Gaoyuan Song, Christian Montes, Damilola Olatunji, Shikha Malik, Chonghui Ji, Natalie M Clark, Yunting Pu, Dior R Kelley, Justin W Walley
Protein activity, abundance, and stability can be regulated by posttranslational modification including ubiquitination. Ubiquitination is conserved among eukaryotes and plays a central role in modulating cellular function, yet we lack comprehensive catalogs of proteins that are modified by ubiquitin in plants. In this study, we describe an antibody-based approach to enrich ubiquitinated peptides coupled with isobaric labeling to enable quantification of up to 18-multiplexed samples. This approach identified 17,940 ubiquitinated lysine sites arising from 6,453 proteins from Arabidopsis (Arabidopsis thaliana) primary roots, seedlings, and rosette leaves. Gene ontology analysis indicated that ubiquitinated proteins are associated with numerous biological processes including hormone signaling, plant defense, protein homeostasis, and metabolism. We determined ubiquitinated lysine residues that directly regulate the stability of three transcription factors, CRYPTOCHROME-INTERACTING BASIC-HELIX-LOOP-HELIX 1 (CIB1), CIB1 LIKE PROTEIN 2 (CIL2), and SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) using in vivo degradation assays. Furthermore, codon mutation of CIB1 to create a K166R conversion to prevent ubiquitination, via CRISPR/Cas9-derived adenosine base editing, led to an early flowering phenotype and increased expression of FLOWERING LOCUS T (FT). These comprehensive site-level ubiquitinome profiles provide a wealth of data for future functional studies related to modulation of biological processes mediated by this posttranslational modification in plants.
蛋白质的活性、丰度和稳定性可通过包括泛素化在内的翻译后修饰进行调节。泛素化在真核生物中是保守的，在调节细胞功能方面起着核心作用，但我们缺乏植物中被泛素修饰的蛋白质的全面目录。在本研究中，我们介绍了一种基于抗体的方法来富集泛素化肽段，并结合等位标记技术对多达 18 个多重样品进行定量。这种方法从拟南芥（Arabidopsis thaliana）的主根、幼苗和莲座叶中的 6,453 个蛋白质中鉴定出了 17,940 个泛素化赖氨酸位点。基因本体分析表明，泛素化蛋白质与许多生物过程有关，包括激素信号转导、植物防御、蛋白质稳态和新陈代谢。我们利用体内降解试验确定了直接调节三种转录因子（CRYPTOCHROME-INTERACTING BASIC-HELIX-LOOP-HELIX 1 (CIB1)、CIB1 LIKE PROTEIN 2 (CIL2)和SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1)）稳定性的泛素化赖氨酸残基。此外，通过 CRISPR/Cas9 衍生的腺苷碱基编辑，对 CIB1 进行密码子突变以产生 K166R 转换，从而阻止泛素化，这导致了早花表型和开花位点 T（FT）表达的增加。这些全面的位点级泛素组图谱为未来有关植物中这种翻译后修饰介导的生物过程调控的功能研究提供了丰富的数据。
{"title":"Quantitative proteomics reveals extensive lysine ubiquitination and transcription factor stability states in Arabidopsis","authors":"Gaoyuan Song, Christian Montes, Damilola Olatunji, Shikha Malik, Chonghui Ji, Natalie M Clark, Yunting Pu, Dior R Kelley, Justin W Walley","doi":"10.1093/plcell/koae310","DOIUrl":"https://doi.org/10.1093/plcell/koae310","url":null,"abstract":"Protein activity, abundance, and stability can be regulated by posttranslational modification including ubiquitination. Ubiquitination is conserved among eukaryotes and plays a central role in modulating cellular function, yet we lack comprehensive catalogs of proteins that are modified by ubiquitin in plants. In this study, we describe an antibody-based approach to enrich ubiquitinated peptides coupled with isobaric labeling to enable quantification of up to 18-multiplexed samples. This approach identified 17,940 ubiquitinated lysine sites arising from 6,453 proteins from Arabidopsis (Arabidopsis thaliana) primary roots, seedlings, and rosette leaves. Gene ontology analysis indicated that ubiquitinated proteins are associated with numerous biological processes including hormone signaling, plant defense, protein homeostasis, and metabolism. We determined ubiquitinated lysine residues that directly regulate the stability of three transcription factors, CRYPTOCHROME-INTERACTING BASIC-HELIX-LOOP-HELIX 1 (CIB1), CIB1 LIKE PROTEIN 2 (CIL2), and SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) using in vivo degradation assays. Furthermore, codon mutation of CIB1 to create a K166R conversion to prevent ubiquitination, via CRISPR/Cas9-derived adenosine base editing, led to an early flowering phenotype and increased expression of FLOWERING LOCUS T (FT). These comprehensive site-level ubiquitinome profiles provide a wealth of data for future functional studies related to modulation of biological processes mediated by this posttranslational modification in plants.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"71 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142684316","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Miaomiao Ma, Pan Wang, Rubin Chen, Mei Bai, Zhuoyuan He, Dan Xiao, Guangyuan Xu, Hong Wu, Jian-Min Zhou, Daolong Dou, Guozhi Bi, Xiangxiu Liang
Plant cell-surface-localized pattern recognition receptors (PRRs) recognize microbial patterns and activate pattern-triggered immunity (PTI). Typical PTI responses include reactive oxygen species (ROS) burst controlled by the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOGUE D (RbohD) and activation of the mitogen-activated protein kinase (MAPK) cascade composed of MAPKKK3/5-MKK4/5-MPK3/6. However, the mechanisms through which PRRs regulate and coordinate these immune responses are not fully understood. Here, we showed that Arabidopsis thaliana OXIDATIVE SIGNAL-INDUCIBLE1 (OXI1), a kinase known to be activated by ROS, is involved in the LYK5-CERK1 receptor complex, which recognizes fungal cell wall-derived chitin. The oxi1 mutant exhibits enhanced susceptibility to various pathogens and reduced chitin-induced MAPK activation and ROS burst. We showed that chitin induces the phosphorylation of OXI1 in an RbohD-dependent manner. H2O2 and chitin treatment causes the oxidation of OXI1 at Cys104 and Cys205, which is essential for the kinase activity of OXI1. These oxidation sites are required for chitin-induced MAPK activation and disease resistance. Activated OXI1 directly phosphorylates MAPKKK5 to regulate MAPK activation. Additionally, OXI1 phosphorylates RbohD, suggesting that it may activate RbohD to promote ROS burst to further enhance the long-term MAPK activation. Together, our findings reveal a pathway linking PRR-mediated ROS production to MAPK activation through OXI1.
{"title":"The OXI1 kinase regulates plant immunity by linking microbial pattern-induced ROS burst to MAPK activation","authors":"Miaomiao Ma, Pan Wang, Rubin Chen, Mei Bai, Zhuoyuan He, Dan Xiao, Guangyuan Xu, Hong Wu, Jian-Min Zhou, Daolong Dou, Guozhi Bi, Xiangxiu Liang","doi":"10.1093/plcell/koae311","DOIUrl":"https://doi.org/10.1093/plcell/koae311","url":null,"abstract":"Plant cell-surface-localized pattern recognition receptors (PRRs) recognize microbial patterns and activate pattern-triggered immunity (PTI). Typical PTI responses include reactive oxygen species (ROS) burst controlled by the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOGUE D (RbohD) and activation of the mitogen-activated protein kinase (MAPK) cascade composed of MAPKKK3/5-MKK4/5-MPK3/6. However, the mechanisms through which PRRs regulate and coordinate these immune responses are not fully understood. Here, we showed that Arabidopsis thaliana OXIDATIVE SIGNAL-INDUCIBLE1 (OXI1), a kinase known to be activated by ROS, is involved in the LYK5-CERK1 receptor complex, which recognizes fungal cell wall-derived chitin. The oxi1 mutant exhibits enhanced susceptibility to various pathogens and reduced chitin-induced MAPK activation and ROS burst. We showed that chitin induces the phosphorylation of OXI1 in an RbohD-dependent manner. H2O2 and chitin treatment causes the oxidation of OXI1 at Cys104 and Cys205, which is essential for the kinase activity of OXI1. These oxidation sites are required for chitin-induced MAPK activation and disease resistance. Activated OXI1 directly phosphorylates MAPKKK5 to regulate MAPK activation. Additionally, OXI1 phosphorylates RbohD, suggesting that it may activate RbohD to promote ROS burst to further enhance the long-term MAPK activation. Together, our findings reveal a pathway linking PRR-mediated ROS production to MAPK activation through OXI1.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"23 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142678865","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Some pathogens colonize plant leaves, but others invade the roots, including the vasculature, causing severe disease symptoms. Plant innate immunity has been extensively studied in leaf pathosystems; however, the precise regulation of immunity against vascular pathogens remains largely unexplored. We previously demonstrated that loss of function of the receptor kinase FERONIA (FER) increases plant resistance to the typical vascular bacterial pathogen Ralstonia solanacearum. Here, we show that upon infection with R. solanacearum, root xylem cell walls in Arabidopsis thaliana become highly lignified. FER is specifically upregulated in the root xylem in response to R. solanacearum infection, and inhibits lignin biosynthesis and resistance to this pathogen. We determined that FER interacts with and phosphorylates the transcription factor RESPONSIVE TO DESICCATION 26 (RD26), leading to its degradation. Overexpression and knockout of RD26 demonstrated that it positively regulates plant resistance to R. solanacearum by directly activating the expression of lignin-related genes. Tissue-specific expression of RD26 in the root xylem confirmed its role in vascular immunity. We confirmed that the FER–RD26 module regulates lignin biosynthesis and resistance against R. solanacearum in tomato (Solanum lycopersicum). Taken together, our findings unveil that the FER–RD26 cascade governs plant immunity against R. solanacearum in vascular tissues by regulating lignin deposition. This cascade may represent a key defense mechanism against vascular pathogens in plants.
一些病原体在植物叶片上定植，但另一些则侵入根部，包括脉管系统，导致严重的病害症状。植物先天免疫在叶片病理系统中得到了广泛的研究；然而，针对维管病原体免疫的精确调控在很大程度上仍未得到探索。我们以前曾证实，受体激酶 FERONIA（FER）的功能缺失会增强植物对典型维管束细菌病原体 Ralstonia solanacearum 的抵抗力。在这里，我们发现当拟南芥感染 R. solanacearum 时，拟南芥根木质部细胞壁会高度木质化。FER 在根木质部中特异性上调，以应对 R. solanacearum 的感染，并抑制木质素的生物合成和对该病原体的抵抗。我们确定 FER 与转录因子 RESPONSIVE TO DESICCATION 26（RD26）相互作用并使其磷酸化，从而导致其降解。RD26的过表达和基因敲除表明，它通过直接激活木质素相关基因的表达，积极调节植物对茄碱菌的抗性。RD26 在根木质部的组织特异性表达证实了它在维管免疫中的作用。我们证实，FER-RD26 模块调控番茄（Solanum lycopersicum）的木质素生物合成和对 R. solanacearum 的抗性。综上所述，我们的研究结果揭示了 FER-RD26 级联通过调节木质素沉积，在维管组织中控制植物对茄红素菌的免疫力。该级联可能代表了植物对维管束病原体的一种关键防御机制。
{"title":"The FERONIA–RESPONSIVE TO DESSICATION 26 module regulates vascular immunity to Ralstonia solanacearum","authors":"Bingqian Wang, Cailin Luo, Xiaoxu Li, Alvaro Jimenez, Jun Cai, Jia Chen, Changsheng Li, Chunhui Zhang, Lijun Ou, Wenxuan Pu, Yu Peng, Zhenchen Zhang, Yong Cai, Marc Valls, Dousheng Wu, Feng Yu","doi":"10.1093/plcell/koae302","DOIUrl":"https://doi.org/10.1093/plcell/koae302","url":null,"abstract":"Some pathogens colonize plant leaves, but others invade the roots, including the vasculature, causing severe disease symptoms. Plant innate immunity has been extensively studied in leaf pathosystems; however, the precise regulation of immunity against vascular pathogens remains largely unexplored. We previously demonstrated that loss of function of the receptor kinase FERONIA (FER) increases plant resistance to the typical vascular bacterial pathogen Ralstonia solanacearum. Here, we show that upon infection with R. solanacearum, root xylem cell walls in Arabidopsis thaliana become highly lignified. FER is specifically upregulated in the root xylem in response to R. solanacearum infection, and inhibits lignin biosynthesis and resistance to this pathogen. We determined that FER interacts with and phosphorylates the transcription factor RESPONSIVE TO DESICCATION 26 (RD26), leading to its degradation. Overexpression and knockout of RD26 demonstrated that it positively regulates plant resistance to R. solanacearum by directly activating the expression of lignin-related genes. Tissue-specific expression of RD26 in the root xylem confirmed its role in vascular immunity. We confirmed that the FER–RD26 module regulates lignin biosynthesis and resistance against R. solanacearum in tomato (Solanum lycopersicum). Taken together, our findings unveil that the FER–RD26 cascade governs plant immunity against R. solanacearum in vascular tissues by regulating lignin deposition. This cascade may represent a key defense mechanism against vascular pathogens in plants.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"36 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142610076","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ningdong Xie, Chetna Sharma, Katherine Rusche, Xin Wang
Cyanobacteria contribute to roughly a quarter of global net carbon fixation. During diel light/dark growth, dark respiration substantially lowers the overall photosynthetic carbon yield in cyanobacteria and other phototrophs. How respiratory pathways participate in carbon resource allocation at night to optimize dark survival and support daytime photosynthesis remains unclear. Here, using the cyanobacterium Synechococcus elongatus PCC 7942, we show that phosphoketolase integrates into a respiratory network in the dark to best allocate carbon resources for amino acid biosynthesis and to prepare for photosynthesis reinitiation upon photoinduction. Moreover, we show that the respiratory Entner-Doudoroff (ED) pathway in S. elongatus is incomplete, with its key enzyme 2-keto-3-deoxy-6-phosphogluconate (KDPG) aldolase exhibiting alternative oxaloacetate decarboxylation activity that modulates daytime photosynthesis. This activity allows for the bypassing of the tricarboxylic acid (TCA) cycle when ATP and NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by the light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Optimizing these metabolic processes offers opportunities to enhance photosynthetic carbon yield in cyanobacteria and other photosynthetic organisms under diel light/dark cycles.
{"title":"Phosphoketolase and KDPG aldolase metabolisms modulate photosynthetic carbon yield in cyanobacteria","authors":"Ningdong Xie, Chetna Sharma, Katherine Rusche, Xin Wang","doi":"10.1093/plcell/koae291","DOIUrl":"https://doi.org/10.1093/plcell/koae291","url":null,"abstract":"Cyanobacteria contribute to roughly a quarter of global net carbon fixation. During diel light/dark growth, dark respiration substantially lowers the overall photosynthetic carbon yield in cyanobacteria and other phototrophs. How respiratory pathways participate in carbon resource allocation at night to optimize dark survival and support daytime photosynthesis remains unclear. Here, using the cyanobacterium Synechococcus elongatus PCC 7942, we show that phosphoketolase integrates into a respiratory network in the dark to best allocate carbon resources for amino acid biosynthesis and to prepare for photosynthesis reinitiation upon photoinduction. Moreover, we show that the respiratory Entner-Doudoroff (ED) pathway in S. elongatus is incomplete, with its key enzyme 2-keto-3-deoxy-6-phosphogluconate (KDPG) aldolase exhibiting alternative oxaloacetate decarboxylation activity that modulates daytime photosynthesis. This activity allows for the bypassing of the tricarboxylic acid (TCA) cycle when ATP and NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by the light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Optimizing these metabolic processes offers opportunities to enhance photosynthetic carbon yield in cyanobacteria and other photosynthetic organisms under diel light/dark cycles.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"16 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142541279","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Longfei Zhu, Julia Dluzewska, Nadia Fernández-Jiménez, Rajeev Ranjan, Alexandre Pelé, Wojciech Dziegielewski, Maja Szymanska-Lejman, Karolina Hus, Julia Górna, Mónica Pradillo, Piotr A Ziolkowski
Meiotic crossover, i.e., the reciprocal exchange of chromosome fragments during meiosis, is a key driver of genetic diversity. Crossover is initiated by the formation of programmed DNA double-strand breaks (DSBs). While the role of ATAXIA-TELANGIECTASIA AND RAD3-RELATED (ATR) kinase in DNA damage signaling is well-known, its impact on crossover formation remains understudied. Here, using measurements of recombination at chromosomal intervals and genome-wide crossover mapping, we showed that ATR inactivation in Arabidopsis (Arabidopsis thaliana) leads to dramatic crossover redistribution, with an increase in crossover frequency in chromosome arms and a decrease in pericentromeres. These global changes in crossover placement were not caused by alterations in DSB numbers, which we demonstrated by analyzing phosphorylated H2A.X foci in zygonema. Using the seed-typing technique, we found that hotspot usage remains mainly unchanged in atr mutants compared to wild-type individuals. Moreover, atr showed no change in the number of crossovers caused by two independent pathways, which implies no effect on crossover pathway choice. Analyses of genetic interaction indicate that while the effects of atr are independent of MMS AND UV SENSITIVE81 (MUS81), ZIPPER1 (ZYP1), FANCONI ANEMIA COMPLEMENTATION GROUP M (FANCM) and D2 (FANCD2), the underlying mechanism may be similar between ATR and FANCD2. This study extends our understanding of ATR’s role in meiosis, uncovering functions in regulating crossover distribution.
减数分裂交叉，即减数分裂过程中染色体片段的相互交换，是遗传多样性的关键驱动因素。交叉是由程序性 DNA 双链断裂（DSB）的形成启动的。虽然ATAXIA-TELANGIECTASIA和RAD3-RELATED（ATR）激酶在DNA损伤信号转导中的作用众所周知，但它对交叉形成的影响仍未得到充分研究。在这里，我们利用染色体间隔重组测量和全基因组交叉图谱研究表明，拟南芥（Arabidopsis thaliana）中 ATR 失活会导致显著的交叉重新分布，染色体臂上的交叉频率增加，而中心粒周围的交叉频率降低。我们通过分析拟南芥中磷酸化的H2A.X病灶证明，这些交叉位置的整体变化并不是由DSB数量的改变引起的。利用种子分型技术，我们发现与野生型个体相比，atr 突变体中的热点使用情况主要保持不变。此外，atr 在两个独立途径引起的交叉数量上没有变化，这意味着它对交叉途径的选择没有影响。遗传交互作用分析表明，虽然atr的影响独立于MMS和UV SENSITIVE81（MUS81）、ZIPPER1（ZYP1）、FANCONI ANEMIA COMPLEMENTATION GROUP M（FANCM）和D2（FANCD2），但ATR和FANCD2的潜在机制可能相似。这项研究拓展了我们对 ATR 在减数分裂中作用的认识，发现了其在调节交叉分布方面的功能。
{"title":"The kinase ATR controls meiotic crossover distribution at the genome scale in Arabidopsis","authors":"Longfei Zhu, Julia Dluzewska, Nadia Fernández-Jiménez, Rajeev Ranjan, Alexandre Pelé, Wojciech Dziegielewski, Maja Szymanska-Lejman, Karolina Hus, Julia Górna, Mónica Pradillo, Piotr A Ziolkowski","doi":"10.1093/plcell/koae292","DOIUrl":"https://doi.org/10.1093/plcell/koae292","url":null,"abstract":"Meiotic crossover, i.e., the reciprocal exchange of chromosome fragments during meiosis, is a key driver of genetic diversity. Crossover is initiated by the formation of programmed DNA double-strand breaks (DSBs). While the role of ATAXIA-TELANGIECTASIA AND RAD3-RELATED (ATR) kinase in DNA damage signaling is well-known, its impact on crossover formation remains understudied. Here, using measurements of recombination at chromosomal intervals and genome-wide crossover mapping, we showed that ATR inactivation in Arabidopsis (Arabidopsis thaliana) leads to dramatic crossover redistribution, with an increase in crossover frequency in chromosome arms and a decrease in pericentromeres. These global changes in crossover placement were not caused by alterations in DSB numbers, which we demonstrated by analyzing phosphorylated H2A.X foci in zygonema. Using the seed-typing technique, we found that hotspot usage remains mainly unchanged in atr mutants compared to wild-type individuals. Moreover, atr showed no change in the number of crossovers caused by two independent pathways, which implies no effect on crossover pathway choice. Analyses of genetic interaction indicate that while the effects of atr are independent of MMS AND UV SENSITIVE81 (MUS81), ZIPPER1 (ZYP1), FANCONI ANEMIA COMPLEMENTATION GROUP M (FANCM) and D2 (FANCD2), the underlying mechanism may be similar between ATR and FANCD2. This study extends our understanding of ATR’s role in meiosis, uncovering functions in regulating crossover distribution.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"86 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142541280","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yingjia Han, Siqi Jiang, Xiaomei Dong, Xing Dai, Shunxi Wang, Ying Zheng, Ge Yan, Shengben Li, Liuji Wu, Virginia Walbot, Blake C Meyers, Mei Zhang
Reproductive phasiRNAs (phased, small interfering RNAs), produced from numerous PHAS loci, are essential for plant anther development. PHAS transcripts are enriched on endoplasmic reticulum-bound ribosomes in maize (Zea mays), but the impact of ribosome binding on phasiRNA biogenesis remains elusive. Through ribosome profiling of maize anthers at 10 developmental stages, we demonstrated that 24-PHAS transcripts are bound by ribosomes, with patterns corresponding to the timing and abundance of 24-PHAS transcripts. Ribosome binding to 24-PHAS transcripts is conserved among different maize inbred lines, with ribosomes enriched upstream of miR2275 target sites. We detected short open reading frames (sORFs) in the ribosome-binding regions of some 24-PHAS transcripts and observed a 3-nt periodicity in most sORFs, but mass spectrometry failed to detect peptides corresponding to the sORFs. Deletion of the entire ribosome-binding region of 24PHAS_NO296 locus eliminated ribosome binding and decreased 24-nt phasiRNA production, without affecting 24PHAS_NO296 transcript levels. In contrast, disrupting only the sORFs in 24PHAS_NO296 did not substantially affect the generation of 24-nt phasiRNAs. A newly formed sORF in these mutants may have re-directed ribosome binding to its transcripts. Overall, these findings demonstrate that sORFs facilitate ribosome binding to 24-PHAS transcripts, thereby promoting phasiRNA biogenesis in meiotic anthers.
{"title":"Ribosome binding of phasiRNA precursors accelerates the 24-nt phasiRNA burst in meiotic maize anthers","authors":"Yingjia Han, Siqi Jiang, Xiaomei Dong, Xing Dai, Shunxi Wang, Ying Zheng, Ge Yan, Shengben Li, Liuji Wu, Virginia Walbot, Blake C Meyers, Mei Zhang","doi":"10.1093/plcell/koae289","DOIUrl":"https://doi.org/10.1093/plcell/koae289","url":null,"abstract":"Reproductive phasiRNAs (phased, small interfering RNAs), produced from numerous PHAS loci, are essential for plant anther development. PHAS transcripts are enriched on endoplasmic reticulum-bound ribosomes in maize (Zea mays), but the impact of ribosome binding on phasiRNA biogenesis remains elusive. Through ribosome profiling of maize anthers at 10 developmental stages, we demonstrated that 24-PHAS transcripts are bound by ribosomes, with patterns corresponding to the timing and abundance of 24-PHAS transcripts. Ribosome binding to 24-PHAS transcripts is conserved among different maize inbred lines, with ribosomes enriched upstream of miR2275 target sites. We detected short open reading frames (sORFs) in the ribosome-binding regions of some 24-PHAS transcripts and observed a 3-nt periodicity in most sORFs, but mass spectrometry failed to detect peptides corresponding to the sORFs. Deletion of the entire ribosome-binding region of 24PHAS_NO296 locus eliminated ribosome binding and decreased 24-nt phasiRNA production, without affecting 24PHAS_NO296 transcript levels. In contrast, disrupting only the sORFs in 24PHAS_NO296 did not substantially affect the generation of 24-nt phasiRNAs. A newly formed sORF in these mutants may have re-directed ribosome binding to its transcripts. Overall, these findings demonstrate that sORFs facilitate ribosome binding to 24-PHAS transcripts, thereby promoting phasiRNA biogenesis in meiotic anthers.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"161 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488634","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zhijuan Chen, Jing Lu, Xiaoyi Li, Danhua Jiang, Zicong Li
The evolutionarily conserved Polycomb repressive complexes (PRC) mediate genome-wide transcriptional silencing and regulate a plethora of development, as well as environmental responses in multicellular organisms. The PRC2-catalyzed trimethylation of lysine 27 on histone H3 (H3K27me3) is recognized by reader-effector modules of PRC1 to implement gene repression. Here, we report that the Arabidopsis (Arabidopsis thaliana) H3K27me3 effector EMBRYONIC FLOWER 1 (EMF1) interacts with and constrains the R2R3 DNA binding transcription factor MYB26 by a eudicot-conserved motif in the stamen. MYB26 activates the transcription of two NAC domain genes, NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) and NST2, whose encoded proteins mediate anther secondary cell thickening in jasmonate (JA)-regulated stamen maturation. In this process, the transcriptional activity of MYB26 is negatively modulated by the JAZ-PRC repressive complex to precisely regulate the expression of NST1 and NST2. Disruption of EMF1 repression stimulates MYB26, leading to the excessive transcription of the two NAC genes and male sterility. Our results reveal a novel mechanism in polycomb-mediated gene silencing and illustrate that the plant Polycomb complex regulates stamen development by preventing the hypersensitivity of JA responses in male reproduction.
{"title":"EMBRYONIC FLOWER 1 regulates male reproduction by repressing the jasmonate pathway downstream transcription factor MYB26","authors":"Zhijuan Chen, Jing Lu, Xiaoyi Li, Danhua Jiang, Zicong Li","doi":"10.1093/plcell/koae287","DOIUrl":"https://doi.org/10.1093/plcell/koae287","url":null,"abstract":"The evolutionarily conserved Polycomb repressive complexes (PRC) mediate genome-wide transcriptional silencing and regulate a plethora of development, as well as environmental responses in multicellular organisms. The PRC2-catalyzed trimethylation of lysine 27 on histone H3 (H3K27me3) is recognized by reader-effector modules of PRC1 to implement gene repression. Here, we report that the Arabidopsis (Arabidopsis thaliana) H3K27me3 effector EMBRYONIC FLOWER 1 (EMF1) interacts with and constrains the R2R3 DNA binding transcription factor MYB26 by a eudicot-conserved motif in the stamen. MYB26 activates the transcription of two NAC domain genes, NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) and NST2, whose encoded proteins mediate anther secondary cell thickening in jasmonate (JA)-regulated stamen maturation. In this process, the transcriptional activity of MYB26 is negatively modulated by the JAZ-PRC repressive complex to precisely regulate the expression of NST1 and NST2. Disruption of EMF1 repression stimulates MYB26, leading to the excessive transcription of the two NAC genes and male sterility. Our results reveal a novel mechanism in polycomb-mediated gene silencing and illustrate that the plant Polycomb complex regulates stamen development by preventing the hypersensitivity of JA responses in male reproduction.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"14 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142487372","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Correction to: Nitrate in 2020: Thirty Years from Transport to Signaling Networks.","authors":"","doi":"10.1093/plcell/koae265","DOIUrl":"https://doi.org/10.1093/plcell/koae265","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"28 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488202","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Building barriers: The role of MYB genes in rice root adaptation.","authors":"Gwendolyn K Kirschner","doi":"10.1093/plcell/koae284","DOIUrl":"https://doi.org/10.1093/plcell/koae284","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"109 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488224","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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