Giovannoni, M.; Scortica, A.; Scafati, V.; Piccirilli, E.; Sorio, D.; Benedetti, M.; Mattei, B.

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. In vitro, the oxidation of oligogalacturonides and cellodextrins by plant FAD-dependent oligosaccharide-oxidases (OSOXs) suppresses their elicitor activity, 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 that 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. Furthermore, our research shows that certain OSOXs can transfer the electrons from the reducing end of these oligosaccharides to phenolic radicals 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 both plant physiology and green technologies.