title: Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists.
abstract: To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall-degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Annegret
authors.initials: A
authors.lastname: Kohler
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Alan
authors.initials: A
authors.lastname: Kuo
authors.affiliation: 1] Department of Biology, Clark University, Worcester, Massachusetts, USA. [2] Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Center, Hungarian Academy of Sciences, Szeged, Hungary.
authors.forename: Laszlo G
authors.initials: LG
authors.lastname: Nagy
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Emmanuelle
authors.initials: E
authors.lastname: Morin
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Kerrie W
authors.initials: KW
authors.lastname: Barry
authors.affiliation: 1] Department of Soil Ecology, Helmholtz Centre for Environmental Research-Helmholtz Zentrum fuer Umweltforschung, Halle, Germany. [2] German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.
authors.forename: Francois
authors.initials: F
authors.lastname: Buscot
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Lund, Sweden.
authors.forename: Björn
authors.initials: B
authors.lastname: Canbäck
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Cindy
authors.initials: C
authors.lastname: Choi
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Cichocki
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Alicia
authors.initials: A
authors.lastname: Clum
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium.
authors.forename: Jan
authors.identifier: 0000000316101861
authors.initials: J
authors.lastname: Colpaert
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Alex
authors.initials: A
authors.lastname: Copeland
authors.affiliation: Departamento de Microbiologia, Bolsista do Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Universidade Federal de Viçosa, Viçosa, Brazil.
authors.forename: Mauricio D
authors.initials: MD
authors.lastname: Costa
authors.affiliation: UMR CNRS 5557, Unité Sous Contrat INRA 1364, Université de Lyon, Université Lyon 1, Villeurbanne, France.
authors.forename: Jeanne
authors.initials: J
authors.lastname: Doré
authors.affiliation: Department of Biology, Clark University, Worcester, Massachusetts, USA.
authors.forename: Dimitrios
authors.initials: D
authors.lastname: Floudas
authors.affiliation: UMR CNRS 5557, Unité Sous Contrat INRA 1364, Université de Lyon, Université Lyon 1, Villeurbanne, France.
authors.forename: Gilles
authors.initials: G
authors.lastname: Gay
authors.affiliation: Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Torino, Italy.
authors.forename: Mariangela
authors.initials: M
authors.lastname: Girlanda
authors.affiliation: 1] CNRS, UMR 7257, Aix-Marseille Université, Marseille, France. [2] Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, Marseille, France. [3] Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: 1] Department of Soil Ecology, Helmholtz Centre for Environmental Research-Helmholtz Zentrum fuer Umweltforschung, Halle, Germany. [2] German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.
authors.forename: Sylvie
authors.initials: S
authors.lastname: Herrmann
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, Norway.
authors.forename: Jaqueline
authors.initials: J
authors.lastname: Hess
authors.affiliation: Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
authors.forename: Nils
authors.initials: N
authors.lastname: Högberg
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Lund, Sweden.
authors.forename: Tomas
authors.initials: T
authors.lastname: Johansson
authors.affiliation: Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Torino, Italy.
authors.forename: Hassine-Radhouane
authors.initials: HR
authors.lastname: Khouja
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Kurt
authors.initials: K
authors.lastname: LaButti
authors.affiliation: Department of Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.
authors.forename: Urs
authors.initials: U
authors.lastname: Lahrmann
authors.affiliation: CNRS, UMR 7257, Aix-Marseille Université, Marseille, France.
authors.forename: Anthony
authors.initials: A
authors.lastname: Levasseur
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Erika A
authors.initials: EA
authors.lastname: Lindquist
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Lipzen
authors.affiliation: UMR CNRS 5557, Unité Sous Contrat INRA 1364, Université de Lyon, Université Lyon 1, Villeurbanne, France.
authors.forename: Roland
authors.initials: R
authors.lastname: Marmeisse
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Torino, Italy.
authors.forename: Elena
authors.initials: E
authors.lastname: Martino
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Claude
authors.initials: C
authors.lastname: Murat
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Chew Y
authors.initials: CY
authors.lastname: Ngan
authors.affiliation: Department of Ecology, Biology/Chemistry, Botany, University of Bremen, Bremen, Germany.
authors.forename: Uwe
authors.initials: U
authors.lastname: Nehls
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Jonathan M
authors.initials: JM
authors.lastname: Plett
authors.affiliation: Harvard Forest, Harvard University, Petersham, Massachusetts, USA.
authors.forename: Anne
authors.identifier: 0000000215266739
authors.initials: A
authors.lastname: Pringle
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Robin A
authors.initials: RA
authors.lastname: Ohm
authors.affiliation: Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Torino, Italy.
authors.forename: Silvia
authors.initials: S
authors.lastname: Perotto
authors.affiliation: Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Forest Dynamics, Birmensdorf, Switzerland.
authors.forename: Martina
authors.initials: M
authors.lastname: Peter
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Robert
authors.initials: R
authors.lastname: Riley
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium.
authors.forename: Francois
authors.initials: F
authors.lastname: Rineau
authors.affiliation: Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium.
authors.forename: Joske
authors.initials: J
authors.lastname: Ruytinx
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Asaf
authors.initials: A
authors.lastname: Salamov
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Lund, Sweden.
authors.forename: Firoz
authors.initials: F
authors.lastname: Shah
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Hui
authors.initials: H
authors.lastname: Sun
authors.affiliation: 1] Department of Soil Ecology, Helmholtz Centre for Environmental Research-Helmholtz Zentrum fuer Umweltforschung, Halle, Germany. [2] German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.
authors.forename: Mika
authors.initials: M
authors.lastname: Tarkka
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Andrew
authors.initials: A
authors.lastname: Tritt
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Claire
authors.initials: C
authors.lastname: Veneault-Fourrey
authors.affiliation: 1] Department of Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany. [2] University of Cologne, Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), Cologne, Germany.
authors.forename: Alga
authors.initials: A
authors.lastname: Zuccaro
authors.affiliation: Department of Biology, Microbial Ecology Group, Lund University, Lund, Sweden.
authors.forename: Anders
authors.initials: A
authors.lastname: Tunlid
authors.affiliation: US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Grigoriev
authors.affiliation: Department of Biology, Clark University, Worcester, Massachusetts, USA.
authors.forename: David S
authors.initials: DS
authors.lastname: Hibbett
authors.affiliation: 1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.
authors.forename: Francis
authors.initials: F
authors.lastname: Martin
mesh_terms: D001483:Base Sequence; D019143:Evolution, Molecular; D017353:Gene Deletion; D015966:Gene Expression Regulation, Fungal / Q000235:genetics; D016681:Genome, Fungal / Q000235:genetics*; D008969:Molecular Sequence Data; D038821:Mycorrhizae / Q000235:genetics* / Q000472:pathogenicity; D010802:Phylogeny; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D018517:Plant Roots / Q000382:microbiology; D012641:Selection, Genetic; D013559:Symbiosis / Q000235:genetics*; D014774:Virulence / Q000235:genetics*