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

Author
item RILEY, ROBERT - Joint Genome Institute
item SALAMOV, ASAF - Joint Genome Institute
item HENRISSAT, BERNARD - Aix-Marseille University
item NAGY, LASZLO - Clark University
item Brown, Daren
item HELD, BENJAMIN - University Of Minnesota
item BAKER, SCOTT - Pacific Northwest National Laboratory
item BLANCHETTE, ROBERT - University Of Minnesota
item BOUSSAU, BASTIEN - University Of California
item DOTY, SHARON - University Of Washington

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/20/2014
Publication Date: 6/23/2014
Citation: Riley, R., Salamov, A., Henrissat, B., Nagy, L., Brown, D.W., Held, B., Baker, S., Blanchette, R., Boussau, B., Doty, S.L., et al. 2014. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proceedings of the National Academy of Sciences. DOI: 10.1073/pnas.1400592111.

Interpretive Summary: Basidiomycetes make up some 37% of the described fungi and are important in forestry, agriculture, medicine, and bioenergy. This research compared the genomic sequences of 35 basidiomycetes with other fungi in order to characterize their genetic diversity and improve understanding of their biology. We determined that 48% of the basidiomycete genes are unique to this group of fungi, with nearly half of those genes (22%) found in only one organism. The large number of unique genes discovered suggests tremendous biological diversity and warrant the continued sequencing of these fungi. Key findings include evidence that the traditional white/brown rot family distinction poorly represents the diversity of wood decaying fungi and that the polyketide synthase gene family, involved in the synthesis of numerous toxins, has an early evolutionary origin and has expanded in brown rot fungi. This research improves understanding of the diversity and metabolic potential of an agriculturally and industrially important group of fungi as well as the evolution and diversity of gene families involved in the production of fungal toxins important to plant pathology and food safety.

Technical Abstract: Fungi of the phylum Basidiomycota (basidiomycetes) make up some 37% of the described fungi and are important in forestry, agriculture, medicine, and bioenergy. This diverse phylum includes symbionts, pathogens, and saprotrophs including the majority of wood decaying and ectomycorrhizal species. To better understand the genetic diversity of this phylum we compared the genomes of 35 basidiomycetes including 6 newly sequenced genomes. These genomes span extremes of genome size, gene number, and repeat content. Analysis of core genes reveals that some 48% of basidiomycete proteins are unique to the phylum with nearly half of those (22%) found in only one organism. Correlations between lifestyle and certain gene families are evident. Phylogenetic patterns of plant biomass-degrading genes in Agaricomycotina suggest a continuum rather than a dichotomy between the white rot and brown rot modes of wood decay. Based on phylogenetically-informed principal component analysis (PCA) of wood decay genes, we predict that that Botryobasidium botryosum and Jaapia argillacea have properties similar to white rot species, although neither has typical ligninolytic class II fungal peroxidases (PODs). This prediction is supported by growth assays in which both fungi exhibit wood decay with white rot-like characteristics. Based on this, we suggest that the white/brown rot dichotomy may be inadequate to describe the full range of wood decaying fungi. Analysis of the rate of discovery of proteins with no or few homologs suggests the value of continued sequencing of basidiomycete fungi.