Species‐wide patterns of DNA methylation variation in Quercus lobata and their association with climate gradients

Abstract

DNA methylation in plants affects transposon silencing, transcriptional regulation and thus phenotypic variation. One unanswered question is whether DNA methylation could be involved in local adaptation of plant populations to their environments. If methylation alters phenotypes to improve plant response to the environment, then methylation sites or the genes that affect them could be a target of natural selection. Using reduced-representation bisulphite sequencing (RRBS) data, we assessed whether climate is associated with variation in DNA methylation levels among 58 naturally occurring, and species-wide samples of valley oak (Quercus lobata) collected across climate gradients. We identified the genomic context of these variants referencing a new draft valley oak genome sequence. Methylation data were obtained for 341 107 cytosines, of which we deemed 57 488 as single-methylation variants (SMVs), found in the CG, CHG and CHH sequence contexts. Environmental association analyses revealed 43 specific SMVs that are significantly associated with any of four climate variables, the majority of which are associated with mean maximum temperature. The 43 climate-associated SMVs tend to occur in or near genes, several of which have known involvement in plant response to environment. Multivariate analyses show that climate and spatial variables explain more overall variance in CG-SMVs among individuals than in SNPs, CHG-SMVs or CHH-SMVs. Together, these results from natural oak populations provide initial evidence for a role of CG methylation in locally adaptive evolution or plasticity in plant response.

Epigenetics in natural animal populations

“…Many studies have quantified epigenetic variation by applying standard statistical measures used in population genetics (Box 3). To provide conclusive evidence that epigenetic variation can result in ecologically relevant phenotypic changes that are autonomous from genotypic variation, we suggest that future studies of pure epigenetic variation could transplant different populations into common environments, and test for the contributions of genetic effects to epigenetic variation by testing for genome-or epigenome-wide associations in sample individuals and their offspring (GWAS and EWAS, respectively), after correcting for confounding by genetic background using a kinship matrix (Dubin et al, 2015;Orozco et al, 2015;Lea et al, 2016;Gugger et al, 2016). Several recent studies have also developed statistical approaches to partition environmental and genetic effects on epigenetic variation.…”

“…Several recent studies have also applied next-generation sequencing techniques to simultaneously analyse the relationships between genetic variation, epigenetic variation, and the environment (e.g. Schmitz et al, 2011;Platt et al, 2015;Gugger et al, 2016). In these studies, genomic DNA treated with sodium bisulphite was sequenced.…”

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

“…While the structure of B1 and B2 can only be shaped through natural selection, B3 could be direct changed by the environment. The epigenetic differentiation was observed in contrast habitats without variation differentiation (Foust et al., 2016; Gugger et al., 2016; Lira‐Medeiros et al., 2010; Schulz et al., 2014), but it remained unexplored how stable and inheritable the B3 variation is in these studies. Common garden filtered the plastic B3 variation in our study, and epigenetic divergence between populations in the introduced region and in its original region was weakened.…”

“…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).…”

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

“…The recent application of molecular techniques to ecological questions has revealed that epigenetic regulatory mechanisms, such as DNA methylation, may respond dynamically and independently to sudden changes in the environment (e.g., Gugger, Fitz‐Gibbon, Pellegrini, & Sork, 2016; Trucchi et al., 2016). Although there are several epigenetic mechanisms that can alter gene expression (e.g., chromatin remodeling, histone modifications, small interfering RNAs), DNA methylation of cytosines is the most widely studied (Schrey et al., 2013; Verhoeven, Vonholdt, & Sork, 2016) and can have important ecological effects.…”