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

Astrid Agorio,Nicolas Bouché,Oded Rechavi,Olivier Loudet,Sarit Anava,Elisa Fiume,Cécile Brousse,Matthieu Simon,Isabelle Gy,Christine Camilleri,Stéphanie Durand

doi:10.1371/journal.pgen.1006551

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.

Highlights

Epialleles, identified in different organisms and predominantly in plants, are gene variants based on epigenetic marks stably transmitted between generations
Since we discovered small RNAs targeting the FOLT genes in Sha, we reasoned that FOLT1 is silenced by RNAdirected DNA methylation (RdDM)
A recombinant inbred lines (RIL) population was generated from a cross between two accessions of Arabidopsis thaliana, Nok-1 and Col-0

Summary

Introduction

Epialleles, identified in different organisms and predominantly in plants (reviewed by [1]), are gene variants based on epigenetic marks stably transmitted between generations. Most of the plant epialleles described so far depend on DNA methylation of cytosines, an epigenetic mark influencing the way genes are transcribed (reviewed by [2]). In natural populations of Arabidopsis, epivariants of QQS [9] or PAI [10] were described, no specific phenotypes associated with the epiallelic version of the gene were discovered, beyond the change in transcription. After a cross between Col-0 and Sha, plants inheriting only the methylated FOLT1 epiallele from Sha are mostly sterile because the function of FOLT is missing. Since we discovered small RNAs (sRNAs) targeting the FOLT genes in Sha, we reasoned that FOLT1 is silenced by RNAdirected DNA methylation (RdDM). We found that unmethylated FOLT1 alleles can be converted in trans when FOLT2 copies are present at the other locus [12]

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Conclusion