Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants

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

doi:10.1111/1462-2920.14596

Title: Broad-specificity GH131 β-glucanases are a hallmark of fungi and oomycetes that colonize plants

Journal Article · Mon Mar 18 00:00:00 EDT 2019 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.14596· OSTI ID:1580846

^[1]; Lebrun, Marc‐Henri ^[2]; Haon, Mireille ^[3]; Champion, Charlotte ^[3]; Kohler, Annegret ^[4]; Lenfant, Nicolas ^[5]; Martin, Francis ^[4]; O'Connell, Richard J. ^[2]; Riley, Robert ^[6]; Grigoriev, Igor V. ^[7]; Henrissat, Bernard ^[8]; Berrin, Jean‐Guy ^[3]; Rosso, Marie‐Noëlle ^[3]

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)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; French National Agency for Research; European Commission (EC)

Grant/Contract Number:: AC02-05CH11231; ANR-11-IDEX-0001-02; ANR-14-CE06-0020-01; ANR-13-BIME-000; FP7-26719

OSTI ID:: 1580846

Alternate ID(s):: OSTI ID: 1508178

Journal Information:: Environmental Microbiology, Vol. 21, Issue 8; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 13 works

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