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Title: 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 tissuemore » colonization by symbionts, pathogens and saprobes.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [4];  [5];  [4];  [2];  [6];  [7];  [8];  [3];  [3]
  1. French National Institute for Agricultural Research (INRA), Paris (France); Aix-Marseille Univ., Marseille (France); French National Centre for Scientific Research (CNRS), Paris (France);
  2. French National Institute for Agricultural Research (INRA), Paris (France); AgroParis Tech, Paris (France); Univ. Paris-Saclay, Gif-sur-Yvette (France); BIOGER, Thiverval-Grignon (France)
  3. French National Institute for Agricultural Research (INRA), Paris (France); Aix-Marseille Univ., Marseille (France). Fungal Biodiversity and Biotechnology Lab.
  4. 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)
  5. French National Centre for Scientific Research (CNRS), Paris (France); Aix-Marseille Univ., Marseille (France)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States). Dept.of Plant and Microbial Biology
  8. 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 Lab. (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:
Journal Article: 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},
url = {https://www.osti.gov/biblio/1580846}, journal = {Environmental Microbiology},
issn = {1462-2912},
number = 8,
volume = 21,
place = {United States},
year = {2019},
month = {3}
}

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