Crosstalk between above- and belowground herbivores is mediated by minute metabolic responses of the host Arabidopsis thaliana

Plants are frequently under attack by multiple herbivores and can be infested at their shoots as well as their roots. As a consequence, plant metabolites are readily induced, mediated by phytohormones such as salicylic acid and jasmonic acid. Thereby, cross-talk between signal transduction pathways may occur if different herbivores attack the plant simultaneously. In turn, modifications in the plant metabolic pattern can affect herbivores infesting local and systemic tissue. Here, an integrative approach combining metabolomics and performance experiments was used to study the induction of plant metabolites in Arabidopsis thaliana by the specialist aphid Brevicoryne brassicae feeding on shoots and the generalist nematode Heterodera schachtii infesting root tissue. In contrast to most other studies, low infestation rates typical for the decisive early stages of infestation were used. Moreover, the consequences of induction responses on plant-mediated indirect interactions between these herbivores were investigated. In aphid-treated plants, several metabolites including glucosinolates, important defence compounds of Brassicaceae, were reduced in the shoot, but only minute changes took part in the systemic root tissue. Primary metabolites as well as phytohormones were not altered 3 days post infestation. In contrast, nematodes did not evoke significant metabolic alterations locally or systemically. In accordance, nematode presence did not affect aphid population growth, whereas aphids mediated a considerably reduced nematode infestation. These results demonstrate that plants respond in a very fine-tuned way to different challenges. Although they show only minute systemic responses to low herbivore stress, these changes can have pronounced effects on plant-mediated interactions between herbivores.