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

Abstract

The leaves of the wild tomato <i>Solanum</i><i>galapagense</i> harbor type-IV glandular trichomes (GT) that produce high levels of acylsugars (AS), conferring insect resistance. Conversely, domesticated tomatoes (<i>S. lycopersicum</i>) 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 <i>S.</i><i>galapagense</i> into cv. Micro-Tom (MT) and created a line named "<i>Galapagos-enhanced trichomes</i>" (MT-<i>Get</i>). Mapping-by-sequencing revealed that five chromosomal regions of <i>S. galapagense</i> were present in MT-<i>Get</i>. Further genetic mapping showed that <i>S. galapagense</i> 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-<i>Get</i>. 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.