Epigenetic variation creates potential for evolution of plant phenotypic plasticity

Abstract

SummaryHeritable variation in plant phenotypes, and thus potential for evolutionary change, can in principle not only be caused by variation in DNA sequence, but also by underlying epigenetic variation. However, the potential scope of such phenotypic effects and their evolutionary significance are largely unexplored.Here, we conducted a glasshouse experiment in which we tested the response of a large number of epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana -lines that are nearly isogenic but highly variable at the level of DNA methylation -to drought and increased nutrient conditions.We found significant heritable variation among epiRILs both in the means of several ecologically important plant traits and in their plasticities to drought and nutrients. Significant selection gradients, that is, fitness correlations, of several mean traits and plasticities suggest that selection could act on this epigenetically based phenotypic variation.Our study provides evidence that variation in DNA methylation can cause substantial heritable variation of ecologically important plant traits, including root allocation, drought tolerance and nutrient plasticity, and that rapid evolution based on epigenetic variation alone should thus be possible.

Genetic and epigenetic changes during the invasion of a cosmopolitan species (Phragmites australis)

“…While adaptation is accomplished by genetic changes through mutation, drift and selection are very slow for some introduced species, so epigenetic mechanisms can provide an alternative source of ecologically phenotypic diversity for rapid adjustment (Medrano, Herrera, & Bazaga, 2014). Epigenetic diversity can generate massive heritable variation of ecologically relevant plant traits such as root allocation, drought tolerance and nutrient plasticity (Zhang, Fischer, Colot, & Bossdorf, 2013), and it appears to increase the productivity and stability of plant populations in Arabidopsis thaliana under artificial conditions (Latzel et al., 2013). An increasing number of studies have also demonstrated the common existence and significant role of epigenetic variation in plant populations of herbs (Foust et al., 2016; Herrera, Medrano, & Bazaga, 2014; Medrano et al., 2014; Preite et al., 2015; Schulz, Eckstein, & Durka, 2014), shrubs (Avramidou, Ganopoulos, Doulis, Tsaftaris, & Aravanopoulos, 2015; Herrera & Bazaga, 2013, 2016), and trees (Guarino, Cicatelli, Brundu, Heinze, & Castiglione, 2015; Gugger, Fitz‐Gibbon, PellEgrini, & Sork, 2016; Lira‐Medeiros et al., 2010; Platt, Gugger, Pellegrini, & Sork, 2015; Sáez‐Laguna et al., 2014) under natural conditions.…”

“…The pattern of DNA methylation can affect ecologically important phenotypes and plasticity (Herrera & Bazaga, 2013; Nicotra et al., 2015; Zhang et al., 2013) and may play a significant role in adaptation to various habitat conditions (Foust et al., 2016; Richards et al., 2012; Schulz et al., 2014). For example, a naturally occurring epiallele named “NMR19‐4” has been discovered in Arabidopsis accessions , and its DNA methylation status is inheritable and independent of genetic variation (He et al., 2018).…”

Genetic and epigenetic divergence between disturbed and undisturbed subpopulations of a Mediterranean shrub: a 20‐year field experiment

“…2014); and (3) increasing evidence showing that epigenetic mechanisms are involved in phenotypic plasticity (Herrera and Bazaga 2013; Jablonka 2013; Zhang et al. 2013), which in turn plays a facilitating role in the colonization of fluctuating environments (Herrera et al. 2012; Lande 2015).…”

Ecological Epigenetics in Marine Metazoans

“…Epigenetic mechanisms have been of interest in evolutionary biology (Richards et al, 2010;Zhang et al, 2013;Deans and Maggert, 2015), in the field of development (Beldade et al, 2011), and in such specialized fields as ecotoxicology (Vandegehuchte and Janssen, 2014). Historically, the research community has debated how to exactly define epigenetics (Deans and Maggert, 2015).…”