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OsPRMT6a-mediated arginine methylation of OsJAZ1 regulates jasmonate signaling and spikelet development in rice

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

Molecular Plant;2024;IF 27.50



Although both protein arginine methylation (PRMT) and jasmonate (JA) signaling are crucial for regulating plant development, the relationship between these processes in spikelet development control remains unclear. Here, we utilized CRISPR/Cas9 technology to generate two OsPRMT6a loss-of-function mutants exhibiting various abnormal spikelet structures. Additionally, we found that OsPRMT6a could methylate arginine residues in the JA signal repressors OsJAZ1 and OsJAZ7. Arginine methylation of OsJAZ1 increased the affinity of OsJAZ1 for the JA receptors OsCOI1a and OsCOI1b in the presence of jasmonates (JAs), subsequently promoting the ubiquitination of OsJAZ1 by the SCFOsCOI1a/OsCOI1b complex and degradation via the 26S proteasome. This process ultimately released 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 impaired the interaction between OsJAZ1 and OsCOI1a/OsCOI1b in the presence of JAs. As a result, OsJAZ1 proteins became more stable, repressing JA responses, thus causing the formation of abnormal spikelet structures. Moreover, we discovered that JA signaling reduced the OsPRMT6a mRNA level in an OsMYC2-dependent manner, thereby establishing a negative feedback loop to balance JA signaling. Furthermore, we 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. Thus, our study established a direct molecular link between arginine methylation and the JA signaling pathway.