A Solanoeclepin A precursor functions as a new rhizosphere signaling molecule recruiting growth-promoting microbes under nitrogen deficiency

Abstract

Solanoeclepin A (SolA) is a triterpenoid exuded from the roots of Solanaceae plants, originally identified as hatching stimulant for plant parasitic cyst nematodes. Assuming that evolution would have selected against the production of such a fitness lowering molecule, we postulated that SolA must serve another, beneficial, role for the plant. In this study, we demonstrate that nitrogen (N) deficiency strongly increases the SolA concentration in tomato root exudate. Moreover, SolA is produced only under non-sterile conditions, indicating that soil microbiota are involved in its production. Time-resolved RNAseq analysis revealed several candidate genes for SolA biosynthesis, which were all upregulated under N deficiency. Transient silencing of two SolA biosynthetic genes (e.g., CYP749A19 and CYP749A20) significantly reduced SolA production. Microbiome analysis on the rhizosphere of these plants demonstrated that the recruitment of beneficial Massilia spp. was inhibited in the transiently silenced plants. Isolation of a Massilia strain, identified as Massilia cellulosiltytica, allowed us to show that it has growth-promoting activity under N deficiency, likely via indole-3-acetic acid production and enhanced N acquisition. Root exudate of N-starved tomato displayed strong chemotactic activity towards this strain. Together, these findings demonstrate that SolA production under N deficiency relies on the interaction between tomato and soil microbiota that convert a plant-produced precursor that is a recruitment signal for beneficial, growth-promoting microbes to SolA, which was hijacked by cyst nematodes as a reliable host presence cue. This dual functionality resembles the microbial transformation of primary into secondary bile acids, important signalling molecules, in the gut of animals, and suggests convergent evolution in host-microbe co-metabolism. Overall, our study positions SolA as a multifunctional signaling molecule in rhizosphere interactions, with potential application for enhancing crop resilience and sustainable pest management.