Entomopathogenic Nematodes-Killed Insect Cadavers in the Rhizosphere Activate Plant Direct and Indirect Defences Aboveground

Plants can perceive and respond to external stimuli by activating both direct and indirect defences against herbivores. Soil-dwelling entomopathogenic nematodes (EPNs), natural enemies of root-feeding herbivores, carry symbiotic bacteria that grow and reproduce once inside arthropod hosts. We hypothesized that the metabolites produced by EPN-infected insect cadavers could be perceived by plants, thereby activating plant defences systemically. We tested this hypothesis by adding three EPN-infected Galleria mellonella cadavers to maize plants and testing plant responses against a major maize pest (Spodoptera frugiperda) and one of its parasitoids (Trichogramma dendrolimi). We found that S. frugiperda females deposited fewer, and caterpillars fed less on maize plants growing near EPN-infected cadavers than on control plants. Accordingly, EPN-infected cadavers triggered the systemic accumulation of defence hormones (SA), genes (PR1), and enzymes (SOD, POD, and CAT) in maize leaves. Furthermore, four volatile organic compounds produced by plants exposed to EPN-infected cadavers deterred S. frugiperda caterpillars and female adults. However, these compounds were more attractive to T. dendrolimi parasitoids. Our study enhances the understanding of the intricate relationships within the above- and belowground ecosystems and provides crucial insights for advancing sustainable pest management strategies.