The Genetic Complexity of Type-IV Trichome Development Reveals the Steps towards an Insect-Resistant Tomato

Abstract

The leaves of the wild tomato Solanum galapagense harbor type-IV glandular trichomes (GT) that produce high levels of acylsugars (AS), conferring insect resistance. Conversely, domesticated tomatoes (S. lycopersicum) lack type-IV trichomes on the leaves of mature plants, preventing high AS production, thus rendering the plants more vulnerable to insect predation. We hypothesized that cultivated tomatoes engineered to harbor type-IV trichomes on the leaves of adult plants could be insect-resistant. We introgressed the genetic determinants controlling type-IV trichome development from S. galapagense into cv. Micro-Tom (MT) and created a line named “Galapagos-enhanced trichomes” (MT-Get). Mapping-by-sequencing revealed that five chromosomal regions of S. galapagense were present in MT-Get. Further genetic mapping showed that S. galapagense alleles in chromosomes 1, 2, and 3 were sufficient for the presence of type-IV trichomes on adult organs but at lower densities. Metabolic and gene expression analyses demonstrated that type-IV trichome density was not accompanied by the AS production and exudation in MT-Get. Although the plants produce a significant amount of acylsugars, those are still not enough to make them resistant to whiteflies. We demonstrate that type-IV glandular trichome development is insufficient for high AS accumulation. The results from our study provided additional insights into the steps necessary for breeding an insect-resistant tomato.

Woollymutation withGet02locus overcomes the polygenic nature of trichome-based pest resistance in tomato

“…Although some individual loci were sufficient for the appearance of type-IV trichomes, the simultaneous presence of the five loci appears to be necessary to increase type-IV trichome density. However, MT- Get plants did not exhibit the same level of resistance to whiteflies as observed in S. galapagense (Firdaus et al, 2013; Firdaus et al, 2012; Vosman et al, 2019; Vendemiatti et al, 2022). Since both the density of type-IV trichomes as well as the levels of AS in MT- Get were inferior to those observed in S. galapagense , it was concluded that there are additional genetic factors linked to insect resistance in S. galapagense , which is likely to be a complex, polygenic trait.…”

“…The Get02/Wo parental line, MT- Get , exhibits several traits that could affect agronomical performance, such as reduced fruit weight (Vendemiatti et al, 2022). Therefore, we evaluated Get02/Wo performance also because there is a concern that breeding based on high trichome densities and enhanced specialized metabolism may negatively impact yield due to the deviation of energy from primary metabolism that contributes to fruit size and, partially, to taste (Tieman et al, 2017).…”

“…The trichome quantification was carried out using the methodology described by Vendemiatti et al, (2017Vendemiatti et al, ( , 2022. In summary, clear nail polish fixed leaflet samples in glass slides.…”

“…Our work focuses on type-IV glandular trichomes, which are elongated multicellular structures consisting of a single flat basal cell, a short uniseriate two- or three-celled stalk (0.2-0.4 mm), and a spherical gland at the tip (Glas et al, 2012). They differ from the type-V non-glandular trichome only by the presence of the apical gland, and many studies reported a negative correlation between the density of these two trichome types (Fernández-Muñoz et al, 2003; Simmons and Gurr, 2005; Vendemiatti et al, 2017; Vendemiatti et al, 2022).…”

“…Aiming to introduce the ability of S. galapagense to retain type-IV trichomes in the adult life stage into a cultivated tomato, the tomato introgression line MT- Galapagos enhanced trichomes (MT- Get ) was developed in a cv. Micro-Tom background (Vendemiatti et al, 2022). This MT- Get genotype exhibits type-IV trichomes throughout all developmental stages.…”