Epigenetic Regulation of Divergent Co-Expression between Whole-Genome Duplication and Transposed Duplication Genes and Its Impact on Catechin Accumulation in Camellia Sinensis

Background/Objectives:Whole-genome duplication (WGD) and transposed duplication (TRD) are two principal evolutionary drivers of plant genome expansion, yet the molecular mechanisms underlying their divergent co-expression patterns remain poorly characterized. Methods:Integrating transcriptomic profiling, ATAC-seq, H3K27ac ChIP-seq, whole-genome bisulfite sequencing (WGBS), and SNP data, we performed a multi-layered analysis of co-expression divergence across 4,071 WGD and 10,174 TRD gene pairs in tea plant (Camellia sinensis). Results:WGD gene pairs exhibited significantly higher co-expression rates (44.3%) than TRD pairs (33.0%), with gene length and sequence similarity exerting synergistic threshold effects on co-expression maintenance. Chromatin accessibility and H3K27ac modification cooperatively promoted co-expression in both duplicate classes; however, TRD gene expression remained systematically attenuated under equivalent chromatin accessibility conditions, attributable to coordinated CG, CHG, and CHH methylation collectively establishing a persistent epigenetic repression barrier. Promoter-proximal SNPs exerted disproportionately disruptive effects on TRD co-expression, demonstrating that genetic variation and epigenetic repression synergistically amplify transcriptional divergence. Weighted gene co-expression network analysis (WGCNA) revealed that WGD genes promote non-esterified catechin accumulation (EC, GC, EGC) via conserved MYB–bHLH–ERF networks, whereas TRD genes regulate esterified catechin biosynthesis (EGCG, ECG) through M-type MADS-box, WOX, and bZIP transcription factors. Conclusions:This study systematically elucidates the hierarchical regulatory mechanisms governing duplicate gene co-expression divergence in tea plant, providing mechanistic insights into catechin metabolic regulation and candidate targets for metabolite-directed breeding.