Context-Dependent Developmental Effects of Parental Shade Versus Sun Are Mediated by DNA Methylation

Parental environment influences progeny development in numerous plant and animal systems. Such inherited environmental effects may alter offspring phenotypes in a consistent way, for instance when resource-deprived parents produce low quality offspring due to reduced maternal provisioning. However, because development of individual organisms is guided by both inherited and immediate environmental cues, parental conditions may have different effects depending on progeny environment. Such context-dependent transgenerational plasticity suggests a mechanism of environmental inheritance that can precisely interact with immediate response pathways, such as epigenetic modification. We show that parental light environment (shade versus sun) resulted in context-dependent effects on seedling development in a common annual plant, and that these effects were mediated by DNA methylation. We grew replicate parents of five highly inbred Polygonum persicaria genotypes in glasshouse shade versus sun and, in a fully factorial design, measured ecologically important traits of their isogenic seedling offspring in both environments. Compared to the offspring of sun-grown parents, the offspring of shade-grown parents produced leaves with greater mean and specific leaf area, and had higher total leaf area and biomass. These shade-adaptive effects of parental shade were pronounced and highly significant for seedlings growing in shade, but slight and generally non-significant for seedlings growing in sun. Based on both regression and covariate analysis, inherited effects of parental shade were not mediated by changes to seed provisioning. To test for a role of DNA methylation, we exposed replicate offspring of isogenic shaded and fully insolated parents to either the demethylating agent zebularine or to control conditions during germination, then raised them in simulated growth chamber shade. Partial demethylation of progeny DNA had no phenotypic effect on offspring of shaded parents, but caused offspring of sun-grown parents to develop as if their parents had been shaded, with larger leaves and greater total canopy area and biomass. These results contribute to the increasing body of evidence that DNA methylation can mediate transgenerational environmental effects, and show that such effects may contribute to nuanced developmental interactions between parental and immediate environments.