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

To deal with arthropod pests the tomato wild relatives produce a variety of defense compounds in their glandular trichomes. In 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 that produces farnesyl diphosphate (-FPP), and () that uses 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- (MT-) 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-, 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-. Since MT- 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 type-VI trichomes.