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.

Highlights

  • Cytosine methylation is a heritable epigenetic modification and a pervasive feature of most plant genomes [1,2,3,4]

  • This review provides a first unified framework for understanding the evolution of methylation in plants, based on the fact that the epigenomic divergence observed at the longer timescales is necessarily the result of processes occurring within populations at shorter timescales

  • Spontaneous epimutations appear to be a major factor in generating methylome diversity. These epimutations are characterized by their high, asymmetric rates, and the fact that they occur at a finite number of cytosines

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Summary

Introduction

Cytosine methylation is a heritable epigenetic modification and a pervasive feature of most plant genomes [1,2,3,4]. A major goal of these comparative approaches is to answer the following questions: ‘What are the factors that generate inter-individual variation in DNA methylation?’ and ‘How do evolutionary forces, such as selection, recombination and drift, act on this variation?’ A recent surge in fully sequenced plant genomes and methylomes is providing the raw material that can be used to begin to answer these questions.

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