The SlMYC2-SlNAC72-SlMIEL1 module contributes to high-temperature tolerance in tomato by regulating jasmonic acid biosynthesis

Amid global climate change, extreme high-temperature events have become increasingly frequent, posing significant threats to ecosystems and agricultural production. NAM, ATAF, and CUC transcription factors (NAC TFs) play a key role in responding to environmental stresses such as drought, salt stress, and temperature changes. This study demonstrates that SlNAC72, a member of the NAC transcription factor family, directly targets and regulates LIPOXYGENASE 10 (SlLOX10), ALLENE OXIDE SYNTHASE 1 (SlAOS1), and ALLENE OXIDE CYCLASE (SlAOC) in tomato (Solanum lycopersicum), inhibiting jasmonic acid (JA) biosynthesis and thereby negatively regulating heat tolerance. Overexpression of SlAOS1 notably increased JA accumulation under high-temperature stress and mitigated excessive reactive oxygen species (ROS) accumulation, whereas slaos1 knockout resulted in the opposite phenotype, indicating the positive role of SlAOS1 in JA biosynthesis and high-temperature stress tolerance. Further investigations revealed that SlNAC72 interacts with the E3 ubiquitin ligase MYB30-INTERACTING E3 LIGASE 1 (SlMIEL1) and that SlMIEL1 promotes JA accumulation by mediating the ubiquitination and degradation of SlNAC72, ultimately enhancing high-temperature tolerance in tomato. Additionally, as a key transcription factor in the JA signaling pathway, MYELOCYTOMATOSIS 2 (SlMYC2) directly bound to SlNAC72 and suppressed its expression. This study uncovers the central role of the SlMYC2-SlNAC72-SlMIEL1 module in regulating JA biosynthesis and elucidates how this module contributes to the molecular mechanisms underlying tomato's response to high-temperature stress via regulating JA accumulation.