DNA hypomethylation of the host tree impairs interaction with mutualistic ectomycorrhizal fungus

• Published in: New Phytologist
• Main Authors: Vigneaud, Julien, Kohler, Annegret, Sow, Mamadou Dia, Delaunay, Alain, Fauchery, Laure, Guinet, Frederic, Daviaud, Christian, Barry, Kerrie, Keymanesh, Keykhosrow, Johnson, Jenifer, Singan, Vasanth, Grigoriev, Igor, Fichot, Régis, Conde, Daniel, Perales, Mariano, Tost, Jörg, Martin, Francis, Allona, Isabel, Strauss, Steven, Veneault-Fourrey, Claire, Maury, Stéphane
• Other Authors: Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans (UO)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Lawrence Berkeley National Laboratory Berkeley (LBNL), Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM), Oregon State University (OSU), ANR-17-CE32-0009,EPITREE,Impacts évolutif et fonctionnel de variations épigénétiques chez des arbres forestiers.(2017), ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2023
• Subjects: DNA METHYLATION 1; DEMETER; DNA demethylatione; Laccaria bicolormy; corrhizas; pigenetic; poplar; [SDV]Life Sciences [q-bio]; DML
• Online Access: https://hal.inrae.fr/hal-04050258; https://doi.org/10.1111/nph.18734

International audience 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 x 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.