Multifunctional NAC transcription factor SlJA2L integrates the ethylene pathway to orchestrate thermotolerance and fruit ripening in tomato.

Abstract

High temperatures driven by climate change are increasingly limiting crop growth and quality. Fruit ripening is a genetically programmed process regulated by transcription factors (TFs), while the phytohormone ethylene plays key roles in both ripening and abiotic stress responses. However, the underlying regulatory mechanisms remain poorly understood. We identified Solanum lycopersicum jasmonic acid 2-like (SlJA2L), a tomato NAC TF that is transcriptionally responsive to both heat stress (HS) and fruit ripening, suggesting that it acts as a molecular integrator of HS adaptation and fruit developmental processes. Overexpression of SlJA2L enhanced heat tolerance and promoted fruit ripening, whereas clustered regularly interspaced short palindromic repeats-CRISPR-associated protein 9 (CRISPR-Cas9)-mediated knockout led to heat sensitivity and ripening delay. Mechanistically, SlJA2L directly activates SlHsfA3 and SlCAT3 under HS. During ripening, it promotes ethylene biosynthesis via the SlJA2L-SlACO1 module and enhances carotenoid accumulation by activating SlCRTISO. Moreover, ethylene was shown to contribute to thermotolerance, as exogenous 1-aminocyclopropane-1-carboxylic acid improved heat tolerance, while silencing SlACO1 reduced it. Our findings demonstrate that SlJA2L integrates ethylene signaling to regulate both thermotolerance and fruit ripening in tomato. This study provides new insights into the molecular coordination of stress responses and developmental transitions, offering a potential strategy for improving crop resilience and fruit ripening under climate stress.