CELLOX1 orchestrates DAMP-Triggered immunity in root responses to symbiotic and pathogenic fungi

Plants constantly interact with fungi which exert beneficial, neutral, or detrimental effects on their survival. A critical checkpoint in this process is the modulation of plant immune responses. Damage to plant cell walls (CW) triggers the release of damage-associated molecular patterns (DAMPs), which are recognized by the plant and activate immunity. While the role of CW DAMPs towards pathogens is widely characterized, their role towards beneficial fungi remains understudied. In Arabidopsis thaliana, the berberine-bridge enzyme-like CELLOX1 oxidizes the CW DAMPs cellodextrins and mixed-linked glucans, impairing their immunogenicity and thereby regulating immunity. This may enhance resistance to pathogenic fungi by converting these DAMPs into a less digestible carbon source as well as by promoting H2O2 production. Here, we show that CELLOX1 regulates root immunity and influences the interaction with the beneficial fungus Serendipita indica. Loss of CELLOX1 enhances both intra and extra-radical fungal colonization leading to stronger growth-promotion and protection against the pathogen Bipolaris sorokiniana. This is accompanied by increased immune responses and S. indica-induced root cell death. Conversely, CELLOX1 overexpression reduces S. indica colonization, diminishes beneficial effects and weaakens immunity. Our results uncover a novel role for CELLOX1 in fine-tuning root immunity and shaping the outcome of the interaction with beneficial and pathogenic fungi.