Natural patterns of DNA methylation

When willing to study the role of epigenetics in plant adaptation and evolution, a fundamental step is to study epigenetic patterns in natural populations. Different environments offer different selective pressures and may induce the presence of different DNA methylation patterns. Moreover, isolation by distance may induce the accumulation of different epimutations in geographically distant populations. The only way to study the occurrence of these phenomena (or whether they occur at all) is to study them in real natural populations. Furthermore, it is important to bear in mind that what happens in one species may differ in another, especially for species with very different life-history traits (see the Chapter “Life history traits”). Several studies have tried to answer this kind of questions but many struggle to overcome the large-scale vs high-accuracy problem (see section “Genetics-Epigenetics”) focusing on either one of the two aspects (Richards et al. 2017). Nevertheless, each approach was able to address some fundamental questions. Studies based on large-scale surveys were able to show that DNA methylation correlates with habitat of origin and environmental variables (Gugger et al. 2016; Lira-Medeirose et al. 2010; Gáspár, Bossdorf, and Durka 2018), with some studies having found correlations with phenotypic traits (see section “Phenotypic effects”). Some experiments analysing subsequent generations also showed that DNA methylation is at least partially heritable (Gáspár, Bossdorf, and Durka 2018), but most of these studies lack the genomic resolution to fully test whether the observed epigenetic variation is independent of genetic polymorphisms. At present, the only plant species where the large-scale vs high-accuracy problem could be effectively overcome is Arabidopsis thaliana. Yet in this species most of the DNA methylation variation seems to be under genetic control (Dubin et al. 2015; Kawakatsu et al. 2016). Nevertheless, Arabidopsis was shown to be an outlier in terms of DNA methylation studies, harbouring a very low global genome methylation and TE content compared to other plant species (Alonso et al. 2015).

In addition to all these approaches, as previously discussed in the section “Phenotypic effects”, few naturally occurring epialleles were discovered in plant populations. These discoveries were made “by chance”, meaning that the studies that found them did not intentionally look for such epigenetic variation. Nevertheless, the presence of naturally occurring pure epialleles constitutes the most evident proof that epigenetic variation could potentially be adaptive.