Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry1Ac and Cry2Ab2 insecticidal proteins in four countries of the west african cotton belt

Journal of Economic Entomology

Volumn 102, Issue 6, 2009, Pages 2301-2309

  Brvault, T ^a,b   Prudent, P ^a,c,d   Vaissayre, M ^a   Carrire, Y ^b  

^a CIRAD   (France)

^b UNIVERSITY OF ARIZONA   (United States)

^c IRAD   (Cameroon)

^d INRAB CRA CF ^*  (Benin)

Author keywords

Bacillus thuringiensis; Bollworm; Cotton; Resistance; Transgenic crops

Indexed keywords

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; INSECTICIDE;

AFRICA; ANIMAL; ARTICLE; COTTON; GENETICS; INSECTICIDE RESISTANCE; MOTH; PARASITOLOGY; TRANSGENIC PLANT;

AFRICA, CENTRAL; AFRICA, WESTERN; ANIMALS; BACTERIAL PROTEINS; ENDOTOXINS; GOSSYPIUM; HEMOLYSIN PROTEINS; INSECTICIDE RESISTANCE; INSECTICIDES; MOTHS; PLANTS, GENETICALLY MODIFIED;

BACILLUS THURINGIENSIS; GOSSYPIUM HIRSUTUM; HELICOVERPA ARMIGERA; HELICOVERPA ZEA; LEPIDOPTERA; NOCTUIDAE;

EID: 72449186278     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1603/029.102.0636     Document Type: Article

References (50)

1. Adamczyk, J. J., L. C. Adams, and D. D. Hardee. 2001. Field efpcacy and seasonal expression proples for terminal leaves of single and double Bacillus thuringiensis toxin cotton genotypes. J. Econ. Entomol. 94: 1589-1593.
2. Akhurst, R. J.,W.James, and L. Bird. 2003. Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 96: 1290-1299.
3. Ali, M. I., R. G. Luttrell, and S. Y. Young. 2006. Susceptibilities of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) populations to Cry1Ac insecticidal protein. J. Econ. Entomol. 99: 164-175.
4. Ali, M. I., and R. G. Luttrell. 2007. Susceptibility of bollworm and tobacco budworm (Lepidoptera: Noctuidae) to Cry2Ab2 Insecticidal Protein. J. Econ. Entomol. 100: 921-931.
5. Anilkumar, K. J., A. Rodrigo-Simon, J. Ferré, M. Pusztai- Carey, S. Sivasupramaniam, and J. Moar. 2008. Production and characterization of Bacillus thuringiensis Cry1Ac-resistant cotton bollworm Helicoverpa zea (Boddie). Appl. Environ. Microbiol. 74: 426-469.
6. Avilla, C., E. Vargas-Osuna, J. Gonzalez-Cabrera, J. Ferré, and J. E. Gonzalez-Zamora. 2005. Toxicity of several delta- endotoxins of Bacillus thuringiensis against Helicoverpa armigera (Lepidoptera: Noctuidae) from Spain. J. Invertebr. Pathol. 90: 51-54.
7. Bird, L. J., and R. J. Akhurst. 2007. Variation in susceptibility of Helicoverpa armigera (Hübner) and Helicoverpa punctigera (Wallengren) (Lepidoptera: Noctuidae) in Australia to two Bacillus thuringiensis toxins. J. Invertebr. Pathol. 94: 84-94.
8. Blanco, C. A., N. P. Storer, C. A. Abel, R. Jackson, R. Leonard, J. D. Lopez, G. Payne, B. D. Siegfried, T. Spencer, and A. P. Teran-Vargas. 2008. Baseline susceptibility of tobacco budworm (Lepidoptera: Noctuidae) to Cry1F toxin from Bacillus thuringiensis. J. Econ. Entomol. 101: 168-173.
9. [CIRAD] Centre de coopération Internationale en Recherche Agronomique pour le Développement. 1999. WINDL, version 2.0. Centre de coopé ration Internationale en Recherche Agronomique pour le Développement, Montpellier, France.
10. Couilloud, R.,andM.Giret. 1980. Multiplication dÕHelicoverpa armigeraHübner: améliorations possibles grâce à lÕadoption dÕune technique dÕélevage en groupe des chenilles. Cot. Fib. Trop. 35: 217-224.
11. Downes, S. J., R. Mahon, and K. Olsen. 2007. Adaptive resistance management in Australia for Bt-cotton: current status and future challenges. J. Invertebr. Pathol. 95: 208-213.
12. Estela, A., B. Escriche, and J. Ferré. 2004. Interaction of Bacillus thuringiensis toxins with larval midgut binding sites of Helicoverpa armigera (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 70: 1378-1384.
13. Finney, D. J. 1971. Probit analysis. Cambridge University Press, Cambridge, United Kingdom.
14. Fitt, G., D. A. Andow, Y. Carrière, W. A. Moar, T. Schuler, C. Omoto, J. Kanya, M. Okech, P. Arama, and N. K. Maniania. 2004. Resistance risks and management associated with Bt maize in Kenya. Chapter 7, pp. 209-250. In A. Hilbeck and D. Andow [eds.], Environmental risk assessment of genetically modiped organisms, volume 1: a case study of Bt maize in Kenya. CABI International, Wallingford, United Kingdom.
15. Gajendra, Babu, B., V. Udayasuriyan, M. Asia Mariam, N. C. Sivakumar, M. Bharathi, and G. Balasubramaniam. 2002. Comparative toxicity of Cry1Ac and Cry2Aa--endotoxins of Bacillus thuringiensis against Helicoverpa armigera (H.). Crop Prot. 21: 817-822.
16. Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43: 701-726.
17. Gould, F., M. B. Cohen, J. S. Bentur, G. G. Kennedy, and J. Van Duyn. 2006. Impact of small ptness costs on pest adaptation to crop varieties with multiple toxins: a heuristic model. J. Econ. Entomol. 99: 2091-2099.
18. Greenplate, J. T., J. W. Mullins, S. R. Penn, A. Dahm, B. J. Reich, J. A. Osborn, P. R. Rahn, L. Ruschke, and Z. W. Shappley. 2003. Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative contribution, toxin interaction, and resistance management. J. Appl. Entomol. 127: 340-347.
19. Gujar, G. T., R. Nair, B. P. Singh, A. Kumari, and V. Kalia. 2008. Toxicity to the cotton bollworm, Helicoverpa armigera, of some Cry1Ac toxins expressed in cotton in India. Crop Prot. 27: 537-544.
20. Gujar, G. T., V. Kalia, A. Kumari, B. P. Singh, A. Mittal, R. Nair, and M. Mohan. 2007. Helicoverpa armigera baseline susceptibility to Bacillus thuringiensis (Bt) Cry toxins and resistance management for Bt cotton in India. J. Invertebr. Pathol. 95: 214-219.
21. Hema, O., H. N. Somé, O. Traoré, J. Greenplate, and M. Abdennadher. 2009. Efpcacy of transgenic cotton plant containing the Cry1Ac and Cry2Ab genes of Bacillus thuringiensis against Helicoverpa armigera and Syllepte derogata in cotton cultivation in Burkina Faso. Crop Prot. 28: 205-214.
22. Ibargutxi, M., D. Muñoz, I. Ruíz de Escudero, and P. Caballero. 2008. Interactions between Cry1Ac, Cry2Ab, and Cry1Fa Bacillus thuringiensis toxins in the cotton pests Helicoverpa armigera (Hübner) and Earias insulana (Boisduval). Biol. Control 47: 89-96.
23. Jalali, S. K., K. S. Mohan, S. P. Singh, T. M. Manjuntah, and Y. Lalitha. 2004. Baseline susceptibility of the old-world bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) populations from India to Bacillus thuringiensis Cry1Ac insecticidal protein. Crop Prot. 23: 53-59.
24. James, C. 2008. Global Status of Commercialized Biotech/ GM crops: 2008. ISAAA Brief No. 39. International Service for the Acquisition of Agri-biotech Applications, Ithaca, NY.
25. Kranthi, K. R., S. Kranthi, and R. R. Wanjari. 2001. Baseline toxicity of Cry1A toxins to Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) in India. Int. J. Pest Manag. 47: 141-145.
26. Kranthi, S., C. S. Dhawad, S. Naidu, A. Bharose, A. Chaudhary, V. Sangode, S. K. Nehare, S. R. Bajaj, and K. R. Kranthi. 2009. Susceptibility of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) to the Bacillus thuringiensis toxin Cry2Ab before and after the introduction of Bollgard-II. Crop Prot. 28: 371-375.
27. Kruger, M., J.B.J. Van Rensburg, and J. Van den Berg. 2009. Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot. 28: 684-689.
28. Liao, C., D. G. Heckel, and R. Akhurst. 2002. Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae), major pests of cotton. J. Invertebr. Pathol. 80: 55-63.
29. Liu, F., Z. Xu, J. Chang, J. Chen, F. Meng, Y. C. Zhu, and J. Shen. 2008. Resistance Allele frequency to Bt cotton in peld populations of Helicoverpa armigera (Lepidoptera: Noctuidae) in China. J. Econ. Entomol. 101: 933-943.
30. Luo, S. D., K. M. Wu, Y. Tian, G. M. Liang, X. Feng, J. Zhang, and Y. Y. Guo. 2007. Cross-resistance studies of Cry1 Cry1Acresistant strains of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry2Ab. J. Econ. Entomol. 100: 909-915.
31. Luttrell, R. G., L. Wan, and K. Knighten. 1999. Variation in susceptibility of noctuid (Lepidoptera) larvae attacking cotton and soybean to puriped endotoxin proteins and commercial formulations of Bacillus thuringiensis. J. Econ. Entomol. 92: 21-32.
32. Mahon, R. J., K. M. Olsen, K. A. Garsia, and S. R. Young. 2007. Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 100: 894-902.
33. Mahon, R. J., and K. M. Olsen. 2009. Limited survival of a Cry2Ab-resistant strain of Helicoverpa armigera (Lepidoptera: Noctuidae) on Bollgard II. J. Econ. Entomol. 102: 708-716.
34. Olsen, K. M., and J. C. Daly. 2000. Plant-toxin interactions in transgenic Bt cotton and their effect on mortality of Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 93: 1293-1299.
35. Rossiter, M., W. G. Yendol, and N. R. Dubois. 1990. Resistance to Bacillus thuringiensis in gypsy moth (Lepidoptera: Lymantriidae): genetic and environmental causes. J. Econ. Entomol. 83: 221-2218.
36. Roush, R. T. 1998. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos. Trans. R. Soc. Lond. B 353: 1777-1786.
37. Siegfried, B. D., T. Spencer, and J. Nearman. 2000. Baseline susceptibility of the Corn Earworm (Lepidoptera: Noctuidae) to the Cry1Ab toxin from Bacillus thuringiensis. J. Econ. Entomol. 93: 1265-1268.
38. Sivasupramaniam, S., W. J. Moar, L. G. Ruschke, A. Osborn, C. Jiang, J. L. Sebaugh, G. R. Brown, Z.W.Shappley, M. E. Oppenhuizen, J. W. Mullins, and J. T. Greenplate. 2008. Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of lepidopteran pests. J. Econ. Entomol. 101: 546-554.
39. Showalter, A. M., S. Heuberger, B. E. Tabashnik, and Y. Carrière. 2009a. A primer for the use of insecticidal transgenic cotton in developing countries. J. Insect Sci. (insectscience.org/9.22).
40. Showalter, A. M., S. Heuberger, B. E. Tabashnik, and Y. Carriè re. 2009b. Development, Agronomic performance and Sustainability of Transgenic Cotton for Insect Control, pp. 49-71. In R. Tripp [ed.], Biotechnology and agricultural development. Transgenic cotton, rural institutions and resource-poor farmers. Routledge, London, United Kingdom.
41. Stone, T. B., and S. R. Sims. 1993. Geographic susceptibility of Heliothis virescens and Helicoverpa zea (Lepidoptera: Noctuidae) to Bacillus thuringiensis. J. Econ. Entomol. 86: 989-994.
42. Tabashnik, B. E. 1992. Evaluation of synergism among Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 58: 3343-3346.
43. Tabashnik, B. E. 2008. Delaying insect resistance to transgenic crops. Proc. Nat. Acad. Sci. USA. 105: 19029-19030.
44. Tabashnik, B. E., A. J. Gassmann, D. W. Crowder, and Y. Carrière. 2008a. Insect resistance to Bt crops: evidence versus theory. Nat. Biotech. 26: 199-202.
45. Tabashnik, B. E., A. J. Gassmann, D. W. Crowder, and Y. Carrière. 2008b. Field-evolved resistance to Bt toxins. Nat. Biotech. 26: 1074-1076.
46. Tabashnik, B. E., G. C. Unnithan, L. Masson, D. W. Crowder, X. Li, and Y. Carrière. 2009. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc. Nat. Acad. Sci. USA. 29: 11889-11894.
47. Vitale, J., H. Glick, J. Greenplate, M. Abdennadher, and O. Traoré. 2008. Second-generation Bt cotton peld trials in Burkina Faso: Analyzing the potential benepts to West African farmers. Crop Sci. 48: 1958-1966.
48. Wu, K., Y. Guo, and N. Lv. 1999. Geographic variation in susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis insecticidal protein in China. J. Econ. Entomol. 92: 273-278.
49. Wu, K., Y. Guo, and G. Head. 2006. Resistance Monitoring of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bt Insecticidal Protein During 2001-2004 in China. J. Econ. Entomol. 99: 893-898.
50. Zhao, J. Z., J. Cao, H. L. Collins, S. L. Bates, R. T. Roush, E. D. Earle, and A. M. Shelton. 2005. Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc. Nat. Acad. Sci. USA. 102: 8426-8430.