Parental DNA methylation influences plasticity of early offspring traits, but offspring DNA methylation influences trait plasticity throughout life

Plants alter their phenotypes in response to both their own environment and that of their parents. Parental environments are hypothesized to more strongly regulate early life stages of offspring, while offspring environments regulate later life stages, since offspring perception becomes more accurate throughout development. DNA methylation in plants is known to respond to environmental conditions and can be transmitted across generations, so DNA methylation of both parents and offspring may be involved in regulating responses to environments within and across generations. However, the relative contribution of each generation's epigenetic regulation is not known. We quantified phenotypic responses to parent and offspring canopy environment and tested whether parental or offspring DNA methylation mediated those responses. To quantify the response to parental versus offspring canopy, we used green filter during the growth of either parents or offspring. To test the contribution of parental versus offspring DNA methylation to regulate offspring phenotypic responses to canopy shade at seed, seedling, and adult life stages, we manipulated parental or offspring DNA methylation using 5-azacytidine. Both parent and offspring shade affected offspring traits. Parental DNA demethylation affected trait responses to both parental and offspring canopy, but it did so only at early life stages, while offspring DNA demethylation influenced responses throughout life. Trait correlations were significantly altered by chemical demethylation of parents and offspring, indicating that DNA methylation in both generations influences integrated phenotypic responses to canopy. These results demonstrate that the influence of parental methylation on offspring phenotypes measured in this study were manifest only early in the life of offspring, while offspring phenotypes were more strongly influenced by their own epigenetic regulation at mature stages. DNA methylation of both parents and offspring appears to coordinate multitrait responses like the shade avoidance syndrome.

Automated summary

This study found that DNA methylation in both parents and offspring plays different roles in regulating plant responses to the environment. Parental DNA demethylation mainly affects phenotype responses in early life stages, while offspring DNA demethylation has an influence throughout life.