Integrated multi-omics analyses elucidate bagging effects on apple fruit quality and regulatory mechanisms underlying flavonoid and sugar metabolism

With the rise in comprehensive production costs, non-bagging cultivation has replaced bagging as the core direction for the sustainable development of the apple ( Malus × domestica ) industry. Thus, a systematic analysis of bagging cultivation is crucial for modern agricultural innovation. However, the metabolic changes in apple fruit quality induced by bagging and their underlying gene regulatory networks remain poorly explored. This study utilized ‘Fuji’ and ‘Ralls’ apples which are distinct in flavor and integrated transcriptomics, metabolomics, and physiological and biochemical analysis to investigate the effects of bagging on fruit quality and the regulatory mechanisms of flavonoid and sugar metabolism. The results showed that bagging significantly improved the appearance quality of apple fruits, as well as soluble solids, soluble sugars, respiration rate, and ethylene release rate. However, it reduced firmness, vitamin C, titratable acid and total phenols. Further analysis revealed variety-specific impacts. The increase in content of ‘Fuji’ soluble sugar relied on the synergistic rises in fructose, sucrose, glucose and sorbitol, while that of ‘Ralls’ mainly depended on fructose and sucrose accumulation. The reduced titratable acid and total phenols in both varieties were linked to lower levels of malic, quinic, citric, shikimic acids, and phenolic acids under bagging. The integrated transcriptomic and metabolomics analysis indicated that differentially accumulated metabolites (DAMs) and differentially expressed genes (DEGs) of the flavonoid pathway in ‘Fuji’ were significantly upregulated, with higher expression levels than those in ‘Ralls’. In addition, through a comprehensive analysis of DAMs and DEGs of sugar metabolism, combined with co-expression networks, the regulatory mechanism of DEGs-DAMs mediated by differentially expressed transcription factors (DETFs) was revealed. These findings provide new insights into apple quality regulation and lay a theoretical foundation for high-quality industry development.