Title: Substrate-Specific Differential Gene Expression and RNA Editing in the Brown Rot Fungus Fomitopsis pinicola

Journal Article · · Applied and Environmental Microbiology
 [1];  [2];  [3];  [3];  [4];  [5];  [6];  [3];  [3];  [4];  [5];  [3];  [2];  [1];  [7]
  1. Clark Univ., Worcester, MA (United States)
  2. US Dept. of Agriculture (USDA), Madison, WI (United States). Forest Products Lab.
  3. Univ. of Minnesota, St. Paul, MN (United States)
  4. Univ. of Toronto, ON (Canada)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Univ. of Tartu (Estonia)
+ Show Author Affiliations

Wood-decaying fungi tend to have characteristic substrate ranges that partly define their ecological niche. Fomitopsis pinicola is a brown rot species of Polyporales that is reported on 82 species of softwoods and 42 species of hardwoods. We analyzed the gene expression levels and RNA editing profiles of F. pinicola from submerged cultures with ground wood powder (sampled at 5 days) or solid wood wafers (sampled at 10 and 30 days), using aspen, pine, and spruce substrates (aspen was used only in submerged cultures). Fomitopsis pinicola expressed similar sets of wood-degrading enzymes typical of brown rot fungi across all culture conditions and time points. Nevertheless, differential gene expression and RNA editing were observed across all pairwise comparisons of substrates and time points. Genes exhibiting differential expression and RNA editing encode diverse enzymes with known or potential function in brown rot decay, including laccase, benzoquinone reductase, aryl alcohol oxidase, cytochrome P450s, and various glycoside hydrolases. There was no overlap between differentially expressed and differentially edited genes, suggesting that these may provide F. pinicola with independent mechanisms for responding to different conditions. Comparing transcriptomes from submerged cultures and wood wafers, we found that culture conditions had a greater impact on global expression profiles than substrate wood species. In contrast, the suites of genes subject to RNA editing were much less affected by culture conditions. These findings highlight the need for standardization of culture conditions in studies of gene expression in wood-decaying fungi.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1544269
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 16 Vol. 84; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (87)

A study of chemical structure of soft and hardwood and wood polymers by FTIR spectroscopy journal March 1999
Lignin-modifying enzymes in filamentous basidiomycetes - ecological, functional and phylogenetic review journal February 2010
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen journal January 2001
Microbial and Enzymatic Degradation of Wood and Wood Components book January 1990
Recent progress in the chemistry of wood hemicelluloses journal January 1967
Immunogold labeling of an extracellular substance producing hydroxyl radicals in wood degraded by brown-rot fungusTyromyces palustris journal February 2000
Influence of fungal decay by different basidiomycetes on the structural integrity of Norway spruce wood journal July 2008
Molecular identification and functional characterization of cytochrome P450 monooxygenases from the brown-rot basidiomycete Postia placenta journal September 2011
Secretome analysis of Phanerochaete chrysosporium strain CIRM-BRFM41 grown on softwood journal July 2008
Proteomic characterization of lignocellulose-degrading enzymes secreted by Phanerochaete carnosa grown on spruce and microcrystalline cellulose journal March 2010
Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass journal March 2012
Substrate-specific transcription of the enigmatic GH61 family of the pathogenic white-rot fungus Heterobasidion irregulare during growth on lignocellulose journal June 2012
Microarray-based global differential expression profiling of P450 monooxygenases and regulatory proteins for signal transduction pathways in the white rot fungus Phanerochaete chrysosporium journal October 2005
Relationship between production of hydroxyl radicals and degradation of wood, crystalline cellulose, and a lignin-related compound or accumulation of oxalic acid in cultures of brown-rot fungi journal June 2005
Significant levels of extracellular reactive oxygen species produced by brown rot basidiomycetes on cellulose journal October 2002
Mechanisms of wood degradation by brown-rot fungi: chelator-mediated cellulose degradation and binding of iron by cellulose journal April 2001
Cell wall alterations in loblolly pine wood decayed by the white-rot fungus, Ceriporiopsis subvermispora journal March 1997
Hydroxyl radical generation by an extracellular low-molecular-weight substance and phenol oxidase activity during wood degradation by the white-rot basidiomycete Trametes versicolor journal September 1999
Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveal complex mixtures of secreted proteins journal May 2006
Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium journal February 2007
Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii journal March 2015
The Phanerochaete chrysosporium secretome: Database predictions and initial mass spectrometry peptide identifications in cellulose-grown medium journal July 2005
Characterization of a hydroxyl-radical-producing glycoprotein and its presumptive genes from the white-rot basidiomycete Phanerochaete chrysosporium journal February 2007
Role of fungal peroxidases in biological ligninolysis journal June 2008
SignalP 4.0: discriminating signal peptides from transmembrane regions journal September 2011
HISAT: a fast spliced aligner with low memory requirements journal March 2015
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
Development and validation of prognostic index based on autophagy-related genes in patient with head and neck squamous cell carcinoma journal July 2020
ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages journal June 2020
Comparative mitochondrial genome analysis reveals intron dynamics and gene rearrangements in two Trametes species journal January 2021
Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion journal February 2009
Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis journal March 2012
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi journal June 2014
Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta journal September 2016
A-to-I RNA editing is developmentally regulated and generally adaptive for sexual reproduction in Neurospora crassa journal August 2017
Wood-Rotting Fungi of North America journal January 1980
Comparison of wood decay among diverse lignicolous fungi journal March 1997
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes journal March 2001
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes journal March 2001
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) journal January 2016
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features journal November 2013
FungiFun2: a comprehensive online resource for systematic analysis of gene lists from fungal species journal October 2014
RNA Editing During Sexual Development Occurs in Distantly Related Filamentous Ascomycetes journal April 2017
Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities journal December 2015
Expression analysis of extracellular proteins from Phanerochaete chrysosporium grown on different liquid and solid substrates journal September 2007
Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes journal March 2016
The molecular response of the white-rot fungus D ichomitus squalens to wood and non-woody biomass as examined by transcriptome and exoproteome analyses : Molecular response of journal January 2017
Fungal hydroquinones contribute to brown rot of wood journal December 2006
Evidence for cleavage of lignin by a brown rot basidiomycete journal July 2008
Multidimensional NMR analysis reveals truncated lignin structures in wood decayed by the brown rot basidiomycete Postia placenta: Ligninolysis during fungal brown rot of wood journal January 2011
Degradation of cellulose by basidiomycetous fungi journal May 2008
A comparative systems analysis of polysaccharide-elicited responses in Neurospora crassa reveals carbon source-specific cellular adaptations : Fungal polysaccharide-specific responses revealed journal December 2013
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal June 2012
Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium journal April 2010
Gene Expression Patterns of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium Are Influenced by Wood Substrate Composition during Degradation journal May 2016
Significant Alteration of Gene Expression in Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium by Plant Species journal May 2011
Transcriptome and Secretome Analyses of the Wood Decay Fungus Wolfiporia cocos Support Alternative Mechanisms of Lignocellulose Conversion journal April 2016
Characteristics of Gloeophyllum trabeum Alcohol Oxidase, an Extracellular Source of H2O2 in Brown Rot Decay of Wood journal July 2007
New Insights into the Ligninolytic Capability of a Wood Decay Ascomycete journal August 2007
Influence of Populus Genotype on Gene Expression by the Wood Decay Fungus Phanerochaete chrysosporium journal July 2014
Transcriptomic Responses of the Softwood-Degrading White-Rot Fungus Phanerochaete carnosa during Growth on Coniferous and Deciduous Wood journal March 2011
Polyporales Brown Rot Species Fomitopsis pinicola : Enzyme Activity Profiles, Oxalic Acid Production, and Fe 3+ -Reducing Metabolite Secretion journal February 2018
Laccase and Its Role in Production of Extracellular Reactive Oxygen Species during Wood Decay by the Brown Rot Basidiomycete Postia placenta journal February 2010
Temporal Alterations in the Secretome of the Selective Ligninolytic Fungus Ceriporiopsis subvermispora during Growth on Aspen Wood Reveal This Organism's Strategy for Degrading Lignocellulose journal January 2014
Proteomic and Functional Analysis of the Cellulase System Expressed by Postia placenta during Brown Rot of Solid Wood journal September 2011
Time-Dependent Profiles of Transcripts Encoding Lignocellulose-Modifying Enzymes of the White Rot Fungus Phanerochaete carnosa Grown on Multiple Wood Substrates journal December 2011
Pathways for Extracellular Fenton Chemistry in the Brown Rot Basidiomycete Gloeophyllum trabeum journal June 2001
Effect of pH and Oxalate on Hydroquinone-Derived Hydroxyl Radical Formation during Brown Rot Wood Degradation journal October 2003
Degradation of the lignocellulose complex in wood journal December 1995
Comparative genomics of the white-rot fungi, Phanerochaete carnosa and P. chrysosporium, to elucidate the genetic basis of the distinct wood types they colonize journal January 2012
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes journal January 2013
JACUSA: site-specific identification of RNA editing events from replicate sequencing data journal January 2017
Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus journal December 2015
Analysis of the Phlebiopsis gigantea Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood journal December 2014
The integrative omics of white-rot fungus Pycnoporus coccineus reveals co-regulated CAZymes for orchestrated lignocellulose breakdown journal April 2017
Production of 2,5-dimethoxyhydroquinone by the brown-rot fungus Serpula lacrymans to drive extracellular Fenton reaction journal May 2004
Chemistry and Microscopy of Wood Decay by Some Higher Ascomycetes journal January 1989
Wood Decay by Brown-Rot Fungi: Changes in Pore Structure and Cell Wall Volume journal January 1991
Relationship Between Production of Hydroxyl Radicals and Degradation of Wood by the Brown-Rot Fungus, Tyromyces palustris journal January 1997
Abundant and Selective RNA-Editing Events in the Medicinal Mushroom Ganoderma lucidum journal February 2014
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) text January 2016
Wood-Rotting Fungi of North America journal January 1980
Comparison of Wood Decay among Diverse Lignicolous Fungi journal March 1997
Genomewide annotation and comparative genomics of cytochrome P450 monooxygenases (P450s) in the polypore species Bjerkandera adusta , Ganoderma sp. and Phlebia brevispora journal November 2013
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w journal April 2012
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features text January 2013

Cited By (5)

A-to-I mRNA editing in fungi: occurrence, function, and evolution journal October 2018
Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi journal February 2019
FairBase: a comprehensive database of fungal A-to-I RNA editing journal January 2019
Decomposition of spruce wood and release of volatile organic compounds depend on decay type, fungal interactions and enzyme production patterns journal August 2019
Dynamics of the Phanerochaete carnosa transcriptome during growth on aspen and spruce journal November 2018

Similar Records

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Basidiomycetes
RNA editing
decay
lignocellulose
transcriptome