Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Simple item page
dc.contributor.authorLewis, Samuel H.en
dc.contributor.authorRoss, Lauraen
dc.contributor.authorBain, Stevie A.en
dc.contributor.authorPahita, Elenien
dc.contributor.authorSmith, Stephen A.en
dc.contributor.authorCordaux, Richarden
dc.contributor.authorMiska, Eric A.en
dc.contributor.authorLenhard, Borisen
dc.contributor.authorJiggins, Francis M.en
dc.contributor.authorSarkies, Peteren
dc.contributor.departmentBiomedical Sciences and Pathobiologyen
dc.date.accessioned2020-08-10T17:59:22Zen
dc.date.available2020-08-10T17:59:22Zen
dc.date.issued2020-06en
dc.description.abstractAuthor summary Animals develop from a single cell to form a complex organism with many specialised cells. Almost all of the fantastic variety of cells must have the same sequence of DNA, and yet they have distinct identities that are preserved even when they divide. This remarkable process is achieved by turning different sets of genes on or off in different types of cell using molecular mechanisms known as "epigenetic gene regulation". Surprisingly, though all animals need epigenetic gene regulation, there is a huge diversity in the mechanisms that they use. Characterising and explaining this diversity is crucial in understanding the functions of epigenetic pathways, many of which have key roles in human disease. We studied how an epigenetic regulation known as DNA methylation has evolved within arthropods. Arthropods are an extraordinarily diverse group of animals ranging from horseshoe crabs to fruit flies. We discovered that the levels of DNA methylation and where it is found within the genome changes rapidly throughout arthropod evolution. Nevertheless, there are some features of DNA methylation that seem to be the same across most arthropods- in particular we found that there is a tendency for a similar set of genes to acquire methylation of DNA in most arthropods, and that this is conserved over 350 million years. We discovered that these genes have distinct features that might explain how methylation gets targeted. Our work provides important new insights into the evolution of DNA methylation and gives new hints to its essential functions. 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.en
dc.description.notesThis research was funded by the Medical Research Council (grant to PS) and the Leverhulme Trust (grant to FMJ and PS).BL was supported by Medical Research Council UK (award MC_UP_1102/1) and Wellcome Trust Investigator Award 106954/Z/15/Z. LR was supported by a NERC fellowship (NE/K009516/1) and the Royal Society (RG160842). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.en
dc.description.sponsorshipMedical Research CouncilMedical Research Council UK (MRC); Leverhulme TrustLeverhulme Trust; Medical Research Council UKMedical Research Council UK (MRC) [MC_UP_1102/1]; Wellcome TrustWellcome Trust [106954/Z/15/Z]; NERC fellowshipNERC Natural Environment Research Council [NE/K009516/1]; Royal SocietyRoyal Society of London [RG160842]en
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1371/journal.pgen.1008864en
dc.identifier.issn1553-7404en
dc.identifier.issue6en
dc.identifier.urihttp://hdl.handle.net/10919/99632en
dc.identifier.volume16en
dc.language.isoenen
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleWidespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropodsen
dc.title.serialPLoS Geneticsen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.dcmitypeStillImageen

Files

Original bundle
Now showing 1 - 1 of 1
Thumbnail Image
Name:
journal.pgen.1008864.pdf
Size:
3.5 MB
Format:
Adobe Portable Document Format
Description:
Published version
Download

Collections

Scholarly Works, Biomedical Sciences and Pathobiology