SlWRKY14 integrates carotenoid and flavonoid biosynthetic pathways to regulate coloration and quality of tomato fruits.

Abstract

Carotenoids and flavonoids are two principal classes of secondary metabolites in tomato fruit, jointly contributing to pigmentation and nutritional quality. Here, we identified SlWRKY14 as a novel regulator of both these two pathways. slwrky14 lines result in redder fruits enriched in carotenoids, whereas fruit-specific overexpression lines produce orange-yellow fruits with reduced carotenoids but elevated flavonoids. SlWRKY14 directly binds to the promoter of carotenoid biosynthetic genes (SlDXS1 and SlPSY1) and represses their transcription by recruiting histone deacetylase SlHDA1, which functions in decreased histone acetylation to inhibit gene expression. Further genetic evidence verifies the role of the SlWRKY14-SlHDA1 module in suppressing carotenoid accumulation. In contrast, SlWRKY14 activates the flavonoid biosynthetic gene SlPALA to promote flavonoid accumulation. Our findings demonstrate SlWRKY14 as a regulatory node of carotenoid and flavonoid biosynthesis, providing a strategy for coloration regulation and quality improvement without penalty of yield in tomato.