Jujube Development and Ripening Process Provides a Two-Stage Coloration Model: <i>ZjHY5</i> -Mediated Flavonoid Biosynthesis Precedes Senescence-Driven Phenolic Oxidation

Fruit coloration is a critical quality trait that determines the market value of jujube. The popular fresh-eating jujube 'Dongzao' exhibits a distinctive two-stage pigmentation pattern during ripening: reddish-brown coloration during fruit expansion, followed by deep-red pigmentation at full maturity. However, the pigment composition and regulatory mechanisms underlying this coloration process remain unclear. In this study, we combined bagging experiments, multi-omics analyses, and gene functional validation to address this question. We demonstrated that the reddish-brown pigmentation during expansion is light-dependent, primarily attributed to the accumulation of flavonols and anthocyanins. This process is mediated by the central light-signaling integrator ZjHY5, which directly activates flavonoid biosynthetic genes. Among these, ZjUFGT and ZjGT3 were identified as enzymes that respectively catalyze the synthesis of anthocyanins and flavonols. However, the reddening during ripening is light-independent and driven by ethylene-promoted quinone production through phenolic oxidation, resulting in deep-red pigmentation. We identified ZjPPO1 as a key ethylene-responsive gene, and transient overexpression of ZjPPO1 in jujube peel in vivo triggered red pigmentation accompanied by phenolic oxidation. Taken together, our results established a novel dual-stage coloration model in jujube fruit, providing fundamental insights into the molecular basis of fruit pigmentation and offering a practical framework for improving color quality through breeding or postharvest strategies.