Abstract
DNA provides the fundamental framework for heritability, yet heritable trait variation need not be completely ‘hard-wired’ into the DNA sequence. In plants, the epigenetic machinery that controls transposable element (TE) activity, and which includes DNA methylation, underpins most known cases of inherited trait variants that are independent of DNA sequence changes. Here, we review our current knowledge of the extent, mechanisms and potential adaptive contribution of epiallelic variation at TE-containing alleles in this group of species. For the purpose of this review, we focus mainly on DNA methylation, as it provides an easily quantifiable readout of such variation. The picture that emerges is complex. On the one hand, pronounced differences in DNA methylation at TE sequences can either occur spontaneously or be induced experimentally en masse across the genome through genetic means. Many of these epivariants are stably inherited over multiple sexual generations, thus leading to transgenerational epigenetic inheritance. Functional consequences can be significant, yet they are typically of limited magnitude and although the same epivariants can be found in nature, the factors involved in their generation in this setting remain to be determined. On the other hand, moderate DNA methylation variation at TE-containing alleles can be reproducibly induced by the environment, again usually with mild effects, and most of this variation tends to be lost across generations. Based on these considerations, we argue that TE-containing alleles, rather than their inherited epiallelic variants, are the main targets of natural selection. Thus, we propose that the adaptive contribution of TE-associated epivariation, whether stable or not, lies predominantly in its capacity to modulate TE mobilization in response to the environment, hence providing hard-wired opportunities for the flexible exploration of the phenotypic space.This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’
Highlights
There is mounting evidence that heritable differences in traits can be transmitted in the absence of any DNA sequence changes
Because transposable element (TE) sequences tend to be methylated across their entire length, they are responsible for the bulk of DNA methylation in plant genomes
Over many TE sequences, this re-establishment is carried out by so-called RNA-directed DNA methylation (RdDM), a pathway involving the production of small RNAs and responsible for de novo methylation in all three sequence contexts
Summary
There is mounting evidence that heritable differences in traits can be transmitted in the absence of any DNA sequence changes. Because the quantitative trait loci (QTLepi) identified in the epiRILs span hundreds of TE-containing alleles with stable epiallelic inheritance [62], we should bear in mind the possibility that it is the concerted epivariation across all of these alleles at any given QTLepi that is causal In this case, given that genome-wide hypomethylation like that induced by ddm has not been observed in nature, the few and genomically dispersed natural counterparts of ddm1-induced royalsocietypublishing.org/journal/rstb Phil. It was even suggested that epiallelic inheritance represents the molecular underpinning of Waddington’s genetic assimilation [139] It is clear from the evidence discussed above that the adaptive potential provided by stable epiallelic variants in the face of environmental challenges suffers from two major limitations: (i) the rate of spontaneous TE-associated epimutations is not significantly higher than that of SNPs, contrary to what was previously thought, and (ii) the amplitude of phenotypic variation they may cause is relatively small. Extending studies to non-model organisms, notably species relying on asexual propagation or with long perennial vegetative phases, may uncover conditions (e.g. invasions, as reviewed by Mounger et al [101] in this issue) where increased heritability of environmentally induced epiallelic variation is favoured
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
