DNA methylation dynamics in gymnosperm duplicate genes: implications for genome evolution and stress adaptation.

SUMMARY: Duplicate genes are pivotal in driving evolutionary innovation, often exhibiting expression divergence that offers a system to investigate the role of DNA methylation in transcriptional regulation. However, previous studies have predominantly focused on angiosperms, leaving the methylation patterns in major lineages of land plants still unclear. This study explores DNA methylation evolution in duplicate genes across representative gymnosperm species with large genomes, spanning over 300 million years, using genomic, transcriptomic, and high‐depth DNA methylomic data. We observed variations in DNA methylation levels along gene bodies, flanking regions, and methylation statuses of coding regions across different duplication types. Biased divergences in DNA methylation and gene expression frequently occurred between duplicate copies. Specifically, methylation divergences in the 2‐kb downstream regions negatively correlated with gene expression. Both CG and CHG DNA methylation in gene bodies were positively correlated with gene length, suggesting these methylation types may function as an epigenomic buffer to mitigate the adverse impact of gene length on expression. Duplicate genes exhibiting both methylation and expression divergences were notably enriched in adaptation‐related biological processes, suggesting that DNA methylation may aid adaptive evolution in gymnosperms by regulating stress response genes. Changes in expression levels correlated with switches in methylation status within coding regions of transposed duplicates. Specifically, depletion for CG methylation or enrichment for non‐CG methylation significantly reduced the expression of translocated copies. This correlation suggests that DNA methylation may reduce genetic redundancy by silencing translocated copies. Our study highlights the significance of DNA methylation in plant genome evolution and stress adaptation. Significance Statement: Through an investigation into the evolutionary dynamics of DNA methylation in duplicate genes in representative gymnosperms, we revealed distinct DNA methylation patterns across various duplication modes, observed common biased divergences in DNA methylation and gene expression between duplicate copies, and explored the potential role of DNA methylation variation in stress adaptation through transcriptional regulation. This study highlights the significance of DNA methylation in plant genome evolution and stress adaptation. [ABSTRACT FROM AUTHOR]