Jasmonates Promote β-Amylase-Mediated Starch Degradation to Confer Cold Tolerance in Tomato Plants

Cold stress severely restricts growth and development, reduces yields, and impairs quality in tomatoes (Solanum lycopersicum). Amylase-associated starch degradation and soluble sugar accumulation have been implicated in adaptation and resistance to abiotic stress. Here, we report a beta-amylase (BAM) gene, SlBAM3, which plays a central role in tomato cold tolerance. The expression of SlBAM3 was triggered by cold stress. SlBAM3 knockout using the CRISPR/Cas9 system retarded starch degradation and reduced soluble sugar accumulation in tomato plants, eventually attenuating cold tolerance. Expression analysis revealed that the SlBAM3 transcript level was boosted by MeJA. Furthermore, MYC2, an essential component of the JA signaling pathway, could bind to the SlBAM3 promoter and directly activate SlBAM3 transcription, as revealed by yeast one-hybrid and dual LUC assays. In addition, the suppression of MYC2 resulted in increased starch accumulation, decreased soluble sugar content, and reduced tolerance to cold stress in tomato plants. Taken together, these findings demonstrate that JA positively regulates beta-amylase-associated starch degradation through the MYC2-SlBAM3 module in tomato during cold stress. The results of the present work expand our understanding of the mechanisms underlying BAM gene activation and starch catabolism under cold stress. The regulatory module of SlBAM3 can be further utilized to breed tomato cultivars with enhanced cold tolerance.