Genome-wide variation in DNA methylation predicts variation in leaf traits in a foundational oak species

<b>Abstract:</b> As forests face the challenge of adapting to a changing climate, epigenetic modifications like DNA methylation are a potential mechanism for trees to respond to unstable environments. However, it remains controversial the extent to which DNA methylation impacts ecologically important traits that influence fitness. In this study, we used reduced-representation bisulfite sequencing to associate genomic and epigenomic variation with seven phenotypic traits related to growth, leaf function, and disease susceptibility in 160 valley oak (Quercus lobata) saplings planted across two common gardens in California. We found that DNA methylation was associated with a significant fraction of phenotypic variance in plant height, leaf lobedness, powdery mildew infection, and trichome density. Two of the seven traits were significantly associated with DNA methylation in the CG context, three traits were significantly associated with CHG methylation, and two traits were significantly associated with CHH methylation. Notably, controlling for genomic variation in SNPs generally reduced the amount of trait variation explained by DNA methylation. Our results suggest that DNA methylation may serve as a useful biomarker to predict phenotypic variation in forest tree species, though it remains unclear the degree to which DNA methylation is a causal mechanism driving phenotypic variation in forest tree species.