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Title: The Transcription Factor Roc1 Is a Key Regulator of Cellulose Degradation in the Wood-Decaying Mushroom Schizophyllum commune

Abstract

Wood-decaying fungi of the class Agaricomycetes (phylum Basidiomycota) are saprotrophs that break down lignocellulose and play an important role in nutrient recycling. They secrete a wide range of extracellular plant cell wall degrading enzymes that break down cellulose, hemicellulose, and lignin, the main building blocks of plant biomass. Although the production of these enzymes is regulated mainly at the transcriptional level, no activating regulators have been identified in any wood-decaying fungus in the class Agaricomycetes. We studied the regulation of cellulase expression in the wood-decaying fungus Schizophyllum commune. Comparative genomics and transcriptomics on two wild isolates revealed a Zn2Cys6-type transcription factor gene (roc1) that was highly upregulated during growth on cellulose, compared to glucose. It is only conserved in the class Agaricomycetes. A roc1 knockout strain showed an inability to grow on medium with cellulose as sole carbon source, and growth on cellobiose and xylan (other components of wood) was inhibited. Growth on non-wood-related carbon sources was not inhibited. Cellulase gene expression and enzyme activity were reduced in the Δroc1 strain. ChIP-Seq identified 1474 binding sites of the Roc1 transcription factor. Promoters of genes involved in lignocellulose degradation were enriched with these binding sites, especially those of LPMO (lytic polysaccharidemore » monooxygenase) CAZymes, indicating that Roc1 directly regulates these genes. A conserved motif was identified as the binding site of Roc1, which was confirmed by a functional promoter analysis. Together, Roc1 is a key regulator of cellulose degradation and the first identified in wood-decaying fungi in the phylum Basidiomycota.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [2];  [2];  [1];  [2];  [3];  [1];  [1];  [2];  [4];  [4];  [1]; ORCiD logo [3];  [1];  [5]; ORCiD logo [6]
  1. Utrecht University (Netherlands)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Korea Univ., Seoul, (Korea, Republic of)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Utrecht University (Netherlands); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); European Research Council (ERC)
OSTI Identifier:
1878514
Grant/Contract Number:  
AC02-05CH11231; 716132
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 13; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ChIP-Seq; comparative genomics; comparative transcriptomics; fungi; gene regulation; lignocellulose degradation

Citation Formats

Marian, Ioana M., Vonk, Peter Jan, Valdes, Ivan D., Barry, Kerrie, Bostock, Benedict, Carver, Akiko, Daum, Chris, Lerner, Harry, Lipzen, Anna, Park, Hongjae, Schuller, Margo B. P., Tegelaar, Martin, Tritt, Andrew, Schmutz, Jeremy, Grimwood, Jane, Lugones, Luis G., Choi, In-Geol, Wösten, Han B., Grigoriev, Igor V., and Ohm, Robin A. The Transcription Factor Roc1 Is a Key Regulator of Cellulose Degradation in the Wood-Decaying Mushroom Schizophyllum commune. United States: N. p., 2022. Web. doi:10.1128/mbio.00628-22.
Marian, Ioana M., Vonk, Peter Jan, Valdes, Ivan D., Barry, Kerrie, Bostock, Benedict, Carver, Akiko, Daum, Chris, Lerner, Harry, Lipzen, Anna, Park, Hongjae, Schuller, Margo B. P., Tegelaar, Martin, Tritt, Andrew, Schmutz, Jeremy, Grimwood, Jane, Lugones, Luis G., Choi, In-Geol, Wösten, Han B., Grigoriev, Igor V., & Ohm, Robin A. The Transcription Factor Roc1 Is a Key Regulator of Cellulose Degradation in the Wood-Decaying Mushroom Schizophyllum commune. United States. https://doi.org/10.1128/mbio.00628-22
Marian, Ioana M., Vonk, Peter Jan, Valdes, Ivan D., Barry, Kerrie, Bostock, Benedict, Carver, Akiko, Daum, Chris, Lerner, Harry, Lipzen, Anna, Park, Hongjae, Schuller, Margo B. P., Tegelaar, Martin, Tritt, Andrew, Schmutz, Jeremy, Grimwood, Jane, Lugones, Luis G., Choi, In-Geol, Wösten, Han B., Grigoriev, Igor V., and Ohm, Robin A. Mon . "The Transcription Factor Roc1 Is a Key Regulator of Cellulose Degradation in the Wood-Decaying Mushroom Schizophyllum commune". United States. https://doi.org/10.1128/mbio.00628-22. https://www.osti.gov/servlets/purl/1878514.
@article{osti_1878514,
title = {The Transcription Factor Roc1 Is a Key Regulator of Cellulose Degradation in the Wood-Decaying Mushroom Schizophyllum commune},
author = {Marian, Ioana M. and Vonk, Peter Jan and Valdes, Ivan D. and Barry, Kerrie and Bostock, Benedict and Carver, Akiko and Daum, Chris and Lerner, Harry and Lipzen, Anna and Park, Hongjae and Schuller, Margo B. P. and Tegelaar, Martin and Tritt, Andrew and Schmutz, Jeremy and Grimwood, Jane and Lugones, Luis G. and Choi, In-Geol and Wösten, Han B. and Grigoriev, Igor V. and Ohm, Robin A.},
abstractNote = {Wood-decaying fungi of the class Agaricomycetes (phylum Basidiomycota) are saprotrophs that break down lignocellulose and play an important role in nutrient recycling. They secrete a wide range of extracellular plant cell wall degrading enzymes that break down cellulose, hemicellulose, and lignin, the main building blocks of plant biomass. Although the production of these enzymes is regulated mainly at the transcriptional level, no activating regulators have been identified in any wood-decaying fungus in the class Agaricomycetes. We studied the regulation of cellulase expression in the wood-decaying fungus Schizophyllum commune. Comparative genomics and transcriptomics on two wild isolates revealed a Zn2Cys6-type transcription factor gene (roc1) that was highly upregulated during growth on cellulose, compared to glucose. It is only conserved in the class Agaricomycetes. A roc1 knockout strain showed an inability to grow on medium with cellulose as sole carbon source, and growth on cellobiose and xylan (other components of wood) was inhibited. Growth on non-wood-related carbon sources was not inhibited. Cellulase gene expression and enzyme activity were reduced in the Δroc1 strain. ChIP-Seq identified 1474 binding sites of the Roc1 transcription factor. Promoters of genes involved in lignocellulose degradation were enriched with these binding sites, especially those of LPMO (lytic polysaccharide monooxygenase) CAZymes, indicating that Roc1 directly regulates these genes. A conserved motif was identified as the binding site of Roc1, which was confirmed by a functional promoter analysis. Together, Roc1 is a key regulator of cellulose degradation and the first identified in wood-decaying fungi in the phylum Basidiomycota.},
doi = {10.1128/mbio.00628-22},
journal = {mBio (Online)},
number = 3,
volume = 13,
place = {United States},
year = {Mon May 23 00:00:00 EDT 2022},
month = {Mon May 23 00:00:00 EDT 2022}
}

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