Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer Tuta absoluta

Tomato plants are attacked by a variety of herbivore pests and among them, the leafminer Tuta absoluta, which is currently a major threat to global tomato production. Although the commercial tomato is susceptible to T. absoluta attacks, a better understanding of the defensive plant responses to this pest will help in defining plant resistance traits and broaden the range of agronomic levers that can be used for an effective integrated pest management strategy over the crop cycle. In this study, we developed an integrative approach combining untargeted metabolomic and transcriptomic analyses to characterize the local and systemic metabolic responses of young tomato plants to T. absoluta larvae herbivory. From metabolomic analyses, the tomato response appeared to be both local and systemic, with a local response in infested leaves being much more intense than in other parts of the plant. The main response was a massive accumulation of phenolamides with great structural diversity, including rare derivatives composed of spermine and dihydrocinnamic acids. The accumulation of this family of specialized metabolites was supported by transcriptomic data, which showed induction of both phenylpropanoid and polyamine precursor pathways. Moreover, our transcriptomic data identified two genes strongly induced by T. absoluta herbivory, that we functionally characterized as putrescine hydroxycinnamoyl transferases. They catalyze the biosynthesis of several phenolamides, among which is caffeoylputrescine. Overall, this study provided new mechanistic clues of the tomato/T. absoluta interaction.