Chandrasekar, Balakumaran ORCID: 0000-0001-5696-6777, Wanke, Alan, Wawra, Stephan ORCID: 0000-0001-8555-1618, Saake, Pia, Mahdi, Lisa, Charura, Nyasha, Neidert, Miriam, Poschmann, Gereon, Malisic, Milena, Thiele, Meik, Stuehler, Kai, Dama, Murali, Pauly, Markus ORCID: 0000-0002-3116-2198 and Zuccaro, Alga ORCID: 0000-0002-8026-0114 (2022). Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging beta-glucan decasaccharide to subvert immune responses. Plant Cell, 34 (7). S. 2765 - 2785. CARY: OXFORD UNIV PRESS INC. ISSN 1532-298X

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Abstract

Plant pathogenic and beneficial fungi have evolved several strategies to evade immunity and cope with host-derived hydrolytic enzymes and oxidative stress in the apoplast, the extracellular space of plant tissues. Fungal hyphae are surrounded by an inner insoluble cell wall layer and an outer soluble extracellular polysaccharide (EPS) matrix. Here, we show by proteomics and glycomics that these two layers have distinct protein and carbohydrate signatures, and hence likely have different biological functions. The barley (Hordeum vulgare) beta-1,3-endoglucanase HvBGLUII, which belongs to the widely distributed apoplastic glycoside hydrolase 17 family (GH17), releases a conserved beta-1,3;1,6-glucan decasaccharide (beta-GD) from the EPS matrices of fungi with different lifestyles and taxonomic positions. This low molecular weight beta-GD does not activate plant immunity, is resilient to further enzymatic hydrolysis by beta-1,3-endoglucanases due to the presence of three beta-1,6-linked glucose branches and can scavenge reactive oxygen species. Exogenous application of beta-GD leads to enhanced fungal colonization in barley, confirming its role in the fungal counter-defensive strategy to subvert host immunity. Our data highlight the hitherto undescribed capacity of this often-overlooked EPS matrix from plant-associated fungi to act as an outer protective barrier important for fungal accommodation within the hostile environment at the apoplastic plant-microbe interface. A beta-1,3;1,6-glucan decasaccharide released from the fungal matrix by an apoplastic host hydrolase contributes to plant immune suppression and fungal accommodation.

Item Type: Journal Article
Creators:
CreatorsEmailORCIDORCID Put Code
Chandrasekar, BalakumaranUNSPECIFIEDorcid.org/0000-0001-5696-6777UNSPECIFIED
Wanke, AlanUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Wawra, StephanUNSPECIFIEDorcid.org/0000-0001-8555-1618UNSPECIFIED
Saake, PiaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Mahdi, LisaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Charura, NyashaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Neidert, MiriamUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Poschmann, GereonUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Malisic, MilenaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Thiele, MeikUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Stuehler, KaiUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Dama, MuraliUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Pauly, MarkusUNSPECIFIEDorcid.org/0000-0002-3116-2198UNSPECIFIED
Zuccaro, AlgaUNSPECIFIEDorcid.org/0000-0002-8026-0114UNSPECIFIED
URN: urn:nbn:de:hbz:38-681242
DOI: 10.1093/plcell/koac114
Journal or Publication Title: Plant Cell
Volume: 34
Number: 7
Page Range: S. 2765 - 2785
Date: 2022
Publisher: OXFORD UNIV PRESS INC
Place of Publication: CARY
ISSN: 1532-298X
Language: English
Faculty: Unspecified
Divisions: Unspecified
Subjects: no entry
Uncontrolled Keywords:
KeywordsLanguage
CELL-WALL; MOLECULAR-PATTERNS; PROTEINS; RECOGNITION; PERCEPTION; ANTIOXIDANT; ELICITORS; RECEPTOR; DOMAINMultiple languages
Biochemistry & Molecular Biology; Plant Sciences; Cell BiologyMultiple languages
URI: http://kups.ub.uni-koeln.de/id/eprint/68124

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