The hormone jasmonate (JA), which functions in plant immunity, regulates resistance to pathogen infection and insect attack through triggering genome-wide transcriptional reprogramming in plants. We show that the basic helix-loop-helix transcription factor (TF) MYC2 in tomato (Solanum lycopersicum) acts downstream of the JA receptor to orchestrate JA-mediated activation of both the wounding and pathogen responses. Using chromatin immunoprecipitation sequencing (ChIP-seq) coupled with RNA sequencing (RNA-seq) assays, we identified 655 MYC2-targeted JA-responsive genes. These genes are highly enriched in Gene Ontology categories related to TFs and the early response to JA, indicating that MYC2 functions at a high hierarchical level to regulate JA-mediated gene transcription. We also identified a group of MYC2-targeted TFs (MTFs) that may directly regulate the JA-induced transcription of late defense genes. Our findings suggest that MYC2 and its downstream MTFs form a hierarchical transcriptional cascade during JA-mediated plant immunity that initiates and amplifies transcriptional output. As proof of concept, we showed that during plant resistance to the necrotrophic pathogen Botrytis cinerea, MYC2 and the MTF JA2-Like form a transcription module that preferentially regulates wounding-responsive genes, whereas MYC2 and the MTF ETHYLENE RESPONSE FACTOR.C3 form a transcription module that preferentially regulates pathogen-responsive genes.
Bibliographical noteFunding Information:
We thank Chang Li for the improvement of the English language. This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant XDB11030200), by the National Key Research and Development Program of China (2016YFD0100603-10), by the Ministry of Agriculture of the People’s Republic of China (Chinese Ministry of Agriculture) (2016ZX08009-003-001), by the National Natural Science Foundation of China (Grants 31030006, 31672157, and 31390423), by the Tai-Shan Scholar Program from the Shandong Province, and by Hong Kong UGC (14104515/ 14119814).