Solanoeclepin C, a root-secreted molecule converted by rhizosphere microbes to hatching factors for potato cyst nematodes.

Abstract

Eclepins are root-secreted compounds that induce the hatching of cyst nematodes. Solanoeclepin A (SEA) and B (SEB) have been isolated as potent hatching factors for potato cyst nematodes (PCNs). SEB is biosynthesized in roots, released into the rhizosphere, and converted into SEA by soil microorganisms. However, given that SEB and SEA exhibit comparable hatching-inducing activity toward PCNs, the ecological significance of microbial solanoeclepin metabolism in eclepin-mediated communication remains unclear. In this study, we identified solanoeclepin C (SEC), a previously unrecognized solanoeclepin secreted by tomato and potato roots. Structural analysis revealed that SEC is an acetylated derivative of SEB. Soil incubation experiments demonstrated that SEC is converted into SEB and subsequently into SEA. SEC exhibits  10 000-fold lower hatching-inducing activity than SEA. Gene expression analysis in hydroponically grown tomatoes showed that solanoeclepin biosynthesis is upregulated under nitrogen and phosphorus deficiencies, with nitrogen starvation having the strongest effect. Our results demonstrate that although SEC itself exhibits low hatching-inducing activity, it is converted by soil microorganisms into SEB and SEA, which are then exploited by PCNs to trigger their hatching. These findings reveal a previously unrecognized three-way interaction among plants, soil microbes, and nematodes mediated by solanoeclepins.