Local diversity of drought resistance and resilience in Populus tomentosa correlates with the variation of DNA methylation

Abstract Little information is known about DNA methylation variation in shaping environment‐specific drought resistance and resilience for tree adaptation. In this study, we leveraged RNA sequencing and whole‐genome bisulfite sequencing data to dissect the distinction of epigenetic regulation under drought stress and rewater condition of Populus tomentosa accessions from three geographical regions. We demonstrated low resistance and high resilience for accessions from South. Non‐CG methylation levels in promoter regions of Southern accessions were lower than accessions from higher latitudes and negatively regulated gene expression. CHH context methylation was more sensitive to drought stress, and the geographical‐specific differentially methylated regions were scarcely changed by environmental fluctuation. We identified 60 conserved hub genes within the co‐expression networks that correlate with photosynthetic and stomatal morphological traits. Epigenome‐wide association studies and genome‐wide association studies of these 60 hub genes revealed the interdependency between genetic and epigenetic variation in GATA9 and LECRK‐VIII.2 , which was associated with stomatal morphology and chlorophyll content. The natural epigenetic variation in GATA9 was also faithfully transmitted to progenies in two family‐based F1 populations. This study indicates a functional relationship of DNA methylation diversity with drought resistance and resilience which offers new insights into plants’ local adaptation to a stressful environment.