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      Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum

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      Nature Communications
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          Abstract

          The most frequently encountered symbiont on tree roots is the ascomycete Cenococcum geophilum, the only mycorrhizal species within the largest fungal class Dothideomycetes, a class known for devastating plant pathogens. Here we show that the symbiotic genomic idiosyncrasies of ectomycorrhizal basidiomycetes are also present in C. geophilum with symbiosis-induced, taxon-specific genes of unknown function and reduced numbers of plant cell wall-degrading enzymes. C. geophilum still holds a significant set of genes in categories known to be involved in pathogenesis and shows an increased genome size due to transposable elements proliferation. Transcript profiling revealed a striking upregulation of membrane transporters, including aquaporin water channels and sugar transporters, and mycorrhiza-induced small secreted proteins (MiSSPs) in ectomycorrhiza compared with free-living mycelium. The frequency with which this symbiont is found on tree roots and its possible role in water and nutrient transport in symbiosis calls for further studies on mechanisms of host and environmental adaptation.

          Abstract

          The ascomycete Cenococcum geophilum is a beneficial mycorrhizal symbiont found frequently on tree roots. Here the authors use comparative genomics and transcriptomics to define genomic signatures that differentiate the beneficial C. geophilum from its saprotrophic and pathogenic relatives.

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          Most cited references33

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          Genesis: cluster analysis of microarray data.

          A versatile, platform independent and easy to use Java suite for large-scale gene expression analysis was developed. Genesis integrates various tools for microarray data analysis such as filters, normalization and visualization tools, distance measures as well as common clustering algorithms including hierarchical clustering, self-organizing maps, k-means, principal component analysis, and support vector machines. The results of the clustering are transparent across all implemented methods and enable the analysis of the outcome of different algorithms and parameters. Additionally, mapping of gene expression data onto chromosomal sequences was implemented to enhance promoter analysis and investigation of transcriptional control mechanisms.
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            SMURF: Genomic mapping of fungal secondary metabolite clusters.

            Fungi produce an impressive array of secondary metabolites (SMs) including mycotoxins, antibiotics and pharmaceuticals. The genes responsible for their biosynthesis, export, and transcriptional regulation are often found in contiguous gene clusters. To facilitate annotation of these clusters in sequenced fungal genomes, we developed the web-based software SMURF (www.jcvi.org/smurf/) to systematically predict clustered SM genes based on their genomic context and domain content. We applied SMURF to catalog putative clusters in 27 publicly available fungal genomes. Comparison with genetically characterized clusters from six fungal species showed that SMURF accurately recovered all clusters and detected additional potential clusters. Subsequent comparative analysis revealed the striking biosynthetic capacity and variability of the fungal SM pathways and the correlation between unicellularity and the absence of SMs. Further genetics studies are needed to experimentally confirm these clusters. 2010 Elsevier Inc. All rights reserved.
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              Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi.

              Basidiomycota (basidiomycetes) make up 32% of the described fungi and include most wood-decaying species, as well as pathogens and mutualistic symbionts. Wood-decaying basidiomycetes have typically been classified as either white rot or brown rot, based on the ability (in white rot only) to degrade lignin along with cellulose and hemicellulose. Prior genomic comparisons suggested that the two decay modes can be distinguished based on the presence or absence of ligninolytic class II peroxidases (PODs), as well as the abundance of enzymes acting directly on crystalline cellulose (reduced in brown rot). To assess the generality of the white-rot/brown-rot classification paradigm, we compared the genomes of 33 basidiomycetes, including four newly sequenced wood decayers, and performed phylogenetically informed principal-components analysis (PCA) of a broad range of gene families encoding plant biomass-degrading enzymes. The newly sequenced Botryobasidium botryosum and Jaapia argillacea genomes lack PODs but possess diverse enzymes acting on crystalline cellulose, and they group close to the model white-rot species Phanerochaete chrysosporium in the PCA. Furthermore, laboratory assays showed that both B. botryosum and J. argillacea can degrade all polymeric components of woody plant cell walls, a characteristic of white rot. We also found expansions in reducing polyketide synthase genes specific to the brown-rot fungi. Our results suggest a continuum rather than a dichotomy between the white-rot and brown-rot modes of wood decay. A more nuanced categorization of rot types is needed, based on an improved understanding of the genomics and biochemistry of wood decay.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                07 September 2016
                2016
                : 7
                : 12662
                Affiliations
                [1 ]Swiss Federal Research Institute WSL, Forest Dynamics, Zuercherstrasse 111 , 8903 Birmensdorf, Switzerland
                [2 ]INRA, UMR INRA-Université de Lorraine ‘Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, INRA-Nancy , 54280 Champenoux, France
                [3 ]US Department of Energy Joint Genome Institute (JGI) , Walnut Creek, California 94598, USA
                [4 ]Microbiology, Department of Biology, Utrecht University , 3508 TB Utrecht, The Netherlands
                [5 ]University of Bremen, Botany, Leobenerstr. 2 , 28359 Bremen, Germany
                [6 ]CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8 , 3584 CT Utrecht, The Netherlands
                [7 ]Institute of Microbiology and Genetics, Department of Genetics of Eukaryotic Microorganisms, Georg-August-University Göttingen , 37077 Göttingen, Germany
                [8 ]Göttingen Center for Molecular Biosciences (GZMB), Georg-August-University Göttingen , 37077 Göttingen, Germany
                [9 ]Department of Ecology and Evolutionary Biology, University of Michigan , Ann Arbor, Michigan 48109 USA
                [10 ]Centre National de la Recherche Scientifique, UMR 7257 , F-13288 Marseille, France
                [11 ]Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille University , F-13288 Marseille, France
                [12 ]INRA, USC 1408 AFMB , F-13288 Marseille, France
                [13 ]Department of Biological Sciences, King Abdulaziz University , Jeddah 21589, Saudi Arabia
                [14 ]Department of Botany and Plant Pathology, Oregon State University , Corvallis, Oregon 97331 USA
                Author notes
                [*]

                These authors contributed equally to this work

                Author information
                http://orcid.org/0000-0002-7268-972X
                http://orcid.org/0000-0002-4737-3715
                Article
                ncomms12662
                10.1038/ncomms12662
                5023957
                27601008
                4e7ddcad-d5f5-47e2-b9b0-054f5a17d527
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 04 November 2015
                : 21 July 2016
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