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. 2014 Jul 8;111(27):9923-8.
doi: 10.1073/pnas.1400592111. Epub 2014 Jun 23.

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

Robert Riley  1 , Asaf A Salamov  1 , Daren W Brown  2 , Laszlo G Nagy  3 , Dimitrios Floudas  3 , Benjamin W Held  4 , Anthony Levasseur  5 , Vincent Lombard  6 , Emmanuelle Morin  7 , Robert Otillar  1 , Erika A Lindquist  1 , Hui Sun  1 , Kurt M LaButti  1 , Jeremy Schmutz  8 , Dina Jabbour  9 , Hong Luo  9 , Scott E Baker  10 , Antonio G Pisabarro  11 , Jonathan D Walton  9 , Robert A Blanchette  4 , Bernard Henrissat  6 , Francis Martin  7 , Dan Cullen  12 , David S Hibbett  13 , Igor V Grigoriev  14
Affiliations

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

Robert Riley et al. Proc Natl Acad Sci U S A. .

Erratum in

  • Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14959

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.

Keywords: bioenergy; lignocellulose; phylogenomics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Lignocellulose-degrading and secondary metabolism in wood-decaying fungi. Organisms use the following abbreviations: Aurde, Auricularia delicata; Botbo, Botryobasidium botryosum; Cersu, Ceriporiopsis subvermispora; Conpu, Coniophora puteana; Dacsp, Dacryopinax sp.; Dicsq, Dichomitus squalens; Fomme, Fomitiporia mediterranea; Fompi, Fomitopsis pinicola; Galma, Galerina marginata; Glotr, Gloeophyllum trabeum; Hetan, Heterobasidion annosum; Jaaar, Jaapia argillacea; Phaca, Phanerochaete carnosa; Phchr, Phanerochaete chrysosporium; Pleos, Pleurotus ostreatus; Pospl, Postia placenta; Punst, Punctularia strigosozonata; Schco, Schizophyllum commune; Serla, Serpula lacrymans; Stehi, Stereum hirsutum; Trave, Trametes versicolor; Wolco, Wolfiporia cocos. Gene number is shaded red/white, and independent-contrasts correlation of enzyme with rot type is shaded orange/blue. Notice a strict white/brown-rot dichotomy with respect to the lignin-attacking PODs and the CAZymes that target crystalline cellulose (CBM1, GH6, and GH7), and a continuum with other lignin-targeting enzymes.
Fig. 2.
Fig. 2.
Wood-decaying basidiomycetes plotted on the first two principal components from phylogenetic PCA of CAZymes (including lignin-related auxiliary activities) of the organisms.
Fig. 3.
Fig. 3.
Wood decay experiments indicating mode of decay by Botryobasidium botryosum and Jaapia argillacea. (A) Micrograph of B. botryosum on aspen wood with vessel, fiber, and parenchyma cell walls degraded. Mycelia are visible growing through the voids. (B) Micrograph of J. argillacea on pine showing an area within the wood where the fungus has caused a localized simultaneous decay of the cells. Residual cell wall material and mycelia fill the degraded zone.
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