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

Plant J. 2024 Jul;119(1):84-99. doi: 10.1111/tpj.16745. Epub 2024 Apr 5.

Abstract

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.

Keywords: Tuta absoluta; benzenoid phenylpropanoid volatiles; defense signals; phenylalanine; plant defense mechanisms; plant–insect interactions.

MeSH terms

  • Acetaldehyde / analogs & derivatives
  • Acetaldehyde / metabolism
  • Acetaldehyde / pharmacology
  • Animals
  • Benzaldehydes / metabolism
  • Benzaldehydes / pharmacology
  • Manduca / physiology
  • Moths / drug effects
  • Moths / physiology
  • Phenylalanine* / metabolism
  • Plant Diseases / immunology
  • Plant Diseases / parasitology
  • Plant Leaves* / drug effects
  • Plant Leaves* / metabolism
  • Plant Leaves* / parasitology
  • Solanum lycopersicum* / genetics
  • Solanum lycopersicum* / metabolism
  • Solanum lycopersicum* / parasitology
  • Volatile Organic Compounds* / metabolism

Substances

  • Phenylalanine
  • Volatile Organic Compounds
  • Benzaldehydes
  • phenylacetaldehyde
  • benzaldehyde
  • Acetaldehyde