Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants

Richard O. Musser, Don F. Cipollini, Sue M. Hum-Musser, Spencer A. Williams, Judith K Brown, Gary W. Felton

Research output: Contribution to journalArticle

123 Citations (Scopus)

Abstract

The insect salivary enzyme glucose oxidase (GOX) can inhibit wound-inducible nicotine production in tobacco, Nicotiana tabacum. We examined whether salivary gland extracts of Helicoverpa zea lacking active GOX could still suppress nicotine in tobacco, Nicotiana tabacum, and whether GOX could suppress wound-inducible defenses of another Solanaceous plant, tomato Lycopersicon esculentum. Tobacco leaves were wounded with a cork borer and treated with water, salivary gland extracts with active GOX (SxG), or salivary gland extracts with inactive GOX (SxI). After three days, leaves treated with SxG had significantly less nicotine than all other wounded treatments. Neonates that fed on the terminal leaves of tobacco plants treated with SxG had significantly higher survival than neonates that fed on leaves treated with either SxI or water. This evidence supports the assertion that GOX is the salivary factor responsible for the suppression of tobacco plant nicotine production by H. zea saliva. Results for the NahG tobacco plants, which lack salicylic acid (SA) due to a transgene for bacterial SA hydroxylase, indicate that suppression of nicotine by GOX does not require SA. However, tobacco leaves that were wounded and treated with SxG had significantly higher levels of the SA-mediated PR-1a protein than leaves treated with SxI or water. Leaves of tomato plants wounded with scissors and then treated with SxG had trypsin inhibitor levels that were moderately lower than plants wounded and treated with purified GOX, water, or SxI. However, all the wounded tomato leaves irrespective of treatment resulted in lower caterpillar growth rates than the non-wounded tomato leaves. Glucose oxidase is the first insect salivary enzyme shown to suppress wound-inducible herbivore defenses of plants.

Original languageEnglish (US)
Pages (from-to)128-137
Number of pages10
JournalArchives of Insect Biochemistry and Physiology
Volume58
Issue number2
DOIs
StatePublished - Feb 2005

Fingerprint

glucose oxidase
Glucose Oxidase
Herbivory
Tobacco
insect larvae
herbivores
nicotine
tobacco
Lycopersicon esculentum
Nicotine
Enzymes
Salicylic Acid
enzymes
salicylic acid
leaves
salivary glands
Salivary Glands
animal injuries
tomatoes
Plant Leaves

Keywords

  • Elicitor
  • Glucose oxidase
  • Helicoverpa zea
  • Hydrogen peroxide
  • Induced resistance
  • Jasmonate
  • Oxidative burst
  • Reactive oxygen species
  • Salicylate
  • Systemic acquired resistance

ASJC Scopus subject areas

  • Insect Science
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physiology
  • Physiology (medical)

Cite this

Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. / Musser, Richard O.; Cipollini, Don F.; Hum-Musser, Sue M.; Williams, Spencer A.; Brown, Judith K; Felton, Gary W.

In: Archives of Insect Biochemistry and Physiology, Vol. 58, No. 2, 02.2005, p. 128-137.

Research output: Contribution to journalArticle

Musser, Richard O. ; Cipollini, Don F. ; Hum-Musser, Sue M. ; Williams, Spencer A. ; Brown, Judith K ; Felton, Gary W. / Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. In: Archives of Insect Biochemistry and Physiology. 2005 ; Vol. 58, No. 2. pp. 128-137.
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abstract = "The insect salivary enzyme glucose oxidase (GOX) can inhibit wound-inducible nicotine production in tobacco, Nicotiana tabacum. We examined whether salivary gland extracts of Helicoverpa zea lacking active GOX could still suppress nicotine in tobacco, Nicotiana tabacum, and whether GOX could suppress wound-inducible defenses of another Solanaceous plant, tomato Lycopersicon esculentum. Tobacco leaves were wounded with a cork borer and treated with water, salivary gland extracts with active GOX (SxG), or salivary gland extracts with inactive GOX (SxI). After three days, leaves treated with SxG had significantly less nicotine than all other wounded treatments. Neonates that fed on the terminal leaves of tobacco plants treated with SxG had significantly higher survival than neonates that fed on leaves treated with either SxI or water. This evidence supports the assertion that GOX is the salivary factor responsible for the suppression of tobacco plant nicotine production by H. zea saliva. Results for the NahG tobacco plants, which lack salicylic acid (SA) due to a transgene for bacterial SA hydroxylase, indicate that suppression of nicotine by GOX does not require SA. However, tobacco leaves that were wounded and treated with SxG had significantly higher levels of the SA-mediated PR-1a protein than leaves treated with SxI or water. Leaves of tomato plants wounded with scissors and then treated with SxG had trypsin inhibitor levels that were moderately lower than plants wounded and treated with purified GOX, water, or SxI. However, all the wounded tomato leaves irrespective of treatment resulted in lower caterpillar growth rates than the non-wounded tomato leaves. Glucose oxidase is the first insect salivary enzyme shown to suppress wound-inducible herbivore defenses of plants.",
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