Schizophyllum commune has an extensive and functional alternative splicing repertoire
Abstract
Recent genome-wide studies have demonstrated that fungi possess the machinery to alternatively splice pre-mRNA. However, there has not been a systematic categorization of the functional impact of alternative splicing in a fungus. We investigate alternative splicing and its functional consequences in the model mushroom forming fungus Schizophyllum commune. Alternative splicing was demonstrated for 2,285 out of 12,988 expressed genes, resulting in 20% additional transcripts. Intron retentions were the most common alternative splicing events, accounting for 33% of all splicing events, and 43% of the events in coding regions. On the other hand, exon skipping events were rare in coding regions (1%) but enriched in UTRs where they accounted for 57% of the events. Specific functional groups, including transcription factors, contained alternatively spliced genes. Alternatively spliced transcripts were regulated differently throughout development in 19% of the 2,285 alternatively spliced genes. Notably, 69% of alternatively spliced genes have predicted alternative functionality by loss or gain of functional domains, or by acquiring alternative subcellular locations. S. commune exhibits more alternative splicing than any other studied fungus. Finally, taken together, alternative splicing increases the complexity of the S. commune proteome considerably and provides it with a rich repertoire of alternative functionality that is exploitedmore »
- Authors:
-
- Delft Univ. of Technology (Netherlands). Delft Bioinformatics Lab.
- Utrecht Univ., Utrecht (The Netherlands). Microbiology Dept. of Biology
- Delft Univ. of Technology (Netherlands). Delft Bioinformatics Lab.; Broad Inst. of MIT and Harvard, Cambridge, MA (United States)
- Publication Date:
- Research Org.:
- Broad Inst. of MIT and Harvard, Cambridge, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Netherlands Organisation for Scientific Research (NWO)
- OSTI Identifier:
- 1378479
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Fungal genetics; Gene regulation; Protein function predictions; RNA sequencing; RNA splicing
Citation Formats
Gehrmann, Thies, Pelkmans, Jordi F., Lugones, Luis G., Wösten, Han A. B., Abeel, Thomas, and Reinders, Marcel J. T. Schizophyllum commune has an extensive and functional alternative splicing repertoire. United States: N. p., 2016.
Web. doi:10.1038/srep33640.
Gehrmann, Thies, Pelkmans, Jordi F., Lugones, Luis G., Wösten, Han A. B., Abeel, Thomas, & Reinders, Marcel J. T. Schizophyllum commune has an extensive and functional alternative splicing repertoire. United States. https://doi.org/10.1038/srep33640
Gehrmann, Thies, Pelkmans, Jordi F., Lugones, Luis G., Wösten, Han A. B., Abeel, Thomas, and Reinders, Marcel J. T. Fri .
"Schizophyllum commune has an extensive and functional alternative splicing repertoire". United States. https://doi.org/10.1038/srep33640. https://www.osti.gov/servlets/purl/1378479.
@article{osti_1378479,
title = {Schizophyllum commune has an extensive and functional alternative splicing repertoire},
author = {Gehrmann, Thies and Pelkmans, Jordi F. and Lugones, Luis G. and Wösten, Han A. B. and Abeel, Thomas and Reinders, Marcel J. T.},
abstractNote = {Recent genome-wide studies have demonstrated that fungi possess the machinery to alternatively splice pre-mRNA. However, there has not been a systematic categorization of the functional impact of alternative splicing in a fungus. We investigate alternative splicing and its functional consequences in the model mushroom forming fungus Schizophyllum commune. Alternative splicing was demonstrated for 2,285 out of 12,988 expressed genes, resulting in 20% additional transcripts. Intron retentions were the most common alternative splicing events, accounting for 33% of all splicing events, and 43% of the events in coding regions. On the other hand, exon skipping events were rare in coding regions (1%) but enriched in UTRs where they accounted for 57% of the events. Specific functional groups, including transcription factors, contained alternatively spliced genes. Alternatively spliced transcripts were regulated differently throughout development in 19% of the 2,285 alternatively spliced genes. Notably, 69% of alternatively spliced genes have predicted alternative functionality by loss or gain of functional domains, or by acquiring alternative subcellular locations. S. commune exhibits more alternative splicing than any other studied fungus. Finally, taken together, alternative splicing increases the complexity of the S. commune proteome considerably and provides it with a rich repertoire of alternative functionality that is exploited dynamically.},
doi = {10.1038/srep33640},
journal = {Scientific Reports},
number = 1,
volume = 6,
place = {United States},
year = {Fri Sep 23 00:00:00 EDT 2016},
month = {Fri Sep 23 00:00:00 EDT 2016}
}
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Works referenced in this record:
Fungal Alternative Splicing is Associated with Multicellular Complexity and Virulence: A Genome-Wide Multi-Species Study
journal, October 2013
- Grutzmann, K.; Szafranski, K.; Pohl, M.
- DNA Research, Vol. 21, Issue 1
Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation: Regulation of mushroom formation
journal, August 2011
- Ohm, Robin A.; de Jong, Jan F.; de Bekker, Charissa
- Molecular Microbiology, Vol. 81, Issue 6
Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis
journal, January 2014
- Kwon, Young-Ju; Park, Mi-Jeong; Kim, Sang-Gyu
- BMC Plant Biology, Vol. 14, Issue 1
RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum
journal, January 2013
- Zhao, Chunzhao; Waalwijk, Cees; de Wit, Pierre J. G. M.
- BMC Genomics, Vol. 14, Issue 1
An efficient gene deletion procedure for the mushroom-forming basidiomycete Schizophyllum commune
journal, February 2010
- Ohm, Robin A.; de Jong, Jan F.; Berends, Elsa
- World Journal of Microbiology and Biotechnology, Vol. 26, Issue 10
mRNAs Encoding Zinc Finger Protein Isoforms are Expressed by Alternative Splicing of an In-frame Intron in Fission Yeast
journal, January 2000
- Okazaki, K.
- DNA Research, Vol. 7, Issue 1
Widespread Polycistronic Transcripts in Fungi Revealed by Single-Molecule mRNA Sequencing
journal, July 2015
- Gordon, Sean P.; Tseng, Elizabeth; Salamov, Asaf
- PLOS ONE, Vol. 10, Issue 7
Cross-kingdom patterns of alternative splicing and splice recognition
journal, January 2008
- McGuire, Abigail M.; Pearson, Matthew D.; Neafsey, Daniel E.
- Genome Biology, Vol. 9, Issue 3
STAR: ultrafast universal RNA-seq aligner
journal, October 2012
- Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
- Bioinformatics, Vol. 29, Issue 1
Complexity of the Alternative Splicing Landscape in Plants
journal, October 2013
- Reddy, Anireddy S. N.; Marquez, Yamile; Kalyna, Maria
- The Plant Cell, Vol. 25, Issue 10
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010
- Trapnell, Cole; Williams, Brian A.; Pertea, Geo
- Nature Biotechnology, Vol. 28, Issue 5
Genome sequence of the model mushroom Schizophyllum commune
journal, July 2010
- Ohm, Robin A.; de Jong, Jan F.; Lugones, Luis G.
- Nature Biotechnology, Vol. 28, Issue 9
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Alternative splicing and RNA selection pressure — evolutionary consequences for eukaryotic genomes
journal, June 2006
- Xing, Yi; Lee, Christopher
- Nature Reviews Genetics, Vol. 7, Issue 7
An alternative splicing event amplifies evolutionary differences between vertebrates
journal, August 2015
- Gueroussov, S.; Gonatopoulos-Pournatzis, T.; Irimia, M.
- Science, Vol. 349, Issue 6250
InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001
- Zdobnov, E. M.; Apweiler, R.
- Bioinformatics, Vol. 17, Issue 9, p. 847-848
Features of Arabidopsis Genes and Genome Discovered using Full-length cDNAs
journal, January 2006
- Alexandrov, Nickolai N.; Troukhan, Maxim E.; Brover, Vyacheslav V.
- Plant Molecular Biology, Vol. 60, Issue 1
Deep RNA sequencing reveals a high frequency of alternative splicing events in the fungus Trichoderma longibrachiatum
journal, January 2015
- Xie, Bin-Bin; Li, Dan; Shi, Wei-Ling
- BMC Genomics, Vol. 16, Issue 1
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
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
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
Genome-wide analyses of alternative splicing in plants: Opportunities and challenges
journal, July 2008
- Barbazuk, W. B.; Fu, Y.; McGinnis, K. M.
- Genome Research, Vol. 18, Issue 9
Genome-Wide Identification of Evolutionarily Conserved Alternative Splicing Events in Flowering Plants
journal, March 2015
- Chamala, Srikar; Feng, Guanqiao; Chavarro, Carolina
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000
- Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren
- Journal of Molecular Biology, Vol. 300, Issue 4
New Universal Rules of Eukaryotic Translation Initiation Fidelity
journal, July 2013
- Zur, Hadas; Tuller, Tamir
- PLoS Computational Biology, Vol. 9, Issue 7
Identifying and characterising key alternative splicing events in Drosophila development
journal, August 2015
- Lees, Jonathan G.; Ranea, Juan A.; Orengo, Christine A.
- BMC Genomics, Vol. 16, Issue 1
A General Definition and Nomenclature for Alternative Splicing Events
journal, August 2008
- Sammeth, Michael; Foissac, Sylvain; Guigó, Roderic
- PLoS Computational Biology, Vol. 4, Issue 8
The Genome Portal of the Department of Energy Joint Genome Institute
journal, November 2011
- Grigoriev, I. V.; Nordberg, H.; Shabalov, I.
- Nucleic Acids Research, Vol. 40, Issue D1
CFGP: a web-based, comparative fungal genomics platform
journal, December 2007
- Park, J.; Park, B.; Jung, K.
- Nucleic Acids Research, Vol. 36, Issue Database
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011
- Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
- Nature Biotechnology, Vol. 29, Issue 7
Landscape of transcription in human cells
journal, September 2012
- Djebali, Sarah; Davis, Carrie A.; Merkel, Angelika
- Nature, Vol. 489, Issue 7414
Alternative splicing in plants – coming of age
journal, October 2012
- Syed, Naeem H.; Kalyna, Maria; Marquez, Yamile
- Trends in Plant Science, Vol. 17, Issue 10
FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors
journal, February 2008
- Park, J.; Park, J.; Jang, S.
- Bioinformatics, Vol. 24, Issue 7
Ribosome profiling: new views of translation, from single codons to genome scale
journal, January 2014
- Ingolia, Nicholas T.
- Nature Reviews Genetics, Vol. 15, Issue 3
Translation from the 5' untranslated region shapes the integrated stress response
journal, January 2016
- Starck, S. R.; Tsai, J. C.; Chen, K.
- Science, Vol. 351, Issue 6272
Alternative splicing and evolution: diversification, exon definition and function
journal, April 2010
- Keren, Hadas; Lev-Maor, Galit; Ast, Gil
- Nature Reviews Genetics, Vol. 11, Issue 5
Defining the Predicted Protein Secretome of the Fungal Wheat Leaf Pathogen Mycosphaerella graminicola
journal, December 2012
- Morais do Amaral, Alexandre; Antoniw, John; Rudd, Jason J.
- PLoS ONE, Vol. 7, Issue 12
The blue light receptor complex WC-1/2 of Schizophyllum commune is involved in mushroom formation and protection against phototoxicity: White collar complex in Schizophyllum commune
journal, September 2012
- Ohm, Robin A.; Aerts, David; Wösten, Han A. B.
- Environmental Microbiology, Vol. 15, Issue 3
The implications of alternative splicing in the ENCODE protein complement
journal, March 2007
- Tress, M. L.; Martelli, P. L.; Frankish, A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 13
An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs
journal, January 1987
- Kozak, Marilyn
- Nucleic Acids Research, Vol. 15, Issue 20
The odyssey of a regulated transcript
journal, December 2000
- Vilardell, Josep; Chartrand, Pascal; Singer, Robert H.
- RNA, Vol. 6, Issue 12
Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress
journal, April 2015
- Filichkin, Sergei; Priest, Henry D.; Megraw, Molly
- Current Opinion in Plant Biology, Vol. 24
Glucoamylases G1 and G2 from Aspergillus niger are synthesized from two different but closely related mRNAs.
journal, May 1984
- Boel, E.; Hjort, I.; Svensson, B.
- The EMBO Journal, Vol. 3, Issue 5
Widespread Polycistronic Transcripts In Fungi Revealed By Single-Molecule Mrna Sequencing
dataset, January 2016
- Gordon, Sean; Tseng, Elizabeth; Salamov, Asaf
- Zenodo
Alternative translation start sites and hidden coding potential of eukaryotic mRNAs
journal, January 2008
- Kochetov, Alex V.
- BioEssays, Vol. 30, Issue 7
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000
- Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren
- Journal of Molecular Biology, Vol. 300, Issue 4
Features of Arabidopsis Genes and Genome Discovered using Full-length cDNAs
journal, January 2006
- Alexandrov, Nickolai N.; Troukhan, Maxim E.; Brover, Vyacheslav V.
- Plant Molecular Biology, Vol. 60, Issue 1
An efficient gene deletion procedure for the mushroom-forming basidiomycete Schizophyllum commune
journal, February 2010
- Ohm, Robin A.; de Jong, Jan F.; Berends, Elsa
- World Journal of Microbiology and Biotechnology, Vol. 26, Issue 10
Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress
journal, April 2015
- Filichkin, Sergei; Priest, Henry D.; Megraw, Molly
- Current Opinion in Plant Biology, Vol. 24
Alternative splicing in plants – coming of age
journal, October 2012
- Syed, Naeem H.; Kalyna, Maria; Marquez, Yamile
- Trends in Plant Science, Vol. 17, Issue 10
Landscape of transcription in human cells
journal, September 2012
- Djebali, Sarah; Davis, Carrie A.; Merkel, Angelika
- Nature, Vol. 489, Issue 7414
Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011
- Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
- Nature Biotechnology, Vol. 29, Issue 7
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
Targeted therapy for melanoma: rational combinatorial approaches
journal, February 2013
- Kwong, L. N.; Davies, M. A.
- Oncogene, Vol. 33, Issue 1
The implications of alternative splicing in the ENCODE protein complement
journal, March 2007
- Tress, M. L.; Martelli, P. L.; Frankish, A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 13
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Fungal Alternative Splicing is Associated with Multicellular Complexity and Virulence: A Genome-Wide Multi-Species Study
journal, October 2013
- Grutzmann, K.; Szafranski, K.; Pohl, M.
- DNA Research, Vol. 21, Issue 1
An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs
journal, January 1987
- Kozak, Marilyn
- Nucleic Acids Research, Vol. 15, Issue 20
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
CFGP: a web-based, comparative fungal genomics platform
journal, December 2007
- Park, J.; Park, B.; Jung, K.
- Nucleic Acids Research, Vol. 36, Issue Database
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Alternative splicing in the regulation of cholesterol homeostasis
journal, January 2013
- Medina, Marisa W.; Krauss, Ronald M.
- Current Opinion in Lipidology, Vol. 24, Issue 2
An alternative splicing event amplifies evolutionary differences between vertebrates
journal, August 2015
- Gueroussov, S.; Gonatopoulos-Pournatzis, T.; Irimia, M.
- Science, Vol. 349, Issue 6250
Translation from the 5' untranslated region shapes the integrated stress response
journal, January 2016
- Starck, S. R.; Tsai, J. C.; Chen, K.
- Science, Vol. 351, Issue 6272
Phleomycin Increases Transformation Efficiency and Promotes Single Integrations in Schizophyllum commune
journal, December 2008
- van Peer, Arend F.; de Bekker, Charissa; Vinck, Arman
- Applied and Environmental Microbiology, Vol. 75, Issue 5
RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum
journal, January 2013
- Zhao, Chunzhao; Waalwijk, Cees; de Wit, Pierre J. G. M.
- BMC Genomics, Vol. 14, Issue 1
Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis
journal, January 2014
- Kwon, Young-Ju; Park, Mi-Jeong; Kim, Sang-Gyu
- BMC Plant Biology, Vol. 14, Issue 1
Cross-kingdom patterns of alternative splicing and splice recognition
journal, January 2008
- McGuire, Abigail M.; Pearson, Matthew D.; Neafsey, Daniel E.
- Genome Biology, Vol. 9, Issue 3
Deep RNA sequencing reveals a high frequency of alternative splicing events in the fungus Trichoderma longibrachiatum
journal, January 2015
- Xie, Bin-Bin; Li, Dan; Shi, Wei-Ling
- BMC Genomics, Vol. 16, Issue 1
A General Definition and Nomenclature for Alternative Splicing Events
journal, August 2008
- Sammeth, Michael; Foissac, Sylvain; Guigó, Roderic
- PLoS Computational Biology, Vol. 4, Issue 8
New Universal Rules of Eukaryotic Translation Initiation Fidelity
journal, July 2013
- Zur, Hadas; Tuller, Tamir
- PLoS Computational Biology, Vol. 9, Issue 7
Works referencing / citing this record:
Transcription factors of Schizophyllum commune involved in mushroom formation and modulation of vegetative growth
journal, March 2017
- Pelkmans, Jordi F.; Patil, Mohini B.; Gehrmann, Thies
- Scientific Reports, Vol. 7, Issue 1
Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi
journal, March 2019
- Krizsán, Krisztina; Almási, Éva; Merényi, Zsolt
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 15
Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae
journal, June 2019
- Almási, Éva; Sahu, Neha; Krizsán, Krisztina
- New Phytologist, Vol. 224, Issue 2
Bioinformatic Analysis of Genomic and Transcriptomic Variation in Fungi
text, January 2018
- Gehrmann, T.
- Delft University of Technology