Early detection of field-evolved resistance to Bt cotton in China: Cotton bollworm and pink bollworm

Journal of Invertebrate Pathology

Volumn 110, Issue 3, 2012, Pages 301-306

  Tabashnik, Bruce E ^a   Wu, Kongming ^b   Wu, Yidong ^c  

^a UNIVERSITY OF ARIZONA   (United States)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Evolution; Genetic engineering; Helicoverpa armigera; Pectinophora gossypiella; Resistance management; Transgenic crops

Indexed keywords

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

ANIMAL; BACILLUS THURINGIENSIS; BIOLOGICAL PEST CONTROL; CHINA; DRUG EFFECT; GENETICS; GOSSYPIUM; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; INSECTICIDE RESISTANCE; LARVA; LD 50; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOTH; PARASITOLOGY; PATHOGENICITY; REVIEW; TRANSGENIC PLANT;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; CHINA; ENDOTOXINS; GOSSYPIUM; HEMOLYSIN PROTEINS; HOST-PARASITE INTERACTIONS; INSECTICIDE RESISTANCE; INSECTICIDES; LARVA; LETHAL DOSE 50; MOTHS; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED;

BACILLUS THURINGIENSIS; GOSSYPIUM HIRSUTUM; HELICOVERPA ARMIGERA; HEXAPODA; PECTINOPHORA GOSSYPIELLA;

EID: 84861926979     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2012.04.008     Document Type: Review

References (45)

1. Alcantara E., Estrada A., Alpuerto V., Head G. Monitoring Cry1Ab susceptibility in Asian corn borer (Lepidoptera: Crambidae) on Bt corn in the Philippines. Crop Prot. 2011, 30:554-559.
2. An J., Gao Y., Wu K., Gould F., Gao J., Shen Z., Lei C. Vip3Aa tolerance response of Helicoverpa armigera populations from a Cry1Ac cotton planting region. J. Econ. Entomol. 2010, 103:2169-2173.
3. Bagla P. Hardy cotton-munching pests are latest blow to GM crops. Science 2010, 327:1439.
4. Carriere Y., Crowder D.W., Tabashnik B.E. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 2010, 3:561-573.
5. Chinese Ministry of Agriculture, 2010. Agricultural Yearbook of China (2000-2010). Chinese Agricultural Press, Beijing, China.
6. Dhurua S., Gujar G.T. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. 2011, 67:898-903.
7. Downes S., Mahon R.J., Rossiter L., Kauter G., Leven T., Fitt G., Baker G. Adaptive management of pest resistance by Helicoverpa species (Noctuidae) in Australia to the Cry2Ab Bt toxin in Bollgard II® cotton. Evol. Appl. 2010, 3:574-584.
8. Downes S., Parker T., Mahon R. Incipient resistance of Helicoverpa punctigera to the Cry2Ab Bt toxin in Bollgard II® cotton. PLoS ONE 2010, 5:e12567.
9. Gao Y., Wu K., Gould F., Shen Z. Cry2Ab tolerance response of Helicoverpa armigera (Lepidoptera: Noctuidae) populations from Cry1Ac cotton planting region. J. Econ. Entomol. 2009, 102:1217-1223.
10. Gassmann A.J., Petzold-Maxwell J.L., Keweshan R.S., Dunbar M.W. Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 2011, 6:e22629.
11. Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 1998, 43:701-726.
12. Guo S. Engineering of insect-resistant plant with Bacillus thuringiensis crystal protein genes. Scientia Agricultura Sinica 1995, 28:8-13. (in Chinese with English abstract).
13. Huang F., Andow D.A., Buschman L.L. Success of the high-dose/refuge resistance management strategy after 15years of Bt crop use in North America. Entomol. Exp. Appl. 2011, 140:1-16.
14. James, C., 2011. Global status of commercialize biotech/GM crops: 2011. ISAAA Brief No. 43. Ithaca, New York.
15. Li G., Wu K., Gould F., Wang J., Miao J., Gao X., Guo Y. Increasing tolerance to Cry1Ac cotton from cotton bollworm, Helicoverpa armigera, was confirmed in Bt cotton farming area of China. Ecol. Entomol. 2007, 32:366-375.
16. Li G.P., Feng H.Q., Gao Y.L., Wyckhuys K.A.C., Wu K.M. Frequency of Bt resistance alleles in Helicoverpa armigera in the Xinjiang cotton-planting region of China. Environ. Entomol. 2010, 39:1698-1704.
17. Liu F., Xu Z., Zhu Y.C., Huang F., Wang Y., Li H., Gao C., Zhou W., Shen J. Evidence of field-evolved resistance to Cry1Ac-expressing Bt cotton in Helicoverpa armigera (Lepidoptera: Noctuidae) in northern China. Pest Manag. Sci. 2010, 66:155-161.
18. Lu Y., Wu K., Jiang Y., Xia B., Li P., Feng H., Wyckhuys K.A., Guo Y. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 2010, 328:1151-1154.
19. Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellers-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carrière Y. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. USA 2003, 100:5004-5009.
20. Sanahuja G., Banakar R., Twyman R.M., Capell T., Christou P. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J. 2011, 9:283-300.
21. Stone G.D. Biotechnology and the political ecology of information in India. Human Organization. 2004, 63:127-140.
22. Storer N.P., Babcock J.M., Schlenz M., Meade T., Thompson G.D., Bing J.W., Huckaba R.M. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 2010, 103:1031-1038.
23. Tabashnik B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 1994, 39:47-79.
24. Tabashnik B.E. Delaying insect resistance to transgenic crops. Proc. Natl. Acad. Sci. USA 2008, 105:19029-19030.
25. Tabashnik B.E., Dennehy T.J., Sims M.A., Larkin K., Head G.P., Moar W.J., Carriere Y. Control of resistant pink bollworm (Pectinophora gossypiella) by transgenic cotton that produces Bacillus thuringiensis toxin Cry2Ab. Appl. Environ. Microbiol. 2002, 68:3790-3794.
26. Tabashnik B.E., Dennehy T.J., Carrière Y. Delayed resistance to transgenic cotton in pink bollworm. Proc. Natl. Acad. Sci. USA 2005, 102:15389-15393.
27. Tabashnik B.E., Gassmann A.J., Crowder D.W., Carrière Y. Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol. 2008, 26:199-202.
28. Tabashnik B.E., Unnithan G.C., Masson L., Crowder D.W., Li X., Carrière Y. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc. Natl. Acad. Sci. USA 2009, 106:11889-11894.
29. Tabashnik B.E., Van Rensburg J., Carrière Y. Field-evolved insect resistance to Bt crops: definition, theory, and data. J. Econ. Entomol. 2009, 102:2011-2025.
30. Tabashnik B.E., Sisterson M.S., Ellsworth P.C., Dennehy T.J., Antilla L., Liesner L., Whitlow M., Staten R.T., Fabrick J.A., Unnithan G.C. Suppressing resistance to Bt cotton with sterile insect releases. Nat. Biotechnol. 2010, 28:1304-1307.
31. Tabashnik, B.E., Morin, S., Unnithan, G.C., Yelich, A.J., Ellers-Kirk, C., 2012. Sustained susceptibility of pink bollworm to Bt Cotton in the United States. GM Crops 3, Available from: <>. http://www.landesbioscience.com/journals/gmcrops/toc/volume/3/issue/3/.
32. Van Rensburg J.B.J. First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S. Afr. J. Plant Soil. 2007, 24:147-151.
33. Wan P., Wu K., Huang M., Wu J. Seasonal pattern of infestation by pink bollworm Pectinophora gossypiella (Saunders) in field plots of Bt transgenic cotton in the Yangtze River Valley of China. Crop Prot. 2004, 23:463-467.
34. Wan P., Zhang Y., Wu K., Huang M. Seasonal expression profiles of insecticidal protein and control efficacy against Helicoverpa armigera for Bt cotton in the Yangtze River valley of China. J. Econ. Entomol. 2005, 98:195-201.
35. Wan P., Huang Y., Wu H., Huang M., Cong S., Tabashnik B.E., Wu K. Increased frequency of pink bollworm resistance to Bt toxin Cry1Ac in China. PLoS ONE 2012, 7:e29975.
36. Wu K. Monitoring and management strategy for Helicoverpa armigera resistance to Bt cotton in China. J. Invertbr. Pathol. 2007, 95:220-223.
37. Wu K., Guo Y. The evolution of cotton pest management practices in China. Annu. Rev. Entomol. 2005, 50:31-52.
38. Wu K., Guo Y., Lv N. Geographic variation in susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis insecticidal protein in China. J. Econ. Entomol. 1999, 92:273-278.
39. Wu K., Guo Y., Gao S. Evaluation of the natural refuge function for Helicoverpa armigera (Lepidoptera: Noctuidae) within Bacillus thuringiensis transgenic cotton growing areas in North China. J. Econ. Entomol. 2002, 95:832-837.
40. Wu K.M., Lu Y.H., Feng H.Q., Jiang Y.Y., Zhao J.Z. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 2008, 321:1676-1678.
41. Xu X., Yu L., Wu Y. Disruption of a cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 2005, 71:948-954.
42. Yang Y., Chen H., Wu Y., Wu S. Mutated cadherin alleles from a field population of Helicoverpa armigera confer resistance to Bacillus thuringiensis toxin Cry1Ac. Appl. Environ. Microbiol. 2007, 73:6939-6944.
43. Yu S., Fan S. Research and commercialization of national Bt cotton in China. Biobusiness 2010, 35-41. (in Chinese).
44. Zhang H., Yin W., Zhao J., Jin L., Yang Y., Wu S., Tabashnik B.E., Wu Y. Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLoS ONE 2011, 6:e22874.
45. Zhao J.Z., Cao J., Li Y., Collins H.L., Roush R.T., Earle E.D., Shelton A.M. Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 2003, 21:1493-1497.