Huang Kai-Yuan, Feng Yuan-Yuan, Du Hong, Ma Chang-Wang, Xie Dan, Wan Tao, Feng Xiu-Yan, Dai Xiao-Gang, Yin Tong-Ming, Wang Xiao-Quan, Ran Jin-Hua
State Key Laboratory of Plant Diversity and Specialty Crops and Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
China National Botanical Garden, Beijing, 100093, China.
Plant J. 2025 Feb;121(4):e70006. doi: 10.1111/tpj.70006.
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.
重复基因在推动进化创新中起着关键作用，通常表现出表达差异，为研究DNA甲基化在转录调控中的作用提供了一个系统。然而，以往的研究主要集中在被子植物上，陆地植物主要谱系中的甲基化模式仍不清楚。本研究利用基因组、转录组和高深度DNA甲基组数据，探索了跨越3亿多年的具有大基因组的代表性裸子植物物种中重复基因的DNA甲基化进化。我们观察到不同复制类型的基因体、侧翼区域的DNA甲基化水平以及编码区域的甲基化状态存在差异。重复拷贝之间经常发生DNA甲基化和基因表达的偏向性差异。具体而言，2kb下游区域的甲基化差异与基因表达呈负相关。基因体中的CG和CHG DNA甲基化均与基因长度呈正相关，表明这些甲基化类型可能作为一种表观基因组缓冲，减轻基因长度对表达的不利影响。表现出甲基化和表达差异的重复基因在与适应相关的生物学过程中显著富集，表明DNA甲基化可能通过调节应激反应基因来帮助裸子植物的适应性进化。转座重复基因编码区域内的表达水平变化与甲基化状态的转换相关。具体而言，CG甲基化的缺失或非CG甲基化的富集显著降低了易位拷贝的表达。这种相关性表明DNA甲基化可能通过沉默易位拷贝来减少遗传冗余。我们的研究突出了DNA甲基化在植物基因组进化和应激适应中的重要性。
