Modulation of above-belowground plant-herbivore interactions by entomopathogenic nematodes

Plants indirectly mediate above-belowground interactions between root- and shoot- herbivores via changes in primary and secondary metabolism. Such effects can cascade up to affect higher trophic level organisms such as predators, however, to what extent predators can in turn influence plant-mediated above-belowground interactions needs to be further elucidated. In this study, we examined the effect of entomopathogenic nematodes (EPNs) (Heterorhabditis bacteriophora and Steinernema carpocapsae) on the interactions between a belowground herbivore, the root-knot nematode (RKN) Meloidogyne arenaria, and an aboveground herbivore, the green-peach aphid Myzus persicae on tobacco (Nicotiana tabacum) plants. We found that the effect of RKNs on aphid population growth and reproduction was negative only when EPNs were inoculated near the rhizosphere. We also observed that the addition of EPNs in the rhizosphere annihilated the positive effect of the aphids on the RKNs feeding on tobacco roots. While aphids and RKNs feeding, respectively, reduced the root and shoot biomass independently of EPNs presence in the rhizosphere, the concentration of glucose and nicotine in tobacco leaves was modified by the presence of EPNs in a species-dependent manner. Our study reveals that tobacco plants detect the presence of EPNs in the rhizosphere and in turn they respond by modifying their interactions with the above- and belowground herbivores. Therefore, soil-dwelling organisms that are not directly associated with the plants can also have community-wide effects that are mediated by changes in plant primary and secondary chemistry.