Function and Evolution of DNA Methylation in Nasonia vitripennis

Xu Wang, David Wheeler, Amanda Avery, Alfredo Rago, Jeong-Hyeon Choi, John K. Colbourne, Andrew G. Clark, John H. Werren

Research output: Contribution to journalArticle

87 Citations (Scopus)

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 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.

Original languageEnglish (US)
Article numbere1003872
JournalPLoS Genetics
Volume9
Issue number10
DOIs
StatePublished - Oct 1 2013

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Nasonia vitripennis
methylation
DNA methylation
DNA Methylation
Methylation
DNA
gene
Nasonia
Genes
genes
genome
Genome
developmental stage
exons
Insects
Exons
developmental stages
insect
bisulfites
Wasps

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Wang, X., Wheeler, D., Avery, A., Rago, A., Choi, J-H., Colbourne, J. K., ... Werren, J. H. (2013). Function and Evolution of DNA Methylation in Nasonia vitripennis. PLoS Genetics, 9(10), [e1003872]. https://doi.org/10.1371/journal.pgen.1003872

Function and Evolution of DNA Methylation in Nasonia vitripennis. / Wang, Xu; Wheeler, David; Avery, Amanda; Rago, Alfredo; Choi, Jeong-Hyeon; Colbourne, John K.; Clark, Andrew G.; Werren, John H.

In: PLoS Genetics, Vol. 9, No. 10, e1003872, 01.10.2013.

Research output: Contribution to journalArticle

Wang, X, Wheeler, D, Avery, A, Rago, A, Choi, J-H, Colbourne, JK, Clark, AG & Werren, JH 2013, 'Function and Evolution of DNA Methylation in Nasonia vitripennis', PLoS Genetics, vol. 9, no. 10, e1003872. https://doi.org/10.1371/journal.pgen.1003872
Wang X, Wheeler D, Avery A, Rago A, Choi J-H, Colbourne JK et al. Function and Evolution of DNA Methylation in Nasonia vitripennis. PLoS Genetics. 2013 Oct 1;9(10). e1003872. https://doi.org/10.1371/journal.pgen.1003872
Wang, Xu ; Wheeler, David ; Avery, Amanda ; Rago, Alfredo ; Choi, Jeong-Hyeon ; Colbourne, John K. ; Clark, Andrew G. ; Werren, John H. / Function and Evolution of DNA Methylation in Nasonia vitripennis. In: PLoS Genetics. 2013 ; Vol. 9, No. 10.
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