DNA methylation signatures of duplicate gene evolution in angiosperms

Abstract

ABSTRACTGene duplication is an ongoing source of genetic novelty and evolutionary innovation. DNA methylation has been proposed as a factor in duplicate gene evolution. However, previous studies have largely been limited to individual species, apply differing methods, and have predominantly focused on CG methylation. The generalizability of these relationships at phylogenetic and population scales remains unknown. Here, we apply a consistent comparative epigenomics approach across 43 diverse angiosperm species and a population of 928 Arabidopsis thaliana accessions examining both CG and non-CG methylation contexts n whole-genome duplicate (WGD) and single-gene duplicate (SGD) genes. We observe several overarching trends, demonstrating that genic DNA methylation is differentially associated with the type of gene duplication, age of gene duplication, sequence evolution, and gene expression. WGDs are typically unmethylated or marked by mCG-only gene-body methylation, while SGDs typically are enriched for unmethylated genes or methylation in both mCG and non-CG contexts (transposon-like methylation or teM). TeM in particular was associated with relatively more recent SGDs and higher sequence divergence. However, we find variation across the phylogeny, as well as phylogenetic effects, which could be key to a deeper understanding of these relationships. Within the A. thaliana population, differences in duplicate age and sequence evolution were observed based on the frequency of genic methylation. Collectively, these results indicate that genic methylation states differently mark duplicate gene evolution.