Integration of transcriptomic and metabolomic analysis reveals light-regulated anthocyanin accumulation in the peel of 'Yinhongli' plum.

Abstract

Background: The 'Yinhongli' cultivar of Chinese plum (Prunus salicina Lindl.) is characterized by a distinctive bicolored peel phenotype, in which anthocyanins serve as crucial determinants of both its visual characteristics and nutritional quality. However, the molecular mechanism of underlying light-dependent anthocyanin biosynthesis of plum, especially its regulatory network and pathway, need to be further studied and explored.

Results: Comprehensive physiological analyses demonstrated distinct pigmentation patterns, revealing that dark-treated (YD) plum peels retained green coloration, whereas light-exposed (YL) and bag-removed samples (YDL) exhibited red pigmentation. Utilizing an integrated approach combining metabolomic and transcriptomic analyses, we identified 266 differentially accumulated flavonoids (DAFs), among which seven anthocyanin metabolites were established as principal determinants of peel coloration. Transcriptomic profiling revealed 6,900 differentially expressed genes (DEGs) between YD and YL, demonstrating significant correlations between the phenylpropanoid and flavonoid biosynthetic pathways. Through Weighted Gene Co-expression Network Analysis (WGCNA) and correlation heatmap analysis, we identified crucial regulatory networks encompassing five structural genes (PAL, 4CL, F3'H, CHI, and UFGT) and 15 candidate regulatory genes, including six light signal transduction factor genes (UVR8, COP1, PHYBs, PIF3, and HY5) and nine transcription factor genes (MYB1, MYB20, MYB73, MYB111, LHY, DRE2B, ERF5, bHLH35, and NAC87). Subsequent RT-qPCR validation demonstrated significant light-mediated up-regulation of key structural genes (PAL, F3H, CHI, 4CL, and UFGT) involved in anthocyanin biosynthesis along with positive regulatory factors (DRE2B and NAC87). Conversely, a cohort of negative regulators, including HY5, MYB1, MYB20, MYB73, MYB111, LHY, ERF5, and bHLH35, showed marked down-regulation in response to light exposure, suggesting their potential repressive roles in the light-dependent anthocyanin biosynthesis pathway.

Conclusions: This investigation provides comprehensive insights into the molecular mechanisms of anthocyanin biosynthesis in light-dependent anthocyanin biosynthesis in 'Yinhongli' plum, identifying critical structural genes and potential regulatory TFs. The findings offer substantial contributions to the understanding of anthocyanin regulation in fruit crops and provide a valuable foundation for molecular breeding initiatives aimed at enhancing quality traits in plum cultivars.