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

• Published in: The Plant journal : for cell and molecular biology 2024-07, Vol.119 (1), p.84-99
• Main Authors: Kumar, Varun, Nadarajan, Stalin, Boddupally, Dayakar, Wang, Ru, Bar, Einat, Davidovich‐Rikanati, Rachel, Doron‐Faigenboim, Adi, Alkan, Noam, Lewinsohn, Efraim, Elad, Yigal, Oren‐Shamir, Michal
• Format: Article
• Language: English
• Subjects: Acetaldehyde - analogs & derivatives; Acetaldehyde - metabolism; Acetaldehyde - pharmacology; Allelochemicals; Animals; Benzaldehyde; Benzaldehydes - metabolism; Benzaldehydes - pharmacology; benzenoid phenylpropanoid volatiles; Chemical pest control; Crop infestation; Cultivars; Defense mechanisms; defense signals; Genes; High resistance; Immune response; Immune system; Insects; Leaves; Manduca - physiology; Metabolomics; Moths - drug effects; Moths - physiology; Pest resistance; Pesticides; Phenylacetaldehyde; Phenylalanine; Phenylalanine - metabolism; plant defense mechanisms; Plant Diseases - immunology; Plant Diseases - parasitology; Plant immunity; Plant Leaves - drug effects; Plant Leaves - metabolism; Plant Leaves - parasitology; Plants (botany); plant–insect interactions; Solanum lycopersicum - genetics; Solanum lycopersicum - metabolism; Solanum lycopersicum - parasitology; Terpenes; Tomatoes; Tuta absoluta; Volatile compounds; Volatile Organic Compounds - metabolism; Volatiles; Weather
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16745

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. Significance Statement Phenylalanine treatment of tomato plants results in increased resistance to Tuta absoluta of them and of neighboring non‐treated plants. The phenylalanine‐derived volatiles overproduced in the treated plants resulted in a repellence effect of the moths, and induced priming in neighboring plants.