Phenylalanine treatment induces tomato resistance to Tuta absoluta via increased accumulation of benzenoid/phenylpropanoid volatiles serving as defense signals

SUMMARY Tuta absoluta (“leafminer”), is a major pest of tomato crops worldwide. Controlling this insect is difficult due to its efficient infestation, rapid proliferation, and resilience to changing weather conditions. Furthermore, chemical pesticides have only a short‐term effect due to rapid development of T. absoluta strains. Here, we show that a variety of tomato cultivars, treated with external phenylalanine solutions exhibit high resistance to T. absoluta , under both greenhouse and open field conditions, at different locations. A large‐scale metabolomic study revealed that tomato leaves absorb and metabolize externally given Phe efficiently, resulting in a change in their volatile profile, and repellence of T. absoluta moths. The change in the volatile profile is due to an increase in three phenylalanine‐derived benzenoid phenylpropanoid volatiles (BPVs), benzaldehyde, phenylacetaldehyde, and 2‐phenylethanol. This treatment had no effect on terpenes and green leaf volatiles, known to contribute to the fight against insects. Phe‐treated plants also increased the resistance of neighboring non‐treated plants. RNAseq analysis of the neighboring non‐treated plants revealed an exclusive upregulation of genes, with enrichment of genes related to the plant immune response system. Exposure of tomato plants to either benzaldehyde, phenylacetaldehyde, or 2‐phenylethanol, resulted in induction of genes related to the plant immune system that were also induced due to neighboring Phe‐treated plants. We suggest a novel role of phenylalanine‐derived BPVs as mediators of plant–insect interactions, acting as inducers of the plant defense mechanisms.