Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants

Abstract

Adaptive evolution is generally thought to be the result of natural selection predominantly acting upon pre-existing DNA sequence polymorphisms through gene-environment interactions. Epigenetic inheritance is, however, recently considered an additional molecular force driving adaptive evolution independent of DNA sequence variation. Through comparative analyses of genome-wide genetic (SNPs) and epigenetic (DMCs) variation of wild strawberry plants raised under distinct drought settings, we demonstrate intermediate levels of genome-wide covariation between SNPs and DMCs. Cases of high SNP-DMC covariation were significantly associated with (i) applied stress, (ii) non-adaptive SNPs, and (iii) solitary DMCs (as opposed to DMC islands). We also found that DMCs, drought-responsive DMCs in particular, typically co-vary with hundreds of SNPs, indicating high genomic redundancy as a basis for polygenic adaptation. Our findings suggest that stress-responsive DMCs initially co-vary with many associated SNPs under increased environmental stress (cfr. co-gradient plasticity), and that natural selection acting upon these SNPs subsequently reduce standing covariation with stress-responsive DMCs. In addition, the degree of covariation between SNPs and DMCs appears independent of their respective genomic distance, indicating that trans-acting associations between SNPs and DMCs are as likely as cis-acting associations. Our study is in favor of DNA methylation profiles representing complex quantitative traits rather than independent evolutionary forces, but further research is required to fully rule out SNP-independence of genome-wide DMCs. We provide a conceptual framework for polygenic regulation and adaptation shaping genome-wide methylation patterns.

DNA methylation dynamics during stress response in woodland strawberry (Fragaria vesca)

“…This is in agreement with previous studies which reported that mCHH was most dynamic in response to different climates [ 9 ]. More specifically, in the case of F. vesca , altitude variations of natural strawberry populations was found to be correlated with a high variability in DNA methylation in the CHH context [ 16 , 49 ]. In our study, cold stress, heat stress, and salt stress resulted in substantial local loss of DNA methylation in all sequence contexts, particularly in regions close to TSS and TES sites ( Fig.…”

DNA methylation dynamics during stress-response in woodland strawberry (Fragaria vesca)

“…This is in agreement with studies which reported that mCHH was most dynamic in response to different climates (Dowen et al , 2012; Dubin et al , 2015; Kenchanmane et al , 2019). More specifically, in the case of F. vesca, altitude variations of natural strawberry populations was found to be correlated with a high variability in DNA methylation in the CHH context (De Kort et al , 2020; Kort et al , 2021). In our study, cold, heat, and salt stress resulted in substantial local loss of DNA methylation in all sequence contexts, particularly in regions close to TSS and TES sites in the F. vesca genome (Fig.…”