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

Abstract

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 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.

Leaf trichome diversity, acylsugar concentration, and their relationships to leaf area inSolanum galapagense

“…As this species can easily hybridize with cultivated tomatoes (Rick, 1961) it has been used as donors for stress tolerance genes, which could be transferred into commercial varieties by introgression breeding (Zamir, 2001). For example, VI037339 (LA1401) and VI007099 accessions have already been utilized as donors of high trichome IV density into modern cultivated tomato cultivars through interspecific crosses (Andrade et al ., 2017; Rakha et al ., 2017b; da Silva et al ., 2019; Vendemiatti et al ., 2021). However, in this study, these accessions were not among those with the highest trichome type IV density and acylsugar concentration.…”

“…Among them, S. galapagense has been identified as one of the most promising sources of insect pest resistance (Firdaus et al ., 2012; Lucatti et al ., 2013). It has been the focus of most tomato breeding programs aiming to improve biotic and abiotic stress resistance due to its close relationship to cultivated tomato (Vendemiatti et al ., 2021). The S. galapagense species originates from the Galápagos Islands, an archipelago 1000 km west of Ecuador where it formed a diverse range of phenotypes due to the islands’ unique ecosystem (Darwin et al ., 2003).…”

“…One of these is the presence of hair-like structures, called trichomes, on the surface of flowers, fruits, stems, and leaves as physical and chemical lines of defence. Numerous studies have been conducted on the nature of these epidermal outgrowths including function, quantification, and effectiveness ( see Glas et al ., 2012; Vendemiatti et al ., 2021). In tomato, among the seven types of trichomes found on plants, four are termed glandular due to the sugar-filled pouches at their tip (Luckwill, 1943).…”

role of tomato wild relatives in breeding disease-free varieties

“…Furthermore, the introgressed gene from a wild relative into advanced lines may disrupt long-accumulated horticultural traits due to linkage drag (Tanksley and Nelson, 1996). For example, S. galapagense has been identified as a source of insect-pest resistance (Rakha et al, 2017;Vendemiatti et al, 2021).…”

Determining the Elemental Compositions in the trichome of five sampled herbarium species in the genus Solanum (Solanaceae) using SEM-EDS

“…Glandular trichomes produce and accumulate (secondary) specialized compounds (Wang, 2014). In the tomato clade, there are species with notable pest resistance due to the presence of type-IV trichomes at a high density, such as S. pennellii and S. galapagense (Vendemiatti, 2020;Vendemiatti et al, 2021;Vendemiatti et al, 2022). Among the sampled species, Solanum lycopersicum (tomato) and Solanum tuberosum (potato) are of particular agricultural importance, while Solanum berthaultii, Solanum galapagense, and Solanum pennellii represent wild relatives with unique ecological niches and genetic diversity.…”