Divergent DNA methylation contributes to duplicated gene evolution and chilling response in tea plants

• Published in: The Plant journal : for cell and molecular biology 2021-06, Vol.106 (5), p.1312-1327
• Main Authors: Tong, Wei, Li, Ruopei, Huang, Jin, Zhao, Huijuan, Ge, Ruoheng, Wu, Qiong, Mallano, Ali I., Wang, Yanli, Li, Fangdong, Deng, Weiwei, Li, Yeyun, Xia, Enhua
• Format: Article
• Language: English
• Subjects: Camellia sinensis; Cash crops; Chilling; chilling stress; Cooling; Deoxyribonucleic acid; Divergence; DNA; DNA methylation; DNA methyltransferase; duplicated gene; Evolution; Evolutionary genetics; Gene duplication; Gene expression; Genes; genome evolution; Genomes; Nucleotide sequence; Reproduction (copying); Tea
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15237

Summary The tea plant (Camellia sinensis) is a thermophilic cash crop and contains a highly duplicated and repeat‐rich genome. It is still unclear how DNA methylation regulates the evolution of duplicated genes and chilling stress in tea plants. We therefore generated a single‐base‐resolution DNA methylation map of tea plants under chilling stress. We found that, compared with other plants, the tea plant genome is highly methylated in all three sequence contexts, including CG, CHG and CHH (where H = A, T, or C), which is further proven to be correlated with its repeat content and genome size. We show that DNA methylation in the gene body negatively regulates the gene expression of tea plants, whereas non‐CG methylation in the flanking region enables a positive regulation of gene expression. We demonstrate that transposable element‐mediated methylation dynamics significantly drives the expression divergence of duplicated genes in tea plants. The DNA methylation and expression divergence of duplicated genes in the tea plant increases with evolutionary age and selective pressure. Moreover, we detect thousands of differentially methylated genes, some of which are functionally associated with chilling stress. We also experimentally reveal that DNA methyltransferase genes of tea plants are significantly downregulated, whereas demethylase genes are upregulated at the initial stage of chilling stress, which is in line with the significant loss of DNA methylation of three well‐known cold‐responsive genes at their promoter and gene body regions. Overall, our findings underscore the importance of DNA methylation regulation and offer new insights into duplicated gene evolution and chilling tolerance in tea plants. Significance Statement Our results show solid evidence that DNA methylation not only drives transposable element (TE)‐mediated functional diversification of duplicated genes in the tea plant, but also facilitates the enhancement of chilling tolerance in the tea plant through suppressing the activities of DNA methyltransferase under chilling stress. The overall findings underscore the importance of DNA methylation regulation on gene expression through TE insertions and broaden our understanding of duplicated gene evolution and chilling tolerance in plants.