Regulation of Root-Knot Nematode Behavior by Seed-Coat Mucilage-Derived Attractants

Seed exudates influence the behavior of soil organisms, but how this occurs remains unclear, particularly for multicellular animals. Here we show that compounds associated with Arabidopsis seed-coat mucilage regulate the behavior of soil-borne animals, specifically root-knot nematodes (RKNs). Infective RKN J2 larvae actively travel toward Arabidopsis seeds through chemotaxis. Analysis of Arabidopsis mucilage mutants demonstrated that the attraction of RKNs to Arabidopsis seeds requires the synthesis and extrusion of seed-coat mucilage. Extracted mucilage alone is not sufficient to attract RKNs, but seed-surface carbohydrates and proteins are required for this process. These findings suggest that the RKN chemoattractant is synthesized de novo upon mucilage extrusion but may be highly unstable. RKNs attracted by this mucilage-dependent mechanism can infect the emerging seedling. However, the attraction signal from seedling roots likely acts independently of the seed-coat signal and may mask the attraction to seed-coat mucilage after germination. Multiple RKN species are attracted by Arabidopsis seeds, suggesting that this mechanism is conserved in RKNs. These findings indicate that seed exudate can regulate the behavior of multicellular animals and highlight the potential roles of seed-coat mucilage in biotic interactions with soil microorganisms.