Epigenetic Variation in Plant Populations: DNA Methylation as a Driver of Phenotypic Diversity and Adaptation

Abstract

DNA methylation constitutes a primary layer of epigenetic regulation in plants, operating across three sequence contexts (CG, CHG, and CHH) through distinct enzymatic pathways. Over the past fifteen years, accumulating evidence has shown that DNA methylation varies substantially among individuals and populations of wild plants, sometimes independently of underlying genetic polymorphism. This variation can influence gene expression, transposable element activity, and phenotypic traits relevant to ecological adaptation. Population epigenetics, the study of methylation variation at the population scale, has matured from initial surveys using methylation-sensitive amplified fragment length polymorphism (MS-AFLP) into a discipline increasingly reliant on reduced-representation bisulfite sequencing (epiGBS, bsRADseq), whole-genome bisulfite sequencing (WGBS), enzymatic methyl-seq (EM-seq), and direct long-read detection by nanopore sequencing. These methodological advances are opening population epigenetics to non-model organisms across the full breadth of the plant phylogeny, from angiosperms and gymnosperms to ferns and bryophytes. We cover (i) the molecular machinery underlying plant DNA methylation, including the debated status of N6-methyladenine (6mA); (ii) empirical evidence for natural epigenetic variation in plant populations, spanning clonal, invasive, and outcrossing species; (iii) the methodological toolkit available for population-scale methylation profiling, with emphasis on approaches suitable for non-model taxa; and (iv) the ecological and evolutionary significance of population epigenetic variation, including transgenerational inheritance, stress memory, epigenetic clocks, conservation applications, and the emerging integration of epigenetics into the extended evolutionary synthesis. We identify critical knowledge gaps, particularly the near-complete absence of population-level epigenetic data for bryophytes, ferns, and lycophytes, and outline priorities for future research.