Identification of Sesquiterpenes in Wild Tomato Accessions with Activities Against the Potato Aphid and Their Tissue-Specific Engineering in Cultivated Tomato

Abstract

The potato aphid (Macrosiphum euphorbiae Thomas) poses a serious problem in the commercial production of horticultural crops including tomato, since it causes damage by stylet feeding and the transmission of viruses for which it serves as the vector. Application of conventional pesticides being the fundamental tactic in the control of the aphid is increasingly considered insufficient and problematic due to emerging pest resistances and biosafety issues, highlighting the continuing need to develop new efficient and sustainable approaches. Alternatively, glandular trichomes of plants are well-known epidermal hairy tissues producing various secondary metabolites that involve in plant-insect interactions, while the terpene compounds produced from type VI glandular trichomes were frequently referred to as antixenotic or antibiotic resistant against both piercing-sucking and chewing-biting herbivores. Recent studies of terpene production in glandular trichomes of tomato, found on leaves and stems, demonstrated significant differences between cultivated (Solanum lycopersicum L.) and wild tomatoes (Solanum habrochaites S.Knapp & D.M.Spooner), as well as quantitative and qualitative variation of sesquiterpenes among the wild tomato accessions. Thus, the current research aimed to explore (1) if certain sesquiterpene chemotypes from the wild accessions support resistance against the potato aphid by affecting its pre- and postlanding behaviors during their interaction, and (2) would the resistance in cultivated tomato be improved if defensive sesquiterpenes were produced in a different tissue along the aphid stylet pathway by metabolic engineering. To determine the effects of glandular trichome derived sesquiterpenes produced from wild tomato, five chemotypes (I-V) from a collection of S. habrochaites accessions were re-confirmed by gas chromatography-mass spectrometry (GC-MS). The performance (longevity and fecundity) of wingless aphids on tomato accessions, their feeding behaviors on an artificial diet, and the choice behaviors of winged aphids in an open Y-track olfactometer were analyzed. The results suggested that chemotype IV and V accessions which respectively produce mixtures of caryophyllene/α-humulene and santalene/bergamotene significantly reduced aphid longevity and fecundity in clip-cages while they were significantly repellent to winged aphids in the olfactometer. The trichome extracts from the two groups significantly affected aphid survivorship, gel saliva investment, and honeydew production in artificial diets, and significantly reduced the attraction of winged aphids to cultivated tomato. The same effects on feeding and choice behaviors were also observed by using pure caryophyllene/α-humulene as well as the trichome extract from one introgression line LA3935 which has santalene/bergamotene isomers predominantly produced in glandular trichomes. Cultivated tomato lines generally produce a large quantity of TPS20-derived monoterpenes