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

Abstract

Summary 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.

Multi‐omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring

“…The M . importuna SCYDJ1‐A1 genome possesses two copies of GH131 gene, a hallmark of plant‐tissue‐colonizing fungi (Anasontzis et al ., ), but none was likely expressed as an enzymatic protein during ENB decomposition, although their transcriptions were indeed observed.…”

“…The high transcription of chitin metabolism-related genes at day 15 might reflect early colonization of ENB by morel mycelium. The M. importuna SCYDJ1-A1 genome possesses two copies of GH131 gene, a hallmark of plant-tissue-colonizing fungi (Anasontzis et al, 2019), but none was likely expressed as an enzymatic protein during ENB decomposition, although their transcriptions were indeed observed.…”

The ectomycorrhizal basidiomycete Laccaria bicolor releases a GH28 polygalacturonase that plays a key role in symbiosis establishment

“…We previously reported that the symbiosisinduced ß-1,4-endoglucanase LbGH5-CBM1 from L. bicolor, acting on poplar cellulose, mannans and galactomannan, is involved in cell wall remodeling during formation of the Hartig net and this enzyme is required for successful symbiotic fungal colonization of poplar rootlets (Zhang et al, 2018). Also L. bicolor ß-glucanase GH131, active on polysaccharides with β-1,4, β-1,3, and mixed β-1,4/1,3 glucosidic linkages, is induced upon ectomycorrhiza formation (Anasontzis et al, 2019), further strengthening the concept of fungal PCWDEs as fundamental factors in the establishment of symbiotic plant-fungus interactions.…”

Proteomic Analysis of Mycelial Exudates of Ustilaginoidea virens

“…According to the identified proteins, it could be speculated that the exudates were involved in the formation of fungal cell walls, the growth of hyphae, and the formation of spores. Some of these proteins participated in the process of cell wall organization, including glucanases (KDB12613.1 and KDB14267.1) [31,32], glycosidases (KDB12546.1, KDB15368.1, and KDB13423.1) [33,34], mannoprotein (KDB10968.1) [35][36][37], and clock-controlled protein 6 (KDB12449.1) [38]. Glucans is an important component of the fungal cell wall, and is highly dynamic during cell wall morphogenesis.…”