Balancing defense and cooperation: the role of the apoplastic oxidoreductase CELLOX1 in shaping root–fungus communication

Plants interact with a wide spectrum of fungi, ranging from mutualists to pathogens, and the outcome of these associations critically depends on the regulation of immunity. A crucial checkpoint in plant–fungal interactions lies in the perception of specific molecular signals that trigger plant innate immune defenses. Reciprocal cell wall degradation during colonization releases elicitors from microbial (MAMPs, microbe- associated molecular patterns) or plant origin (DAMPs, damage-associated molecular pattern), which activate pattern-triggered immunity (PTI) responses such as transcriptional regulation, reactive oxygen species burst and callose deposition. In Arabidopsis thaliana, the berberine bridge enzyme-like oxidase CELLOX1 oxidizes specific cell-wall derived oligosaccharides, including cellulose-derived cellodextrins and hemicellulose-derived mixed-linked glucans. This reaction impairs their elicitor activity, restrict their use as fungal carbon sources, and generates H₂O₂ as a reaction product, which act as an immune cue per se. Previous studies identified CELLOX1 as a modulator of the trade-off between growth and defense in leaves and seeds. This work demonstrates that CELLOX1 activity extends to the root system, where the enzyme is spatially and dynamically regulated and transcriptional responsive to fungal colonization. Through the analysis of interactions with the beneficial root endophyte Serendipita indica and the necrotrophic pathogen Bipolaris sorokiniana, it is shown that CELLOX1 limits fungal proliferation in both mutualistic and pathogenic contexts, indicating a general role in controlling fungal accommodation. Functional analysis further reveals that CELLOX1 influences immune signaling outputs, uncovering novel mechanisms by which plants coordinate defense activation at the root interface. Collectively, these findings expand the framework of CELLOX1 from foliar and seed context to root tissues, encompassing both pathogenic and mutualistic interactions and establishing it as a pivotal redox-based regulator of plant-fungus interactions and of the growth-defense balance at the root interface.