SlMYB72 regulates the metabolism of chlorophylls, carotenoids, and flavonoids in tomato fruit

Tomato (Solanum lycopersicum) fruit ripening is accompanied by the degradation of chlorophylls and the accumulation of carotenoids and flavonoids. Tomato SlMYB72 belongs to the R2R3 MYB subfamily, is located in the nucleus, and possesses transcriptional activator activity. Downregulation of the SlMYB72 gene produced uneven-colored fruits, that is, dark green spots appeared on immature and mature green fruits, whereas yellow spots appeared on red fruits. Downregulation of SlMYB72 increased chlorophyll accumulation, chloroplast biogenesis and development, and photosynthesis rate in fruits. This downregulation decreased lycopene content, promoted β-carotene production and chromoplast development, and increased flavonoid accumulation in fruits. RNA-seq analysis revealed that downregulation of SlMYB72 altered the expression levels of genes involved in the biosynthesis of chlorophylls, carotenoids, and flavonoids. SlMYB72 protein interacted with auxin response factor SlARF4. SlMYB72 directly targeted protochlorophyllide reductase (POR), Mg-chelatase H subunit (CHLH), and knotted 1-like homeobox 2 (TKN2) genes, and regulated chlorophyll biosynthesis and chloroplast development. SlMYB72 directly bound to phytoene synthase (PSY), zeta-carotene isomerase (ZISO), and lycopene beta-cyclase (LCYB) genes and regulated carotenoid biosynthesis. SlMYB72 directly targeted 4-coumarate-CoA ligase (4CL) and chalcone synthase (CHS) genes and regulated the biosynthesis of flavonoids and phenolic acid. The uneven color phenotype in RNAi-SlMYB72 fruits was due to uneven silencing of SlMYB72 and uneven expression of chlorophyll, carotenoid, and flavonoid biosynthesis genes. In summary, this study identified important roles for SlMYB72 in the regulation of chlorophyll, carotenoid, and flavonoid metabolism and provided a potential target to improve fruit nutrition in horticultural crops.