A herbivore-induced salicylic acid carboxyl methyl transferase produces methyl salicylate in tomato to mediate defense signaling and deter pests

Methyl salicylate (MeSA) is a component of the herbivore-induced volatile blend of tomato (Solanum lycopersicum), and an intermediate in long distance salicylic acid (SA) signaling. To investigate the role of MeSA in interactions between tomato and the lepidopteran pests Helicoverpa zea and Manduca sexta, we used transgenic tomato lines that were antisense (AS) or overexpressors (OE) of the tomato SA carboxyl methyl transferase SlSAMT1, which under- or over-produce MeSA, respectively. Transgenic AS plants produced less MeSA and were more susceptible to both insects compared to wild-type plants, while OE plants had elevated MeSA production but displayed increased resistance only to M. sexta. Pairwise choice and toxicity assays revealed that MeSA itself impacted the larvae as a deterrent rather than a toxin, and metabolic profiling indicated that increased susceptibility in the AS lines and resistance in the OE lines may be related to altered jasmonic acid and ABA mediated herbivore-induced defense signaling, and modified production of inducible defense compounds such as flavonoids and phenolamides. To expand beyond Lepidoptera, the settling preference of the piercing-sucking insect Bemisia tabaci was also examined and it displayed a strong preference for lines with less SlSAMT1 expression. These data indicate that herbivore-inducible SlSAMT1 expression and its associated MeSA production play an important and complex role in the defense of tomato against insect pests.