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Environ Microbiol. 2019 Aug;21(8):2724-2739. doi: 10.1111/1462-2920.14596. Epub 2019 Apr 21.

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

Author information

1
INRA, Aix-Marseille Univ, UMR1163, Biodiversité et Biotechnologie Fongiques, BBF, Marseille, France.
2
CNRS, Aix-Marseille Univ, UMR7257, Architecture et Fonction des Macromolecules Biologiques, Marseille, France.
3
INRA, AgroParisTech, Université Paris-Saclay, BIOGER, Thiverval-Grignon, France.
4
INRA, University of Lorraine, Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France.
5
US Department of Energy Joint Genome Institute (JGI), Walnut Creek, CA, 94598, USA.
6
Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, 94598, USA.
7
INRA, USC 1408, AFMB, Marseille, France.

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. 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.

PMID:
30887618
DOI:
10.1111/1462-2920.14596

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