An Arabidopsis Natural Epiallele Maintained by a Feed-Forward Silencing Loop between Histone and DNA

PLoS Genet. 2017 Jan 6;13(1):e1006551. doi: 10.1371/journal.pgen.1006551. eCollection 2017 Jan.

Abstract

The extent of epigenetic variation is currently well documented, but the number of natural epialleles described so far remains very limited. Determining the relevance of epigenetic changes for natural variation is an important question of research that we investigate by isolating natural epialleles segregating in Arabidopsis recombinant populations. We previously described a genetic incompatibility among Arabidopsis strains based on the silencing of a gene involved in fitness. Here, we isolated a new epiallele resulting from the silencing of a transfer-RNA editing gene in an Arabidopsis accession from the Netherlands (Nok-1). Crosses with the reference accession Col-0 show a complete incompatibility between this epiallele and another locus localized on a different chromosome. We demonstrate that conversion of an unmethylated version of this allele occurs in hybrids, associated with modifications of small RNA populations. These epialleles can also spontaneously revert within the population. Furthermore, we bring evidence that neither METHYLTRANSFERASE 1, maintaining methylation at CGs, nor components of RNA-directed DNA methylation, are key factors for the transmission of the epiallele over generations. This depends only on the self-reinforcing loop between CHROMOMETHYLASE 3 and KRYPTONITE, involving DNA methylated in the CHG context and histone H3 lysine 9 methylation. Our findings reveal a predominant role of this loop in maintaining a natural epiallele.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • DNA Methylation*
  • DNA, Plant / genetics
  • Epigenesis, Genetic*
  • Feedback, Physiological*
  • Gene Silencing*
  • Histones / genetics
  • Histones / metabolism*
  • Methyltransferases / genetics
  • Methyltransferases / metabolism
  • Protein Processing, Post-Translational

Substances

  • Arabidopsis Proteins
  • DNA, Plant
  • Histones
  • Methyltransferases

Grants and funding

We acknowledge funding from the Agence Nationale de la Recherche (Project 11-JSV7-0013) and PHC Maimonide Campus France (France/Israel, project 33583WA) to NB. The Institut Jean-Pierre Bourgin benefits from the support of the LabEx Saclay Plant Sciences-SPS (Project 10-LABX-0040-SPS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.