365-313X.2009.03907.x

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We have previously reported that Al-induces citrate and malate efflux from P-sufficient and P-deficient plants of rape (Brassica napus L.) and that P-deficiency alone could not induce this response. Further investigation showed that the transcript of two genes designated BnALMT1 and BnALMT2 is accumulated in roots by Al-treatment. Transgenic tobacco cells (Nicotiana tabacum) and Xenopus laevis oocytes expressing the BnALMT1 and BnALMT2 proteins released more malate than control cells in the presence of Al, indicating that the BnALMT genes encode an Al-activated malate transporter. The transgenic tobacco cells exposed to toxic level of Al grew better than control cells indicating that the genes can enhance Al-resistance of plant cells. In this study we showed the subcellular localization of BnALMT1 fused to the green fluoresce protein (GFP). The BnALMT1:: GFP construct was transiently expressed in protoplasts prepared from Arabidopsis leaves using the polyethylene glycol (PEG) method. The result showed that the BnALMT1 protein is localized in the plasma membrane. This provides further evidence that the BnALMT proteins facilitate the transport of malate across the plasma membrane (PM).

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DOI： 10.1146/annurev.arplant.57.032905.105401

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DOI： 10.1046/j.1365-2443.2002.00558.x

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Language：Japanese   Publisher：日本育種学会  

イネにおけるアントシアニン生合成の転写制御遺伝子の発現解析に必要なトランジェントアッセイ系を, 常時材料を準備できるイネ完熟種子糊粉層で確立した. まず, 岡大資生研紫米 (RIB-PI) の完熟種子を用いて糊粉層を露出するための吸水時間と温度を検討した. 露出できた糊粉層にトウモロコシのアントシアニン生合成の転写制御遺伝子, ClとB-Peruをパーティクルガンで導入したところ, アントシアニンのスポットが観察されたので, 両遺伝子を用いたトランジェントアッセイ系について至適条件を検討した. その結果, 28℃ で4時間吸水させて露出した糊粉層でアントシアニンのスポット数が最大になった. また, 導入するプラスミドの量は, ClとBPeruがともに5μgかClが5μgでB-Peruが10μgのときに, アントシアニンのスポット数が多くなった. 以上の結果から, イネの完熟種子糊粉層を用いたトランジェントアッセイとして, 28℃ で4時間吸水させて糊粉層を露出させ, C1とB-Pmをともに5μgずつ導入することによって, 安定的にアントシアニンを誘導できることが明らかとなった.

DOI： 10.1270/jsbbr.2.181

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Publishing type：Research paper (scientific journal)  

DOI： 10.1023/A:1006072014605

Web of Science

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Publishing type：Research paper (scientific journal)  

DOI： 10.1016/S0378-1119(98)00417-X

Web of Science

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Publishing type：Research paper (scientific journal)  

Web of Science

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

Web of Science

CiNii Article

CiNii Books

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Publishing type：Research paper (scientific journal)  

DOI： 10.1046/j.1365-313x.1997.12061319.x

Web of Science

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

DOI： 10.1266/ggs.72.311

Web of Science

CiNii Article

CiNii Books

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Other Link： https://jlc.jst.go.jp/DN/JALC/00084483256?from=CiNii

Publishing type：Research paper (scientific journal)  

DOI： 10.1007/BF00020217

Web of Science

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Publishing type：Research paper (scientific journal)  

DOI： 10.1105/tpc.8.8.1377

Web of Science

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Publishing type：Research paper (scientific journal)  

Web of Science

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Publishing type：Research paper (scientific journal)  

DOI： 10.1046/j.1365-313X.1994.6040503.x

Web of Science

CiNii Article

CiNii Books

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Publishing type：Research paper (scientific journal)  

Web of Science

CiNii Article

CiNii Books

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Publishing type：Research paper (scientific journal)  

Web of Science

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Publishing type：Research paper (scientific journal)  

Web of Science

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Publishing type：Research paper (scientific journal)  

DOI： 10.1073/pnas.90.2.497

Web of Science

CiNii Article

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

DOI： 10.1266/jjg.67.309

Web of Science

CiNii Article

CiNii Books

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Other Link： https://jlc.jst.go.jp/DN/JALC/00079223454?from=CiNii

Publishing type：Research paper (scientific journal)  

Web of Science

CiNii Article

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

DOI： 10.1266/jjg.66.597

Web of Science

CiNii Article

CiNii Books

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Other Link： http://agriknowledge.affrc.go.jp/RN/2010472559

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

Web of Science

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

DOI： 10.1266/jjg.65.1

Web of Science

CiNii Article

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Language：English  

DOI： 10.1093/nar/17.18.7519

Web of Science

PubMed

CiNii Article

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Publishing type：Research paper (scientific journal)  

DOI： 10.1266/jjg.64.49

Web of Science

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Event date： 2023.6.5 - 2023.6.9

Presentation type：Poster presentation  

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Event date： 2023.6.3 - 2023.6.4

Presentation type：Poster presentation  

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Event date： 2023.6.3 - 2023.6.4

Presentation type：Poster presentation  

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Event date： 2023.6.3 - 2023.6.4

Presentation type：Poster presentation  

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Event date： 2023.3.15 - 2023.3.17

Presentation type：Poster presentation  

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Event date： 2023.3.15 - 2023.3.17

Presentation type：Poster presentation  

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Event date： 2023.3.15 - 2023.3.17

Presentation type：Oral presentation (general)  

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Event date： 2023.3.15 - 2023.3.17

Presentation type：Poster presentation  

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Event date： 2023.3.15 - 2023.3.17

Presentation type：Poster presentation  

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Event date： 2022.7.31 - 2022.8.5

Presentation type：Poster presentation  

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Event date： 2022.7.31 - 2022.8.5

Presentation type：Poster presentation  

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Event date： 2022.7.9 - 2022.7.13

Presentation type：Poster presentation  

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Event date： 2022.3.22 - 2022.3.24

Presentation type：Oral presentation (general)  

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Event date： 2022.3.22 - 2022.3.24

Presentation type：Oral presentation (general)  

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Event date： 2021.8.25 - 2021.8.27

Presentation type：Oral presentation (invited, special)  

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Event date： 2021.7.14 - 2021.7.16

Presentation type：Oral presentation (invited, special)  

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Event date： 2020.10.10 - 2020.10.11

Presentation type：Poster presentation  

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Event date： 2020.10.10 - 2020.10.11

Presentation type：Oral presentation (general)  

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Event date： 2020.10.10 - 2020.10.11

Presentation type：Poster presentation  

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Event date： 2020.9.19 - 2020.9.21

Presentation type：Oral presentation (general)  

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Event date： 2020.3.28 - 2020.3.29

Presentation type：Poster presentation  

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Event date： 2020.3.28 - 2020.3.29

Presentation type：Oral presentation (general)  

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Event date： 2020.3.28 - 2020.3.29

Presentation type：Poster presentation  

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Event date： 2020.3.19 - 2020.3.21

Presentation type：Oral presentation (general)  

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Event date： 2020.3.19 - 2020.3.21

Presentation type：Poster presentation  

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Event date： 2020.3.19 - 2020.3.21

Presentation type：Oral presentation (general)  

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Event date： 2020

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Event date： 2020

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Event date： 2019.9.6 - 2019.9.7

Presentation type：Symposium, workshop panel (nominated)  

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Event date： 2019.5.25 - 2019.5.26

Presentation type：Poster presentation  

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Event date： 2019.3.13 - 2019.3.15

Presentation type：Poster presentation  

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Event date： 2019.3.13 - 2019.3.15

Presentation type：Oral presentation (general)  

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Event date： 2019.3.13 - 2019.3.15

Presentation type：Oral presentation (general)  

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Event date： 2019.3.13 - 2019.3.15

Presentation type：Poster presentation  

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Event date： 2018.11.29

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：名古屋  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Poster presentation  

Venue：Kurashiki, Japan  

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Event date： 2018.11.7 - 2018.11.10

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Kurashiki, Japan  

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Event date： 2018.9.24 - 2018.9.27

Language：English   Presentation type：Poster presentation  

Venue：Kobe, Japan  

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Event date： 2018.9.24 - 2018.9.27

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Kobe, Japan  

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Event date： 2018.9.24 - 2018.9.27

Language：English   Presentation type：Poster presentation  

Venue：Kobe, Japan  

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Event date： 2018.9.24 - 2018.9.27

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Kobe, Japan  

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Event date： 2018.9.24

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Shanghai, China  

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Event date： 2018.9.22 - 2018.9.24

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：岡山  

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Event date： 2018.9.22 - 2018.9.24

Language：Japanese   Presentation type：Poster presentation  

Venue：岡山  

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Event date： 2018.9.22 - 2018.9.24

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：岡山  

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Event date： 2018.9.19 - 2018.9.23

Language：English   Presentation type：Poster presentation  

Venue：Beijing, China  

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Event date： 2018.9.19 - 2018.9.23

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Beijing, China  

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Event date： 2018.5.26 - 2018.5.27

Language：Japanese   Presentation type：Poster presentation  

Venue：仙台  

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Event date： 2018.5.26 - 2018.5.27

Language：Japanese   Presentation type：Poster presentation  

Venue：仙台  

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Event date： 2018.5.11

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Tainan, Taiwan  

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Event date： 2018.4.27

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：London, UK  

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Event date： 2018.4.26

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Cambridge, UK  

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Event date： 2018.4.25

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Egham, UK  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Poster presentation  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Poster presentation  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Poster presentation  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Poster presentation  

Venue：札幌  

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Event date： 2018.3.28 - 2018.3.30

Language：Japanese   Presentation type：Oral presentation (general)  

Venue：札幌  

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Event date： 2018.3.27

Language：Japanese   Presentation type：Oral presentation (invited, special)  

Venue：札幌  

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Event date： 2018.3.25 - 2018.3.26

Language：Japanese   Presentation type：Poster presentation  

Venue：福岡  

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Event date： 2018.3.25 - 2018.3.26

Language：Japanese   Presentation type：Poster presentation  

Venue：福岡  

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Event date： 2018.3.25 - 2018.3.26

Language：Japanese   Presentation type：Poster presentation  

Venue：福岡  

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Event date： 2017.11.3 - 2017.11.6

Language：English   Presentation type：Oral presentation (general)  

Venue：Taipei, Taiwan  

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Event date： 2017.11.3 - 2017.11.6

Language：English   Presentation type：Poster presentation  

Venue：Taipei, Taiwan  

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Event date： 2017.11.3 - 2017.11.6

Language：English   Presentation type：Oral presentation (general)  

Venue：Taipei, Taiwan  

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Event date： 2017.11.3 - 2017.11.6

Language：English   Presentation type：Poster presentation  

Venue：Taipei, Taiwan  

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Event date： 2017.11.3 - 2017.11.6

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Taipei, Taiwan  

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Event date： 2017.10.7 - 2017.10.9

Language：Japanese   Presentation type：Poster presentation  

Venue：盛岡  

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Event date： 2017.10.7 - 2017.10.9

Language：Japanese   Presentation type：Poster presentation  

Venue：盛岡  

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Event date： 2017.5.22 - 2017.5.26

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Hangzhou, China  

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Event date： 2017.5.22 - 2017.5.26

Language：English   Presentation type：Poster presentation  

Venue：Honolulu, Hawaii, USA  

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Event date： 2017.5.22

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Hangzhou, China  

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Event date： 2017.5.22

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Taichung, Taiwan  

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Event date： 2017.3.28 - 2017.3.30

Language：Japanese   Presentation type：Poster presentation  

Venue：名古屋  

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Event date： 2017.3.20

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Nairobi, Kenya  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.3.16 - 2017.3.18

Language：Japanese   Presentation type：Poster presentation  

Venue：鹿児島  

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Event date： 2017.2.23

Language：English   Presentation type：Oral presentation (invited, special)  

Venue：Shanghai, China  

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Event date： 2016.11.10 - 2016.11.11

Language：English   Presentation type：Oral presentation (general)  

Venue：Nairobi, Kenya  

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Event date： 2016.10.31 - 2016.11.4

Language：English   Presentation type：Oral presentation (general)  

Venue：Jeju, Korea  

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Event date： 2016.10.3 - 2016.10.7

Language：English   Presentation type：Poster presentation  

Venue：Brisbane, Australia  

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Event date： 2016.9.30

Language：Japanese   Presentation type：Oral presentation (invited, special)  

Venue：生駒  

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Event date： 2016.9.23 - 2016.9.24