Zymoseptoria tritici stealth infection is facilitated by stage-specific downregulation of a β-glucanase

Plant cell walls constitute a major defence barrier against pathogens, although it is unclear how specific cell wall components impact pathogen colonisation. Pathogens secrete cell wall-degrading enzymes (CWDEs) to facilitate plant colonisation, but damaged or infected cells are often a source of cell wall-derived oligosaccharides that trigger host immunity. The mechanisms by which pathogens minimise the release of cell wall-derived oligosaccharides while colonising the host remain to be elucidated. We combined biochemical, molecular, and transcriptomic analyses to functionally characterise a glycoside hydrolase (ZtGH45) from the wheat pathogen Zymoseptoria tritici. ZtGH45 gene is expressed during the necrotrophic phase. At this stage, wheat beta-1,3/1,4-mixed-linked glucan (MLG)-derived oligosaccharides are also accumulated. We show that overexpression of ZtGH45 in Z. tritici enhances hydrolysis of MLG from wheat cell walls, and the released MLG oligosaccharides trigger an immune response in wheat. The results demonstrate that tight regulation of ZtGH45 is critical for the infection process as it prevents early accumulation of MLG oligosaccharides that would prematurely induce host immunity, thereby counterbalancing fungal virulence. We suggest that the balance between plant cell wall degradation by fungal CWDEs and the release of immunogenic wall-derived oligosaccharides governs the outcome of host invasion by pathogens.