Glycosylated sterols enhance cold tolerance in tomato via membrane stabilization and jasmonate signaling

Free and glycosylated sterols play a central role in maintaining the structural integrity and proper functioning of the plasma membrane, which serves as the primary sensor of cold and initiates signaling cascades to mitigate chilling-induced damage. Here, we characterize the cold-response of tomato (Solanum lycopersicum cv. Micro-Tom) mutants with higher and lower ratios of glycosylated to free sterols than wild-type plants, resulting from the overexpression and silencing of the STEROL GLYCOSYLTRANSFERASES 1 and 2 (SlSGT2 and SlSGT1), respectively. The SlSGT2 overexpressing mutants show increased cold tolerance, membrane stability, and oxidative stress responses, while silencing of the SlSGT1 gene causes the opposite phenotypes. Furthermore, changes in the glycosylated to free sterols ratio activate distinct transcriptional programs that establish a preconditioned stress-responsive state under basal conditions and trigger a more efficient response to cold in the SlSGT2 overexpressing mutants, as well as compromise the capacity to withstand the effects of cold stress in the SlSGT1-silenced mutants. The SlSGT2 overexpressing mutants also contain higher levels of jasmonates under basal conditions and display enhanced biosynthesis of these hormones under cold stress compared to SlSGT1-silenced and control plants. The facilitating effect of elevated glycosylated to free sterols ratio on jasmonic acid (JA) biosynthesis and signaling leads to the activation of cold-responsive genes, including those of the CBF-COR pathway, antioxidant defenses, and polyamine biosynthesis. Our findings provide key insights into the mechanisms by which glycosylated sterols help improve cold tolerance in tomato.