Acer palmatum ‘Duocai’ is an excellent ornamental cultivar maintained through asexual propagation. In spring and autumn, it exhibits red leaves, and in summer, it displays green leaves. To investigate the genetic and epigenetic regulation underlying these seasonal pigmentation shifts, we implemented a comprehensive multi-omics approach. Metabolomic profiling identified cyanidin-3-O-glucoside as the predominant biochemical factor governing seasonal leaf color transitions. RNA-seq, ATAC-seq, Hi-C, and WGBS were utilized to examine transcriptomic and chromatin remodeling dynamics. Multi-omics regulatory network analysis identified ApMYB2 as a key transcription factor (TF) affecting anthocyanin accumulation by regulating ApF3'H2 expression. Functional analyses demonstrated that the TF ApWRKY26 positively modulates ApMYB2 expression, while ApERF4 exerts an inhibitory effect on its expression. These regulatory interactions were corroborated by seasonal RNA-seq-based correlation analyses. Genetic manipulation experiments, including overexpression and silencing of these genes in A. palmatum, provided empirical evidence supporting their functional roles in the anthocyanin biosynthetic pathway. Together, our study elucidates the molecular mechanism by which ApWRKY26 and ApERF4 coordinate the activity of ApMYB2 to govern seasonal anthocyanin synthesis in A. palmatum foliage.

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