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

Abstract

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: In this study, based on the reference genome of tea plant (Camellia sinensis ‘Yunkang 10’, YK10), we integrated publicly available transcriptomic, ATAC-seq, H3K27ac ChIP-seq, whole-genome bisulfite sequencing (WGBS), and SNP data from eight tissues and performed a multi-layered analysis of co-expression divergence across 4071 WGD and 10,174 TRD gene pairs. Results: WGD gene pairs exhibited significantly higher co-expression rates (44.3%) than TRD pairs (33.0%), with gene length and sequence similarity jointly promoting co-expression. Chromatin accessibility and H3K27ac modification were each positively correlated with expression and co-expression; however, under equivalent chromatin accessibility conditions, TRD gene expression remained systematically attenuated, and this reduced expression state was significantly associated with elevated levels of CG, CHG, and CHH methylation, suggesting that these epigenetic marks may collectively participate in the transcriptional repression of TRD genes. Promoter-proximal SNPs exerted disproportionately deleterious effects on TRD co-expression, demonstrating that the combined effects of genetic variation and epigenetic modifications are associated with enhanced transcriptional divergence. Weighted gene co-expression network analysis (WGCNA) revealed that WGD modules showed significant associations with EC, GC, and EGC accumulation, whereas WRKY and bHLH transcription factors in the TRD MEblue module exhibited strong associations with EGCG and ECG. Conclusions: This study systematically characterizes multi-omics association patterns related to duplicate gene co-expression divergence, providing insights into potential hierarchical regulation. It offers mechanistic clues for catechin metabolic regulation and provides candidate targets for metabolite-directed breeding.