Methylome evolution in plants

Abstract

Despite major progress in dissecting the molecular pathways that control DNA methylation patterns in plants, little is known about the mechanisms that shape plant methylomes over evolutionary time. Drawing on recent intra- and interspecific epigenomic studies, we show that methylome evolution over long timescales is largely a byproduct of genomic changes. By contrast, methylome evolution over short timescales appears to be driven mainly by spontaneous epimutational events. We argue that novel methods based on analyses of the methylation site frequency spectrum (mSFS) of natural populations can provide deeper insights into the evolutionary forces that act at each timescale.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1127-5) contains supplementary material, which is available to authorized users.

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

“…Importantly, our demographic inferences suggesting a relatively recent (20–33 KYA) evolutionary establishment of Newfoundland Canada lynx supports DNA methylation as a marker to examine rapid evolutionary change. Evolutionary theory in model organisms has predicted that epimutations and methylome evolution often precede genomic changes (Smith, Martin, Nguyen, & Mendelson, ; Vidalis et al, ), which has been further substantiated with empirical evidence examining epigenetic changes over structural genomic variants in the absence of (Ichikawa et al, ) and phenotypic responses in the absence of standing genetic variation (Sentis et al, ).…”

Interspecific variation across angiosperms in globalDNAmethylation: phylogeny, ecology and plant features in tropical and Mediterranean communities

“…The present results confirmed that global methylation of plant genomes can vary 10‐fold across angiosperm species, and that such variation is significantly associated with phylogenetic relatedness in a broader taxonomic and ecological sampling than addressed previously (Alonso et al ., ; Vidalis et al ., ). Tropical species in the present sample, however, exhibited a looser phylogenetic relationship suggesting lower strength of species differentiation strictly due to their divergence time (Brownian motion, BM) in this particular sample (Münkemüller et al ., ).…”

“…The molecular understanding of epigenetic regulation, significance of DNA methylation and connections between different epigenetic traits in model plants, has considerably improved in the last decades (Diez et al ., ; Matzke et al ., ). Furthermore, recent comparative analyses of model and commercial plant species whose methylomes have been fully sequenced suggest that genomic distribution of methylated cytosines, regulation of chromatin modifications, and even the activity of different DNA methylation pathways, vary among distant lineages (Niederhuth et al ., ; Takuno et al ., ; Vidalis et al ., ) and even closely related species (Seymour et al ., ; Song & Cao, ). By contrast, next to nothing is known about the possible correlations between interspecific patterns of DNA methylation in wild plants, on the one hand, and plant features and ecological or geographical gradients, on the other.…”

The sources of adaptive variation

“…The methylation status of such C sites is, however, quite unstable, with a higher frequency of losses than gains, and overall 'mutation' rates of around 10 -4 per basepair per generation, 5000 times higher than those for DNA nucleotide changes. Despite this instability, such epiallelic variants could have a role in evolution [59]: with reversion at a rate of 10 -4 , a selective advantage of 1% in heterozygotes would allow an advantageous epiallele to spread to an equilibrium frequency of 99% [60]. However, mutations to deleterious alleles create a genetic load.…”