B‐ BOX DOMAIN PROTEIN 19 shapes tea quality by modulating the ratio of catechins and theanine and confers cold tolerance in tea plants

Abstract

Summary Early spring cold spells threaten tea plant ( Camellia sinensis ) yield and disrupt the catechins‐to‐theanine ratio that determines the desirable balance of umami and astringency taste of tea. However, the molecular mechanism coordinating cold tolerance with this key quality trait remains unclear. Here, we identified a light‐responsive B‐BOX DOMAIN PROTEIN CsBBX19 as a core regulator simultaneously shaping tea quality and cold tolerance. Results demonstrated that silencing CsBBX19 relieves the transcriptional repression of theanine‐biosynthetic genes ( CsTSI and CsAlaDC ) to elevate theanine levels, yet weakens the activation of catechins‐biosynthetic genes ( CsANS1 , CsANR1 , CsLAR1 , and CsSCPL1 /2/5) to reduce catechins content. The CsBBX19 ‐modulated theanine accumulation also enhanced the cold tolerance of tea plants by suppressing cell‐wall‐loosening EXPANSIN ( CsEXPA10/20/21 ) and activating the CsCBF3 ‐mediated cold response pathway. Furthermore, the expression of CsBBX19 significantly reduced by light via a feedback loop involving CsHY5, which directly binds to the promoter of CsBBX19 to repress its transcription, while CsBBX19 conversely interacts with CsHY5 to reinforce its autoactivation, thereby fine‐tuning the catechins‐to‐theanine ratio and cold resilience in tea plants. Our findings underscore the central roles of CsBBX19 in light‐mediated cold response and tea quality formation, providing valuable targets for synchronously improving cold resilience and quality in tea plants.