Evolutionary Implications of the RNA N(6)-Methyladenosine Methylome in Plants

Epigenetic modifications play important roles in genome evolution and innovation. However, most analyses have focused on the evolutionary role of DNA modifications, and little is understood about the influence of posttranscriptional RNA modifications on genome evolution. To explore the evolutionary significance of RNA modifications, we generated transcriptome-wide profiles of N(6)-methyladenosine (m(6)A), the most prevalent internal modification of mRNA, for 13 representative plant species spanning over half a billion years of evolution. These data reveal the evolutionary conservation and divergence of m(6)A methylomes in plants, uncover the preference of m(6)A modifications on ancient orthologous genes, and demonstrate less m(6)A divergence between orthologous gene pairs with earlier evolutionary origins. Further investigation revealed that the evolutionary divergence of m(6)A modifications is related to sequence variation between homologs from whole-genome duplication and gene family expansion from local-genome duplication. Unexpectedly, a significant negative correlation was found between the retention ratio of m(6)A modifications and the number of family members. Moreover, the divergence of m(6)A modifications is accompanied by variation in the expression level and translation efficiency of duplicated genes from whole- and local-genome duplication. Our work reveals new insights into evolutionary patterns of m(6)A methylomes in plant species and their implications, and provides a resource of plant m(6)A profiles for further studies of m(6)A regulation and function in an evolutionary context.