Tong Xu, Tingting Ran, Ying Shi, Fengjun Yang, Xinlin Chen, Ewa Sobieszczuk‐Nowicka, Vasileios Fotopoulos, Jie Zhou
Heat stress is a major environmental challenge affecting agricultural productivity and food security. The jasmonate (JA)-myelocytomatosis protein 2 (MYC2) pathway plays a critical role in plant growth and stress response. However, the mechanisms of how the JA-MYC2 pathway participates in the heat stress response in tomato remain unclear. Here, using approaches of reverse genetics, biochemical and molecular biology, we explore the molecular mechanism by which the JA signaling pathway and the histone demethylase Jumonji C domain - containing protein C3 (JMJC3) synergistically regulate thermotolerance in tomato. The JA biosynthetic mutant spr2 exhibited reduced thermotolerance, which was rescued by exogenous methyl jasmonate. Further analysis revealed that the transcription factor MYC2, a key JA signaling component, directly binds to the promoters of heat shock proteins (HSPs), activating their expression under heat stress. Moreover, MYC2 interacts with the histone demethylase JMJC3, which specifically removes repressive histone marks (H3K9me1/3 and H3K27me3) at HSP loci, facilitating their transcription. Genetic evidence showed that JMJC3 silencing compromises MYC2-mediated thermotolerance and HSP induction. Notably, MYC2 also transcriptionally activates JMJC3, forming a positive feedback loop. Collectively, the study unveiled a JA-MYC2-JMJC3 module that integrates hormonal signaling and epigenetic regulation to enhance HSP expression and thermotolerance in tomato, providing insights into plant adaptation to heat stress.