Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant

PLoS One. 2012;7(4):e36168. doi: 10.1371/journal.pone.0036168. Epub 2012 Apr 30.

Abstract

Caterpillars produce oral secretions that may serve as cues to elicit plant defenses, but in other cases these secretions have been shown to suppress plant defenses. Ongoing work in our laboratory has focused on the salivary secretions of the tomato fruitworm, Helicoverpa zea. In previous studies we have shown that saliva and its principal component glucose oxidase acts as an effector by suppressing defenses in tobacco. In this current study, we report that saliva elicits a burst of jasmonic acid (JA) and the induction of late responding defense genes such as proteinase inhibitor 2 (Pin2). Transcripts encoding early response genes associated with the JA pathway were not affected by saliva. We also observed a delayed response to saliva with increased densities of Type VI glandular trichomes in newly emerged leaves. Proteomic analysis of saliva revealed glucose oxidase (GOX) was the most abundant protein identified and we confirmed that it plays a primary role in the induction of defenses in tomato. These results suggest that the recognition of GOX in tomato may represent a case for effector-triggered immunity. Examination of saliva from other caterpillar species indicates that saliva from the noctuids Spodoptera exigua and Heliothis virescens also induced Pin2 transcripts.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cyclopentanes / metabolism
  • Gene Expression Regulation, Plant*
  • Glucose Oxidase / metabolism*
  • Lepidoptera / enzymology*
  • Lepidoptera / metabolism
  • Organ Specificity
  • Oxylipins / metabolism
  • Plant Proteins / genetics
  • Proteomics
  • Saliva / enzymology*
  • Saliva / metabolism
  • Signal Transduction / immunology
  • Solanum lycopersicum / cytology
  • Solanum lycopersicum / genetics*
  • Solanum lycopersicum / immunology*
  • Solanum lycopersicum / metabolism
  • Telomeric Repeat Binding Protein 1 / genetics
  • Time Factors
  • Transcriptional Activation / immunology*

Substances

  • Cyclopentanes
  • Oxylipins
  • Plant Proteins
  • Telomeric Repeat Binding Protein 1
  • jasmonic acid
  • Glucose Oxidase