Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Annegret Kohler; Alan Kuo; Laszlo G Nagy; Emmanuelle Morin; Kerrie W Barry; Francois Buscot; Björn Canbäck; Cindy Choi; Nicolas Cichocki; Alicia Clum; Jan Colpaert; Alex Copeland; Mauricio D Costa; Jeanne Doré; Dimitrios Floudas; Gilles Gay; Mariangela Girlanda; Bernard Henrissat; Sylvie Herrmann; Jaqueline Hess; Nils Högberg; Tomas Johansson; Hassine-Radhouane Khouja; Kurt LaButti; Urs Lahrmann; Anthony Levasseur; Erika A Lindquist; Anna Lipzen; Roland Marmeisse; Elena Martino; Claude Murat; Chew Y Ngan; Uwe Nehls; Jonathan M Plett; Anne Pringle; Robin A Ohm; Silvia Perotto; Martina Peter; Robert Riley; Francois Rineau; Joske Ruytinx; Asaf Salamov; Firoz Shah; Hui Sun; Mika Tarkka; Andrew Tritt; Claire Veneault-Fourrey; Alga Zuccaro; Mycorrhizal Genomics Initiative Consortium; Anders Tunlid; Igor V Grigoriev; David S Hibbett; Francis Martin

doi:10.1038/ng.3223

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Nat Genet. 2015 Apr;47(4):410-5. doi: 10.1038/ng.3223. Epub 2015 Feb 23.

Authors

Annegret Kohler¹, Alan Kuo², Laszlo G Nagy³, Emmanuelle Morin¹, Kerrie W Barry², Francois Buscot⁴, Björn Canbäck⁵, Cindy Choi², Nicolas Cichocki¹, Alicia Clum², Jan Colpaert⁶, Alex Copeland², Mauricio D Costa⁷, Jeanne Doré⁸, Dimitrios Floudas⁹, Gilles Gay⁸, Mariangela Girlanda¹⁰, Bernard Henrissat¹¹, Sylvie Herrmann⁴, Jaqueline Hess¹², Nils Högberg¹³, Tomas Johansson⁵, Hassine-Radhouane Khouja¹⁰, Kurt LaButti², Urs Lahrmann¹⁴, Anthony Levasseur¹⁵, Erika A Lindquist², Anna Lipzen², Roland Marmeisse⁸, Elena Martino¹⁶, Claude Murat¹, Chew Y Ngan², Uwe Nehls¹⁷, Jonathan M Plett¹, Anne Pringle¹⁸, Robin A Ohm², Silvia Perotto¹⁰, Martina Peter¹⁹, Robert Riley², Francois Rineau⁶, Joske Ruytinx⁶, Asaf Salamov², Firoz Shah⁵, Hui Sun², Mika Tarkka⁴, Andrew Tritt², Claire Veneault-Fourrey¹, Alga Zuccaro²⁰; Mycorrhizal Genomics Initiative Consortium; Anders Tunlid⁵, Igor V Grigoriev², David S Hibbett⁹, Francis Martin¹

Collaborators

Mycorrhizal Genomics Initiative Consortium:
Marc Buée, Yi Din, Monique Gardes, Gwen Grelet, Hervé Gryta, Patricia Jargeat, Yaron Sitrit, Sabine Zimmermann

Affiliations

¹ 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.
² US Department of Energy Joint Genome Institute (JGI), Walnut Creek, California, USA.
³ 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.
⁴ 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.
⁵ Department of Biology, Microbial Ecology Group, Lund University, Lund, Sweden.
⁶ Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium.
⁷ Departamento de Microbiologia, Bolsista do Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Universidade Federal de Viçosa, Viçosa, Brazil.
⁸ UMR CNRS 5557, Unité Sous Contrat INRA 1364, Université de Lyon, Université Lyon 1, Villeurbanne, France.
⁹ Department of Biology, Clark University, Worcester, Massachusetts, USA.
¹⁰ Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Torino, Italy.
¹¹ 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.
¹² Department of Biosciences, University of Oslo, Oslo, Norway.
¹³ Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
¹⁴ Department of Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.
¹⁵ CNRS, UMR 7257, Aix-Marseille Université, Marseille, France.
¹⁶ 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.
¹⁷ Department of Ecology, Biology/Chemistry, Botany, University of Bremen, Bremen, Germany.
¹⁸ Harvard Forest, Harvard University, Petersham, Massachusetts, USA.
¹⁹ Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Forest Dynamics, Birmensdorf, Switzerland.
²⁰ 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.

PMID: 25706625
DOI: 10.1038/ng.3223

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.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Base Sequence
Evolution, Molecular
Gene Deletion
Gene Expression Regulation, Fungal / genetics
Genome, Fungal / genetics*
Molecular Sequence Data
Mycorrhizae / genetics*
Mycorrhizae / pathogenicity
Phylogeny
Plant Diseases / genetics
Plant Diseases / microbiology
Plant Roots / microbiology
Selection, Genetic*
Symbiosis / genetics*
Virulence / genetics*

Associated data

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