Integrated transcriptomic and metabolomic analyses elucidate the molecular mechanisms underlying quality formation during Rosa acicularis fruit ripening.

Fruits of Rosa acicularis are recognized for their high nutritional value owing to accumulation of diverse bioactive metabolites. However, the physiological processes and regulatory mechanisms underlying quality formation remain incompletely understood. In this study, developmental changes in fruit quality were assessed across four stages: the mature green stage (MGS), breaker stage (BS), maturity stage (MS), and ripening stage (RS), using morphological, physicochemical, and antioxidant analyses. To further elucidate the molecular regulatory basis of ripening, three representative stages (MGS, BS, and RS) were selected for transcriptomic and metabolomic profiling. Results indicated coordinated fruit enlargement and pigmentation, accompanied by stage-dependent alterations in sugars, organic acids, pectin, polysaccharides, and vitamin C. Antioxidant capacity exhibited distinct radical-specific response patterns throughout ripening. Transcriptomic profiling identified 10,841 differentially expressed genes, which were predominantly enriched in pathways associated with hormone signal transduction, carbohydrate metabolism, flavonoid biosynthesis, and phenylpropanoid biosynthesis. Metabolomic analysis detected 1305 metabolites, among which flavonoids constituted the dominant class and displayed pronounced temporal dynamics. Integrated temporal expression analysis demonstrated strong co-expression between gene expression and metabolite accumulation. WGCNA further identified the MEblack module as the module most closely associated with flavonoid traits, with hub genes including RaWRKY56, RaC3H53, RaNF-YA4, and RaF3'H predicted as key regulatory factors, a result supported by qRT-PCR expression profiles. These findings establish an integrated molecular framework for elucidating quality formation in R. acicularis and provide potential genetic targets for future improvement and utilization.