The contrasting roles of trichome-derived monoterpenes and sesquiterpenes in the interaction of cultivated tomato and potato aphid

Volatile secondary metabolites produced in glandular trichomes of plants are heavily involved in interactions with herbivores. In glandular trichomes of cultivated tomato, Solanum lycopersicum, the characteristic volatiles are primarily a mixture of monoterpenes and a few less abundant sesquiterpenes. These terpenes are derived from the enzymatic activities of three terpene synthases, namely TPS20, TPS9 and TPS12. Here, the performance and choice behavior of potato aphid, Macrosiphum euphorbiae, were studied using two tomato trichome mutants, hairless (hl) and odorless-2 (od-2), and their respective background accessions Alisa Craig and Castlemart. The mutants were confirmed to differ quantitatively in the production of glandular trichome derived terpenes compared to respective controls. Principal component analysis indicated that each performance variable (longevity and fecundity) of wingless aphids determined by non-choice assays was negatively correlated with production of TPS12-derived sesquiterpenes across all tested plants. Adding pure TPS12-derived sesquiterpenes (β-caryophyllene and α-humulene) to artificial feeding diets affected aphid survival, investment of gel saliva and honeydew production. In open Y-track olfactometer assays winged aphids displayed differential choice behaviors to odors from the hl and od-2 mutants compared to controls. Their attraction towards TPS20-derived monoterpenes as well as the dose-dependent repellence by TPS12-derived sesquiterpenes was further confirmed using pure terpene compounds. In summary, TPS20-derived monoterpenes, including β-phellandrene, were involved in orientation by winged aphids, whereas TPS12-derived sesquiterpenes conferred antibiosis and antixenosis resistance to wingless aphids. The identification of contrasting roles of trichome-derived terpenes provides valuable information for developing control strategies of potato aphid.