Evolution of the RNA <i>N</i>⁶-Methyladenosine Methylome Mediated by Genomic Duplication

Abstract

RNA <i>N</i> ⁶-methyladenosine (m⁶A) modification is the most abundant form of RNA epigenetic modification in eukaryotes. Given that m⁶A evolution is associated with the selective constraints of nucleotide sequences in mammalian genomes, we hypothesize that m⁶A evolution can be linked, at least in part, to genomic duplication events in complex polyploid plant genomes. To test this hypothesis, we presented the maize (<i>Zea mays</i>) m⁶A modification landscape in a transcriptome-wide manner and identified 11,968 m⁶A peaks carried by 5,893 and 3,811 genes from two subgenomes (maize1 and maize2, respectively). Each of these subgenomes covered over 2,200 duplicate genes. Within these duplicate genes, those carrying m⁶A peaks exhibited significant differences in retention rate. This biased subgenome fractionation of m⁶A-methylated genes is associated with multiple sequence features and is influenced by asymmetric evolutionary rates. We also characterized the coevolutionary patterns of m⁶A-methylated genes and transposable elements, which can be mediated by whole genome duplication and tandem duplication. We revealed the evolutionary conservation and divergence of duplicated m⁶A functional factors and the potential role of m⁶A modification in maize responses to drought stress. This study highlights complex interplays between m⁶A modification and gene duplication, providing a reference for understanding the mechanisms underlying m⁶A evolution mediated by genome duplication events.