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Author Summary It continues to be hotly debated to what extent environmentally induced epigenetic change is stably inherited and thereby contributes to short-term adaptation. It has been shown before that natural Arabidopsis thaliana lines differ substantially in their methylation profiles. How much of this is independent of genetic changes remains, however, unclear, especially given that there is very little conservation of methylation between species, simply because the methylated sequences themselves, mostly repeats, are not conserved over millions of years. On the other hand, there is no doubt that artificially induced epialleles can contribute to phenotypic variation. To investigate whether epigenetic differentiation, at least in the short term, proceeds very differently from genetic variation, and whether genome-wide epigenetic fingerprints can be used to uncover local adaptation, we have taken advantage of a near-clonal North American A. thaliana population that has diverged under natural conditions for at least a century. We found that both patterns and rates of methylome variation were in many aspects similar to those of lines grown in stable environments, which suggests that environment-induced changes are only minor contributors to durable genome-wide heritable epigenetic variation.