Loss of function of STAY-GREEN 1 enhances cold tolerance in tomato (Solanum lycopersicum L.) associated with jasmonic acid signaling and metabolic reprogramming.

Abstract

Photosynthetic machinery reprogramming is essential for Cold Stress Tolerance (CST) in plants. STAY-GREEN 1 (SlSGR1) plays vital roles in chlorophyll breakdown and leaf senescence, but its function in tomato cold acclimation has not been clarified. Here, we constructed two inbred tomato lines (T048, T069) carrying SlSGR1 homozygous knockout mutants via CRISPR/Cas9 editing, and conducted integrated physiological, biochemical, metabolomic, and transcriptome analyses to dissect the role of SlSGR1 in regulating cold tolerance. Loss of function of SlSGR1 triggered extensive physiological, metabolic and transcriptional readjustments that improved tomato cold tolerance. sgr1 mutant seedlings maintained higher water retention and proline levels, along with reduced MDA and reactive oxygen species (ROS) accumulation, alongside elevated SOD, POD and CAT antioxidant enzyme activities. Multi-omics data revealed prominent activation of jasmonic acid (JA) biosynthesis and signaling in cold-stressed sgr1 lines, accompanied by elevated JA-Ile and strong upregulation of JA synthetic and signaling genes including multiple JAZ family members. Activated JA cascades further induced the master cold regulators ICE1, CBF1 and CBF2, driving downstream shifts in carbohydrate and amino acid metabolism as well as widespread ethylene-responsive transcription factor expression. Our multi-line genetic and multi-omics evidence collectively confirms that SlSGR1 acts as a negative regulator of tomato cold adaptation via restraining JA-ICE-CBF signaling. This study expands the biological functions of SlSGR1 beyond chlorophyll breakdown and leaf senescence, and provides valuable resources for molecular breeding.