Glandular Trichome-Derived Mono- and Sesquiterpenes of Tomato Have Contrasting Roles in the Interaction with the Potato Aphid Macrosiphum euphorbiae

Secondary metabolites produced in glandular trichomes of tomato are involved in interactions with herbivores. In cultivated tomato (Solanum lycopersicum) glandular trichomes accumulate a blend of abundant monoterpenes and smaller amounts of a few sesquiterpenes. These mono- and sesquiterpenes are synthesized by three terpene synthases, TPS20 as well as TPS9 and TPS12, respectively. To study effects of these terpenes on performance and choice behavior of potato aphid (Macrosiphum euphorbiae), we utilized two tomato trichome mutants, hairless and odorless-2, that are differently affected in mono- and sesquiterpene production. Non-choice assays demonstrated that longevity and fecundity of M. euphorbiae were increased when kept on the trichome mutants. A principal component analysis of these aphid performance parameters and terpene production in the trichome mutants indicated that longevity and fecundity of M. euphorbiae were negatively correlated with production of the TPS12-derived sesquiterpenes beta-caryophyllene and alpha-humulene. While we had previously shown that addition of pure beta-caryophyllene/alpha-humulene to an artificial feeding diet affected M. euphorbiae apterae survivorship and feeding behavior, no such effects were observed here upon addition of a mixture of pure TPS20-derived monoterpenes. In olfactometer assays M. euphorbiae alates displayed differential choice behaviors towards the hairless and odorless-2 mutants suggesting a role of TPS20-derived monoterpenes in aphid attraction, which was further confirmed using a mixture of pure monoterpenes. Our analyses revealed contrasting roles of glandular trichome-derived terpenes in S. lycopersicum. While TPS12-derived sesquiterpenes contribute to host plant resistance against M. euphorbiae, TPS20-derived monoterpenes appear to be exploited as cue for host plant orientation by aphids.

Automated summary

Secondary metabolites produced in glandular trichomes of tomato, specifically mono- and sesquiterpenes, have contrasting roles in interactions with the potato aphid Macrosiphum euphorbiae. While sesquiterpenes derived from TPS12 contribute to host plant resistance against M. euphorbiae, monoterpenes derived from TPS20 appear to be exploited as cues for aphid orientation towards host plants.