Vendemiatti, E. | Search bioRxiv

bioRxiv2021

Introgression of type-IV glandular trichomes from Solanum galapagense to cultivated tomato reveals genetic complexity for the development of acylsugar-based insect resistance

Glandular trichomes are involved in the production of food- and medicine-relevant chemicals in plants, besides being associated with pest resistance. In some wild Solanum species closely related to the cultivated tomato (S. lycopersicum), the presence of type-IV glandular trichomes leads to the production of high levels of insecticide acylsugars (AS). Conversely, low AS production observed in the cultivated tomato is attributed to its incapacity to develop type-IV trichomes in adult organs. Therefore, we hypothesized that cultivated tomatoes engineered to harbor type-IV trichomes on the leaves of mature plants can be pest resistant. We introgressed into the tomato cultivar Micro-Tom (MT) the capability of S. galapagense to maintain the development of type-IV trichomes throughout all plant stages, thus creating a line named "Galapagos enhanced trichomes" (MT-Get). Mapping-by-sequencing of MT-Get revealed that five chromosomal regions of S. galapagense were present in MT-Get. Further mapping reveled that S. galapagense alleles on chromosomes 1, 2 and 3 are sufficient for the presence of type-IV trichomes, but in lower densities. GC-MS, LC-MS, and gene expression analyses demonstrated that the increased density of type-IV trichomes was not accompanied by high AS production and exudation in MT-Get. Moreover, MT-Get did not differ from MT in its susceptibility to whitefly (Bemisia tabaci). Our findings demonstrates that type-IV glandular trichome development along with AS production and exudation are partially uncoupled at the genetic level. The MT-Get genotype represents a valuable resource for further studies involving the biochemical manipulation of type-IV trichome content through either genetic introgression or transgenic approaches. Significance StatementThis work identified loci in the tomato genome that control the heterochronic development of type-IV glandular trichomes and uncoupled the genetic control of this type of trichome ontogeny from acylsugar biosynthesis and accumulation, revealing a higher than anticipated genetic complexity of acylsugar-based insect resistance. The findings reported herein will contribute to further dissect the genetics of trichome development in tomato as well as to introgress broad and durable insect resistance in tomato and other Solanaceae.

plant biology↗

bioRxiv2020

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 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 -santalene, {beta}-bergamotene, and -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 -santalene, {beta}-bergamotene, and -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 summaryCultivated tomatoes harboring the plastid-derived sesquiterpenes from S. habrochaites need additional genetic components necessary to convert them into effective insecticides.

plant biology↗