State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
State Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing 210095, China.
Mol Plant. 2024 Jun 3;17(6):900-919. doi: 10.1016/j.molp.2024.04.014. Epub 2024 May 4.
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 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.
尽管蛋白精氨酸甲基化 (PRMT) 和茉莉酸 (JA) 信号都对植物发育的调控至关重要,但这些过程在小穗发育控制中的关系尚不清楚。在这项研究中,我们使用 CRISPR/Cas9 技术生成了两个 OsPRMT6a 功能丧失突变体,它们表现出各种异常的小穗结构。有趣的是,我们发现 OsPRMT6a 可以甲基化 JA 信号抑制剂 OsJAZ1 和 OsJAZ7 中的精氨酸残基。我们表明,在 JA 存在的情况下,OsJAZ1 的精氨酸甲基化增强了 OsJAZ1 与 JA 受体 OsCOI1a 和 OsCOI1b 的结合亲和力,从而促进了 SCF 复合物对 OsJAZ1 的泛素化和通过 26S 蛋白酶体降解。这一过程最终释放了 JA 信号通路中的核心转录调节剂 OsMYC2,以激活或抑制 JA 响应基因,从而维持正常的植物(小穗)发育。然而,在 osprmt6a-1 突变体中,OsJAZ1 的精氨酸甲基化减少会损害 JA 存在时 OsJAZ1 与 OsCOI1a/OsCOI1b 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 OsPRMT6a mRNA 水平,从而建立了一个负反馈环来平衡 JA 信号。我们进一步发现,OsPRMT6a 介导的 OsJAZ1 精氨酸甲基化可能作为一个开关来调节 JA 信号,以在高温等恶劣环境条件下维持正常的小穗发育。总之,我们的研究在水稻中建立了精氨酸甲基化和 JA 信号之间的直接分子联系。