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Tradeoff between reproduction and resistance evolution to Bt-toxin in Helicoverpa armigera: regulated by vitellogenin gene expression

Published online by Cambridge University Press:  21 February 2014

W.N. Zhang ,
H.J. Xiao ,
G.M. Liang ,
Y.Y. Guo  and
K.M. Wu
W.N. Zhang
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
H.J. Xiao
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China Institute of Entomology, Jiangxi Agricultural University, Nanchang 330045, China
G.M. Liang*
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Y.Y. Guo
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
K.M. Wu
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
*
*Author for correspondence: Phone: +86 10 61815929 Fax: +86 10 61815929 E-mail: gmliang@ippcaas.cn
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Abstract

Evolution of resistance to insecticides usually has fitness tradeoffs associated with adaptation to the stress. The basic regulation mechanism of tradeoff between reproduction and resistance evolution to Bacillus thuringiensis (Bt) toxin in the cotton bollworm, Helicoverpa armigera (Ha), based on the vitellogenin (Vg) gene expression was analyzed here. The full-length cDNA of the Vg gene HaVg (JX504706) was cloned and identified. HaVg has 5704 base pairs (bp) with an open reading frame (ORF) of 5265 bp, which encoded 1756 amino acid protein with a predicted molecular mass of 197.28 kDa and a proposed isoelectric point of 8.74. Sequence alignment analysis indicated that the amino acid sequence of HaVg contained all of the conserved domains detected in the Vgs of the other insects and had a high similarity with the Vgs of the Lepidoptera insects, especially Noctuidae. The resistance level to Cry1Ac Bt toxin and relative HaVg mRNA expression levels among the following four groups: Cry1Ac-susceptible strain (96S), Cry1Ac-resistant strain fed on artificial diet with Bt toxin for 135 generations (BtR stands for the Cry1Ac Bt resistance), progeny of the Cry1Ac-resistant strain with a non-Bt-toxin artificial diet for 38 generations (CK1) and the direct descendants of the 135th-generation resistant larvae which were fed on an artificial diet without the Cry1Ac protein (CK2) were analyzed. Compared with the 96S strain, the resistance ratios of the BtR strain, the CK1 strain and the CK2 strain were 2917.15-, 2.15- and 2037.67-fold, respectively. The maximum relative HaVg mRNA expression levels of the BtR strain were approximately 50% less than that of the 96S strain, and the coming of maximum expression was delayed for approximately 4 days. The overall trend of the HaVg mRNA expression levels in the CK1 strain was similar to that in the 96S strain, and the overall trend of the HaVg mRNA expression levels in the CK2 strain was similar to that in the BtR strain. Our results suggest that the changes in reproduction due to the Bt-toxin resistance evolution in the BtR strain may be regulated by the Vg gene expression. The down-regulation of HaVg at the early stages resulted in a period of delayed reproduction and decreased fecundity in the BtR strain. This performance disappeared when the Bt-toxin selection pressure was lost.

Keywords

tradeoffreproductionBt-toxin resistancevitellogeninmRNA expression
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 4 , August 2014 , pp. 444 - 452
Copyright
Copyright © Cambridge University Press 2014 

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Footnotes

†

Both of the authors contributed equally to this manuscript.

References

Akasaka, M., Harada, Y. & Sawada, H. (2010) Vitellogenin C-terminal fragments participate in fertilization as egg-coat binding partners of sperm trypsin-like proteases in the ascidian Halocynthia roretzi . Biochemical and Biophysical Research Communications 392, 479–484.CrossRefGoogle ScholarPubMed
Akhurst, R.J., James, W., Bird, L.J. & Beard, C. (2003) Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 96, 1290–1299.CrossRefGoogle Scholar
Amdam, G.V., Norberg, K., Page, R.E., Erber, J. & Scheiner, R. (2006) Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behavioral Brain Research 169, 201–205.CrossRefGoogle ScholarPubMed
Baker, M.E. (1988) Invertebrate vitellogenin is homologous to human von Willebrand factor. Journal of Biological Chemistry 256, 1059–1061.Google ScholarPubMed
Cervera, A., Maymo, A.C., Martinez-Pardo, R. & Garcera, M.D. (2006) Vitellogenin polypeptide levels in one susceptible and one cadmium-resistant strain of Oncopeltus fasciatus (Heteroptera: Lygaeidae), and its role in cadmium resistance. Journal of Insect Physiology 52, 158–168.CrossRefGoogle ScholarPubMed
Chen, J.S., Sappington, T.W. & Raikhel, A.S. (1997) Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals ancient common ancestry. Journal of Molecular Evolution 44, 440–451.CrossRefGoogle ScholarPubMed
Corona, M., Velarde, R.A., Remolina, S., Moran-Laute, A., Wang, Y., Hughes, K.A. & Robinson, G.E. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences, USA 104, 7128–7133.CrossRefGoogle ScholarPubMed
Fitt, G.P. (1989) The ecology of Heliothissp in relation to agro ecological system. Annual Review of Entomology 34, 17–52.CrossRefGoogle Scholar
Gonzalez-Cabrera, J., Escriche, B., Tabashnik, B.E. & Ferre, J. (2003) Binding of Bacillus thuringiensis toxins in resistant and susceptible strains of pink bollworm (Pectinophora gossypiella). Insect Biochemistry and Molecular Biology 33, 929–935.CrossRefGoogle ScholarPubMed
Guidugli, K.R., Piulachs, M.D., Belles, X., Lourenco, A.P. & Simoes, Z.L. (2005) Vitellogenin expression in queen ovaries and in larvae of both sexes of Apis mellifera . Archives of Insect Biochemistry and Physiology 59, 211–218.CrossRefGoogle ScholarPubMed
Guo, Y.Y. (1997) Progress in the researches on migration regularity of Helicoverpa armigera and relationships between the pest and its host plants. Acta Entomologica Sinica 40, 1–6.Google Scholar
Hagedorn, H.H., Maddison, D.R. & Tu, Z.J. (1998) The evolution of vitellogenins, cyclorrhaphan yolk proteins and related molecules. Advances in Insect Physiology 27, 335–384.CrossRefGoogle Scholar
Havukainen, H., Halskau, O. & Amdam, G.V. (2011) Social pleiotropy and the molecular evolution of honey bee vitellogenin. Molecular Ecology 20, 5111–5113.CrossRefGoogle ScholarPubMed
Hirai, M., Watanabe, D., Kiyota, A. & Chinzei, Y. (1998) Nucleotide sequence of vitellogenin mRNA in the bean bug, Riptortus clavatus: analysis of processing in the fat body and ovary. Insect Biochemistry and Molecular Biology 28, 537–547.CrossRefGoogle ScholarPubMed
Hiremath, S. & Lehtoma, K. (1997) Complete nucleotide sequence of the vitellogenin mRNA from the Gypsy Moth . Insect Biochemistry and Molecular Biology 27, 27–25.CrossRefGoogle ScholarPubMed
Hwang, D.S., Lee, W., Han, J., Park, H.G., Lee, J., Lee, Y.M. & Lee, J.S. (2010) Molecular characterization and expression of vitellogenin (Vg) genes from the cyclopoid copepod, Paracyclopina nana exposed to heavy metals. Comparative Biochemistry and Physiology C-toxicology & Pharmacology 151, 360–368.CrossRefGoogle ScholarPubMed
James, C. (2007) Global Status of Commercialized Biotech/GM Crops. ISAAA Briefs No. 37. Ithaca, NY, International Service for the Acquisition of Agri-Biotech Applications.Google Scholar
Koywiwattrakul, P. & Sittipraneed, S. (2009) Expression of vitellogenin and transferrin in activated ovaries of worker honey bees, Apis mellifera . Biochemical Genetics 47, 19–26.CrossRefGoogle ScholarPubMed
Li, A.K., Sadasivam, M. & Ding, J.L. (2003) Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E-The first three ligand-binding repeats of VtgR interact with the amino-terminal region on Vtg. Journal of Biological Chemistry 278, 2799–2806.CrossRefGoogle ScholarPubMed
Liang, G.M., Tan, W.J. & Guo, Y.Y. (2000) Study on screening and inheritance mode of resistance to Bt transgenic cotton in cotton bollworm. Acta Entomologica Sinica 43, 57–62.Google Scholar
Liang, G.M., Wu, K.M., Rector, B. & Guo, Y.Y. (2007) Diapause, cold hardiness and flight ability of Cry1Ac-resistant and -susceptible strains of Helicoverpa armigera (Lepidoptera: Noctuidae). European Journal of Entomology 104, 699–704.CrossRefGoogle Scholar
Liang, G.M., Wu, K.M., Yu, H.K., Li, K.K., Feng, X. & Guo, Y.Y. (2008) Changes of inheritance mode and fitness in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) along with its resistance evolution to Cry1Ac toxin. Journal of Invertebrate Pathology 97, 142–149.CrossRefGoogle ScholarPubMed
Liu, C.X., Li, Y.H., Gao, Y.L., Ning, C.M. & Wu, K.M. (2010) Cotton bollworm resistance to Bt transgenic cotton: A case analysis. Science China Life Sciences 53, 934–941.CrossRefGoogle Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data usingreal-time quantitative PCR and the 2−ΔΔCT Method. Methods 25, 402–408.CrossRefGoogle Scholar
Lu, Y.H., Wu, K.M., Jiang, Y.Y., Guo, Y.Y. & Desneux, N. (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487, 362–365.CrossRefGoogle ScholarPubMed
Luttrell, R.G., Fitt, G.P., Ramalho, F.S. & Sugonyaev, E.S. (1994) Cotton pest management: part I A worldwide perspective. Annual Review of Entomology 39, 517–526.CrossRefGoogle Scholar
Nakamura, A., Yasuda, K., Adachi, H., Sakurai, Y., Ishii, N. & Goto, S. (1999) Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans . Biochemical and Biophysical Research Communications 264, 580–583.CrossRefGoogle Scholar
Pateraki, L.E. & Stratakis, E. (2000) Synthesis and organization of vitellogenin and vitellin molecules from the land crab Potamon potamios . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 125, 53–61.CrossRefGoogle ScholarPubMed
Piulachs, M.D., Guidugli, K.R., Barchuk, A.R., Cruz, J., Simões, Z.L.P. & Bellés, X. (2003) The vitellogenin of the honey bee, Apis mellifera: structural analysis of the cDNA and expression studies. Insect Biochemistry and Molecular Biology 33, 459–465.CrossRefGoogle ScholarPubMed
Provost-Javier, K.N., Chen, S. & Rasgon, J.L. (2010) Vitellogenin gene expression in autogenous Culex tarsalis . Insect Molecular Biology 19, 423–429.CrossRefGoogle ScholarPubMed
Raybould, A. (2012) Can science justify regulatory decisions about the cultivation of transgenic crops? Transgenic Research 21, 691–698.CrossRefGoogle ScholarPubMed
Russell, R.M., Robertson, J.L. & Savin, N.E. (1977) POLO: a new computer program for probit analysis. Review Entomology Socity Amercian 23, 209–215.Google Scholar
Sappington, T.W. & Raikhel, A.S. (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology 28, 277–300.CrossRefGoogle ScholarPubMed
Shinoda, T., Miura, K., Taylor, D. & Chinzei, Y. (1996) Vitellogenin and vitellin in the bean bug, Riptortus clavatus (Hemiptera:Alydidae): purification, immunological identification, and induction by juvenile hormone. Archives of Insect Biochemistry and Physiology 31, 395–412.3.0.CO;2-V>CrossRefGoogle Scholar
Shu, Y.H., Zhou, J.J., Tang, W.C., Lu, K.L., Zhou, Q. & Zhang, G.R. (2009) Molecular characterization and expression pattern of Spodoptera litura (Lepidoptera: Noctuidae) vitellogenin, and its response to lead stress. Journal of Insect Physiology 55, 608–616.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Carriere, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M. & Zhao, J.Z. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology 96, 1031–1038.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Dennehy, T.J. & Carriere, Y. (2005) Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences, USA 102, 15389–15393.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. & Carriere, Y. (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotechnology 26, 199–202.CrossRefGoogle ScholarPubMed
Tabashnik, B.E., Wu, K.M. & Wu, Y.D. (2012) Early detection of field-evolved resistance to Bt cotton in China: cotton bollworm and pink bollworm. Journal of Invertebrate Pathology 110, 301–306.CrossRefGoogle Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Telfer, W.H. (2009) Egg formation in Lepidoptera. Journal of Insect Science 9, 1–21.CrossRefGoogle ScholarPubMed
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Thompson, J.R. & Banaszak, L.J. (2002) Lipid-protein interactions in lipovitellin. Biochemistry 41, 9398–9409.CrossRefGoogle ScholarPubMed
Tufail, M. &Takeda, M. (2008) Molecular characteristics of insect vitellogenins. Journal of Insect Physiology 54, 1447–1458.CrossRefGoogle ScholarPubMed
Tufail, M. & Takeda, M. (2009) Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. Journal of Insect Physiology 55, 87–103.CrossRefGoogle ScholarPubMed
Tufail, M., Lee, J.M., Hatakeyama, M., Oishi, K. & Takeda, M. (2000) Cloning of vitellogenin cDNA of the American cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Archives of Insect Biochemistry and Physiology 45, 37–46.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Tufail, M., Naeemullah, M., Elmogy, M., Sharma, P.N., Takeda, M. & Nakamura, C. (2010) Molecular cloning, transcriptional regulation, and differential expression profiling of vitellogenin in two wing-morphs of the brown planthopper, Nilaparvata lugens Stal (Hemiptera: Delphacidae). Insect Molecular Biology 19, 787–798.CrossRefGoogle ScholarPubMed
Wu, K.M. & Guo, Y.Y. (2005) The evolution of cotton pest management practices in China. Annual Review of Entomology 50, 31–52.CrossRefGoogle ScholarPubMed
Wu, K.M., Guo, Y.Y. & Gao, S.S. (2002 a) Evaluation of the natural refuge function for Helicoverpa armigera (Lepidoptera: Noctuidae) within Bacillus thuringiensis transgenic cotton growing areas in north China. Journal of Economic Entomology 95, 832–837.CrossRefGoogle ScholarPubMed
Wu, K.M., Guo, Y.Y., Lv, N., Greenplate, J.T. & Deaton, R. (2002 b) Resistance monitoring of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis insecticidal protein in China. Journal of Economic Entomology 95, 826–831.CrossRefGoogle ScholarPubMed
Wu, K.M., Lu, Y.H., Feng, H.Q., Jiang, Y.Y. & Zhao, J.Z. (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321, 1676–1678.CrossRefGoogle Scholar
Ye, G.Y., Dong, S.Z., Song, Q.S., Shi, M., Chen, X.X. & Hu, C. (2008) Molecular cloning and developmental expression of the vitellogenin gene in the endoparasitoid, Pteromalus puparum . Insect Molecular Biology 17, 227–233.CrossRefGoogle ScholarPubMed
Zhang, H.N., Wei, Y., Zhao, J., Jin, L., Yang, Y.H., Wu, S.W., Tabashnik, B.E. & Wu, Y.D. (2011) Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLOS ONE 6, e22874.CrossRefGoogle ScholarPubMed
Zhang, H.N., Tian, W., Zhao, J., Jin, L., Yang, J., Liu, C.H., Yang, Y.H., Wu, S.W., Wu, K.M., Cui, J.J., Tabashnik, B.E. & Wu, Y.D. (2012) Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proceedings of the National Academy of Sciences, USA 109, 10275–10280.CrossRefGoogle ScholarPubMed
Zhao, X.C., Wu, K.M. & Guo, Y.Y. (2007) Comparisons of calling behaviour of different geographical populations of Helicoverpa armigera . Journal of Applied Entomology 131, 684–689.CrossRefGoogle Scholar
Zhao, X.C., Wu, K.M., Liang, G.M. & Guo, Y.Y. (2008) Altered mating behaviour in a Cry1Ac-resistant strain of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Applied Entomology 132, 360–365.CrossRefGoogle Scholar
Zou, L.Y., Li, Y.M., Zhang, Y., Wei, J.Z., Liang, G.M. & Guo, Y.Y. (2012) Stability of resistance to Cry1Ac and its effects on relative fitness in Helicoverpa armigera (Hübner). Acta Phytophylacica Sinica 39(1), 70–74.Google Scholar
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