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Enhanced Toxicity and Induction of Cytochrome P450s Suggest a Cost of “Eavesdropping” in a Multitrophic Interaction

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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.

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Acknowledgments

This work was supported by National Science Foundation grant IOB0614726 to M.R.B., National Institutes of Health grant R01 GM071826 to M.A.S., and an UIUC Environmental Toxicology Fellowship to G.N., grants from the National 973 project of China (2006CB100200), Natural Science Foundation of China (30670331, 30870390) and Guangdong (2008B021500001), and Doctoral Program Foundation of the Ministry of Education of China (20060564017) to R.S.Z. We thank Drs. Arthur Zangerl, Jack Schultz, and Patrick Dowd for comments on the manuscript and Allen Lawrence and Henan Zeng for assistance with insect rearing.

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Authors and Affiliations

  1. Research Center for Chemical Ecology, South China Agricultural University, Guangzhou, 510642, People’s Republic of China

    Ren Sen Zeng

  2. Department of Entomology, University of Illinois, Urbana, IL, 61801, USA

    Ren Sen Zeng, Guodong Niu & May R. Berenbaum

  3. Department of Cell and Developmental Biology, University of Illinois, Urbana, IL, 61801, USA

    Zhimou Wen & Mary A. Schuler

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  1. Ren Sen Zeng
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Correspondence to Ren Sen Zeng or May R. Berenbaum.

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Zeng, R.S., Wen, Z., Niu, G. et al. Enhanced Toxicity and Induction of Cytochrome P450s Suggest a Cost of “Eavesdropping” in a Multitrophic Interaction. J Chem Ecol 35, 526–532 (2009). https://doi.org/10.1007/s10886-009-9640-6

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