Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi
Abstract
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.
- Authors:
-
- Clark Univ., Worcester, MA (United States)
- US Dept. of Agriculture (USDA), Madison, WI (United States)
- Univ. of Minnesota, St. Paul, MN (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
- Univ. of Toronto, ON (Canada)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1619121
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 6; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; functional genomics; fungal ecology; molecular evolution
Citation Formats
Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, and Hibbett, David S. Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi. United States: N. p., 2019.
Web. doi:10.1038/s41396-019-0359-2.
Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, & Hibbett, David S. Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi. United States. https://doi.org/10.1038/s41396-019-0359-2
Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, and Hibbett, David S. Mon .
"Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi". United States. https://doi.org/10.1038/s41396-019-0359-2. https://www.osti.gov/servlets/purl/1619121.
@article{osti_1619121,
title = {Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi},
author = {Wu, Baojun and Gaskell, Jill and Zhang, Jiwei and Toapanta, Christina and Ahrendt, Steven and Grigoriev, Igor V. and Blanchette, Robert A. and Schilling, Jonathan S. and Master, Emma and Cullen, Daniel and Hibbett, David S.},
abstractNote = {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.},
doi = {10.1038/s41396-019-0359-2},
journal = {The ISME Journal},
number = 6,
volume = 13,
place = {United States},
year = {Mon Feb 04 00:00:00 EST 2019},
month = {Mon Feb 04 00:00:00 EST 2019}
}
Web of Science
Works referenced in this record:
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006
- Suyama, M.; Torrents, D.; Bork, P.
- Nucleic Acids Research, Vol. 34, Issue Web Server
Sporocarp ontogeny in Panus (Basidiomycotina): evolution and classification
journal, November 1993
- Hibbett, David S.; Murakami, Shigeyuki; Tsuneda, Akihiko
- American Journal of Botany, Vol. 80, Issue 11
Genome-wide gene expression patterns in dikaryon of the basidiomycete fungus Pleurotus ostreatus
journal, April 2017
- Liu, Tianxiang; Li, Huiru; Ding, Yatong
- Brazilian Journal of Microbiology, Vol. 48, Issue 2
Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay
journal, November 2013
- Hori, Chiaki; Gaskell, Jill; Igarashi, Kiyohiko
- Mycologia, Vol. 105, Issue 6
Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta
journal, September 2016
- Zhang, Jiwei; Presley, Gerald N.; Hammel, Kenneth E.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 39
MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis
journal, August 2012
- Kumar, S.; Stecher, G.; Peterson, D.
- Bioinformatics, Vol. 28, Issue 20
Gene Expression Patterns of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium Are Influenced by Wood Substrate Composition during Degradation
journal, May 2016
- Skyba, Oleksandr; Cullen, Dan; Douglas, Carl J.
- Applied and Environmental Microbiology, Vol. 82, Issue 14
The Molecular Mechanism of a Cis-Regulatory Adaptation in Yeast
journal, September 2013
- Chang, Jessica; Zhou, Yiqi; Hu, Xiaoli
- PLoS Genetics, Vol. 9, Issue 9
Degradation of the lignocellulose complex in wood
journal, December 1995
- Blanchette, Robert A.
- Canadian Journal of Botany, Vol. 73, Issue S1
Transcriptome and Secretome Analyses of the Wood Decay Fungus Wolfiporia cocos Support Alternative Mechanisms of Lignocellulose Conversion
journal, April 2016
- Gaskell, Jill; Blanchette, Robert A.; Stewart, Philip E.
- Applied and Environmental Microbiology, Vol. 82, Issue 13
Gene expression divergence recapitulates the developmental hourglass model
journal, December 2010
- Kalinka, Alex T.; Varga, Karolina M.; Gerrard, Dave T.
- Nature, Vol. 468, Issue 7325
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Divergence of Noncoding Regulatory Elements Explains Gene–Phenotype Differences between Human and Mouse Orthologous Genes
journal, April 2018
- Han, Seong Kyu; Kim, Donghyo; Lee, Heetak
- Molecular Biology and Evolution, Vol. 35, Issue 7
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes
journal, March 2001
- Hibbett, David S.; Donoghue, Michael J.
- Systematic Biology, Vol. 50, Issue 2
Evolutionary dynamics of host specialization in wood-decay fungi
journal, August 2018
- Krah, Franz-Sebastian; Bässler, Claus; Heibl, Christoph
- BMC Evolutionary Biology, Vol. 18, Issue 1
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Intra and Interspecific Variations of Gene Expression Levels in Yeast Are Largely Neutral: (Nei Lecture, SMBE 2016, Gold Coast)
journal, May 2017
- Yang, Jian-Rong; Maclean, Calum J.; Park, Chungoo
- Molecular Biology and Evolution, Vol. 34, Issue 9
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
JACUSA: site-specific identification of RNA editing events from replicate sequencing data
journal, January 2017
- Piechotta, Michael; Wyler, Emanuel; Ohler, Uwe
- BMC Bioinformatics, Vol. 18, Issue 1
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
De Novo Synthesis of 4,5-Dimethoxycatechol and 2,5-Dimethoxyhydroquinone by the Brown Rot FungusGloeophyllum trabeum
journal, February 1999
- Paszczynski, Andrzej; Crawford, Ronald; Funk, David
- Applied and Environmental Microbiology, Vol. 65, Issue 2
Fungal hydroquinones contribute to brown rot of wood
journal, December 2006
- Suzuki, Melissa R.; Hunt, Christopher G.; Houtman, Carl J.
- Environmental Microbiology, Vol. 8, Issue 12
Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis
journal, March 2011
- Irie, Naoki; Kuratani, Shigeru
- Nature Communications, Vol. 2, Issue 1
Substrate-Specific Differential Gene Expression and RNA Editing in the Brown Rot Fungus Fomitopsis pinicola
journal, June 2018
- Wu, Baojun; Gaskell, Jill; Held, Benjamin W.
- Applied and Environmental Microbiology, Vol. 84, Issue 16
Stepwise Modification of a Modular Enhancer Underlies Adaptation in a Drosophila Population
journal, December 2009
- Rebeiz, M.; Pool, J. E.; Kassner, V. A.
- Science, Vol. 326, Issue 5960
Pathways for Extracellular Fenton Chemistry in the Brown Rot Basidiomycete Gloeophyllum trabeum
journal, June 2001
- Jensen, K. A.; Houtman, C. J.; Ryan, Z. C.
- Applied and Environmental Microbiology, Vol. 67, Issue 6
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
A-to-I RNA editing is developmentally regulated and generally adaptive for sexual reproduction in Neurospora crassa
journal, August 2017
- Liu, Huiquan; Li, Yang; Chen, Daipeng
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
Gene Regulation by Transcription Factors and MicroRNAs
journal, March 2008
- Hobert, O.
- Science, Vol. 319, Issue 5871
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
- Rytioja, Johanna; Hildén, Kristiina; Di Falco, Marcos
- Environmental Microbiology, Vol. 19, Issue 3
RNA Editing During Sexual Development Occurs in Distantly Related Filamentous Ascomycetes
journal, April 2017
- Teichert, Ines; Dahlmann, Tim A.; Kück, Ulrich
- Genome Biology and Evolution, Vol. 9, Issue 4
Adaptive Evolution of Pelvic Reduction in Sticklebacks by Recurrent Deletion of a Pitx1 Enhancer
journal, December 2009
- Chan, Y. F.; Marks, M. E.; Jones, F. C.
- Science, Vol. 327, Issue 5963
Biodegradative mechanism of the brown rot basidiomycete Gloeophyllum trabeum : evidence for an extracellular hydroquinone-driven fenton reaction
journal, March 1999
- Kerem, Zohar; Jensen, Kenneth A.; Hammel, Kenneth E.
- FEBS Letters, Vol. 446, Issue 1
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012
- Floudas, Dimitrios; Binder, Manfred; Riley, Robert
- Science, Vol. 336, Issue 6089
Gene ontology analysis for RNA-seq: accounting for selection bias
journal, January 2010
- Young, Matthew D.; Wakefield, Matthew J.; Smyth, Gordon K.
- Genome Biology, Vol. 11, Issue 2
RNA Editing Underlies Temperature Adaptation in K+ Channels from Polar Octopuses
journal, January 2012
- Garrett, S.; Rosenthal, J. J. C.
- Science, Vol. 335, Issue 6070
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009
- Robinson, M. D.; McCarthy, D. J.; Smyth, G. K.
- Bioinformatics, Vol. 26, Issue 1
Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes
journal, March 2016
- Liu, Huiquan; Wang, Qinhu; He, Yi
- Genome Research, Vol. 26, Issue 4
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood
journal, June 2010
- Csuos, M.
- Bioinformatics, Vol. 26, Issue 15
Time-Dependent Profiles of Transcripts Encoding Lignocellulose-Modifying Enzymes of the White Rot Fungus Phanerochaete carnosa Grown on Multiple Wood Substrates
journal, December 2011
- MacDonald, Jacqueline; Master, Emma R.
- Applied and Environmental Microbiology, Vol. 78, Issue 5
Effect of pH and Oxalate on Hydroquinone-Derived Hydroxyl Radical Formation during Brown Rot Wood Degradation
journal, October 2003
- Varela, E.; Tien, M.
- Applied and Environmental Microbiology, Vol. 69, Issue 10
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
- Suzuki, Hitoshi; MacDonald, Jacqueline; Syed, Khajamohiddin
- BMC Genomics, Vol. 13, Issue 1
Transcriptome Sequencing and Comparative Analysis of Piptoporus betulinus in Response to Birch Sawdust Induction
journal, October 2017
- Yang, Lixia; Peng, Mu; Shah, Syed
- Forests, Vol. 8, Issue 10
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
A Neutral Model of Transcriptome Evolution
journal, May 2004
- Khaitovich, Philipp; Weiss, Gunter; Lachmann, Michael
- PLoS Biology, Vol. 2, Issue 5
Influence of Populus Genotype on Gene Expression by the Wood Decay Fungus Phanerochaete chrysosporium
journal, July 2014
- Gaskell, Jill; Marty, Amber; Mozuch, Michael
- Applied and Environmental Microbiology, Vol. 80, Issue 18
New Insights into the Ligninolytic Capability of a Wood Decay Ascomycete
journal, August 2007
- Shary, S.; Ralph, S. A.; Hammel, K. E.
- Applied and Environmental Microbiology, Vol. 73, Issue 20
The integrative omics of white-rot fungus Pycnoporus coccineus reveals co-regulated CAZymes for orchestrated lignocellulose breakdown
journal, April 2017
- Miyauchi, Shingo; Navarro, David; Grisel, Sacha
- PLOS ONE, Vol. 12, Issue 4
Abundant and Selective RNA-Editing Events in the Medicinal Mushroom Ganoderma lucidum
journal, February 2014
- Zhu, Yingjie; Luo, Hongmei; Zhang, Xin
- Genetics, Vol. 196, Issue 4
Optimization of gene expression by natural selection
journal, January 2009
- Bedford, T.; Hartl, D. L.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 4
Trade-off between Transcriptome Plasticity and Genome Evolution in Cephalopods
journal, April 2017
- Liscovitch-Brauer, Noa; Alon, Shahar; Porath, Hagit T.
- Cell, Vol. 169, Issue 2
Gene expression drives local adaptation in humans
journal, March 2013
- Fraser, H. B.
- Genome Research, Vol. 23, Issue 7
Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus
journal, December 2015
- Couturier, Marie; Navarro, David; Chevret, Didier
- Biotechnology for Biofuels, Vol. 8, Issue 1
Wood-Rotting Fungi of North America
journal, January 1980
- Gilbertson, Robert L.
- Mycologia, Vol. 72, Issue 1
Chemistry and Microscopy of Wood Decay by Some Higher Ascomycetes
journal, January 1989
- Nilsson, Thomas; Daniel, Geoffrey
- Holzforschung, Vol. 43, Issue 1
Comparison of wood decay among diverse lignicolous fungi
journal, March 1997
- Worrall, James J.; Anagnost, Susan E.; Zabel, Robert A.
- Mycologia, Vol. 89, Issue 2
Transcriptomic Responses of the Softwood-Degrading White-Rot Fungus Phanerochaete carnosa during Growth on Coniferous and Deciduous Wood
journal, March 2011
- MacDonald, Jacqueline; Doering, Matt; Canam, Thomas
- Applied and Environmental Microbiology, Vol. 77, Issue 10
Significant Alteration of Gene Expression in Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium by Plant Species
journal, May 2011
- Vanden Wymelenberg, Amber; Gaskell, Jill; Mozuch, Michael
- Applied and Environmental Microbiology, Vol. 77, Issue 13
Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities
journal, December 2015
- Nagy, László G.; Riley, Robert; Tritt, Andrew
- Molecular Biology and Evolution, Vol. 33, Issue 4
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy
journal, August 2015
- Emms, David M.; Kelly, Steven
- Genome Biology, Vol. 16, Issue 1
How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use?
journal, March 2016
- Schurch, Nicholas J.; Schofield, Pietá; Gierliński, Marek
- RNA, Vol. 22, Issue 6
The evolution and adaptation of A-to-I RNA editing
journal, November 2017
- Yablonovitch, Arielle L.; Deng, Patricia; Jacobson, Dionna
- PLOS Genetics, Vol. 13, Issue 11
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014
- Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
HISAT: a fast spliced aligner with low memory requirements
journal, March 2015
- Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 12, Issue 4
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
- Zambelli, Federico; Pesole, Graziano; Pavesi, Giulio
- Current Protocols in Bioinformatics, Vol. 47, Issue 1
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
- Cingolani, Pablo; Platts, Adrian; Wang, Le Lily
- Fly, Vol. 6, Issue 2
Wood-Rotting Fungi of North America
journal, January 1980
- Gilbertson, Robert L.
- Mycologia, Vol. 72, Issue 1
ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020
- Yin, Jinlong; Kim, Sung Soo; Choi, Eunji
- Nature Communications, Vol. 11, Issue 1
Comparative mitochondrial genome analysis reveals intron dynamics and gene rearrangements in two Trametes species
journal, January 2021
- Chen, Cheng; Li, Qiang; Fu, Rongtao
- Scientific Reports, Vol. 11, Issue 1
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes
journal, March 2001
- Hibbett, David S.; Donoghue, Michael J.
- Systematic Biology, Vol. 50, Issue 2
Sporocarp Ontogeny in Panus (Basidiomycotina): Evolution and Classification
journal, November 1993
- Hibbett, David S.; Murakami, Shigeyuki; Tsuneda, Akihiko
- American Journal of Botany, Vol. 80, Issue 11
Comparison of Wood Decay among Diverse Lignicolous Fungi
journal, March 1997
- Worrall, James J.; Anagnost, Susan E.; Zabel, Robert A.
- Mycologia, Vol. 89, Issue 2
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features
text, January 2013
- Liao, Yang; Smyth, Gordon K.; Shi, Wei
- arXiv
The molecular mechanism of a cis-regulatory adaptation in yeast
preprint, January 2013
- Chang, Jessica; Zhou, Yiqi; Hu, Xiaoli
- arXiv