Enhanced toxicity and induction of cytochrome P450s suggest a cost of "eavesdropping" in a multitrophic interaction

Ren Sen Zeng, Zhimou Wen, Guodong Niu, Mary A. Schuler, May R. Berenbaum

Research output: Contribution to journalArticle

Abstract

The inducibility of cytochrome P450 monooxygenases (P450s) and other xenobiotic-metabolizing enzymes is thought to reflect material and energy costs of biosynthesis. Efforts to detect such costs of detoxification enzyme induction, however, have had mixed success. Although they are rarely considered, ecological costs of induction may be a more significant evolutionary constraint on herbivores than material and energy costs. Because some P450-mediated metabolic transformations are bioactivation reactions that increase, rather than reduce, toxicity, maintaining high levels of P450 activity places an organism at risk of greater mortality in the presence of compounds that are bioactivated. We show that P450 inducibility in the generalist moth Helicoverpa zea in response to plant signaling substances, an adaptive response in a ditrophic interaction between herbivore and plant, becomes detrimental in the presence of a third trophic association with a plant pathogen that produces aflatoxin, a toxin that can be bioactivated by P450s. Consumption of plant signaling molecules, such as methyl jasmonate (MeJA) and salicylic acid (SA) enhanced the toxicity of aflatoxin B1 (AFB1) to H. zea that resulted in substantially more damage to larval growth and development. Among the P450 transcripts already cloned from this organism, two in the CYP6B and CYP321A subfamilies are shown to be induced in response to MeJA and SA, suggesting that they may mediate some of the observed bioactivations.

Original languageEnglish (US)
Pages (from-to)526-532
Number of pages7
JournalJournal of Chemical Ecology
Volume35
Issue number5
DOIs
StatePublished - May 1 2009

Fingerprint

Mixed Function Oxygenases
cytochrome P-450
Cytochrome P-450 Enzyme System
cytochrome
Toxicity
Helicoverpa zea
methyl jasmonate
energy costs
toxicity
Costs and Cost Analysis
salicylic acid
Herbivory
Salicylic Acid
herbivores
cost
Zea mays
Costs
herbivore
gene induction
organisms

Keywords

  • Aflatoxin B1
  • Bioactivation
  • Cytochrome P450 monooxygenase
  • Detoxification induction
  • Ecological cost
  • Helicoverpa zea
  • Multitrophic interaction
  • Plant signaling molecule
  • RT-PCR
  • Southern analysis

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry

Cite this

Enhanced toxicity and induction of cytochrome P450s suggest a cost of "eavesdropping" in a multitrophic interaction. / Zeng, Ren Sen; Wen, Zhimou; Niu, Guodong; Schuler, Mary A.; Berenbaum, May R.

In: Journal of Chemical Ecology, Vol. 35, No. 5, 01.05.2009, p. 526-532.

Research output: Contribution to journalArticle

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