Organisms survive in naturally fluctuating environments by responding to long-term signals, such as seasonality, by filtering out short-term noise. DNA methylation has been considered a stable epigenetic mark but has also been reported to change in response to experimental manipulations of biotic and abiotic factors. However, it is unclear how they behave in natural environments. Here, we analyzed seasonal patterns of genome-wide DNA methylation at a single-base resolution using a single clone from a natural population of the perennial Arabidopsis halleri. The genome-wide pattern of DNA methylation was primarily stable, and most of the repetitive regions were methylated across the year. Although the proportion was small, we detected seasonally methylated cytosines (SeMCs) in the genome. SeMCs in the different contexts showed distinct seasonal patterns of methylation. SeMCs in CHH context were detected predominantly at repetitive sequences in intergenic regions. Additionally, we found that CHH methylation within AhgFLC locus showed a seasonal pattern that was negatively associated with changes in gene expression. Gene-body CG methylation (gbM) itself was generally stable across seasons, but the levels of gbM were positively associated with seasonal stability of RNA expression of the genes. These results suggest the existence of two distinct aspects of DNA methylation in natural environments: sources of epigenetic variation and epigenetic marks for stable gene expression.

Seasonal stability and dynamics of DNA methylation in plants in a natural environment