PT  - JOURNAL ARTICLE
AU  - Balakumaran Chandrasekar
AU  - Alan Wanke
AU  - Stephan Wawra
AU  - Pia Saake
AU  - Lisa Mahdi
AU  - Nyasha Charura
AU  - Miriam Neidert
AU  - Milena Malisic
AU  - Meik Thiele
AU  - Murali Dama
AU  - Markus Pauly
AU  - Alga Zuccaro
TI  - Fungi hijack a plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses
AID  - 10.1101/2021.05.10.443455
DP  - 2021 Jan 01
TA  - bioRxiv
PG  - 2021.05.10.443455
4099  - http://biorxiv.org/content/early/2021/05/10/2021.05.10.443455.short
4100  - http://biorxiv.org/content/early/2021/05/10/2021.05.10.443455.full
AB  - 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 (CW) 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, implicating different biological functions. The barley (Hordeum vulgare) β-1,3-endoglucanase HvBGLUII, which belongs to the widely distributed apoplastic glycoside hydrolase 17 family (GH17), releases a conserved β-1,3;1,6-glucan decasaccharide (β-GD) from the EPS matrices of fungi with different lifestyles and taxonomic positions. This low molecular weight β-GD does not activate plant immunity, is resilient to further enzymatic hydrolysis by β-1,3-endoglucanases due to the presence of three β-1,6-linked glucose branches and can scavenge reactive oxygen species. Additionally, exogenous application of β-GD leads to enhanced fungal colonization in barley. Our data highlights the hitherto undescribed capacity of this often overseen fungal EPS layer to act as an outer protective barrier important for fungal accommodation within the hostile environment at the apoplastic plant-microbe interface.Significance Here we identify and characterize a conserved β-1,3;1,6-glucan decasaccharide with antioxidant activity released from the fungal extracellular polysaccharide (EPS) matrix by the activity of a plant apoplastic endoglucanase. In addition, we provide a quantitative proteomic analysis of the fungal EPS and cell wall (CW) layers.The fungal extracellular polysaccharide (EPS) matrix and the cell wall (CW) are specific layers with distinct protein and carbohydrate signaturesA conserved β-1,3;1,6-glucan decasaccharide (β-GD) is released from the EPS matrices of different fungi by the activity of the barley β-1,3-endoglucanase BGLUII, a member of the widely distributed apoplastic GH17 familyThe β-GD efficiently scavenges reactive oxygen species (ROS) and enhances fungal colonizationThe immunomodulatory potential as microbe-associated molecular pattern (MAMP) as well as the biochemical activity as ROS scavenger of soluble low molecular weight β-glucans are defined by the presence of β-1,6-glucose branchesCompeting Interest StatementThe authors have declared no competing interest.