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      Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi.

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          Abstract

          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
          Proc Natl Acad Sci U S A
          Proceedings of the National Academy of Sciences of the United States of America
          Proceedings of the National Academy of Sciences
          1091-6490
          0027-8424
          Jul 08 2014
          : 111
          : 27
          Affiliations
          [1 ] US Department of Energy (DOE) Joint Genome Institute, Walnut Creek, CA 94598;
          [2 ] US Department of Agriculture (USDA), Peoria, IL 61604;
          [3 ] Department of Biology, Clark University, Worcester, MA 01610;
          [4 ] University of Minnesota, St. Paul, MN 55108;
          [5 ] Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1163, Aix-Marseille Université, 13288 Marseille, France;
          [6 ] Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7257, Aix-Marseille Université, 13288 Marseille, France;
          [7 ] Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique-Université de Lorraine, Interactions Arbres/Micro-organismes, 54280 Champenoux, France;
          [8 ] US Department of Energy (DOE) Joint Genome Institute, Walnut Creek, CA 94598;HudsonAlpha Institute of Biotechnology, Huntsville, AL 35806;
          [9 ] DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI 48824;
          [10 ] Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA 99354;
          [11 ] Departamento de Producción Agraria, Universidad Pública de Navarra, 31006 Pamplona, Spain; and.
          [12 ] USDA Forest Products Laboratory, Madison, WI 53726.
          [13 ] Department of Biology, Clark University, Worcester, MA 01610; IVGrigoriev@lbl.gov dhibbett@clarku.edu.
          [14 ] US Department of Energy (DOE) Joint Genome Institute, Walnut Creek, CA 94598; IVGrigoriev@lbl.gov dhibbett@clarku.edu.
          Article
          1400592111
          10.1073/pnas.1400592111
          4103376
          24958869
          201c1fb7-050c-4f79-b453-6dc85ca883b5
          History

          bioenergy,lignocellulose,phylogenomics
          bioenergy, lignocellulose, phylogenomics

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