skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

Journal Article · · Fungal Genetics and Biology
 [1];  [2];  [3];  [4];  [5];  [5]; ORCiD logo [5];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [6];  [7];  [2];  [3];  [5];  [8]
  1. Clark Univ., Worcester, MA (United States); MEMEG, Lund (Sweden)
  2. Univ. of Minnesota, Minneapolis, MN (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Clark Univ., Worcester, MA (United States); Biological Research Centre of the Hungarian Academy of Sciences, Szeged (Hungary)
  5. Indiana Univ.-Purdue Univ., Indianapolis, IN (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of Utrecht (Netherlands)
  7. Univ. of Goettingen (Germany)
  8. Clark Univ., Worcester, MA (United States)

Wood decay mechanisms in Agaricomycotina have been traditionally separated in two categories termed white and brown rot. Recently the accuracy of such a dichotomy has been questioned. In this paper, we present the genome sequences of the white-rot fungus Cylindrobasidium torrendii and the brown-rot fungus Fistulina hepatica both members of Agaricales, combining comparative genomics and wood decay experiments. C. torrendii is closely related to the white-rot root pathogen Armillaria mellea, while F. hepatica is related to Schizophyllum commune, which has been reported to cause white rot. Our results suggest that C. torrendii and S. commune are intermediate between white-rot and brown-rot fungi, but at the same time they show characteristics of decay that resembles soft rot. Both species cause weak wood decay and degrade all wood components but leave the middle lamella intact. Their gene content related to lignin degradation is reduced, similar to brown-rot fungi, but both have maintained a rich array of genes related to carbohydrate degradation, similar to white-rot fungi. These characteristics appear to have evolved from white-rot ancestors with stronger ligninolytic ability. F. hepatica shows characteristics of brown rot both in terms of wood decay genes found in its genome and the decay that it causes. However, genes related to cellulose degradation are still present, which is a plesiomorphic characteristic shared with its white-rot ancestors. Four wood degradation-related genes, homologs of which are frequently lost in brown-rot fungi, show signs of pseudogenization in the genome of F. hepatica. These results suggest that transition toward a brown-rot lifestyle could be an ongoing process in F. hepatica. Finally, our results reinforce the idea that wood decay mechanisms are more diverse than initially thought and that the dichotomous separation of wood decay mechanisms in Agaricomycotina into white rot and brown rot should be revisited.

Research Organization:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1344454
Alternate ID(s):
OSTI ID: 1233941
Journal Information:
Fungal Genetics and Biology, Vol. 76; ISSN 1087-1845
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 110 works
Citation information provided by
Web of Science

References (93)

Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass journal March 2012
Gene Ontology: tool for the unification of biology journal May 2000
Degradation of cellulose by basidiomycetous fungi journal May 2008
Sequencing and Comparative Analysis of the Straw Mushroom (Volvariella volvacea) Genome journal March 2013
Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte journal April 2006
Amylocorticiales ord. nov. and Jaapiales ord. nov.: Early diverging clades of Agaricomycetidae dominated by corticioid forms journal July 2010
Using GeneWise in the Drosophila Annotation Experiment journal April 2000
Resistance of hardwood vessels to degradation by white rot Basidiomycetes journal September 1988
Degradation of the lignocellulose complex in wood journal December 1995
An Antarctic Hot Spot for Fungi at Shackleton's Historic Hut on Cape Royds journal April 2010
Carbohydrate-binding modules: fine-tuning polysaccharide recognition journal September 2004
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis journal April 2000
Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation journal November 1997
Processive Endoglucanase Active in Crystalline Cellulose Hydrolysis by the Brown Rot Basidiomycete Gloeophyllum trabeum journal May 2005
Genomic and Proteomic Dissection of the Ubiquitous Plant Pathogen, Armillaria mellea : Toward a New Infection Model System journal May 2013
A non-modular type B feruloyl esterase from Neurospora crassa exhibits concentration-dependent substrate inhibition journal March 2003
Pyranose Oxidase, a Major Source of H 2 O 2 during Wood Degradation by Phanerochaete chrysosporium, Trametes versicolor, and Oudemansiella mucida journal July 1994
Characteristics of Gloeophyllum trabeum Alcohol Oxidase, an Extracellular Source of H2O2 in Brown Rot Decay of Wood journal July 2007
A Hybrid Micro–Macroevolutionary Approach to Gene Tree Reconstruction journal March 2006
A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase journal August 1996
Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology journal November 2012
An efficient algorithm for large-scale detection of protein families journal April 2002
Identification of a new member of the dye-decolorizing peroxidase family from Pleurotus ostreatus journal November 2006
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal June 2012
Porodisculus pendulus : systematics, cultural characters, and Canadian records journal February 1997
High-quality draft assemblies of mammalian genomes from massively parallel sequence data journal December 2010
Iron-reducing capacity of low-molecular-weight compounds produced in wood by fungi journal November 2006
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
Oxidation of milled wood lignin with laccase, tyrosinase and horseradish peroxidase journal December 2004
Regioselective oxygenation of fatty acids, fatty alcohols and other aliphatic compounds by a basidiomycete heme-thiolate peroxidase journal October 2011
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family journal April 2010
A critical review of cellobiose dehydrogenases journal March 2000
Transposable Element Dynamics among Asymbiotic and Ectomycorrhizal Amanita Fungi journal June 2014
Heme-thiolate haloperoxidases: versatile biocatalysts with biotechnological and environmental significance journal July 2006
Repbase Update, a database of eukaryotic repetitive elements journal January 2005
Phylogeny of the Pluteaceae (Agaricales, Basidiomycota): taxonomy and character evolution journal January 2011
From genomics to chemical genomics: new developments in KEGG journal January 2006
BLAT---The BLAST-Like Alignment Tool journal March 2002
Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium journal February 2007
Quantitative Changes in Structural Components of Conifer Woods During Decay by White- and Brown-Rot Fungi journal January 1973
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
A modular esterase from Penicillium funiculosum which releases ferulic acid from plant cell walls and binds crystalline cellulose contains a carbohydrate binding module: Modular cinnamoyl esterase from P. funiculosum journal December 2000
Multiple Multi-Copper Oxidase Gene Families in Basidiomycetes – What for? journal April 2011
Identification of genes encoding microbial glucuronoyl esterases journal July 2007
Novel Family of Carbohydrate Esterases, Based on Identification of the Hypocrea jecorina Acetyl Esterase Gene journal December 2008
DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes journal September 2009
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser journal November 2010
Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution journal September 2001
Pectin methylesterases: sequence-structural features and phylogenetic relationships journal September 2004
Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads journal January 2010
Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 journal May 2004
Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion journal February 2009
Phylogenetic placement of Marasmiellus juniperinus journal June 2004
Major clades of Agaricales: a multilocus phylogenetic overview journal November 2006
Reliability Measures for Membrane Protein Topology Prediction Algorithms journal March 2003
Creating the CIPRES Science Gateway for inference of large phylogenetic trees conference November 2010
One hundred and seventeen clades of euagarics journal June 2002
A genome survey of Moniliophthora perniciosa gives new insights into Witches' Broom Disease of cacao journal January 2008
Rhamnogalacturonan acetylesterase elucidates the structure and function of a new family of hydrolases journal April 2000
Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche journal October 2012
Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites journal January 1997
Demethoxylation of [O14CH3]-labelled lignin model compounds by the brown-rot fungi Gloeophyllum trabeum and Poria (Postia) placenta journal November 2007
Cellulolytic Activity and the Taxonomic Position of Selected Brown-Rot Fungi journal January 1979
Genome sequence of the model mushroom Schizophyllum commune journal July 2010
Genomics of wood-degrading fungi journal November 2014
Ecology of ligninolytic fungi associated with leaf litter decomposition journal June 2007
Carbon isotope dynamics during leaf litter decomposition with reference to lignin fractions journal January 2007
Anatomical changes in Syzygium cumuini Linn. wood decayed by two white rot fungi Schizophyllum commune Fries. and Flavodon flavus (Klotzsch) Ryvarden journal June 2011
Feasibility of bioremediation by white-rot fungi journal October 2001
De novo identification of repeat families in large genomes journal June 2005
InterProScan: protein domains identifier journal July 2005
Molecular and structural modeling of the Phanerochaete flavido-alba extracellular laccase reveals its ferroxidase structure journal August 2010
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi journal June 2014
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Cloning and characterization of the Thcut1 gene encoding a cutinase of Trichoderma harzianum T34 journal November 2008
Manganese Oxidation Site in Pleurotus eryngii Versatile Peroxidase:  A Site-Directed Mutagenesis, Kinetic, and Crystallographic Study , journal January 2007
Ab initio Gene Finding in Drosophila Genomic DNA journal April 2000
Variability of Wood Degrading Enzymes of Schizophyllum commune journal January 1980
Dual modes of degradation by Fistulina hepatica in xylem cell walls of Quercus robur journal July 2000
Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus) journal June 2010
A Rapid Bootstrap Algorithm for the RAxML Web Servers journal October 2008
Schizophyllum commune as a Ubiquitous Plant Parasite journal January 2010
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training journal October 2008
Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling journal February 2010
Schizophyllum commune Fr. as a destructive mycoparasite journal July 1978
Only C-2 specific glucose oxidase activity is expressed in ligninolytic cultures of the white rot fungus Phanerochaete chrysosporium journal June 1996
Draft Genome of Omphalotus olearius Provides a Predictive Framework for Sesquiterpenoid Natural Product Biosynthesis in Basidiomycota journal June 2012
Comparison of wood decay among diverse lignicolous fungi journal March 1997
Evidence for cleavage of lignin by a brown rot basidiomycete journal July 2008
Degradation of cellulose by the major endoglucanase produced from the brown-rot fungus Fomitopsis pinicola journal April 2008
Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies journal September 2010

Cited By (2)


Figures / Tables (7)