Jasmonate ZIM-domain protein 2 orchestrates ABA/JA signaling and flavonoid biosynthesis to suppress cold tolerance in grapevine.

Abstract

Low temperature is a significant abiotic stressor that severely constrains grape cultivation and productivity. Jasmonate ZIM-domain (JAZ) proteins, which function as critical transcriptional repressors in the jasmonic acid signaling pathway, play essential roles in plant stress adaptation. Nevertheless, their specific functions and regulatory mechanisms in grape cold tolerance remain unclear. This work investigated the role and regulatory network of a cold-inducible VvJAZ2 gene by integrating physiological, molecular, and transcriptomic approaches. Functional analyses revealed that overexpression of VvJAZ2 compromised cold tolerance in Arabidopsis and grape calli, manifested as aggravated oxidative damage and compromised antioxidant capacity. Furthermore, transgenic materials exhibited decreased endogenous ABA and JA levels, reduced flavonoid accumulation, and downregulation of the ICE-CBF-COR regulatory module. Consistently, transcriptomic profiling further indicated that VvJAZ2 functions as a negative regulator by coordinating the suppression of ABA/JA signaling cascades, MAPK pathway activity, and flavonoid biosynthetic processes. Mechanistically, the transcription factor VvMSA (Abscisic acid-stress-ripening protein) was identified as an upstream activator that directly binds to the VvJAZ2 promoter and induces its expression under normal conditions; however, this activation is markedly attenuated during cold stress. Moreover, VvJAZ2 physically interacts with VvUGT74F5 (UDP-glycosyltransferase 74F5) implicated in flavonoid modification. Collectively, these findings suggest that VvJAZ2 may function as a potential regulatory node, and support a working model of a dynamic "transcription-protein interaction" module to coordinate hormone signaling and metabolic reprogramming under cold stress. This study provides novel insights into the molecular basis of cold adaptation in grapevine and identifies potential genetic targets for improving cold resilience in viticulture.