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Ectomycorrhizas are an intrinsic component of tree nutrition and responses to environmental variations. How epigenetic mechanisms might regulate these mutualistic interactions is unknown. By manipulating the level of expression of the chromatin remodeler DECREASE IN DNA METHYLATION 1 (DDM1) and two demethylases DEMETER-LIKE (DML) in Populus tremula × Populus alba lines, we examined how host DNA methylation modulates multiple parameters of the responses to root colonization with the mutualistic fungus Laccaria bicolor. We compared the ectomycorrhizas formed between transgenic and wild-type (WT) trees and analyzed their methylomes and transcriptomes. The poplar lines displaying lower mycorrhiza formation rate corresponded to hypomethylated overexpressing DML or RNAi-ddm1 lines. We found 86 genes and 288 transposable elements (TEs) differentially methylated between WT and hypomethylated lines (common to both OX-dml and RNAi-ddm1) and 120 genes/1441 TEs in the fungal genome suggesting a host-induced remodeling of the fungal methylome. Hypomethylated poplar lines displayed 205 differentially expressed genes (cis and trans effects) in common with 17 being differentially methylated (cis). Our findings suggest a central role of host and fungal DNA methylation in the ability to form ectomycorrhizas including not only poplar genes involved in root initiation, ethylene and jasmonate-mediated pathways, and immune response but also terpenoid metabolism., (© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.)

Plants are fixed organisms with continuous development throughout their life and great sensitivity to environmental variations. They react in this way by exhibiting large developmental phenotypic plasticity. This plasticity is partly controlled by (phyto)hormones, but recent studies also suggest the involvement of epigenetic mechanisms. It seems that these two factors may interact in a complex way and especially in the stem cells grouped together in meristems. The objective of this review is to present the current arguments about this interaction which would promote developmental plasticity. Three major points are thus addressed to justify this interaction between hormonal control and epigenetics (control at the chromatin level) for the developmental plasticity of plants: the arguments in favor of an effect of hormones on chromatin and vice versa, the arguments in favor of their roles on developmental plasticity and finally the arguments in favor of the central place of these interactions, the meristems. Various perspectives and applications are discussed., (© Société de Biologie, 2020.)