SlBES1-mediated brassinosteroid signaling suppresses flavonoid biosynthesis in tomato fruit.

With the improvement of living standards, consumers' demands for color diversity and nutritional quality of tomato products have increased. Flavonoid is a considerable index of peel color and nutritional quality in tomato fruit, where flavonoid biosynthesis is controlled by various phytohormones, including brassinosteroids (BRs). However, the underlying mechanism by which BR regulates flavonoid biosynthesis is still unknown. Here, we found that exogenous BR inhibits flavonoid accumulation, while reduced endogenous BR in RNA interference (RNAi) lines of SlCYP90B3, a rate-limiting BR biosynthetic gene, results in increased flavonoid content in fruit peel. Furthermore, we observed that BRI1-EMS-suppressor1 (SlBES1), a bHLH transcription factor essential for BR signaling, not only regulates fruit firmness, but also suppresses flavonoid accumulation by directly binding to the promoters of flavonoid biosynthetic genes SlCHS1, SlCHS2, and SlF3'H. Additionally, SlBES1 modulates a hierarchical transcriptional cascade to suppress flavonoid biosynthesis via repressing SlMYB12. Moreover, the homologous gene Brassinazole-resistant1 (SlBZR1) enhances the SlBES1-mediated repression of flavonoid accumulation. Specifically, SlBES1 predominantly inhibits the flavonoid biosynthesis, whereas SlBZR1 primarily enhances the carotenoid pathway. Interestingly, the variation of SlBES1 was correlated with flavonoid content during tomato domestication. Collectively, these findings provide new insights into novel role of SlBES1 as a negative regulator of flavonoid biosynthesis with potential for biofortification of flavonoid in tomato.