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

Authors
  • Vigneaud, Julien1
  • Kohler, Annegret2
  • Sow, Mamadou Dia1
  • Delaunay, Alain1
  • Fauchery, Laure2
  • Guinet, Frederic2
  • Daviaud, Christian3
  • Barry, Kerrie W4
  • Keymanesh, Keykhosrow4
  • Johnson, Jenifer4
  • Singan, Vasanth4
  • Grigoriev, Igor4, 5
  • Fichot, Régis1
  • Conde, Daniel6
  • Perales, Mariano6, 7
  • Tost, Jörg3
  • Martin, Francis M2
  • Allona, Isabel6, 7
  • Strauss, Steven H8
  • Veneault-Fourrey, Claire2
  • And 1 more
  • 1 LBLGC, INRAE, Université d'Orleans, EA 1207 USC 1328, Orléans, 45067, France. , (France)
  • 2 UMR 1136 Interactions Arbres-Microorganismes, Centre INRAE Grand Est-Nancy, INRAE, Université de Lorraine, Champenoux, 54280, France. , (France)
  • 3 Laboratory for Epigenetics and Environment Centre National de Recherche en Génomique Humaine, CEA-Institut de Biologie Francois Jacob, Université Paris-Saclay, Evry, 91000, France. , (France)
  • 4 Lawrence Berkeley National Laboratory, US Department of Energy Joint Genome Institute, Berkeley, CA, 94720, USA.
  • 5 Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, 94720, USA.
  • 6 Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo UPM, Pozuelo de Alarcón, Madrid, 28223, Spain. , (Spain)
  • 7 Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid (UPM), Madrid, 28040, Spain. , (Spain)
  • 8 Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, 97331-5752, USA.
Type
Published Article
Journal
New Phytologist
Publisher
Wiley (Blackwell Publishing)
Publication Date
Jun 01, 2023
Volume
238
Issue
6
Pages
2561–2577
Identifiers
DOI: 10.1111/nph.18734
PMID: 36807327
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

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.

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