Pub Date : 2024-11-01Epub Date: 2024-09-30DOI: 10.1111/tpj.17043
Xian-Min Chen, Zhi-Wei Wang, Xiao-Gui Liang, Feng-Yuan Li, Bin-Bin Li, Gong Wu, Fei Yi, Tim L Setter, Si Shen, Shun-Li Zhou
Starch synthesis in maize endosperm adheres to the basipetal sequence from the apex downwards. However, the mechanism underlying nonuniformity among regions of the endosperm in starch accumulation and its significance is poorly understood. Here, we examined the spatiotemporal transcriptomes and starch accumulation dynamics in apical (AE), middle (ME), and basal (BE) regions of endosperm throughout the filling stage. Results demonstrated that the BE had lower levels of gene transcripts and enzymes facilitating starch synthesis, corresponding to incomplete starch storage at maturity, compared with AE and ME. Contrarily, the BE showed abundant gene expression for genetic processing and slow progress in physiological development (quantified by an index calculated from the expression values of development progress marker genes), revealing a sustained cell vitality of the BE. Further analysis demonstrated a significant parabolic correlation between starch synthesis and physiological development. An in-depth examination showed that the BE had more active signaling pathways of IAA and ABA than the AE throughout the filling stage, while ethylene showed the opposite pattern. Besides, SNF1-related protein kinase1 (SnRK1) activity, a regulator for starch synthesis modulated by trehalose-6-phosphate (T6P) signaling, was kept at a lower level in the BE than the AE and ME, corresponding to the distinct gene expression in the T6P pathway in starch synthesis regulation. Collectively, the findings support an improved understanding of the timing of starch synthesis and cell vitality in regions of the endosperm during development, and potential regulation from hormone signaling and T6P/SnRK1 signaling.
玉米胚乳中的淀粉合成遵循从顶点向下的基瓣序列。然而,人们对胚乳各区域淀粉积累不均匀的机制及其意义还知之甚少。在这里,我们研究了胚乳顶端(AE)、中间(ME)和基部(BE)区域在整个灌浆期的时空转录组和淀粉积累动态。结果表明,与 AE 和 ME 相比,BE 中促进淀粉合成的基因转录本和酶的水平较低,这与成熟时淀粉储存不完全有关。与此相反,BE 的基因处理基因表达量丰富,生理发育进度缓慢(根据发育进度标记基因的表达值计算出的指数进行量化),显示出 BE 细胞的持续活力。进一步分析表明,淀粉合成与生理发育之间存在明显的抛物线相关性。深入研究表明,在整个灌浆期,BE 的 IAA 和 ABA 信号通路比 AE 更活跃,而乙烯则相反。此外,SNF1相关蛋白激酶1(SnRK1)的活性(SNF1相关蛋白激酶1是淀粉合成的调控因子,受6-磷酸三卤淀粉(T6P)信号调控)在BE中保持在低于AE和ME的水平,这与淀粉合成调控中T6P通路的不同基因表达相对应。总之,这些发现有助于人们更好地了解胚乳发育过程中淀粉合成和细胞活力的时间以及激素信号和T6P/SnRK1信号的潜在调控。
{"title":"Incomplete filling in the basal region of maize endosperm: timing of development of starch synthesis and cell vitality.","authors":"Xian-Min Chen, Zhi-Wei Wang, Xiao-Gui Liang, Feng-Yuan Li, Bin-Bin Li, Gong Wu, Fei Yi, Tim L Setter, Si Shen, Shun-Li Zhou","doi":"10.1111/tpj.17043","DOIUrl":"10.1111/tpj.17043","url":null,"abstract":"<p><p>Starch synthesis in maize endosperm adheres to the basipetal sequence from the apex downwards. However, the mechanism underlying nonuniformity among regions of the endosperm in starch accumulation and its significance is poorly understood. Here, we examined the spatiotemporal transcriptomes and starch accumulation dynamics in apical (AE), middle (ME), and basal (BE) regions of endosperm throughout the filling stage. Results demonstrated that the BE had lower levels of gene transcripts and enzymes facilitating starch synthesis, corresponding to incomplete starch storage at maturity, compared with AE and ME. Contrarily, the BE showed abundant gene expression for genetic processing and slow progress in physiological development (quantified by an index calculated from the expression values of development progress marker genes), revealing a sustained cell vitality of the BE. Further analysis demonstrated a significant parabolic correlation between starch synthesis and physiological development. An in-depth examination showed that the BE had more active signaling pathways of IAA and ABA than the AE throughout the filling stage, while ethylene showed the opposite pattern. Besides, SNF1-related protein kinase1 (SnRK1) activity, a regulator for starch synthesis modulated by trehalose-6-phosphate (T6P) signaling, was kept at a lower level in the BE than the AE and ME, corresponding to the distinct gene expression in the T6P pathway in starch synthesis regulation. Collectively, the findings support an improved understanding of the timing of starch synthesis and cell vitality in regions of the endosperm during development, and potential regulation from hormone signaling and T6P/SnRK1 signaling.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338081","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-09-27DOI: 10.1111/tpj.17046
Landi Feng, Yingjun Yao, Minghui Kang, Wengjie Yang, Yu Han, Wei Liu, Xiaonan Li, Na Li, Yongqi Hu, Jianquan Liu, Quanjun Hu
Ilex is known for its rich content of secondary metabolites, particularly triterpenoid saponins. These compounds hold significant value in natural remedies and herbal medicine. However, the molecular mechanisms responsible for triterpenoid biosynthesis in plants of this genus remain largely unexplored. In this study, we successfully generated the first chromosome-scale genome of Ilex hylonoma. The assembly, comprising 20 anchored chromosomes, has an N50 contig size of 2.13 Mb and a scaffold size of 33.68 Mb. Comparative genome analyses with two other congeners with available chromosome-level genomes suggested that an end-to-end chromosome fusion event likely contributed to the reduction in chromosome number from n = 20 to n = 19 within this genus. By integrating transcriptomic and metabolomic data, we identified the gene expression patterns and metabolite profiles of I. hylonoma across three commonly utilized medicinal tissues. We subsequently pinpointed candidate genes involved in the regulation of triterpenoid saponin biosynthesis, including CYP450 genes, UGT genes, and associated transcription factors. Furthermore, yeast heterologous expression analysis revealed that ihyl08363 catalyzed the conversion of β-amyrin into oleanolic acid, while ihyl04303 catalyzed the C-2α hydroxylation of oleanolic acid to produce maslinic acid. This integrated analysis provides valuable insights into the biosynthesis of important triterpenoid saponins in medicinal Ilex plants.
{"title":"Integrated genomic, transcriptomic, and metabolomic analyses of Ilex hylonoma provide insights into the triterpenoid saponin biosynthesis.","authors":"Landi Feng, Yingjun Yao, Minghui Kang, Wengjie Yang, Yu Han, Wei Liu, Xiaonan Li, Na Li, Yongqi Hu, Jianquan Liu, Quanjun Hu","doi":"10.1111/tpj.17046","DOIUrl":"10.1111/tpj.17046","url":null,"abstract":"<p><p>Ilex is known for its rich content of secondary metabolites, particularly triterpenoid saponins. These compounds hold significant value in natural remedies and herbal medicine. However, the molecular mechanisms responsible for triterpenoid biosynthesis in plants of this genus remain largely unexplored. In this study, we successfully generated the first chromosome-scale genome of Ilex hylonoma. The assembly, comprising 20 anchored chromosomes, has an N50 contig size of 2.13 Mb and a scaffold size of 33.68 Mb. Comparative genome analyses with two other congeners with available chromosome-level genomes suggested that an end-to-end chromosome fusion event likely contributed to the reduction in chromosome number from n = 20 to n = 19 within this genus. By integrating transcriptomic and metabolomic data, we identified the gene expression patterns and metabolite profiles of I. hylonoma across three commonly utilized medicinal tissues. We subsequently pinpointed candidate genes involved in the regulation of triterpenoid saponin biosynthesis, including CYP450 genes, UGT genes, and associated transcription factors. Furthermore, yeast heterologous expression analysis revealed that ihyl08363 catalyzed the conversion of β-amyrin into oleanolic acid, while ihyl04303 catalyzed the C-2α hydroxylation of oleanolic acid to produce maslinic acid. This integrated analysis provides valuable insights into the biosynthesis of important triterpenoid saponins in medicinal Ilex plants.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338082","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cold stress restricts the metabolic and physiological activities of plants, thereby affecting their growth and development. Although broad-complex, tramtrack, and bric-à-brac (BTB) proteins are essential for diverse biological processes and stress responses, the mechanisms underlying BTB-mediated cold responses remain not fully understood. Here, we characterize the function of the cold-induced SlBTB19 protein in tomato (Solanum lycopersicum). Overexpression of SlBTB19 resulted in increased plant sensitivity to cold stress, whereas SlBTB19 knockout mutants exhibited a cold-tolerance phenotype. Further analyses, including protein-protein interaction studies and cell-free degradation assays, revealed that SlBTB19 interacts with and destabilizes the transcription factor SlWRKY2. Using virus-induced gene silencing (VIGS) to silence SlWRKY2 in both wild-type and slbtb19 mutants, we provided genetic evidence that SlWRKY2 acts downstream of SlBTB19 in regulating cold tolerance. Importantly, we demonstrated that SlWRKY2 positively regulates cold tolerance in a CRT/DRE binding factor (CBF)-dependent manner. Under cold stress, SlWRKY2 binds to the W-box in the CBF1 and CBF3 promoters, directly activating their expression. In summary, our findings identify a SlBTB19-SlWRKY2 module that negatively regulates the CBF-dependent cold tolerance pathway in tomato.
{"title":"SlBTB19 interacts with SlWRKY2 to suppress cold tolerance in tomato via the CBF pathway.","authors":"Jin Xu, Sidi Liu, Jiachen Hong, Rui Lin, Xiaojian Xia, Jingquan Yu, Yanhong Zhou","doi":"10.1111/tpj.17040","DOIUrl":"10.1111/tpj.17040","url":null,"abstract":"<p><p>Cold stress restricts the metabolic and physiological activities of plants, thereby affecting their growth and development. Although broad-complex, tramtrack, and bric-à-brac (BTB) proteins are essential for diverse biological processes and stress responses, the mechanisms underlying BTB-mediated cold responses remain not fully understood. Here, we characterize the function of the cold-induced SlBTB19 protein in tomato (Solanum lycopersicum). Overexpression of SlBTB19 resulted in increased plant sensitivity to cold stress, whereas SlBTB19 knockout mutants exhibited a cold-tolerance phenotype. Further analyses, including protein-protein interaction studies and cell-free degradation assays, revealed that SlBTB19 interacts with and destabilizes the transcription factor SlWRKY2. Using virus-induced gene silencing (VIGS) to silence SlWRKY2 in both wild-type and slbtb19 mutants, we provided genetic evidence that SlWRKY2 acts downstream of SlBTB19 in regulating cold tolerance. Importantly, we demonstrated that SlWRKY2 positively regulates cold tolerance in a CRT/DRE binding factor (CBF)-dependent manner. Under cold stress, SlWRKY2 binds to the W-box in the CBF1 and CBF3 promoters, directly activating their expression. In summary, our findings identify a SlBTB19-SlWRKY2 module that negatively regulates the CBF-dependent cold tolerance pathway in tomato.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338085","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Exit control: the role of Arabidopsis hydathodes in auxin storage and nutrient recovery.","authors":"Gwendolyn Kirschner","doi":"10.1111/tpj.17118","DOIUrl":"https://doi.org/10.1111/tpj.17118","url":null,"abstract":"","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142542443","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-09-23DOI: 10.1111/tpj.17034
Huiyu Qin, Junyuan Cheng, Guan-Zhu Han, Zhen Gong
Plants use nucleotide-binding leucine-rich repeat receptors (NLRs) to sense pathogen effectors, initiating effector-triggered immunity (ETI). NLRs containing RESISTANCE TO POWDERY MILDEW 8 domain (RNLs) function as "helper" NLRs in flowering plants and support the immune responses mediated by "sensor" NLRs in cooperation with lipase-EP domain fused proteins (EP proteins). Despite their crucial roles in ETI, much remains unclear about the evolutionary trajectories of RNLs and their functional partners EP proteins. Here, we perform phylogenomic analyses of RNLs in 90 plants, covering the major diversity of plants, and identify the presence of RNLs in land plants and green algae, expanding the distribution of RNLs. We uncover a neglected major RNL group in gymnosperms, besides the canonical major group with NRG1s and ADR1s, and observe a drastic increase in RNL repertoire size in conifers. Phylogenetic analyses indicate that RNLs originated multiple times through domain shuffling, and the evolution of RNLs underwent a birth-and-death process. Moreover, we trace the origin of EP proteins back to the last common ancestor of vascular plants. We find that both RNLs and EP proteins evolve mainly under negative selection, revealing strong constraints on their function. Concerted losses and positive correlation in copy number are observed between RNL and EP sublineages, suggesting their cooperation in function. Together, our findings provide insights into the origin and evolution of plant helper NLRs, with implications for predicting novel innate immune signaling modules.
植物利用核苷酸结合富亮氨酸重复受体(NLRs)感知病原体效应因子,启动效应因子触发免疫(ETI)。在开花植物中,含有抗粉尘微粒 8 结构域(RNLs)的 NLRs 起着 "辅助 "NLRs 的作用,它们与脂肪酶-EP 结构域融合蛋白(EP 蛋白)合作,支持由 "传感器 "NLRs 介导的免疫反应。尽管 RNLs 及其功能伙伴 EP 蛋白在 ETI 中起着至关重要的作用,但它们的进化轨迹仍有许多不清楚之处。在这里,我们对 90 种植物中的 RNLs 进行了系统进化分析,涵盖了植物的主要多样性,并确定了陆生植物和绿藻中 RNLs 的存在,扩大了 RNLs 的分布范围。我们在裸子植物中发现了一个被忽视的主要 RNL 组,此外还有 NRG1s 和 ADR1s 的典型主要组,并观察到针叶树中 RNL 的剧增。系统发育分析表明,RNLs是通过结构域的洗牌多次起源的,RNLs的进化经历了一个出生-死亡的过程。此外,我们将 EP 蛋白的起源追溯到维管植物的最后一个共同祖先。我们发现,RNLs 和 EP 蛋白都主要是在负选择下进化的,这揭示了对其功能的强烈限制。在 RNL 和 EP 亚系之间观察到了拷贝数的协同损失和正相关性,这表明它们在功能上是相互合作的。总之,我们的发现为植物辅助 NLRs 的起源和进化提供了见解,对预测新型先天性免疫信号模块具有重要意义。
{"title":"Phylogenomic insights into the diversity and evolution of RPW8-NLRs and their partners in plants.","authors":"Huiyu Qin, Junyuan Cheng, Guan-Zhu Han, Zhen Gong","doi":"10.1111/tpj.17034","DOIUrl":"10.1111/tpj.17034","url":null,"abstract":"<p><p>Plants use nucleotide-binding leucine-rich repeat receptors (NLRs) to sense pathogen effectors, initiating effector-triggered immunity (ETI). NLRs containing RESISTANCE TO POWDERY MILDEW 8 domain (RNLs) function as \"helper\" NLRs in flowering plants and support the immune responses mediated by \"sensor\" NLRs in cooperation with lipase-EP domain fused proteins (EP proteins). Despite their crucial roles in ETI, much remains unclear about the evolutionary trajectories of RNLs and their functional partners EP proteins. Here, we perform phylogenomic analyses of RNLs in 90 plants, covering the major diversity of plants, and identify the presence of RNLs in land plants and green algae, expanding the distribution of RNLs. We uncover a neglected major RNL group in gymnosperms, besides the canonical major group with NRG1s and ADR1s, and observe a drastic increase in RNL repertoire size in conifers. Phylogenetic analyses indicate that RNLs originated multiple times through domain shuffling, and the evolution of RNLs underwent a birth-and-death process. Moreover, we trace the origin of EP proteins back to the last common ancestor of vascular plants. We find that both RNLs and EP proteins evolve mainly under negative selection, revealing strong constraints on their function. Concerted losses and positive correlation in copy number are observed between RNL and EP sublineages, suggesting their cooperation in function. Together, our findings provide insights into the origin and evolution of plant helper NLRs, with implications for predicting novel innate immune signaling modules.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142306822","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-09-25DOI: 10.1111/tpj.17036
Vanessa Scherer, Leo Bellin, Serena Schwenkert, Martin Lehmann, Jannis Rinne, Claus-Peter Witte, Kathrin Jahnke, Andreas Richter, Tobias Pruss, Anne Lau, Lisa Waller, Sebastian Stein, Dario Leister, Torsten Möhlmann
Arabidopsis uracil phosphoribosyltransferase (UPP) is an essential enzyme and plants lacking this enzyme are strongly compromised in chloroplast function. Our analysis of UPP amiRNA mutants has confirmed that this vital function is crucial to establish a fully functional photosynthesis as the RIESKE iron sulfur protein (PetC) is almost absent, leading to a block in photosynthetic electron transport. Interestingly, this function appears to be unrelated to nucleotide homeostasis since nucleotide levels were not altered in the studied mutants. Transcriptomics and proteomic analysis showed that protein homeostasis but not gene expression is most likely responsible for this observation and high light provoked an upregulation of protease levels, including thylakoid filamentation temperature-sensitive 1, 5 (FtsH), caseinolytic protease proteolytic subunit 1 (ClpP1), and processing peptidases, as well as components of the chloroplast protein import machinery in UPP amiRNA lines. Strongly reduced PetC amounts were not only detected by immunoblot from mature plants but in addition in a de-etiolation experiment with young seedlings and are causing reduced high light-induced non-photochemical quenching Φ(NPQ) but increased unregulated energy dissipation Φ(NO). This impaired photosynthesis results in an inability to induce flavonoid biosynthesis. In addition, the levels of the osmoprotectants raffinose, proline, and fumarate were found to be reduced. In sum, our work suggests that UPP assists in stabilization PetC during import, processing or targeting to the thylakoid membrane, or protects it against proteolytic degradation.
{"title":"Uracil phosphoribosyltransferase is required to establish a functional cytochrome b<sub>6</sub>f complex.","authors":"Vanessa Scherer, Leo Bellin, Serena Schwenkert, Martin Lehmann, Jannis Rinne, Claus-Peter Witte, Kathrin Jahnke, Andreas Richter, Tobias Pruss, Anne Lau, Lisa Waller, Sebastian Stein, Dario Leister, Torsten Möhlmann","doi":"10.1111/tpj.17036","DOIUrl":"10.1111/tpj.17036","url":null,"abstract":"<p><p>Arabidopsis uracil phosphoribosyltransferase (UPP) is an essential enzyme and plants lacking this enzyme are strongly compromised in chloroplast function. Our analysis of UPP amiRNA mutants has confirmed that this vital function is crucial to establish a fully functional photosynthesis as the RIESKE iron sulfur protein (PetC) is almost absent, leading to a block in photosynthetic electron transport. Interestingly, this function appears to be unrelated to nucleotide homeostasis since nucleotide levels were not altered in the studied mutants. Transcriptomics and proteomic analysis showed that protein homeostasis but not gene expression is most likely responsible for this observation and high light provoked an upregulation of protease levels, including thylakoid filamentation temperature-sensitive 1, 5 (FtsH), caseinolytic protease proteolytic subunit 1 (ClpP1), and processing peptidases, as well as components of the chloroplast protein import machinery in UPP amiRNA lines. Strongly reduced PetC amounts were not only detected by immunoblot from mature plants but in addition in a de-etiolation experiment with young seedlings and are causing reduced high light-induced non-photochemical quenching Φ<sub>(NPQ)</sub> but increased unregulated energy dissipation Φ<sub>(NO)</sub>. This impaired photosynthesis results in an inability to induce flavonoid biosynthesis. In addition, the levels of the osmoprotectants raffinose, proline, and fumarate were found to be reduced. In sum, our work suggests that UPP assists in stabilization PetC during import, processing or targeting to the thylakoid membrane, or protects it against proteolytic degradation.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338087","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
A series of polyploidizations in higher-order polyploids is the main event affecting gene content in a genome. Each polyploidization event can lead to massive functional divergence because of the subsequent decrease in selection pressure on duplicated genes; however, the causal relationship between multiple rounds of polyploidization and the functional divergence of duplicated genes is poorly understood. We focused on the Triticum-Aegilops complex lineage and compared selection pressure before and after tetraploidization and hexaploidization events. Although both events led to decreased selection pressure on homoeologous gene pairs (compared with diploids and tetraploids), the initial tetraploidization had a greater impact on selection pressure on homoeologous gene pairs than did subsequent hexaploidization. Consistent with this, selection pressure on expression patterns for the initial event relaxed more than those for the subsequent event. Surprisingly, the decreased selection pressure on these homoeologous genes was independent of the existence of in-paralogs within the same subgenome. Wheat homoeologous pairs had different evolutionary consequences compared with orthologs related to other mechanisms (ancient allopolyploidization, ancient autopolyploidization, and small-scale duplication). Furthermore, tetraploidization and hexaploidization also seemed to have different evolutionary consequences. This suggests that homoeologous genes retain unique functions, including functions that are unlikely to be preserved in genes generated by the other duplication mechanisms. We found that their unique functions differed between tetraploidization and hexaploidization (e.g., reproductive and chromosome segregation processes). These findings imply that the substantial number of gene pairs resulting from multiple allopolyploidization events, especially initial tetraploidization, may have been a unique source of functional divergence.
{"title":"Decrease in purifying selection pressures on wheat homoeologous genes: tetraploidization versus hexaploidization.","authors":"Akihiro Ezoe, Daisuke Todaka, Yoshinori Utsumi, Satoshi Takahashi, Kanako Kawaura, Motoaki Seki","doi":"10.1111/tpj.17047","DOIUrl":"10.1111/tpj.17047","url":null,"abstract":"<p><p>A series of polyploidizations in higher-order polyploids is the main event affecting gene content in a genome. Each polyploidization event can lead to massive functional divergence because of the subsequent decrease in selection pressure on duplicated genes; however, the causal relationship between multiple rounds of polyploidization and the functional divergence of duplicated genes is poorly understood. We focused on the Triticum-Aegilops complex lineage and compared selection pressure before and after tetraploidization and hexaploidization events. Although both events led to decreased selection pressure on homoeologous gene pairs (compared with diploids and tetraploids), the initial tetraploidization had a greater impact on selection pressure on homoeologous gene pairs than did subsequent hexaploidization. Consistent with this, selection pressure on expression patterns for the initial event relaxed more than those for the subsequent event. Surprisingly, the decreased selection pressure on these homoeologous genes was independent of the existence of in-paralogs within the same subgenome. Wheat homoeologous pairs had different evolutionary consequences compared with orthologs related to other mechanisms (ancient allopolyploidization, ancient autopolyploidization, and small-scale duplication). Furthermore, tetraploidization and hexaploidization also seemed to have different evolutionary consequences. This suggests that homoeologous genes retain unique functions, including functions that are unlikely to be preserved in genes generated by the other duplication mechanisms. We found that their unique functions differed between tetraploidization and hexaploidization (e.g., reproductive and chromosome segregation processes). These findings imply that the substantial number of gene pairs resulting from multiple allopolyploidization events, especially initial tetraploidization, may have been a unique source of functional divergence.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454411","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-10-14DOI: 10.1111/tpj.17041
Adéla Machelová, Martina Nešpor Dadejová, Michal Franek, Guillaume Mougeot, Lauriane Simon, Samuel Le Goff, Céline Duc, Jasmin Bassler, Martin Demko, Jana Schwarzerová, Sophie Desset, Aline V Probst, Martina Dvořáčková
Genome stability is significantly influenced by the precise coordination of chromatin complexes that facilitate the loading and eviction of histones from chromatin during replication, transcription, and DNA repair processes. In this study, we investigate the role of the Arabidopsis H3 histone chaperones ANTI-SILENCING FUNCTION 1 (ASF1) and HISTONE REGULATOR A (HIRA) in the maintenance of telomeres and 45S rDNA loci, genomic sites that are particularly susceptible to changes in the chromatin structure. We find that both ASF1 and HIRA are essential for telomere length regulation, as telomeres are significantly shorter in asf1a1b and hira mutants. However, these shorter telomeres remain localized around the nucleolus and exhibit a comparable relative H3 occupancy to the wild type. In addition to regulating telomere length, ASF1 and HIRA contribute to silencing 45S rRNA genes and affect their copy number. Besides, ASF1 supports global heterochromatin maintenance. Our findings also indicate that ASF1 transiently binds to the TELOMERE REPEAT BINDING 1 protein and the N terminus of telomerase in vivo, suggesting a physical link between the ASF1 histone chaperone and the telomere maintenance machinery.
{"title":"The histone chaperones ASF1 and HIRA are required for telomere length and 45S rDNA copy number homeostasis.","authors":"Adéla Machelová, Martina Nešpor Dadejová, Michal Franek, Guillaume Mougeot, Lauriane Simon, Samuel Le Goff, Céline Duc, Jasmin Bassler, Martin Demko, Jana Schwarzerová, Sophie Desset, Aline V Probst, Martina Dvořáčková","doi":"10.1111/tpj.17041","DOIUrl":"10.1111/tpj.17041","url":null,"abstract":"<p><p>Genome stability is significantly influenced by the precise coordination of chromatin complexes that facilitate the loading and eviction of histones from chromatin during replication, transcription, and DNA repair processes. In this study, we investigate the role of the Arabidopsis H3 histone chaperones ANTI-SILENCING FUNCTION 1 (ASF1) and HISTONE REGULATOR A (HIRA) in the maintenance of telomeres and 45S rDNA loci, genomic sites that are particularly susceptible to changes in the chromatin structure. We find that both ASF1 and HIRA are essential for telomere length regulation, as telomeres are significantly shorter in asf1a1b and hira mutants. However, these shorter telomeres remain localized around the nucleolus and exhibit a comparable relative H3 occupancy to the wild type. In addition to regulating telomere length, ASF1 and HIRA contribute to silencing 45S rRNA genes and affect their copy number. Besides, ASF1 supports global heterochromatin maintenance. Our findings also indicate that ASF1 transiently binds to the TELOMERE REPEAT BINDING 1 protein and the N terminus of telomerase in vivo, suggesting a physical link between the ASF1 histone chaperone and the telomere maintenance machinery.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454424","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In plants, RNA silencing constitutes a strong defense against viral infection, which viruses counteract with RNA-silencing suppressors (RSSs). Understanding the interactions between viral RSSs and host factors is crucial for elucidating the molecular arms race between viruses and host plants. We report that the helicase motif (Hel) of the replicase encoded by apple stem grooving virus (ASGV)-the main virus affecting pear trees in China-is an RSS that can inhibit both local and systemic RNA silencing, possibly by binding double-stranded (ds) siRNA. The transcription factor related to ABSCISIC ACID INSENSITIVE3/VIVIPAROUS1 from pear (PbRAV1) enters the cytoplasm and binds Hel through its C terminus, thereby attenuating its RSS activity by reducing its binding affinity to 21- and 24-nt ds siRNA, and suppressing ASGV infection. PbRAV1 can also target p24, an RSS encoded by grapevine leafroll-associated virus 2 (GLRaV-2), with similar negative effects on p24's suppressive function and inhibition of GLRaV-2 infection. Moreover, like the positive role of the PbRAV1 homolog from grapevine (VvRAV1) in p24's previously reported RSS activity, ASGV Hel can also hijack VvRAV1 and employ the protein to sequester 21-nt ds siRNA, thereby enhancing its own RSS activity and promoting ASGV infection. Furthermore, PbRAV1 neither interacts with CP, an RSS encoded by grapevine inner necrosis virus, nor has any obvious effect on CP's RSS activity. Our results identify an RSS encoded by ASGV and demonstrate that PbRAV1, representing a novel type of RAV transcription factor, plays a defensive role against viral infection by targeting viral RSSs.
{"title":"A novel RAV transcription factor from pear interacts with viral RNA-silencing suppressors to inhibit viral infection.","authors":"Yin-Shuai Xie, Qi Zeng, Wen-Ting Huang, Jin-Ying Wang, Han-Wei Li, Shang-Zhen Yu, Can Liu, Xue-Qing Zhang, Chen-Lu Feng, Wen-Hao Zhang, Tian-Zhong Li, Yu-Qin Cheng","doi":"10.1111/tpj.17037","DOIUrl":"10.1111/tpj.17037","url":null,"abstract":"<p><p>In plants, RNA silencing constitutes a strong defense against viral infection, which viruses counteract with RNA-silencing suppressors (RSSs). Understanding the interactions between viral RSSs and host factors is crucial for elucidating the molecular arms race between viruses and host plants. We report that the helicase motif (Hel) of the replicase encoded by apple stem grooving virus (ASGV)-the main virus affecting pear trees in China-is an RSS that can inhibit both local and systemic RNA silencing, possibly by binding double-stranded (ds) siRNA. The transcription factor related to ABSCISIC ACID INSENSITIVE3/VIVIPAROUS1 from pear (PbRAV1) enters the cytoplasm and binds Hel through its C terminus, thereby attenuating its RSS activity by reducing its binding affinity to 21- and 24-nt ds siRNA, and suppressing ASGV infection. PbRAV1 can also target p24, an RSS encoded by grapevine leafroll-associated virus 2 (GLRaV-2), with similar negative effects on p24's suppressive function and inhibition of GLRaV-2 infection. Moreover, like the positive role of the PbRAV1 homolog from grapevine (VvRAV1) in p24's previously reported RSS activity, ASGV Hel can also hijack VvRAV1 and employ the protein to sequester 21-nt ds siRNA, thereby enhancing its own RSS activity and promoting ASGV infection. Furthermore, PbRAV1 neither interacts with CP, an RSS encoded by grapevine inner necrosis virus, nor has any obvious effect on CP's RSS activity. Our results identify an RSS encoded by ASGV and demonstrate that PbRAV1, representing a novel type of RAV transcription factor, plays a defensive role against viral infection by targeting viral RSSs.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142306821","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-01Epub Date: 2024-09-24DOI: 10.1111/tpj.17039
Xiaoqian Yang, Ruen Yu, Jiahao Liu, Dandan Xiao, Chun Wang, Tiantian Fu, Yuzhang Yang, Kaijing Rong, Yanwei Wang
Canker disease caused by the bacterium Lonsdalea populi is one of the most destructive diseases affecting poplar stems. However, the detailed stress response mechanisms of poplar have not been widely characterized. To explore the diverse regulatory RNA landscape and the function of key regulators in poplar subjected to L. populi stress, we integrated time-course experiment with mock-inoculation (CK) and inoculation (IN) with L. populi at the first, third, and sixth day (IN1, IN3, IN6) on Populus × euramericana cv. '74/76' (107), small RNA-seq, whole transcriptome-wide analysis, degradome analysis and transgenic experiments. A total of 98 differentially expressed (DE) miRNA, 17 974 DEmRNA, and 807 DElncRNA were identified in poplar infected by L. populi, presenting dynamic changes over the infection course. Regulatory networks among RNAs were further constructed. Notably, a network centered on ptc-miR482a in CK-vs-IN3 contained most DEGs. We show that miR482a and miR1448 are located in one transcript as a polycistron. Overexpression of pre-miR482a-miR1448 (OX482-1448) and pre-miR482a (OX482) increased poplar susceptibility to canker pathogen with reduced accumulation of reactive oxygen species, while the suppression of miR482a (STTM482) conferred poplar disease resistance. PHA7 was validated as the target of miR482a with degradome sequencing and tobacco transient co-transformation, its expression being downregulated in OX482-1448 and OX482 lines. Additionally, a series of phasiRNAs were triggered by miR482a targeting PHA7, forming regulatory cascades with more RLP, NBS-LRR, and PK genes, further verifying the defense function of miR482a. These findings provide insights for understanding the roles of ncRNAs and regulatory networks involved in poplar immunity.
{"title":"Integrating multiregulatory analysis reveals the negative regulatory function of miR482a in the response of poplar to canker pathogen infection.","authors":"Xiaoqian Yang, Ruen Yu, Jiahao Liu, Dandan Xiao, Chun Wang, Tiantian Fu, Yuzhang Yang, Kaijing Rong, Yanwei Wang","doi":"10.1111/tpj.17039","DOIUrl":"10.1111/tpj.17039","url":null,"abstract":"<p><p>Canker disease caused by the bacterium Lonsdalea populi is one of the most destructive diseases affecting poplar stems. However, the detailed stress response mechanisms of poplar have not been widely characterized. To explore the diverse regulatory RNA landscape and the function of key regulators in poplar subjected to L. populi stress, we integrated time-course experiment with mock-inoculation (CK) and inoculation (IN) with L. populi at the first, third, and sixth day (IN1, IN3, IN6) on Populus × euramericana cv. '74/76' (107), small RNA-seq, whole transcriptome-wide analysis, degradome analysis and transgenic experiments. A total of 98 differentially expressed (DE) miRNA, 17 974 DEmRNA, and 807 DElncRNA were identified in poplar infected by L. populi, presenting dynamic changes over the infection course. Regulatory networks among RNAs were further constructed. Notably, a network centered on ptc-miR482a in CK-vs-IN3 contained most DEGs. We show that miR482a and miR1448 are located in one transcript as a polycistron. Overexpression of pre-miR482a-miR1448 (OX482-1448) and pre-miR482a (OX482) increased poplar susceptibility to canker pathogen with reduced accumulation of reactive oxygen species, while the suppression of miR482a (STTM482) conferred poplar disease resistance. PHA7 was validated as the target of miR482a with degradome sequencing and tobacco transient co-transformation, its expression being downregulated in OX482-1448 and OX482 lines. Additionally, a series of phasiRNAs were triggered by miR482a targeting PHA7, forming regulatory cascades with more RLP, NBS-LRR, and PK genes, further verifying the defense function of miR482a. These findings provide insights for understanding the roles of ncRNAs and regulatory networks involved in poplar immunity.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":null,"pages":null},"PeriodicalIF":6.2,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142338083","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}