Root damage to apple plants by cockchafer larvae induces a change in volatile signals below- and above-ground

Volatile organic compounds (VOCs) mediate communication between plants and insects. Plants under insect herbivore attack release VOCs either at the site of attack or systemically, indicating within-plant communication. Some of these VOCs, which may be induced only upon herbivore attack, recruit parasitoids and predatory insects to feed on the attacking insects. Moreover, some plants are able to ‘eavesdrop’ on herbivore-induced plant volatiles (HIPVs) to prime themselves against impending attack; such eavesdropping exemplifies plant–plant communication. In apple orchards, the beetle Melolontha melolontha L. (Coleoptera: Scarabaeidae) is an important insect pest whose larvae live and feed on roots for about 4 years. In this study, we investigated whether the feeding activity of M. melolontha larvae (1) alters the volatile profile of apple roots, (2) induces the release of HIPVs systemically in the leaves, and (3) whether infested plants communicate to neighbouring non-infested conspecifics through HIPVs. To answer these questions, we collected constitutive VOCs from intact M9 roots as well as M. melolontha larvae-damaged roots using a newly designed ‘rhizobox’, to collect root-released volatiles in situ, without damaging the plant root system. We also collected VOCs from the leaf-bearing shoots of M9 whose roots were under attack by M. melolontha larvae and from shoots of neighbouring non-infested conspecifics. Gas chromatography-mass spectrometry analysis showed that feeding activity of M. melolontha larvae induces the release of specific HIPVs; for instance, camphor was found in the roots only after larvae caused root damage. Melolontha melolontha also induced the systemic release of methyl salicylate and (E,E)-α-farnesene from the leaf-bearing shoots. Methyl salicylate and (E,E)-α-farnesene were also released by the shoots of non-infested neighbouring conspecifics. These phenomena indicate the induction of specific VOCs below- and above-ground upon M. melolontha larvae feeding on apple roots as well as plant–plant communication in apple plants.