{"title":"OsPRMT6a 介导的 OsJAZ1 精氨酸甲基化调控水稻的茉莉酸信号传导和小穗发育。","authors":"Kun Dong, Fuqing Wu, Siqi Cheng, Shuai Li, Feng Zhang, Xinxin Xing, Xin Jin, Sheng Luo, Miao Feng, Rong Miao, Yanqi Chang, Shuang Zhang, Xiaoman You, Peiran Wang, Xin Zhang, Cailin Lei, Yulong Ren, Shanshan Zhu, Xiuping Guo, Chuanyin Wu, Dong-Lei Yang, Qibing Lin, Zhijun Cheng, Jianmin Wan","doi":"10.1016/j.molp.2024.04.014","DOIUrl":null,"url":null,"abstract":"<p><p>Although both protein arginine methylation (PRMT) and jasmonate (JA) signaling are crucial for regulating plant development, the relationship between these processes in the control of spikelet development remains unclear. In this study, we used the CRISPR/Cas9 technology to generate two OsPRMT6a loss-of-function mutants that exhibit various abnormal spikelet structures. Interestingly, we found that OsPRMT6a can methylate arginine residues in JA signal repressors OsJAZ1 and OsJAZ7. We showed that arginine methylation of OsJAZ1 enhances the binding affinity of OsJAZ1 with the JA receptors OsCOI1a and OsCOI1b in the presence of JAs, thereby promoting the ubiquitination of OsJAZ1 by the SCF<sup>OsCOI1a/OsCOI1b</sup> complex and degradation via the 26S proteasome. This process ultimately releases OsMYC2, a core transcriptional regulator in the JA signaling pathway, to activate or repress JA-responsive genes, thereby maintaining normal plant (spikelet) development. However, in the osprmt6a-1 mutant, reduced arginine methylation of OsJAZ1 impaires the interaction between OsJAZ1 and OsCOI1a/OsCOI1b in the presence of JAs. As a result, OsJAZ1 proteins become more stable, repressing JA responses, thus causing the formation of abnormal spikelet structures. Moreover, we discovered that JA signaling reduces the OsPRMT6a mRNA level in an OsMYC2-dependent manner, thereby establishing a negative feedback loop to balance JA signaling. We further found that OsPRMT6a-mediated arginine methylation of OsJAZ1 likely serves as a switch to tune JA signaling to maintain normal spikelet development under harsh environmental conditions such as high temperatures. Collectively, our study establishes a direct molecular link between arginine methylation and JA signaling in rice.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"900-919"},"PeriodicalIF":17.1000,"publicationDate":"2024-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"OsPRMT6a-mediated arginine methylation of OsJAZ1 regulates jasmonate signaling and spikelet development in rice.\",\"authors\":\"Kun Dong, Fuqing Wu, Siqi Cheng, Shuai Li, Feng Zhang, Xinxin Xing, Xin Jin, Sheng Luo, Miao Feng, Rong Miao, Yanqi Chang, Shuang Zhang, Xiaoman You, Peiran Wang, Xin Zhang, Cailin Lei, Yulong Ren, Shanshan Zhu, Xiuping Guo, Chuanyin Wu, Dong-Lei Yang, Qibing Lin, Zhijun Cheng, Jianmin Wan\",\"doi\":\"10.1016/j.molp.2024.04.014\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Although both protein arginine methylation (PRMT) and jasmonate (JA) signaling are crucial for regulating plant development, the relationship between these processes in the control of spikelet development remains unclear. In this study, we used the CRISPR/Cas9 technology to generate two OsPRMT6a loss-of-function mutants that exhibit various abnormal spikelet structures. Interestingly, we found that OsPRMT6a can methylate arginine residues in JA signal repressors OsJAZ1 and OsJAZ7. We showed that arginine methylation of OsJAZ1 enhances the binding affinity of OsJAZ1 with the JA receptors OsCOI1a and OsCOI1b in the presence of JAs, thereby promoting the ubiquitination of OsJAZ1 by the SCF<sup>OsCOI1a/OsCOI1b</sup> complex and degradation via the 26S proteasome. This process ultimately releases OsMYC2, a core transcriptional regulator in the JA signaling pathway, to activate or repress JA-responsive genes, thereby maintaining normal plant (spikelet) development. However, in the osprmt6a-1 mutant, reduced arginine methylation of OsJAZ1 impaires the interaction between OsJAZ1 and OsCOI1a/OsCOI1b in the presence of JAs. As a result, OsJAZ1 proteins become more stable, repressing JA responses, thus causing the formation of abnormal spikelet structures. Moreover, we discovered that JA signaling reduces the OsPRMT6a mRNA level in an OsMYC2-dependent manner, thereby establishing a negative feedback loop to balance JA signaling. We further found that OsPRMT6a-mediated arginine methylation of OsJAZ1 likely serves as a switch to tune JA signaling to maintain normal spikelet development under harsh environmental conditions such as high temperatures. Collectively, our study establishes a direct molecular link between arginine methylation and JA signaling in rice.</p>\",\"PeriodicalId\":19012,\"journal\":{\"name\":\"Molecular Plant\",\"volume\":\" \",\"pages\":\"900-919\"},\"PeriodicalIF\":17.1000,\"publicationDate\":\"2024-06-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular Plant\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1016/j.molp.2024.04.014\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/5/4 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Plant","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.molp.2024.04.014","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/5/4 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
尽管蛋白质精氨酸甲基化(PRMT)和茉莉酸盐(JA)信号传导对植物的生长发育具有重要的调控作用,但这两个过程在小穗生长发育调控中的关系仍不清楚。在这里,我们利用 CRISPR/Cas9 技术产生了两个 OsPRMT6a 功能缺失突变体,它们表现出各种异常的小穗结构。此外,我们还发现OsPRMT6a可以甲基化JA信号抑制因子OsJAZ1和OsJAZ7中的精氨酸残基。OsJAZ1 的精氨酸甲基化增加了 OsJAZ1 与 JA 受体 OsCOI1a 和 OsCOI1b 的亲和力,从而促进 OsJAZ1 被 SCFOsCOI1a/OsCOI1b 复合物泛素化,并通过 26S 蛋白酶体降解。这一过程最终释放出 JA 信号通路中的核心转录调节因子 OsMYC2,以激活或抑制 JA 响应基因,从而维持植株(小穗)的正常发育。然而,在osprmt6a-1突变体中,OsJAZ1的精氨酸甲基化程度降低,在JA存在的情况下影响了OsJAZ1与OsCOI1a/OsCOI1b之间的相互作用。结果,OsJAZ1 蛋白变得更加稳定,抑制了 JA 反应,从而导致异常小穗结构的形成。此外,我们发现 JA 信号以 OsMYC2 依赖的方式降低了 OsPRMT6a 的 mRNA 水平,从而建立了平衡 JA 信号的负反馈回路。此外,我们还发现 OsPRMT6a 介导的 OsJAZ1 精氨酸甲基化很可能是调节 JA 信号的开关,从而在高温等恶劣环境条件下维持小穗的正常发育。因此,我们的研究建立了精氨酸甲基化与 JA 信号通路之间的直接分子联系。
OsPRMT6a-mediated arginine methylation of OsJAZ1 regulates jasmonate signaling and spikelet development in rice.
Although both protein arginine methylation (PRMT) and jasmonate (JA) signaling are crucial for regulating plant development, the relationship between these processes in the control of spikelet development remains unclear. In this study, we used the CRISPR/Cas9 technology to generate two OsPRMT6a loss-of-function mutants that exhibit various abnormal spikelet structures. Interestingly, we found that OsPRMT6a can methylate arginine residues in JA signal repressors OsJAZ1 and OsJAZ7. We showed that arginine methylation of OsJAZ1 enhances the binding affinity of OsJAZ1 with the JA receptors OsCOI1a and OsCOI1b in the presence of JAs, thereby promoting the ubiquitination of OsJAZ1 by the SCFOsCOI1a/OsCOI1b complex and degradation via the 26S proteasome. This process ultimately releases OsMYC2, a core transcriptional regulator in the JA signaling pathway, to activate or repress JA-responsive genes, thereby maintaining normal plant (spikelet) development. However, in the osprmt6a-1 mutant, reduced arginine methylation of OsJAZ1 impaires the interaction between OsJAZ1 and OsCOI1a/OsCOI1b in the presence of JAs. As a result, OsJAZ1 proteins become more stable, repressing JA responses, thus causing the formation of abnormal spikelet structures. Moreover, we discovered that JA signaling reduces the OsPRMT6a mRNA level in an OsMYC2-dependent manner, thereby establishing a negative feedback loop to balance JA signaling. We further found that OsPRMT6a-mediated arginine methylation of OsJAZ1 likely serves as a switch to tune JA signaling to maintain normal spikelet development under harsh environmental conditions such as high temperatures. Collectively, our study establishes a direct molecular link between arginine methylation and JA signaling in rice.
期刊介绍:
Molecular Plant is dedicated to serving the plant science community by publishing novel and exciting findings with high significance in plant biology. The journal focuses broadly on cellular biology, physiology, biochemistry, molecular biology, genetics, development, plant-microbe interaction, genomics, bioinformatics, and molecular evolution.
Molecular Plant publishes original research articles, reviews, Correspondence, and Spotlights on the most important developments in plant biology.