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Function and evolution of DNA methylation in Nasonia vitripennis

Wang, Xu; Wheeler, David; Avery, Amanda; Rago, Alfredo LU ; Choi, Jeong-Hyeon; Colbourne, John K; Clark, Andrew G and Werren, John H (2013) In PLoS Genetics 9(10). p.1003872-1003872
Abstract

The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over... (More)

The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5' regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5' and 3' UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in Nasonia. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. Nasonia methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the Nasonia lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of Nasonia genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.

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subject
keywords
Alternative Splicing, Animals, Conserved Sequence, CpG Islands, DNA Methylation, Evolution, Molecular, Exons, Genome, Hymenoptera, Introns, Phylogeny, RNA Splicing, Journal Article, Research Support, American Recovery and Reinvestment Act, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't
in
PLoS Genetics
volume
9
issue
10
pages
1003872 - 1003872
publisher
Public Library of Science
external identifiers
  • scopus:84887312009
ISSN
1553-7404
DOI
10.1371/journal.pgen.1003872
language
English
LU publication?
no
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a61a7e5c-f1a1-4e46-a632-a47e4d6e6d0c
date added to LUP
2018-01-15 13:26:59
date last changed
2018-03-11 04:46:09
@article{a61a7e5c-f1a1-4e46-a632-a47e4d6e6d0c,
  abstract     = {<p>The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5' regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5' and 3' UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in Nasonia. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. Nasonia methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the Nasonia lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of Nasonia genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.</p>},
  author       = {Wang, Xu and Wheeler, David and Avery, Amanda and Rago, Alfredo and Choi, Jeong-Hyeon and Colbourne, John K and Clark, Andrew G and Werren, John H},
  issn         = {1553-7404},
  keyword      = {Alternative Splicing,Animals,Conserved Sequence,CpG Islands,DNA Methylation,Evolution, Molecular,Exons,Genome,Hymenoptera,Introns,Phylogeny,RNA Splicing,Journal Article,Research Support, American Recovery and Reinvestment Act,Research Support, N.I.H., Extramural,Research Support, Non-U.S. Gov't},
  language     = {eng},
  number       = {10},
  pages        = {1003872--1003872},
  publisher    = {Public Library of Science},
  series       = {PLoS Genetics},
  title        = {Function and evolution of DNA methylation in Nasonia vitripennis},
  url          = {http://dx.doi.org/10.1371/journal.pgen.1003872},
  volume       = {9},
  year         = {2013},
}