Genetic factors outside the metabolic cluster for plastid-derived sesquiterpenes are required to pursue arthropod-resistant tomatoes

ABSTRACT To deal with arthropod pests the tomato wild relatives produce a variety of defense compounds in their glandular trichomes. In Solanum habrochaites LA1777, a functional cluster of genes on chromosome 8 controls plastid-derived sesquiterpene synthesis not found in cultivated tomatoes. The main genes at the cluster are Z-prenyltransferase (zFPS) that produces Z-Z- farnesyl diphosphate ( Z,Z -FPP), and Santalene and Bergamotene Synthase ( SBS ) that uses Z,Z- FPP to produce α-santalene, β-bergamotene, and α-bergamotene in type-VI glandular trichomes. Both LA1777 and cultivated tomatoes have type-VI trichomes, but the gland in cultivated tomato is much smaller containing low levels of monoterpenes and cytosolic-derived sesquiterpenes, which do not provide tomato with the same pest resistance as in LA1777. We successfully transferred the plastid-derived sesquiterpene pathway from LA1777 to type-VI trichomes of a cultivated tomato (cv. Micro-Tom, MT) by a back-crossing approach. The trichomes of the introgressed line named MT- Sesquiterpene synthase 2 (MT- Sst2 ) produced even higher levels of α-santalene, β-bergamotene, and α-bergamotene than the type-VI glandular trichomes of LA1777. We also noticed that the type-VI trichome internal storage-cavity size increases in MT- Sst2 , probably as an “inflated balloon” effect of the increased amount of sesquiterpenes. Surprisingly, the presence of high amounts of plastid-derived sesquiterpenes was not sufficient to confer resistance to various tomato pests in MT- Sst2 . Since MT- Sst2 made the same sesquiterpenes as LA1777, this points to additional factors, outside the genomic region thought to be the metabolic cluster, necessary to obtain arthropod-resistant tomatoes. Our results also provide a better understanding of the morphology of S. habrochaites type-VI trichomes. One-sentence summary Cultivated tomatoes harboring the plastid-derived sesquiterpenes from S. habrochaites need additional genetic components necessary to convert them into effective insecticides.