Flavonoids as Signals Mediate Plant-nematode Communication Through Regulating Nematode Perceptual Ability

Plant root exudates serve as critical mediators of rhizospheric cross-kingdom interactions. Beneficial microorganisms have been demonstrated to promote plant fitness by re-assembling the soil nematode community, yet the mechanisms by which beneficial microorganisms alter the nematode community remain unclear. This study elucidates the fungal-induced nematode recruitment mechanisms through root exudate signaling. By testing the chemotactic responses of nematodes to 14 primary metabolites in root exudates, we identified low concentrations of flavonoids (Biochanin A, Isoliquiritigenin, and Quercetin) that significantly attract nematodes. Furthermore, transcriptome analysis of nematodes revealed that genes related to olfactory transduction and neural network pathways were activated when these compounds attracted them. Molecular modeling and docking further showed that the three flavonoids were tightly bound to the proteins of the nematode, Deg-3, Y70D2A.1, Lgc-27, and B0207.7, providing supportive data for flavonoids as signaling molecules for nematode recruitment. Finally, soil microcosm experiments revealed that flavonoids can alter soil nematode community composition, increase community diversity, and selectively enrich omnivorous nematodes. Overall, our findings highlight the pivotal role of flavonoids in mediating plant-nematode interactions and guide us toward novel nematode management strategies.