Abstract

Cold tolerance and tea quality are essential for profitable tea cultivation, yet the genetic interplay between them remains elusive. Here, we systematically evaluated cold tolerance and quantified 12 key tea quality-related metabolites over two consecutive years of 108 geographically diverse tea accessions in China. Multi-trait genome-wide association mapping identified a central hub regulator, COLD AND CATECHINS REGULATOR 1 (CCR1), significantly associated with cold tolerance and catechins biosynthesis in tea plants. Functional analysis demonstrated that CsCCR1 positively regulates cold tolerance and catechins accumulation in tea plants, and that a missense variation (A-to-C) in CsCCR1 significantly enhances cold tolerance and catechins accumulation. Exogenous application of catechins (EGCG/EGC/EC) could also significantly alleviate cold-induced oxidative damage through ROS scavenging. We demonstrated that CsCCR1, activated by upstream regulators CsLUX and CsKUA1, directly activates catechin biosynthetic genes (CsCHS1, CsFLS1, CsSCPL4, CsSCPL5) and a novel cold-responsive gene CsELIP1. Furthermore, CsCCR1 physically interacts with CsCBF1/3 to form a transcriptional activation complex that synergistically amplifies expression of these downstream targets, thereby simultaneously modulating cold tolerance and catechins biosynthesis. Our findings underscore the importance of CsCCR1 in linking cold tolerance with quality formation of tea plants, offering targets for breeding elite tea cultivars with superior cold resistance and quality.