1. Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom‐forming fungi
- Author
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Anna Lipzen, Pierre-Emmanuel Courty, Robert Riley, Brian Looney, Alan Kuo, Elodie Drula, Igor V. Grigoriev, Annegret Kohler, Andrew Tritt, David S. Hibbett, Kerrie Barry, Jesse L. Labbé, László Nagy, Matt Nolan, P. Brandon Matheny, Francis Martin, Shingo Miyauchi, Jenifer Johnson, Emmanuelle Morin, Jasmyn Pangilinan, Bernard Henrissat, Guifen He, Kurt LaButti, William Andreopoulos, Clark University, Worcester, USA, INRA Centre de Recherches Forestières de Nancy, Unité d'Ecologie Forestière, Biodiversité et Biotechnologie Fongiques (BBF), Aix Marseille Université (AMU)-École Centrale de Marseille (ECM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Architecture et fonction des macromolécules biologiques (AFMB), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Agroécologie [Dijon], Université de Bourgogne (UB)-Université Bourgogne Franche-Comté [COMUE] (UBFC)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Dijon, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA, University of California, Berkeley Berkeley, California, USA, Institute of Biochemistry Szeged Hungary, Clark University Worcester USA, Centre Interdisciplinaire de Nanoscience de Marseille (CINaM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia, Professor, University of Tennessee, USA, Department of Energy, Oak Ridge USA, Beijing Forestry University Beijing, China, This research was supported by the Genomic Science Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area, at the Oak Ridge National Laboratory. The Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05-00OR22725. The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231.Research in the Martin laboratory is also funded by the Laboratory of Excellence Advanced Research onthe Biology of Tree and Forest Ecosystems (ARBRE, grant ANR-11-LABX-0002-01), the Region Lorraine ResearchCouncil and the European Commission (European Regional Development Fund)., ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011), Clark University, Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Joint Genome Institute (JGI), United States Department of Energy, Biological Research Centre [Szeged] (BRC), Eötvös Loránd University (ELTE), The University of Tennessee [Knoxville], BioSciences Division [Oak Ridge], Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC-UT-Battelle, LLC, and Community Sequencing Program 1974 305US Department of Energyunder contract DE-AC05-00OR22725 no. DE-AC02-05CH1123
- Subjects
Transposable element ,Physiology ,[SDV]Life Sciences [q-bio] ,Lineage (evolution) ,russulaceae ,Plant Science ,russulales ,Genome ,Evolution, Molecular ,Habits ,Mycorrhizae ,evolutionary transition ,Symbiosis ,Secondary metabolism ,Gene ,Genome size ,ComputingMilieux_MISCELLANEOUS ,Phylogeny ,biology ,[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] ,synteny ,biology.organism_classification ,Evolutionary biology ,DNA Transposable Elements ,secondary metabolism cluster ,Russulaceae ,transposable elements ,Agaricales ,ectomycorrhizal habit ,Russulales - Abstract
International audience; Summary The ectomycorrhizal (ECM) symbiosis has independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic signatures of the transition to the ECM habit within the hyper-diverse Russulaceae. We present comparative analyses of the genomic architecture and the total and secreted gene repertoires of 18 species across the order Russulales of which 13 are newly sequenced, including a representative of a saprotrophic member of Russulaceae, Gloeopeniophorella convolvens. The genomes of ECM Russulaceae are characterized by a loss of genes for plant cell-wall degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of small secreted proteins (SSPs) with TE “nests”, or dense aggregations of TEs. Some PCWDEs have been retained or even expanded, mostly in a species-specific manner. The genome of Gloeopeniophorella convolvens possesses some characteristics of ECM genomes (e.g., loss of some PCWDEs, TE expansion, reduction in secondary metabolism clusters). Functional specialization in ectomycorrhizal decomposition may drive diversification. Accelerated gene evolution predates the evolution of the ECM habit, indicating that changes in genome architecture and gene content may be necessary to prime the evolutionary switch.
- Published
- 2022
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