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Title: Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi

Journal Article · · The ISME Journal
 [1];  [2];  [3];  [3];  [4]; ORCiD logo [5];  [3];  [3];  [6];  [2];  [1]
  1. Clark Univ., Worcester, MA (United States)
  2. US Dept. of Agriculture (USDA), Madison, WI (United States)
  3. Univ. of Minnesota, St. Paul, MN (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Univ. of Toronto, ON (Canada)

Fungi that decay wood have characteristic associations with certain tree species, but the mechanistic bases for these associations are poorly understood. We studied substrate-specific gene expression and RNA editing in six species of wood-decaying fungi from the 'Antrodia clade' (Polyporales, Agaricomycetes) on three different wood substrates (pine, spruce, and aspen) in submerged cultures. We identified dozens to hundreds of substrate-biased genes (i.e., genes that are significantly upregulated in one substrate relative to the other two substrates) in each species, and these biased genes are correlated with their host ranges. Evolution of substrate-biased genes is associated with gene family expansion, gain and loss of genes, and variation in cis- and trans- regulatory elements, rather than changes in protein coding sequences. We also demonstrated widespread RNA editing events in the Antrodia clade, which differ from those observed in the Ascomycota in their distribution, substitution types, and the genomic environment. Moreover, we found that substrates could affect editing positions and frequency, including editing events occurring in mRNA transcribed from wood-decay-related genes. Finally, this work shows the extent to which gene expression and RNA editing differ among species and substrates, and provides clues into mechanisms by which wood-decaying fungi may adapt to different hosts.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1619121
Journal Information:
The ISME Journal, Journal Name: The ISME Journal Journal Issue: 6 Vol. 13; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (80)

Using Weeder, Pscan, and PscanChIP for the Discovery of Enriched Transcription Factor Binding Site Motifs in Nucleotide Sequences: Using Weeder, Pscan, and PscanChIP for the Discovery of Transcription Factor Binding Site Motifs journal September 2014
Sporocarp ontogeny in Panus (Basidiomycotina): evolution and classification journal November 1993
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen journal January 2001
Biodegradative mechanism of the brown rot basidiomycete Gloeophyllum trabeum : evidence for an extracellular hydroquinone-driven fenton reaction journal March 1999
Genome-wide gene expression patterns in dikaryon of the basidiomycete fungus Pleurotus ostreatus journal April 2017
Trade-off between Transcriptome Plasticity and Genome Evolution in Cephalopods journal April 2017
Gene expression divergence recapitulates the developmental hourglass model journal December 2010
Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis journal March 2011
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
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
Optimization of gene expression by natural selection journal January 2009
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
The Secotioid Syndrome journal January 1984
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
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood journal June 2010
MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis journal August 2012
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features journal November 2013
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
Intra and Interspecific Variations of Gene Expression Levels in Yeast Are Largely Neutral: (Nei Lecture, SMBE 2016, Gold Coast) journal May 2017
Divergence of Noncoding Regulatory Elements Explains Gene–Phenotype Differences between Human and Mouse Orthologous Genes journal April 2018
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments journal July 2006
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Gene expression drives local adaptation in humans journal March 2013
Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes journal March 2016
WebLogo: A Sequence Logo Generator journal May 2004
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
Gene Regulation by Transcription Factors and MicroRNAs journal March 2008
Stepwise Modification of a Modular Enhancer Underlies Adaptation in a Drosophila Population journal December 2009
Adaptive Evolution of Pelvic Reduction in Sticklebacks by Recurrent Deletion of a Pitx1 Enhancer journal December 2009
RNA Editing Underlies Temperature Adaptation in K+ Channels from Polar Octopuses journal January 2012
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal June 2012
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
Substrate-Specific Differential Gene Expression and RNA Editing in the Brown Rot Fungus Fomitopsis pinicola journal June 2018
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
Time-Dependent Profiles of Transcripts Encoding Lignocellulose-Modifying Enzymes of the White Rot Fungus Phanerochaete carnosa Grown on Multiple Wood Substrates journal December 2011
De Novo Synthesis of 4,5-Dimethoxycatechol and 2,5-Dimethoxyhydroquinone by the Brown Rot FungusGloeophyllum trabeum journal February 1999
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
Gene ontology analysis for RNA-seq: accounting for selection bias journal January 2010
JACUSA: site-specific identification of RNA editing events from replicate sequencing data journal January 2017
Evolutionary dynamics of host specialization in wood-decay fungi journal August 2018
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy journal August 2015
Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus journal December 2015
How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? journal March 2016
A Neutral Model of Transcriptome Evolution journal May 2004
The Molecular Mechanism of a Cis-Regulatory Adaptation in Yeast journal September 2013
The evolution and adaptation of A-to-I RNA editing journal November 2017
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
The integrative omics of white-rot fungus Pycnoporus coccineus reveals co-regulated CAZymes for orchestrated lignocellulose breakdown journal April 2017
Chemistry and Microscopy of Wood Decay by Some Higher Ascomycetes journal January 1989
Abundant and Selective RNA-Editing Events in the Medicinal Mushroom Ganoderma lucidum journal February 2014
Sporocarp Ontogeny in Panus (Basidiomycotina): Evolution and Classification journal November 1993
Wood-Rotting Fungi of North America journal January 1980
Comparison of Wood Decay among Diverse Lignicolous Fungi journal March 1997
The Secotioid Syndrome journal January 1984
Transcriptome Sequencing and Comparative Analysis of Piptoporus betulinus in Response to Birch Sawdust Induction journal October 2017
Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay 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
The molecular mechanism of a cis-regulatory adaptation in yeast preprint January 2013
Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus collection January 2015
JACUSA: site-specific identification of RNA editing events from replicate sequencing data collection January 2017
Evolutionary dynamics of host specialization in wood-decay fungi collection January 2018