Impacts of Bt rice expressing Cry1C or Cry2A protein on the performance of nontarget leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae), under laboratory and field conditions

Environmental Entomology

Volumn 43, Issue 1, 2014, Pages 209-217

  Lu, Z B ^a   Tian, J C ^b   Wang, W ^a   Xu, H X ^b   Hu, C ^a   Guo, Y Y ^c   Peng, Y F ^c   Ye, G Y ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Bt rice; Cry1C; Cry2A; Nephotettix cincticeps; Nontarget herbivore

Indexed keywords

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

ANIMAL; ARTICLE; DRUG EFFECT; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; MALE; NYMPH; POPULATION DENSITY; POPULATION DYNAMICS; REPRODUCTION; RICE; TRANSGENIC PLANT;

ANIMALS; BACTERIAL PROTEINS; ENDOTOXINS; FEMALE; HEMIPTERA; HEMOLYSIN PROTEINS; INSECTICIDES; MALE; NYMPH; ORYZA SATIVA; PLANTS, GENETICALLY MODIFIED; POPULATION DENSITY; POPULATION DYNAMICS; REPRODUCTION;

EID: 84893707018     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN13160     Document Type: Article

References (64)

1. Akhtar, Z. R., J. C. Tian, Y. Chen, Q. Fang, C. Hu, M. Chen, Y. F. Peng, and G. Y. Ye. 2010. Impacts of six Bt rice lines on nontarget rice feeding thrips under laboratory and field conditions. Environ. Entomol. 39: 715-726.
2. Akhtar, Z. R., J. C. Tian, Y. Chen, Q. Fang, C. Hu, Y. F. Peng, and G. Y. Ye. 2013. Impact of six transgenic Bacillus thuringiensis rice lines on four nontarget thrips species attacking rice panicles in the paddy field. Environ. Entomol. 42: 173-180.
3. Alcantara, E. P., R. M. Aguda, A. Curtiss, D. H. Dean, and M. B. Cohen. 2004. Bacillus thuringiensis delta-endotoxin binding to brush border membrane vesicles of rice stem borers. Arch. Insect Biochem. 55: 169-177.
4. Bashir, K., T. Husnain, T. Fatima, Z. Latif, S. A. Mehdi, and S. Riazuddin. 2004. Field evaluation and risk assessment of transgenic indica basmati rice. Mol. Breed. 13: 301-312.
5. Bernal, C. C., R. M. Aguda, and M. B. Cohen. 2002. Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol. Exp. Appl. 102: 21-28.
6. Carino, F. O., P. E. Kenmore, and V. A. Dyck. 1979. The FARMCOP suction sampler for hoppers and predators in flooded rice fields. Int. Rice Res. News 4: 21-22.
7. Carriere, Y., D. W. Crowder, and B. E. Tabashnik. 2010. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3: 561-573.
8. Chen, H., W. Tang, C. G. Xu, X. H. Li, Y. J. Lin, and Q. F. Zhang. 2005. Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theor. Appl. Genet. 111: 1330-1337.
9. Chen, H., G. A. Zhang, Q. F. Zhang, and Y. J. Lin. 2008. Effect of transgenic Bacillus thuringiensis rice lines on mortality and feeding behavior of rice stem borers (Lepidoptera: Crambidae). J. Econ. Entomol. 101: 182-189.
10. Chen, M., G. Y. Ye, C. Hu, and S. K. Datta. 2003. Effects of transgenic Bt indica rice on the feeding and oviposition behavior of the brown planthopper, Nilaparvata lugens. Acta Phytophyl. Sin. 30: 366-370.
11. Chen, M., G. Y. Ye, Z. C. Liu, H. W. Yao, X. X. Chen, S. Z. Shen, C. Hu, and S. K. Datta. 2006. Field assessment of the effects of transgenic rice expressing a fused gene of cry1Ab and cry1Ac from Bacillus thuringiensis Berliner on nontarget planthopper and leafhopper populations. Environ. Entomol. 35: 127-134.
12. Chen, M., Z. C. Liu, G. Y. Ye, Z. C. Shen, C. Hu, Y. F. Peng, I. Altosaar, and A. M. Shelton. 2007. Impacts of transgenic cry1Ab rice on non-target planthoppers and their main predator Cyrtorhinus lividipennis (Hemiptera: Miridae) - a case study of the compatibility of Bt rice with biological control. Biol. Control 42: 242-250.
13. Chen, M., A. M. Shelton, and G. Y. Ye. 2011. Insect-resistant genetically modified rice in China: from research to commercialization. Annu. Rev. Entomol. 56: 81-101.
14. Chen, Y., J. C. Tian, Z. C. Shen, Y. F. Peng, C. Hu, Y. Y. Guo, and G. Y. Ye. 2010. Transgenic rice plants expressing a fused protein of Cry1Ab/Vip3H has resistance to rice stem borers under laboratory and field conditions. J. Econ. Entomol. 103: 1444-1453.
15. Chen, Y., J. C. Tian, W. Wang, Q. Fang, Z. R. Akhtar, Y. F. Peng, H. Cui, Y. Y. Guo, Q. S. Song, and G. Y. Ye. 2012. Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens. Transgenic Res. 21: 279-291.
16. Cheng, J. A., and J. H. He. 1996. Rice insect pests. China Agriculture Press, Beijing, China.
17. Cheng, X. A., C. Chang, and S. M. Dai. 2010. Responses of striped stem borer, Chilo suppressalis (Lepidoptera: Pyralidae), from Taiwan to a range of insecticides. Pest Manag. Sci. 66: 762-766.
18. Cohen, M. B., M. Chen, J. S. Bentur, K. L. Heong, and G. Y. Ye. 2008. Bt rice in Asia: potential benefits, impact, and sustainability, pp. 223-248. In J. Romeis, A. M. Shelton, and E. J. Kennedy (eds.), Integration of insect-resistant genetically modified crops within IPM programs. Springer, Dordrecht, The Netherlands.
19. Conner, A. J., T. R. Glare, and J. P. Nap. 2003. The release of genetically modified crops into the environment - part II. Overview of ecological risk assessment. Plant J. 33: 19-46.
20. Fang, J. 2008. Vegetative insecticidal protein genes of Bacillus thuringiensis and expression in transgenic rice. Ph.D dissertation, Zhejiang University, Hangzhou, Zhejiang Province, China.
21. FAO. 2013. FAOSTAT. (http://faostat.fao.org/site/567/default.aspx).
22. Faria, C. A., F. L. Wäckers, J. Pritchard, D. A. Barrett, and T. C. Turlings. 2007. High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE 2: e600. doi:10.1371/journal.pone.0000600.
23. Fu, Q., F. Wang, D. H. Li, Q. Yao, F. X. Lai, and Z. T. Zhang. 2003. Effects of insect-resistant transgenic rice linesMSA andMSBon non-target pests Nilaparvata lugens and Sogatella fucifera. Acta Entomol. Sin. 46: 697-704.
24. Fujimoto, H., K. Itoh, M. Yamamoto, J. Kyozuka, and K. Shimamoto. 1993. Insect-resistant rice generated by introduction of a modified delta-endotoxin gene of Bacillus thuringiensis. Biotechnology 11: 1151-1155.
25. Haccou, P., and E. Meelis. 1992. Statistical analysis of behavioural data: an approach based on time-structured models. Oxford University Press, Oxford.
26. Hattori, M., M. Nakamura, S. Komatsu, K. Tsuchihara, Y. Tamura, and T. Hasegawa. 2012. Molecular cloning of a novel calcium-binding protein in the secreted saliva of the green rice leafhopper Nephotettix cincticeps. Insect Biochem. Mol. 42: 1-9.
27. He, Y. P., J. F. Zhang, J. M. Chen, and J. L. Shen. 2012. Using synergists to detect multiple insecticide resistance in field populations of rice stem borer. Pestic. Biochem. Physiol. 103: 121-126.
28. He, Y. P., J. F. Zhang, C. F. Gao, J. Y. Su, J. M. Chen, and J. L. Shen. 2013. Regression analysis of dynamics of insecticide resistance in field populations of Chilo suppressalis (Lepidoptera: Crambidae) during 2002-2011 in China. J. Econ. Entomol. 106: 1832-1837.
29. Heinrichs, E. A., F. G. Medrano, and H. R. Rapusas. 1985. Genetic evaluation for insect resistance in rice. International Rice Research Institute, Los Baños, Laguna, Philippines.
30. High, S. M., M. B. Cohen, Q. Y. Shu, and I. Altosaar. 2004. Achieving successful deployment of Bt rice. Trends Plant Sci. 9: 286-292.
31. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6: 65-70.
32. Huang, J. K., R. F. Hu, S. Rozelle, and C. Pray. 2005. InsectresistantGMrice in farmers' fields: assessing productivity and health effects in China. Science 308: 688-690.
33. Hutchison,W.D., E. C. Burkness, P. D. Mitchell, R. D. Moon, T. W. Leslie, S. J. Fleischer, M. Abrahamson, K. L. Hamilton, K. L. Steffey, M. E. Gray, et al. 2010. Area wide suppression of European corn borer with Bt maize reaps savings to non-Bt Maize growers. Science 330: 222-225.
34. James, C. 2012. Global status of commercialized biotech/GM crops: 2012, ISAAA Brief No. 44. ISAAA, Ithaca, NY.
35. Karim, S., and D. H. Dean. 2000. Toxicity and receptor binding properties of Bacillus thuringiensis delta-endotoxins to the midgut brush border membrane vesicles of the rice leaf folders, Cnaphalocrocis medinalis and Marasmia patnalis. Curr. Microbiol. 41: 276-283.
36. Kawabe, S. 1985. Mechanism of varietal resistance to the rice green leafhopper (Nephotettix cincticeps Uhler). Jpn. Agric. Res. Q. 19: 115-124.
37. Littell, R. C., G. A. Milliken, W. W. Stroup, R. D. Wolfinger, and O. Schabenberger. 2006. SAS for mixed models. SAS Institute, Cary, NC.
38. Liu, Z. C., G. Y. Ye, C. Hu, and S. K. Datta. 2002. Effects of Bt transgenic rice on population dynamics of main nontarget insect pests and dominant spider species in rice paddies. Acta. Phytophyl. Sin. 29: 138-144.
39. Lu, Y. H., K. M. Wu, Y. Y. Jiang, Y. Y. Guo, and N. Desneux. 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487: 362-365.
40. [MAPRC]Ministry of Agriculture of People's Republic of China. 2009. The second list of approval agricultural genetically modified organisms'safety certificates in 2009. (http://www.stee.agri.gov.cn/biosafety/spxx/ P020091127591594596689.pdf).
41. Maqbool, S. B., T. Husnain, S. Riazuddin, L. Masson, and P. Christou. 1998. Effective control of yellow stem borer and rice leaf folder in transgenic rice indica varieties Basmati 370 and M7 using the novel delta-endotoxin cry2A Bacillus thuringiensis gene. Mol. Breed. 4: 501-507.
42. Maqbool, S. B., S. Riazuddin, N. T. Loc, A.M.R. Gatehouse, J. A. Gatehouse, and P. Christou. 2001. Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Mol. Breed. 7: 85-93.
43. Naranjo, S. E. 2005. Long-term assessment of the effects of transgenic Bt cotton on the abundance of nontarget arthropod natural enemies. Environ. Entomol. 34: 1193-1210.
44. Oya, S. 1980. Feeding habits and honeydew components of the green rice leafhopper, Nephotettix cincticeps Uhler (Hemiptera, Deltocephalidae). Appl. Entomol. Zool. 15: 392-399.
45. Rodriguez-Saona, C. R., J. A. Byers, and D. Schiffhauer. 2012. Effect of trap color and height on captures of blunt-nosed and sharp-nosed leafhoppers (Hemiptera: Cicadellidae) and non-target arthropods in cranberry bogs. Crop Prot. 40: 132-144.
46. SAS Institute. 2001. SAS V9.1 help. SAS Institute, Cary, NC.
47. Shelton, A. M., J. Z. Zhao, and R. T. Roush. 2002. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47: 845-881.
48. Sheng, C. F., H. T. Wang, L. D. Gao, and J. W. Xuan. 2003. The occurrence status, damage cost estimate and control strategies of stem borers in China. Plant Prot. 29: 37-39.
49. Shu, Q. Y., G. Y. Ye, H. R. Cui, X. Y. Cheng, Y. B. Xiang, D. X. Wu, M. W. Gao, Y. W. Xia, C. Hu, R. Sardana, et al. 2000. Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran rice pest species. Mol. Breed. 6: 433-439.
50. Tang, W., H. Chen, C. G. Xu, X. H. Li, Y. J. Lin, and Q. F. Zhang. 2006. Development of insect-resistant trans-genic indica rice with a synthetic cry1C* gene. Mol. Breed. 18: 1-10.
51. Tu, J. M., G. A. Zhang, K. Datta, C. G. Xu, Y. Q. He, Q. F. Zhang, G. S. Khush, and S. K. Datta. 2000. Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis -endotoxin. Nat. Biotechnol. 18: 1101-1104.
52. Wang, Y. M., G. A. Zhang, J. P. Du, M. C. Wang, and B. A. Liu. 2010. Influence of transgenic hybrid rice expressing a fused gene derived from cry1Ab and cry1Ac on primary insect pests and rice yield. Crop Prot. 29: 128-133.
53. Whitehouse, M.E.A., L. J. Wilson, and G. P. Fitt. 2005. A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environ. Entomol. 34: 1224-1241.
54. Wu, K. M., Y. H. Lu, H. Q. Feng, Y. Y. Jiang, and J. Z. Zhao. 2008. Suppression of cotton bollworm in multiple crops in china in areas with Bt toxin-containing cotton. Science 321: 1676-1678.
55. Xu, X. L., Y. Han, G. Wu, W. L. Cai, B. Q. Yuan, H. Wang, F. Z. Liu, M. Q. Wang, and H. X. Hua. 2011. Field evaluation of effects of transgenic cry1Ab/cry1Ac, cry1C and cry2A rice on Cnaphalocrocis medinalis and its arthropod predators. Sci. China Life Sci. 54: 1019-1028.
56. Yang, H., J. X. Li, S. D. Guo, X. J. Chen, and Y. L. Fan. 1989. Transgenic rice plants produced by direct uptake of -endotoxin protein gene from Bacillus thuringiensis into rice protoplasts. Sci. Agric. Sin. 22: 1-5.
57. Yang, Z., H. Chen, W. Tang, H. X. Hua, and Y. J. Lin. 2011. Development and characterisation of transgenic rice expressing two Bacillus thuringiensis genes. Pest Manag. Sci. 67: 414-422.
58. Ye, G. Y., Q. Y. Shu, H. W. Yao, H. R. Cui, X. Y. Cheng, C. Hu, Y. W. Xia, M. W. Gao, and I. Altosaar. 2001a. Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. J. Econ. Entomol. 94: 271-276.
59. Ye, G. Y., J. Tu, C. Hu, K. Datta, and S. Datta. 2001b. Transgenic IR72 with fused Bt gene cry1Ab/cry1Ac from Bacillus thuringiensis is resistant against four lepidopteran species under field conditions. Plant Biotechnol. 18: 125-133.
60. Ye, G. Y., H. W. Yao, Q. Y. Shu, X. Cheng, C. Hu, Y. W. Xia, M. W. Gao, and I. Altosaar. 2003. High levels of stable resistance in transgenic rice with a cry1Ab gene from Bacillus thuringiensis Berliner to rice leaffolder, Cnaphalocrocis medinalis (Guenée) under field conditions. Crop Prot. 22: 171-178.
61. Zhang, Q. F. 2007. Strategies for developing green super rice. Proc. Natl. Acad. Sci. U.S.A. 104: 16402-16409.
62. Zheng, X. S., Y. J. Yang, H. X. Xu, H. Chen, B. J. Wang, Y. J. Lin, and Z. X. Lu. 2011. Resistance performances of transgenic Bt rice lines T2A-1 and T1C-19 against Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J. Econ. Entomol. 104: 1730-1735.
63. Zhou, X., J. A. Cheng, Y. Hu, and Y. G. Lou. 2005. Effects of transgenic Bt rice on the population development of Nephotettix cincticeps. Chin. J. Rice Sci. 19: 74-78.
64. Zhu, J., Y. P. He, M. X. Gao, W. J. Zhou, J. Hu, J. L. Shen, and Y. C. Zhu. 2011. Photodegradation of emamectin benzoate and its influence on efficacy against the rice stem borer, Chilo suppressalis. Crop Prot. 30: 1356-1362.