Light Intensity-Mediated Induction of Trichome-Associated Allelochemicals Increases Resistance Against Thrips in Tomato

In cultivated tomato (Solanum lycopersicum), increases in photosynthetically active radiation (PAR) induce type VI leaf glandular trichomes, which are important defensive structures against arthropod herbivores. Yet, how PAR affects the type VI trichome-associated leaf chemistry and its biological significance with respect to other photomorphogenic responses in this agronomically important plant species is unknown. We used the type VI trichome-deficient tomato mutant odorless-2 (od-2) and its wild type to investigate the influence of PAR on trichome-associated chemical defenses against thrips (Frankliniella occidentalis). High PAR increased thrips resistance in wild-type plants, but not in od-. Furthermore, under high PAR, thrips preferred od-2 over the wild type. Both genotypes increased type VI trichome densities under high PAR. Wild-type plants, however, produced more trichome-associated allelochemicals, i.e. terpenes and phenolics, these being undetectable or barely altered in od-2. High PAR increased leaf number and thickness, and induced profound but similar metabolomic changes in wild-type and od-2 leaves. Enhanced PAR also increased levels of ABA in wild-type and od-2 plants, and of auxin in od-2, while the salicylic acid and jasmonate concentrations were unaltered. However, in both genotypes, high PAR induced the expression of jasmonic acid-responsive defense-related genes. Taken together, our results demonstrate that high PAR-mediated induction of trichome-associated chemical defenses plays a prominent role in tomato-thrips interactions.