The bifunctional transcription factor DEAR1 oppositely regulates chlorophyll biosynthesis and degradation in tomato fruits

Chlorophyll metabolism plays a key role in fruit development and ripening in tomato (Solanum lycopersicum). In immature fruits, chlorophyll facilitates photosynthesis, thereby supplying energy for growth. In contrast, chlorophyll degradation is an integral feature of ripening in most tomato varieties. Understanding how developing tomato fruit balances chlorophyll levels provides important information for crop improvement. Here, we report that the APETALA2/Ethylene Response Factor (AP2/ERF) family transcription factor SlDEAR1 is a key bifunctional regulator that activates chlorophyll biosynthesis and represses chlorophyll degradation in tomato fruits. Knocking out SlDEAR1 reduced chlorophyll accumulation compared to wild type, downregulated the chlorophyll biosynthesis gene Protochlorophyllide oxidoreductase 1 (SlPOR1), and upregulated the chlorophyll degradation gene Stay-green 1 (SlSGR1). SlDEAR1 overexpression led to the opposite results. Moreover, SlDEAR1 recruits the TOPLESS 2 (TPL2)-Histone deacetylase 1(HDA1)/HDA3 complex through its C-terminal EAR motif to decrease histone acetylation along the SlSGR1 promoter, leading to transcriptional repression. Simultaneously, SlDEAR1 upregulates SlPOR1 via a previously unidentified RKK motif. Furthermore, we showed that SlDEAR1 expression is light-regulated and mediated by the upstream transcriptional activator ELONGATED HYPOCOTYL 5 (SlHY5). Thus, the SlHY5-SlDEAR1-SlPOR1/SlSGR1 module regulates chlorophyll accumulation during tomato fruit development. This study sheds light on the regulatory network controlling chlorophyll metabolism in tomato.