A GH81-type β-glucan-binding protein enhances colonization by mutualistic fungi in barley

Wanke, Alan, van Boerdonk, Sarah, Mahdi, Lisa Katharina, Wawra, Stephan, Neidert, Miriam, Chandrasekar, Balakumaran, Saake, Pia, Saur, Isabel M. L., Derbyshire, Paul, Holton, Nicholas, Menke, Frank L. H. ORCID: https://orcid.org/0000-0003-2490-4824, Brands, Mathias, Pauly, Markus, Acosta, Ivan F., Zipfel, Cyril and Zuccaro, Alga (2023) A GH81-type β-glucan-binding protein enhances colonization by mutualistic fungi in barley. Current Biology, 33 (23). 5071-5084.E7. ISSN 0960-9822

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Abstract

Cell walls are important interfaces of plant-fungal interactions, acting as robust physical and chemical barriers against invaders. Upon fungal colonization, plants deposit phenolics and callose at the sites of fungal penetration to prevent further fungal progression. Alterations in the composition of plant cell walls significantly impact host susceptibility. Furthermore, plants and fungi secrete glycan hydrolases acting on each other’s cell walls. These enzymes release various sugar oligomers into the apoplast, some of which activate host immunity via surface receptors. Recent characterization of cell walls from plant-colonizing fungi has emphasized the abundance of β-glucans in different cell wall layers, which makes them suitable targets for recognition. To characterize host components involved in immunity against fungi, we performed a protein pull-down with the biotinylated β-glucan laminarin. Thereby, we identified a plant glycoside hydrolase family 81-type glucan-binding protein (GBP) as a β-glucan interactor. Mutation of GBP1 and its only paralog, GBP2, in barley led to decreased colonization by the beneficial root endophytes Serendipita indica and S. vermifera, as well as the arbuscular mycorrhizal fungus Rhizophagus irregularis. The reduction of colonization was accompanied by enhanced responses at the host cell wall, including an extension of callose-containing cell wall appositions. Moreover, GBP mutation in barley also reduced fungal biomass in roots by the hemibiotrophic pathogen Bipolaris sorokiniana and inhibited the penetration success of the obligate biotrophic leaf pathogen Blumeria hordei. These results indicate that GBP1 is involved in the establishment of symbiotic associations with beneficial fungi—a role that has potentially been appropriated by barley-adapted pathogens.

Item Type: Article
Additional Information: Funding information: A.Z., M.P., P.S., I.M.L.S., and B.C. acknowledge support from the Cluster of Excellence on Plant Sciences (CEPLAS) funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy–EXC 2048/1–Project ID: 390686111. A.Z. and L.K.M. acknowledge support from project ZU 263/11-1 (SPP 2125 DECRyPT). A.W., S.v.B., and L.K.M. acknowledge support by the International Max Planck Research School (IMPRS) on “Understanding Complex Plant Traits using Computational and Evolutionary Approaches” and the University of Cologne. I.M.L.S. was funded by the DFG Emmy Noether Programme (SA 4093/1-1). P.D., N.H., F.L.H.M., and C.Z. acknowledge support from the Gatsby Charitable Foundation.
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
Depositing User: LivePure Connector
Date Deposited: 24 Nov 2023 02:19
Last Modified: 06 Dec 2023 02:20
URI: https://ueaeprints.uea.ac.uk/id/eprint/93736
DOI: 10.1016/j.cub.2023.10.048

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