Epigenetic variation reflects dynamic habitat conditions in a rare floodplain herb

Abstract

Variation of DNA methylation is thought to play an important role for rapid adjustments of plant populations to dynamic environmental conditions, thus compensating for the relatively slow response time of genetic adaptations. However, genetic and epigenetic variation of wild plant populations has not yet been directly compared in fast changing environments. Here, we surveyed populations of Viola elatior from two adjacent habitat types along a successional gradient characterized by strong differences in light availability. Using amplified fragment length polymorphisms (AFLP) and methylation-sensitive amplification polymorphisms (MSAP) analyses, we found relatively low levels of genetic (H'gen = 0.19) and epigenetic (H'epi = 0.23) diversity and high genetic (ϕST = 0.72) and epigenetic (ϕST = 0.51) population differentiation. Diversity and differentiation were significantly correlated, suggesting that epigenetic variation partly depends on the same driving forces as genetic variation. Correlation-based genome scans detected comparable levels of genetic (17.0%) and epigenetic (14.2%) outlier markers associated with site specific light availability. However, as revealed by separate differentiation-based genome scans for AFLP, only few genetic markers seemed to be actually under positive selection (0-4.5%). Moreover, principal coordinates analyses and Mantel tests showed that overall epigenetic variation was more closely related to habitat conditions, indicating that environmentally induced methylation changes may lead to convergence of populations experiencing similar habitat conditions and thus may play a major role for the transient and/or heritable adjustment to changing environments. Additionally, using a new MSAP-scoring approach, we found that mainly the unmethylated (ϕST = 0.60) and CG-methylated states (ϕST = 0.46) of epiloci contributed to population differentiation and putative habitat-related adaptation, whereas CHG-hemimethylated states (ϕST = 0.21) only played a marginal role.

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

“…2013; Schulz et al. 2014), such as those ordinarily accompanying ecological disturbance, lend additional support to the hypothesis of disturbance‐mediated epigenetic changes in natural plant populations. This hypothesis, however, does not seem to have been explicitly addressed to date.…”

“…Differential spatial patterns for different marker types were also reported by Schulz et al. (2014) in an investigation on geographical and habitat‐dependent structuring of epigenetic variation in the perennial herb Viola elatior . It is tempting to speculate that these differences are related to differences between cytosine methylation in CHG ( h ‐type markers) and CG ( m ‐type markers) contexts in maintenance mechanisms and predominant genomic location (genes vs. transposable elements) (Cokus et al.…”

Genetic and epigenetic variation in Spartina alterniflora following the Deepwater Horizon oil spill

“…We treated type IV variation as missing data, because the methylation state cannot be specified (Salmon et al., 2008). Although some advocate for discriminating between type II and type III methylation as these types are expected to capture methylation in CG versus CHG contexts (Medrano, Herrera, & Bazaga, 2014; Schulz, Eckstein, & Durka, 2014), type II variation and type III variation cannot simply be interpreted as CG versus CHG methylation as apparent CHG methylation can be caused by the nesting of internal restriction sites within MS‐AFLP fragments that exhibit differential CG methylation (Fulneček & Kovařík, 2014). Therefore, we combined type II variation and type III variation to represent the presence of DNA methylation in any context.…”

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

“…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. Therefore, epigenetic variation can be a very important mechanism for invasive plant success in a broad range of environments (Douhovnikoff & Dodd, 2014; Richards, Schrey, & Pigliucci, 2012).…”

“…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).…”