Natural variation in soybean perception of bacterial quorum-sensing signals shapes primed defense

Abstract

Plants perceive N-acyl homoserine lactones (AHLs), the quorum-sensing signals of rhizobacteria, and can translate them into a primed state of enhanced inducible immunity. Whether this perception-to-defense translation varies heritably among genotypes is largely unknown. Using soybean (Glycine max) responses to N-3-oxo-tetradecanoyl-L-homoserine lactone (oxo-C14-HSL), with root invasion by the nematode Pratylenchus penetrans as a quantitative challenge revealing the primed state, we tested whether AHL-triggered priming is genotype-dependent. Priming with the oxo-C14-HSL-producing rhizobacterium Ensifer meliloti ExpR+ potentiated defense in the responsive cultivar Primus, reducing nematode invasion (P < 0.001), but not in the weakly responsive Sigalia (P = 0.082). The purified molecule reproduced this contrast, localizing the difference to signal transduction within the plant rather than bacterial colonization. Correspondingly, the phytoalexin glyceollin accumulated in a priming- and challenge-dependent manner in Primus but not Sigalia, the formal signature of priming. Across a Sigalia × Primus recombinant inbred line population and an independent diversity panel, responsiveness was heritable, continuously distributed, and transgressive. Two genome-wide association studies and a cross-population meta-analysis converged on a well-calibrated null, indicating a polygenic or strongly environment-dependent architecture rather than a common-variant, large-effect-size model. Translating a bacterial signal into primed defense is thus a quantitatively varying plant trait. Highlight Soybean genotypes differ heritably in their ability to convert a bacterial quorum-sensing signal into primed phytoalexin defense, revealing this translation step as a quantitative, polygenic trait.