The reducing end of cell wall oligosaccharides is critical for DAMP activity in Arabidopsis thaliana and can be exploited by oligosaccharide oxidases in the reduction of oxidized phenolics

The enzymatic hydrolysis of cell wall polysaccharides results in the production of oligosaccharides with nature of damage-associated molecular patterns (DAMPs) that are perceived by plants as danger signals. The in vitro oxidation of oligogalacturonides and cellodextrins by plant FAD-dependent oligosaccharide-oxidases (OSOXs) suppresses their elicitor activity in vivo, suggesting a protective role of OSOXs against a prolonged activation of defense responses potentially deleterious for plant health. However, OSOXs are also produced by phytopathogens and saprotrophs, complicating the understanding of their role in plant-microbe interactions. Here, we demonstrate the oxidation catalyzed by specific fungal OSOXs also converts the elicitor-active cello-tetraose and xylo-tetraose into elicitor-inactive forms, indicating that the oxidation state of cell wall oligosaccharides is crucial for their DAMP function, irrespective of whether the OSOX originates from fungi or plants. In addition, we also found that certain OSOXs can transfer the electrons from the reducing end of these oligosaccharides to oxidized phenolics (bi-phenoquinones) instead of molecular O2, highlighting an unexpected sub-functionalization of these enzymes. The activity of OSOXs may be crucial for a thorough understanding of cell wall metabolism since these enzymes can redirect the reducing power from sugars to phenolic components of the plant cell wall, an insight with relevant implications for plant physiology and biotechnology. [Display omitted] •C1-oxidized oligosaccharides have a reduced DAMP activity in A. thaliana.•Fungal OSOXs inactivate cell wall DAMPs similarly to plant OSOXs.•OSOXs can transfer electrons from oligosaccharides to bi-phenoquinones.•Bi-phenoquinones can be converted into oligo-phenols by specific OSOXs.