A dynamic epigenetic perspective on above- and belowground phenotypic responses to drought: Insights from global DNA methylation in Erodium cicutarium.

There is mounting evidence that plant responses to environmental stress are mediated by epigenetic factors, including DNA methylation. Understanding relationships between DNA methylation, plant development and individual fitness in contrasting environments is key to uncover potential impacts of epigenetic regulation on plant adaptation. Here, we used an experimental approach combining controlled alteration of epigenetic features with exposure to stress. Two provenances of Erodium cicutarium were exposed to a demethylating agent (5-azacytidine) and recurrent drought, and effects on above- and belowground phenotypic traits related to early development, phenology and fitness assessed. Application of 5-azacytidine significantly reduced DNA methylation in leaf and root tissues. This slowed plant development, delayed flowering, and reduced the number of inflorescences produced, independent of water regime. Recurrent drought reduced final above- and belowground biomass and inflorescence production, regardless of the 5-azacytidine exposure. Increased fruit and seed-set were the only adaptations to drought in E. cicutarium, together with an increased number of flowers per inflorescence in water-stressed plants previously treated with 5-azacytidine. Epigenetic effects can desynchronize plant growth, flowering and senescence in both favourable and adverse environments. Future studies should focus on understanding intraspecific variation in ability to change the plant methylome in response to stress, and transgenerational transmission of such responses.