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Epigenetic Variation in Tree Evolution: a case study in black poplar (Populus nigra)
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DATA AVAILABILITY STATEMENT: The raw data for WGS, WGBS and RNAseq are stored in the NCBI website under the following accession numbers PRJNA818172 BioProject (WGS), PRJNA828400 BioProject (WGBS), GSE128482 (RNA-seq). The processed SNPs, methylation matrices, LF/MF, duplicated genes, pcadapt, hypo/up and Hyper/Down candidate genes can be found at: https://entrepot.recherche.data.gouv.fr/privateurl.xhtml.We are grateful to the to the genotoul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, https://doi.org/10.15454/1.5572369328961167E12) and the Mesocentre Clermont Auvergne bioinformatics platform (https://doi.org/10.18145/aubi) for providing computing and storage resources and to the GBFOR, INRAE, 2018, Forest Genetics and Biomass Facility (https://doi.org/10.15454/1.5572308287502317E12) for the experimental design setup andsamples collection. We thank COST action (European Cooperation in Science and Technology) EPIgenetic mechanisms of Crop Adaptation To Climate cHange (EPICATCH; grant number CA19125) for active discussion.. How perennial organisms adapt to environments is a key question in biology. To address this question, we investigated ten natural black poplar ( Populus nigra ) populations from Western Europe, a keystone forest tree of riparian ecosystems. We assessed the role of (epi)genetic regulation in driving tree species evolution and adaptation over several millions of years (macro-evolution) up to a few generations (micro-evolution). At the macro-evolution scale, polar experienced differential structural (gene loss) and regulation (expression and methylation) reprogramming between sister genomic compartments inherited from polyploidization events. More interestingly, at the micro-evolution scale, both genetic and epigenetic variations differentiate populations from different geographic origins, targeting specifically genes involved in disease resistance, immune response, hormonal and stress response that can be considered as key functions of local adaptation of long lifespan species. Moreover, genes involved in cambium formation, an important functional trait for forest trees, as well as basal functions for cell survival are constitutively expressed though methylation control. These results highlight DNA methylation as a marker of population differentiation, evolutionary adaptation to diverse ecological environments and ultimately opening the need to take epigenetic marks into account in breeding strategies, especially for woody plants.