Distinctive DNA methylation patterns induced by abiotic and biotic factors in the widely distributed clonal tree Populus nigra var. italica

Summary

Epigenetic mechanisms have the potential to mediate long-term plastic responses to environmental changes. Part of this plastic response occurs almost immediately after new stress exposure, where the epigenetic machinery is thought to play a role in the modulation of gene expression. In plants, DNA methylation is the most studied epigenetic mark and is found in three sequence contexts: CG, CHG and CHH (where H correspond to A, T or C). Changes in DNA methylation can occur either spontaneously or in response to the environment, causing epimutations. In long-lived species, such as trees, accumulated environmental-induced epimutations have the potential to influence plant ability to respond to novel situations. However, precise epigenetic patterns triggered by specific stress factors are still unknown in most species. In this study, we examined the effects of abiotic (heat, cold, drought) and biotic stresses (herbivory, rust infection, and salicylic acid signalling) on the DNA methylation in the clonal tree Populus nigra var. italica. Cuttings were collected from diverse European regions, grown in common greenhouse conditions for 4 months, and subsequently exposed to different stresses under controlled conditions. DNA Methylation status in poplar leaves was assessed by whole-genome bisulfite sequencing (WGBS) in 8 replicate individuals per treatment. Variation in CG and CHG methylation was mainly explained by tree provenance, while CHH methylation showed higher stress responsiveness. A total of 729 differentially methylated regions (DMRs) were identified (659 stress-specific). Drought stress induced the largest number of DMRs (477), most of them in CHH context and hypermethylated status compared to the control group. However, all stresses induced distinctive DMR patterns in terms of sequence context in combination with hyper/hypo methylation. These results could potentially help to discriminate specific environmental responses in natural populations, and also show how plants are able to remodel the background landscape of DNA methylation depending on the environment.