Comprehensive analysis of widely targeted metabolic profiling and transcriptome reveals the grafting-mediated stress tolerance

Grafting is widely used in fruit trees for propagation and improvement of the scion's stress tolerance and fruit quality. Malus prunifolia ‘Fupingqiuzi’ (‘FPQZ’) is a unique germplasm with strong environmental stress tolerance and can enhance scion tolerance when used as a rootstock. Previous studies have demonstrated altered DNA methylation patterns and enhanced expression of stress-related genes in scion tissue when 'Golden Delicious' ( Malus× domestica ) was grafted onto M. prunifolia 'FPQZ'. However, the global metabolic changes involved in the grafting events remain unclear. In this study, we investigated metabolite and gene differences between M. prunifolia 'FPQZ' and 'Golden Delicious' using the widely targeted UPLC-MS/MS-based metabolic approach, and further analyzed the effects of grafting on the scion and rootstock. Metabolomic analysis suggested that M. prunifolia ‘FPQZ’ accumulated higher levels of metabolites, including phenylpropanoids, flavonoids, and lipids, compared with ‘Golden Delicious’. After grafted onto the M. prunifolia ‘FPQZ’, 154 differentially accumulated metabolites were identified in ‘Golden Delicious’, including a large proportion of flavonoids, suggesting a critical role of flavonoid metabolism in grafting-mediated stress tolerance. Furthermore, exogenous application of naringenin and dihydroquercetin enhanced drought tolerance in apple plants, highlighting their functional roles in grafting-mediated stress responses. Overall, our study provides a comprehensive analysis and new insights into grafting-induced metabolic reprogramming and transcriptional regulation.