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 temporally and spatially separated, limiting direct interactions between them. Nevertheless, they can reciprocally influence each other via systemically induced plant responses, as observed in numerous study systems. In contrast, examples of such plant-mediated interactions between belowground herbivores are scarce, but we postulated that they similarly occur given the large diversity of root-interacting soil organisms. To test this hypothesis, we analyzed the performance of Delia radicum larvae feeding on main roots of Brassica rapa plants whose fine roots were infected by the root-knot nematode Meloidogyne incognita. Simultaneously, we studied the effects of M. incognita on D. radicum-induced defense responses and the accumulation of primary metabolites in the main root. We observed that almost 1.5 times as many D. radicum adults emerged from nematode-infected plants, indicating a facilitation effect of M. incognita infection. Although we observed increases in the accumulation of proteins and two essential amino-acids, the strongest effect of nematode-infection was visible in the defense response to D. radicum. We observed a 1.5 times higher accumulation of the defense-related phytohormone JA-Ile in response to D. radicum on nematode-infected plants, coinciding with a 75% increase in indole glucosinolate concentrations. Contrastingly, concentrations of aliphatic glucosinolates, secondary metabolites negatively affecting D. radicum, were 10-25% lower in nematode-infected plants. We hypothesize that the attenuated aliphatic glucosinolate concentrations result from antagonistic interactions between biosynthetic pathways of both glucosinolate classes, which was reflected in the expression of key biosynthesis genes. Our results provide explicit evidence of plant-mediated interactions between belowground organisms via systemically induced responses in roots.