Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses

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.

Automated summary

Plant pathogenic and beneficial fungi have evolved strategies to resist plant immune response. The different layers of fungal cell wall and extracellular polysaccharide matrix have different functions. A low molecular weight β-glucan decasaccharide released by plant hydrolase plays an important role in fungal adaption and suppression of plant immunity.