Polyphenols represent a significant class of nutrients in apples, contributing to human health and well-being. Among these, procyanidins stand out as the most prevalent polyphenolic compounds in apple fruits. These compounds are abundant in wild apples and generally low in modern apple cultivars. Therefore, it is crucial to identify and recover genetically lost genes that regulate polyphenol accumulation in order to improve the apple quality. To achieve this, we conducted a genome-wide association study (GWAS) on 15 traits related to polyphenol content, utilizing 134 Malus accessions. We identified 1204 marker–trait associations (MTAs) and 840 candidate genes, including known polyphenol biosynthetic and regulatory genes, such as MYB7, TT4, and HCT/HQT. Notably, we pinpointed a protein S-acyl transferase 10 (PAT10), which is significantly associated with procyanidin content. Through experiments with transgenic calli, we determined that apple (Malus domestica) MdPAT10 positively regulated procyanidin accumulation. Furthermore, we identified a 51-bp insertion variant (In-868) on the promoter of the PAT10, which influences its expression. Both a yeast one-hybrid (Y1H) assay and an electrophoretic mobility shift assay (EMSA) revealed that MdDof2.4 was able to bind to the promoter of MdPAT10 containing In-868 (MdPAT10_proIn-868), but not to the promoter of MdPAT10 without In-868 (MdPAT10_pro). Moreover, MdDof2.4 promoted MdPAT10 (with MdPAT10_proIn-868) expression and increased procyanidin accumulation in fruits. Overall, our results enhance the understanding of the biosynthetic regulation of apple polyphenols and provide a theoretical foundation and genetic resources for breeding apple varieties with optimal polyphenol content.

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