Abnormally high digestive enzyme activity and gene expression explain the contemporary evolution of a Diabrotica biotype able to feed on soybeans

Authors

  • Matías J. Curzi,

    1. Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL
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    • Funded by United States Department of Agriculture (USDA)-National Institute of Food and Agriculture (NIFA) to MJS.
  • Jorge A. Zavala,

    1. Cátedra de Bioquímica/INBA (CONICET/UBA), Facultad de Agronomía, Universidad de Buenos Aires, Universidad Católica Argentina, Buenos Aires, Argentina
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    • Funded by United States Department of Agriculture (USDA)-National Institute of Food and Agriculture (NIFA) to MJS.
  • Joseph L. Spencer,

    1. Illinois Natural History Survey, University of Illinois at Urbana-Champaign, Champaign, IL
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  • Manfredo J. Seufferheld

    Corresponding author
    1. Cátedra de Bioquímica/INBA (CONICET/UBA), Facultad de Agronomía, Universidad de Buenos Aires, Universidad Católica Argentina, Buenos Aires, Argentina
    • Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL
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    • Funded by United States Department of Agriculture (USDA)-National Institute of Food and Agriculture (NIFA) to MJS.

  • M.J.C. and J.A.Z. contributed equally to this work.

Correspondence

Manfredo J. Seufferheld, Department of Crop Sciences, University of Illinois at Urbana-Champaign, 1201 W. Gregory Drive, Room 311A, Urbana, IL 61801. Tel: +1 217-333-6505; Fax: +1 217-333-4777; E-mail: seufferh@illinois.edu

Abstract

Western corn rootworm (Diabrotica virgifera) (WCR) depends on the continuous availability of corn. Broad adoption of annual crop rotation between corn (Zea mays) and nonhost soybean (Glycine max) exploited WCR biology to provide excellent WCR control, but this practice dramatically reduced landscape heterogeneity in East-central Illinois and imposed intense selection pressure. This selection resulted in behavioral changes and “rotation-resistant” (RR) WCR adults. Although soybeans are well defended against Coleopteran insects by cysteine protease inhibitors, RR-WCR feed on soybean foliage and remain long enough to deposit eggs that will hatch the following spring and larvae will feed on roots of planted corn. Other than documenting changes in insect mobility and egg laying behavior, 15 years of research have failed to identify any diagnostic differences between wild-type (WT)- and RR-WCR or a mechanism that allows for prolonged RR-WCR feeding and survival in soybean fields. We documented differences in behavior, physiology, digestive protease activity (threefold to fourfold increases), and protease gene expression in the gut of RR-WCR adults. Our data suggest that higher constitutive activity levels of cathepsin L are part of the mechanism that enables populations of WCR to circumvent soybean defenses, and thus, crop rotation. These new insights into the mechanism of WCR tolerance of soybean herbivory transcend the issue of RR-WCR diagnostics and management to link changes in insect gut proteolytic activity and behavior with landscape heterogeneity. The RR-WCR illustrates how agro-ecological factors can affect the evolution of insects in human-altered ecosystems.

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