Tissue-specific DNA methylation is conserved across human, mouse, and rat, and driven by primary sequence conservation

BMC Genomics. 2017 Sep 12;18(1):724. doi: 10.1186/s12864-017-4115-6.

Abstract

Background: Uncovering mechanisms of epigenome evolution is an essential step towards understanding the evolution of different cellular phenotypes. While studies have confirmed DNA methylation as a conserved epigenetic mechanism in mammalian development, little is known about the conservation of tissue-specific genome-wide DNA methylation patterns.

Results: Using a comparative epigenomics approach, we identified and compared the tissue-specific DNA methylation patterns of rat against those of mouse and human across three shared tissue types. We confirmed that tissue-specific differentially methylated regions are strongly associated with tissue-specific regulatory elements. Comparisons between species revealed that at a minimum 11-37% of tissue-specific DNA methylation patterns are conserved, a phenomenon that we define as epigenetic conservation. Conserved DNA methylation is accompanied by conservation of other epigenetic marks including histone modifications. Although a significant amount of locus-specific methylation is epigenetically conserved, the majority of tissue-specific DNA methylation is not conserved across the species and tissue types that we investigated. Examination of the genetic underpinning of epigenetic conservation suggests that primary sequence conservation is a driving force behind epigenetic conservation. In contrast, evolutionary dynamics of tissue-specific DNA methylation are best explained by the maintenance or turnover of binding sites for important transcription factors.

Conclusions: Our study extends the limited literature of comparative epigenomics and suggests a new paradigm for epigenetic conservation without genetic conservation through analysis of transcription factor binding sites.

Keywords: Comparative epigenomics; Comparative genomics; DNA methylation; Epigenetic conservation; Tissue-specific.

MeSH terms

  • Animals
  • Binding Sites
  • Conserved Sequence*
  • DNA Methylation / genetics*
  • Epigenomics
  • Evolution, Molecular
  • Humans
  • Mice
  • Organ Specificity
  • Rats
  • Transcription Factors / metabolism

Substances

  • Transcription Factors