Phenylalanine-driven metabolic induced resistance activates phenylpropanoid defenses in tomato against Tetranychus...

Tetranychus urticae (Koch), the two-spotted spider mite (TSSM), is a highly polyphagous agricultural pest, infesting more than 1100 plant species. Chemical control of TSSM is limited by the rapid development of resistant mite populations. Previous studies have shown that exogenous application of phenylalanine to plants is efficiently absorbed and metabolized into phenylpropanoids, thereby enhancing plant resistance to fungal and insect pests. Here, we demonstrate that phenylalanine treatment also increases plant resistance to TSSM. In choice assays, mites preferentially colonized non-treated plants over treated plants. In no-choice experiments, phenylalanine-treated plants constituted a hostile environment for TSSM: mites attempted to leave treated leaflets, exhibited increased oviposition, and showed a reduced rate of development from nymphs to mature adults. Three mechanisms underlying phenylalanine-induced resistance have previously been identified, including the accumulation of metabolites toxic to pathogens, the induction of a priming effect that enables rapid and targeted activation of plant defense genes following infection, and enhanced immunity in neighboring untreated plants. Here we present an additional mechanism involving metabolomic induced resistance, in which phenylalanine treatment triggers an early and enhanced accumulation of phenylpropanoids associated with plant immunity. These metabolites accumulate gradually in non-treated plants following TSSM infestation, ultimately reaching levels comparable to those observed in phenylalanine-treated plants. These findings demonstrate that phenylalanine accelerates the deployment of defense-associated metabolites and enhances resistance to arthropod pests.