Glandular trichome-derived sesquiterpenes of wild tomato accessions (Solanum habrochaites) affect aphid performance and feeding behavior

Glandular trichomes of tomato produce a number of secondary metabolites including terpenes that contribute to host plant resistance against pests. While glandular trichomes of cultivated tomato Solanum lycopersicum primarily accumulate a monoterpene blend, those of wild tomato species like Solanum habrochaites produce various sesquiterpenes. Previous studies have shown that glandular trichome derived terpenes in cultivated and wild tomato species have repellent and toxic activity against multiple biting-chewing herbivores. In contrast, considerably less is known about the effect of these glandular trichome derived terpenes on piercing-sucking herbivores such as aphids. Here, we have screened a collection of S. habrochaites accessions representing five chemotypes that produce distinct sets of sesquiterpenes to identify those affecting the potato aphid (Macrosiphum euphorbiae). Non-choice assays demonstrated that the longevity and fecundity of M. euphorbiae was significantly reduced when kept on the leaf surface of S. habrochaites accessions producing β-caryophyllene and α-humulene, or α-santalene, α-bergamotene, and β-bergamotene, respectively. When M. euphorbiae apterae were feeding on artificial diets with added terpene containing leaf dip extracts, the same β-caryophyllene/α-humulene and α-santalene/α-bergamotene/β-bergamotene producing S. habrochaites accessions were found to affect aphid survivorship and feeding behavior as indicated by gel saliva investment and honeydew production. Olfactometer assays revealed that the sesquiterpenes emitted from these S. habrochaites accessions also have repellent activity against M. euphorbiae alatae affecting their choice behavior prior to landing on host plants. Assays performed with pure sesquiterpene compounds and an introgression line carrying respective S. habrochaites terpene biosynthetic genes in the S. lycopersicum background confirmed that β-caryophyllene/α-humulene and α-santalene/α-bergamotene/β-bergamotene were responsible for the observed effects on performance, feeding and choice behavior of M. euphorbiae.

Keywords: Glandular trichomes; Macrosiphum euphorbiae; Potato aphid; Sesquiterpenes; Solanaceae; Solanum habrochaites; Solanum lycopersicum; Tomato.