Abstract
Cytosine methylation is an ancient epigenetic modification yet its function and extent within genomes is highly variable across eukaryotes. In mammals, methylation controls transposable elements and regulates the promoters of genes. In insects, DNA methylation is generally restricted to a small subset of transcribed genes, with both intergenic regions and transposable elements (TEs) depleted of methylation. The evolutionary origin and the function of these methylation patterns are poorly understood. Here we characterise the evolution of DNA methylation across the arthropod phylum. While the common ancestor of the arthropods had low levels of TE methylation and did not methylate promoters, both of these functions have evolved independently in centipedes and mealybugs. In contrast, methylation of the exons of a subset of transcribed genes is ancestral and widely conserved across the phylum, but has been lost in specific lineages. A similar set of genes is methylated in all species that retained exon-enriched methylation. We show that these genes have characteristic patterns of expression correlating to broad transcription initiation sites and well-positioned nucleosomes, providing new insights into potential mechanisms driving methylation patterns over hundreds of millions of years.
Highlights
In most organisms DNA bases are adorned with a variety of chemical modifications
We carried out high-coverage whole-genome bisulphite sequencing (WGBS) on 14 species of arthropod and quantified the levels of DNA methylation with base-pair resolution
The ancestral arthropod likely had moderate methylation levels (9.1±4.8%; Fig 1A) but higher methylation levels evolved in S. maritima
Summary
In most organisms DNA bases are adorned with a variety of chemical modifications. Amongst the most common of these is methylation at the 5 position of cytosine (C5me), which is present from bacteria to humans [1,2,3]. A key property of cytosine DNA methylation is its ability to act epigenetically—that is, once introduced, methylation at specific cytosines can remain in place through cell division [4],[5]. This relies on the activity of “maintenance” methyltransferases, DNMT1 in animals [6], which recognise CG dinucleotides (CpG sites) where one strand is methylated and one strand unmethylated and catalyse the introduction of methylation on the unmethylated strand [4]. “de novo” methyltransferases act on unmethylated DNA In animals this role is performed by DNMT3 enzymes, which introduce 5meC predominantly within CpG sites [4]. As the maintenance and de novo methylation of CG sequences occurs through the activity of homologous enzymes in plants and animals [6], CpG methylation was likely present among the earliest eukaryotic organisms
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