The PavDREB1E–PavD8–PavHY5 module integrates light and gibberellin signals to regulate sweet cherry anthocyanin biosynthesis

Light stimulates anthocyanin accumulation in bicolored sweet cherry (Prunus avium cv. Rainier) fruits, resulting in red pigmentation. The phytohormone gibberellin (GA) plays an important role in fruit coloration, but the molecular mechanisms that integrate light and GA signaling pathways during anthocyanin biosynthesis remain poorly understood. We show that light induces anthocyanin accumulation but reduces the gibberellic acid (GA3) content in "Rainier" sweet cherry fruits and that GA3 treatment inhibits light-induced anthocyanin accumulation. Light exposure and low GA3 levels induce the transcription of a DEHYDRATION RESPONSIVE ELEMENT-BINDING PROTEIN (DREB) gene, PavDREB1E, which encodes a protein that directly activates the transcription of key anthocyanin biosynthesis genes, including chalcone synthase (PavCHS), dihydroflavonol-4-reductase (PavDFR), and UDP glucose-flavonoid-3-O-glycosyltransferase (PavUFGT). The DELLA protein PavDWARF8 (PavD8), which is stabilized under low GA3 levels, interacts with PavDREB1E to strengthen its transcriptional activation activity. Furthermore, light-induced ELONGATED HYPOCOTYL5 (PavHY5) promotes this interaction. In the dark, PavDREB1E and PavHY5 transcript levels are low. Moreover, PavDREB1E, PavD8, and PavHY5 are degraded in the dark and accumulate in the light via the light-induced nuclear depletion of the E3 ubiquitin ligases CONSTITUTIVELY PHOTOMORPHOGENIC 1 (PavCOP1-1 and PavCOP1-2). We present a mechanism by which the PavDREB1E-PavD8-PavHY5 module integrates light and GA signaling to regulate anthocyanin biosynthesis in sweet cherry fruits.