Positive selective sweeps of epigenetic mutations regulating specialized metabolites in plants

Abstract

DNA methylation is an important factor regulating gene expression in organisms. However, whether DNA methylation plays a key role in adaptive evolution is unknown. Here, we show evidence of naturally selected DNA methylation in Arabidopsis thaliana. In comparison with single nucleotide polymorphisms, three types of methylation—methylated CGs (mCGs), mCHGs, and mCHHs—contributed highly to variable gene expression levels among an A. thaliana population. Such variably expressed genes largely affect a large variation of specialized metabolic quantities. Among the three types of methylations, only mCGs located in promoter regions of genes associated with specialized metabolites show a selective sweep signature in the A. thaliana population. Thus, naturally selected mCGs appear to be key mutations that cause the expressional diversity associated with specialized metabolites during plant evolution.

Epigenetic induction may speed up or slow down speciation with gene flow

“…However, in nature the broad-scale importance of epigenetic variation in evolution remains uncertain. There are a number of situations where epigenetic variation does appear to play an important role, including heritable phenotypic variation (Blewitt et al 2006, Cubas et al 1999, Duempelmann et al 2019, stress-induced heritable epigenetic variation (Verhoeven et al 2010), environmentally induced epigenetic traits that can be heritable over multiple generations (Klosin et al 2017, Rechavi et al 2014, and fitness effects that are caused by heritable epigenetic changes (Herman & Sultan 2016, Shirai et al 2021). Yet our understanding of these phenomena is still in its infancy, and current data on epigenetic variation and transgenerational plasticity do not permit estimation of the rate of adaptively biased epimutation, although estimates of unbiased epimutation have been made (van der Graaf et al 2015).…”

“…Recent evidence also suggests that epimutations can experience positive natural selection in the form of selective sweeps (Shirai et al. 2021).…”

“…Empirical evidence for adaptively relevant epigenetic variation comes from studies of plants (Wilschut et al 2016), unicellular organisms (Kronholm et al 2017), and animals (Hu & Barrett 2017). Recent evidence also suggests that epimutations can experience positive natural selection in the form of selective sweeps (Shirai et al 2021).…”

“…2021a, Shirai et al. 2021). Pointing to a possible role in population divergence, epigenetic variation has been found to correlate with environmental variables, a sign of local adaptation (Herrera & Bazaga 2010, Heckwolf et al.…”

“…The role of nongenetic inheritance in adaptation, including that which is mediated by epigenetic inheritance of DNA methylation states, chromatin modifications, or small RNAs, has been largely overlooked until recently (Bonduriansky & Day 2018, Smith & Ritchie 2013. Accumulating evidence suggests that phenotypes can be inherited through nongenetic means and that epigenetic markers can be adaptively relevant and heritable (Herman & Sultan 2016, Kelley et al 2021a, Shirai et al 2021. Pointing to a possible role in population divergence, epigenetic variation has been found to correlate with environmental variables, a sign of local adaptation (Herrera & Bazaga 2010, Heckwolf et al 2020, Kelley et al 2021b, McNew et al 2017, Platt et al 2015, Richards et al 2012, Robertson et al 2017, Thorson et al 2017, Wilschut et al 2016.…”