Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants
Abstract
Plant-tissue-colonizing fungi fine-tune the deconstruction of plant-cell walls (PCW) using different sets of enzymes according to their lifestyle. However, some of these enzymes are conserved among fungi with dissimilar lifestyles. In this work, we identified genes from Glycoside Hydrolase family GH131 as commonly expressed during plant-tissue colonization by saprobic, pathogenic and symbiotic fungi. By searching all the publicly available genomes, we found that GH131-coding genes were widely distributed in the Dikarya subkingdom, except in Taphrinomycotina and Saccharomycotina, and in phytopathogenic Oomycetes, but neither other eukaryotes nor prokaryotes. The presence of GH131 in a species was correlated with its association with plants as symbiont, pathogen or saprobe. We propose that GH131-family expansions and horizontal-gene transfers contributed to this adaptation. We analysed the biochemical activities of GH131 enzymes whose genes were upregulated during plant-tissue colonization in a saprobe (Pycnoporus sanguineus), a plant symbiont (Laccaria bicolor) and three hemibiotrophic-plant pathogens (Colletotrichum higginsianum, C. graminicola, Zymoseptoria tritici). These enzymes were all active on substrates with β-1,4, β-1,3 and mixed β-1,4/1,3 glucosidic linkages. Combined with a cellobiohydrolase, GH131 enzymes enhanced cellulose degradation. We propose that secreted GH131 enzymes unlock the PCW barrier and allow further deconstruction by other enzymes during plant tissue colonization by symbionts,more »
- Authors:
-
[1];
- French National Institute for Agricultural Research (INRA), Paris (France); Aix-Marseille Univ., Marseille (France); French National Centre for Scientific Research (CNRS), Paris (France);
- French National Institute for Agricultural Research (INRA), Paris (France); AgroParis Tech, Paris (France); Univ. Paris-Saclay, Gif-sur-Yvette (France); BIOGER, Thiverval-Grignon (France)
- French National Institute for Agricultural Research (INRA), Paris (France); Aix-Marseille Univ., Marseille (France). Fungal Biodiversity and Biotechnology Lab.
- French National Institute for Agricultural Research (INRA), Paris (France); Univ. of Lorraine, Champenoux (France). Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE)
- French National Centre for Scientific Research (CNRS), Paris (France); Aix-Marseille Univ., Marseille (France)
- 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). Dept.of Plant and Microbial Biology
- French National Centre for Scientific Research (CNRS), Paris (France); Aix-Marseille Univ., Marseille (France); French National Institute for Agricultural Research (INRA), Marseille (France)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; French National Agency for Research; European Commission (EC)
- OSTI Identifier:
- 1580846
- Alternate Identifier(s):
- OSTI ID: 1508178
- Grant/Contract Number:
- AC02-05CH11231; ANR-11-IDEX-0001-02; ANR-14-CE06-0020-01; ANR-13-BIME-000; FP7-26719
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 21; Journal Issue: 8; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Anasontzis, George E., Lebrun, Marc‐Henri, Haon, Mireille, Champion, Charlotte, Kohler, Annegret, Lenfant, Nicolas, Martin, Francis, O'Connell, Richard J., Riley, Robert, Grigoriev, Igor V., Henrissat, Bernard, Berrin, Jean‐Guy, and Rosso, Marie‐Noëlle. Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants. United States: N. p., 2019.
Web. doi:10.1111/1462-2920.14596.
Anasontzis, George E., Lebrun, Marc‐Henri, Haon, Mireille, Champion, Charlotte, Kohler, Annegret, Lenfant, Nicolas, Martin, Francis, O'Connell, Richard J., Riley, Robert, Grigoriev, Igor V., Henrissat, Bernard, Berrin, Jean‐Guy, & Rosso, Marie‐Noëlle. Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants. United States. https://doi.org/10.1111/1462-2920.14596
Anasontzis, George E., Lebrun, Marc‐Henri, Haon, Mireille, Champion, Charlotte, Kohler, Annegret, Lenfant, Nicolas, Martin, Francis, O'Connell, Richard J., Riley, Robert, Grigoriev, Igor V., Henrissat, Bernard, Berrin, Jean‐Guy, and Rosso, Marie‐Noëlle. Mon .
"Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants". United States. https://doi.org/10.1111/1462-2920.14596. https://www.osti.gov/servlets/purl/1580846.
@article{osti_1580846,
title = {Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants},
author = {Anasontzis, George E. and Lebrun, Marc‐Henri and Haon, Mireille and Champion, Charlotte and Kohler, Annegret and Lenfant, Nicolas and Martin, Francis and O'Connell, Richard J. and Riley, Robert and Grigoriev, Igor V. and Henrissat, Bernard and Berrin, Jean‐Guy and Rosso, Marie‐Noëlle},
abstractNote = {Plant-tissue-colonizing fungi fine-tune the deconstruction of plant-cell walls (PCW) using different sets of enzymes according to their lifestyle. However, some of these enzymes are conserved among fungi with dissimilar lifestyles. In this work, we identified genes from Glycoside Hydrolase family GH131 as commonly expressed during plant-tissue colonization by saprobic, pathogenic and symbiotic fungi. By searching all the publicly available genomes, we found that GH131-coding genes were widely distributed in the Dikarya subkingdom, except in Taphrinomycotina and Saccharomycotina, and in phytopathogenic Oomycetes, but neither other eukaryotes nor prokaryotes. The presence of GH131 in a species was correlated with its association with plants as symbiont, pathogen or saprobe. We propose that GH131-family expansions and horizontal-gene transfers contributed to this adaptation. We analysed the biochemical activities of GH131 enzymes whose genes were upregulated during plant-tissue colonization in a saprobe (Pycnoporus sanguineus), a plant symbiont (Laccaria bicolor) and three hemibiotrophic-plant pathogens (Colletotrichum higginsianum, C. graminicola, Zymoseptoria tritici). These enzymes were all active on substrates with β-1,4, β-1,3 and mixed β-1,4/1,3 glucosidic linkages. Combined with a cellobiohydrolase, GH131 enzymes enhanced cellulose degradation. We propose that secreted GH131 enzymes unlock the PCW barrier and allow further deconstruction by other enzymes during plant tissue colonization by symbionts, pathogens and saprobes.},
doi = {10.1111/1462-2920.14596},
journal = {Environmental Microbiology},
number = 8,
volume = 21,
place = {United States},
year = {Mon Mar 18 00:00:00 EDT 2019},
month = {Mon Mar 18 00:00:00 EDT 2019}
}
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