DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation

TLDR

Epigenome modulation may enable organisms to adapt across generations, but the extent and mechanisms of such adaptation remain largely unknown. This study investigates DNA methylation variation in Swedish Arabidopsis thaliana accessions. Accessions were grown at two temperatures to assess methylation changes. CHH methylation of transposons increased with temperature, while CpG gene body methylation correlated with latitude and was higher in colder regions; GWAS linked both CHH and GBM variation to cis and trans genetic variants—including a major trans locus near CMT2—indicating local adaptation.

Abstract

Epigenome modulation potentially provides a mechanism for organisms to adapt, within and between generations. However, neither the extent to which this occurs, nor the mechanisms involved are known. Here we investigate DNA methylation variation in Swedish Arabidopsis thaliana accessions grown at two different temperatures. Environmental effects were limited to transposons, where CHH methylation was found to increase with temperature. Genome-wide association studies (GWAS) revealed that the extensive CHH methylation variation was strongly associated with genetic variants in both cis and trans, including a major trans-association close to the DNA methyltransferase CMT2. Unlike CHH methylation, CpG gene body methylation (GBM) was not affected by growth temperature, but was instead correlated with the latitude of origin. Accessions from colder regions had higher levels of GBM for a significant fraction of the genome, and this was associated with increased transcription for the genes affected. GWAS revealed that this effect was largely due to trans-acting loci, many of which showed evidence of local adaptation.