Root-knot nematode infection of Brassica rapa enhances the performance of a specialist root herbivore via systemically induced responses

·   Herbivores sharing host plants are often separated in time or space, which limits direct interactions between them. Nevertheless, herbivores can influence each other’s performance via systemically induced defence responses. Numerous studies have addressed plant-mediated interactions between aboveground organisms, but examples of such interactions between belowground herbivores are scarce. Considering the large diversity of soil organisms interacting with roots, we postulate that plant-mediated interactions between below-ground herbivores are just as common. We assessed plant-mediated interactions by analysing the performance of Delia radicum larvae feeding on the main root of Brassica rapa, whose fine roots were infected by the root-knot nematode Meloidogyne incognita. Additionally, we studied the influence of M. incognita on D. radicum-induced defence responses and the accumulation of primary and secondary metabolites in the main root. More D. radicum adults emerged from roots of nematode-infected plants, indicating that M. incognita infection facilitates the performance of D. radicum. This enhanced performance on M. incognita-infected plants coincided with a decreased accumulation of aliphatic glucosinolates, an attenuated induction of defence-related phytohormones and an increased accumulation of proteins and two essential amino acids. Combined, our results demonstrate that nematode infection can facilitate D. radicum performance and provide explicit evidence of plant-mediated interactions between belowground organisms via systemically induced responses in the roots.