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Title: 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 tomore » 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.« less
Authors:
 [1] ;  [1] ;  [2] ;  [3] ;  [3] ;  [4] ;  [5] ;  [6] ;  [7] ;  [1] ;  [1] ;  [1] ;  [1] ;  [8] ;  [9] ;  [9] ;  [10] ;  [11] ;  [9] ;  [4] more »;  [6] ;  [12] ;  [13] ;  [3] ;  [1] « less
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. US Dept. of Agriculture (USDA)., Peoria, IL (United States)
  3. Clark Univ., Worcester, MA (United States). Dept. of Biology
  4. Univ. of Minnesota, St. Paul, MN (United States)
  5. Aix-Marseille Univ., Marseille (France). Inst. National de la Recherche Agronomique
  6. Aix-Marseille Univ., Marseille (France). Centre National de la Recherche Scientifique
  7. Inst. National de la Recherche Agronomique (INRA), Champenoux (France). Inst. National de la Recherche Agronomique-Université de Lorraine, Interactions Arbres/Micro-organismes
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States)
  9. Michigan State Univ., East Lansing, MI (United States). DOE Great Lakes Bioenergy Research Center
  10. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  11. Univ. Pública de Navarra, Pamplona (Spain). Dept. de Producción Agraria
  12. Inst. National de la Recherche Agronomique (INRA), Champenoux (France). Inst. National de la Recherche Agronomique-Université de Lorraine, Interactions Arbres/Micro-organismes
  13. USDA Forest Products Lab., Madison, WI (United States)
Publication Date:
Report Number(s):
LBNL-178088
Journal ID: ISSN 0027-8424; ir:178088
Grant/Contract Number:
AC02-05CH11231; FC02-07ER64494
Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 111; Journal Issue: 27; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; lignocellulose; phylogenomics; bioenergy
OSTI Identifier:
1469149

Riley, Robert, Salamov, Asaf A., Brown, Daren W., Nagy, Laszlo G., Floudas, Dimitrios, Held, Benjamin W., Levasseur, Anthony, Lombard, Vincent, Morin, Emmanuelle, Otillar, Robert, Lindquist, Erika A., Sun, Hui, LaButti, Kurt M., Schmutz, Jeremy, Jabbour, Dina, Luo, Hong, Baker, Scott E., Pisabarro, Antonio G., Walton, Jonathan D., Blanchette, Robert A., Henrissat, Bernard, Martin, Francis, Cullen, Dan, Hibbett, David S., and Grigoriev, Igor V.. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. United States: N. p., Web. doi:10.1073/pnas.1400592111.
Riley, Robert, Salamov, Asaf A., Brown, Daren W., Nagy, Laszlo G., Floudas, Dimitrios, Held, Benjamin W., Levasseur, Anthony, Lombard, Vincent, Morin, Emmanuelle, Otillar, Robert, Lindquist, Erika A., Sun, Hui, LaButti, Kurt M., Schmutz, Jeremy, Jabbour, Dina, Luo, Hong, Baker, Scott E., Pisabarro, Antonio G., Walton, Jonathan D., Blanchette, Robert A., Henrissat, Bernard, Martin, Francis, Cullen, Dan, Hibbett, David S., & Grigoriev, Igor V.. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. United States. doi:10.1073/pnas.1400592111.
Riley, Robert, Salamov, Asaf A., Brown, Daren W., Nagy, Laszlo G., Floudas, Dimitrios, Held, Benjamin W., Levasseur, Anthony, Lombard, Vincent, Morin, Emmanuelle, Otillar, Robert, Lindquist, Erika A., Sun, Hui, LaButti, Kurt M., Schmutz, Jeremy, Jabbour, Dina, Luo, Hong, Baker, Scott E., Pisabarro, Antonio G., Walton, Jonathan D., Blanchette, Robert A., Henrissat, Bernard, Martin, Francis, Cullen, Dan, Hibbett, David S., and Grigoriev, Igor V.. 2014. "Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi". United States. doi:10.1073/pnas.1400592111. https://www.osti.gov/servlets/purl/1469149.
@article{osti_1469149,
title = {Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi},
author = {Riley, Robert and Salamov, Asaf A. and Brown, Daren W. and Nagy, Laszlo G. and Floudas, Dimitrios and Held, Benjamin W. and Levasseur, Anthony and Lombard, Vincent and Morin, Emmanuelle and Otillar, Robert and Lindquist, Erika A. and Sun, Hui and LaButti, Kurt M. and Schmutz, Jeremy and Jabbour, Dina and Luo, Hong and Baker, Scott E. and Pisabarro, Antonio G. and Walton, Jonathan D. and Blanchette, Robert A. and Henrissat, Bernard and Martin, Francis and Cullen, Dan and Hibbett, David S. and Grigoriev, Igor V.},
abstractNote = {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.},
doi = {10.1073/pnas.1400592111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 27,
volume = 111,
place = {United States},
year = {2014},
month = {6}
}