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One of the responses of plants to insect attack is the production of volatile organic compounds that mediate indirect defence of plants by attracting natural enemies of the attacking herbivores. Herbivore-induced plant volatiles (HIPVs) include terpenoids that play key roles in the attraction of natural enemies. Crosstalk between phytohormonal signalling pathways is well known to affect the regulation of plant defences, including the emission of HIPVs. Thus, simultaneous feeding on the same plant by caterpillars and aphids, can affect the attraction of parasitoids by the plant compared to single insect attack. The role of aphid density in the regulation of HIPV emission by plants under dual attack has not been studied previously. Here, we investigated the attraction of Diadegma semiclausum, a parasitoid of the Diamondback moth Plutella xylostella, to volatiles emitted by Arabidopsis thaliana plants, simultaneously attacked by host caterpillars, and by the non-host aphid Brevicoryne brassicae. Our study shows that the effect of aphid infestation on parasitoid attraction is influenced by the density of the aphids. Biosynthesis and emission of (E,E)-α-farnesene could be linked to the observed preference of D. semiclausum parasitoids for the HIPV blend emitted by plants dually infested by caterpillars and aphids at a high density compared to dually infested plants with a low aphid density. Parasitoids such as D. semiclausum are important enemies of herbivorous insects and a better understanding of how plants express indirect defence mechanisms in response to multiple insect attack will provide important knowledge on plant-herbivore-parasitoid interactions under multiple stress conditions.

Terpenoid biosynthesis in Arabidopsis attacked by caterpillars and aphids: effects of aphid density on the attraction of a caterpillar parasitoid