Epigenome modulation in response to the environment potentially provides a
mechanism for organisms to adapt, both within and between generations. However,
neither the extent to which this occurs, nor the molecular mechanisms involved
are known. Here we investigate DNA methylation variation in Swedish Arabidopsis
thaliana accessions grown at two different temperatures. Environmental effects
on DNA methylation were limited to transposons, where CHH methylation was found
to increase with temperature. Genome-wide association mapping 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) on the coding region of genes was not affected by growth
temperature, but was instead strongly 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 correlated with elevated transcription
levels for the genes affected. Genome-wide association mapping revealed that
this effect was largely due to trans-acting loci, a significant fraction of
which showed evidence of local adaptation. These findings constitute the first
direct link between DNA methylation and adaptation to the environment, and
provide a basis for further dissecting how environmentally driven and
genetically determined epigenetic variation interact and influence organismal
fitness.Comment: 38 pages 4 figure