Impact of insect-resistant transgenic rice on target insect pests and non-target arthropods in China

Insect Science

Volumn 13, Issue 6, 2006, Pages 409-420

  Chen, Mao ^a   Zhao, Jian Zhou ^a   Ye, Gong Yin ^b   Fu, Qiang ^c   Shelton, Anthony M ^a  

^a New York State Agricultural Experiment Station   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Bt toxin; Insect resistance; Non target effect; Target insects; Transgenic rice

Indexed keywords

EID: 34347335109     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2006.00110.x     Document Type: Article

References (86)

1. An, H.B., Zhu, Z., Li, H.F., Wu, Q., Zhou, Z.L., Xu, H.L., Xu, J. W., An, L.J. and Li, X.H. (2001) Obtaining fertile transgenic plants of resistant-insect rice (Oryza sativa L.) via particle bombardment. High Technology Letters, 11, 12 - 16.
2. Bai, Y.Y., Jiang, M.X. and Cheng, J.A. (2005) Impacts of transgenic cry1Ab rice on two collembolan species and predation of Microvelia horvathi (Hemiptera: Veliidae). Acta Entomologica Sinica, 48, 42 - 47. (in Chinese).
3. Bashir, K., Husnain, T., Fatima, T., Latif, Z., Mehdi, S.A. and Riazuddin, S. (2004) Field evaluation and risk assessment of transgenic indica basmati rice. Molecular Breeding, 13, 301 - 312.
4. Bates, S.L., Zhao, J.-Z., Roush, R.T. and Shelton, A.M. (2005) Insect resistance management in GM crops: Past, present and future. Nature Biotechnology, 23, 57 - 62.
5. Chen, H., Tang, W., Xu, C.G., Li, X.H., Lin, Y.J. and Zhang, Q. F. (2005a) Transgenic indica rice plants harboring a synthetic cry2A gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theoretical and Applied Genetics, 111, 1330 - 1337.
6. Chen, M. (2005b) Ecological safety assessments of transgenic rice with insect or virus resistance on their non-target organisms. PhD Dissertation, Zhejiang University, Hangzhou, China. (in Chinese).
7. Chen, M., Ye, G.Y., Liu, Z.C., Yao, H.W., Chen, X.X., Sheng, Z. C., Hu, C. and Datta, S.K. (2006) Field assessment of the effects of transgenic rice expressing a fused gene of cry1Ab and cry1Ac from Bacillus thuringiensis Berliner on non-target planthoppers and leafhoppers. Environmental Entomology, 35, 127 - 134.
8. Chen, M., Ye, G.Y., Hu, C. and Datta, S.K. (2003a) Effects of transgenic Bt indica rice on the feeding and oviposition behavior of the brown planthopper, Nilaparvata lugens. Acta Phytophylacica Sinica, 30, 366 - 370. (in Chinese).
9. Chen, M., Ye, G.Y., Hu, C. and Datta, S.K. (2003b) Effect of transgenic Bt rice on the dispersal of planthoppers and leafhop-pers as well as their egg parasitic wasps. Journal of Zhejiang University (Agriculture and Life Science), 29, 29 - 33. (in Chinese).
10. Chen, M., Ye, G.Y., Lu, X.M., Hu, C., Peng, Y.F., Shu, Q.Y. and Altosaar, I. (2005c) Biotransfer and bioaccumulation of Cry1Ab insecticidal protein in rice plant-brown planthopper-wolf spider food chain. Acta Entomologica Sinica, 48, 208 - 213. (in Chinese).
11. Chen, M., Ye, G.Y., Yao, H.W., Hu, C. and Shu, Q.Y. (2003c) Impact evaluation of insect-resistant transgenic rice on the feeding and oviposition behavior of its non-target insect, the brown planthopper, Nilaparvata lugens (Homptera: Delphacidae). Agricultural Sciences in China, 2, 1000 - 1006.
12. Chen, X.J., Hu, S.L., Cheng, K.L. and Ren, G.J. (2003d) Effect of Bt-transgenic rice on organism community in paddy-field. Journal of Sichuan Agricultural University, 21, 185 - 186. (in Chinese).
13. Cheng, X.Y., Sardana, R., Kaplan, H. and Altosaar, I. (1998) Agrobacterium-transformed rice plants expressing synthetic cry1Ab and cry1Ac genes are highly toxic to striped stem borer and yellow stem borer. Proceedings of the National Academy of Sciences of United States of America, 95, 2767 - 2772.
14. Chi, S.Y., Peng, Y., Wang, Y.C., Han, Z.J. and Chen, C.K. (2005) Advance in the research of insecticide resistance of Chilo suppressalis. Plant Protection, 31(6), 3 - 6. (in Chinese).
15. Ci, X.Y., Yao, F.Y., Zhu, C.X., Song, Y.Z., Wen, F.J. and Jiang M.S. (2005) Breeding resistant rice varieties from transgenic parental lines with cry1Ab and Xa21 genes and their field performance. Scientia Agricultura Sinica, 38, 313 - 319. (in Chinese).
16. Cohen, M.B., Gould, F. and Bentur, J.S. (2000) Bt rice: practical steps to sustainable use. International Rice Research Notes, 25, 4 - 10.
17. Dorcey, E. and Serrano, A. (2002) GM foods in Spanish newspaper. Trends in Biotechnology, 20, 285 - 286.
18. Fu, Q., Wang, F., Li, D.H., Yao, Q., Lai, F.X. and Zhang, Z.T. (2003) Effects of insect-resistant transgenic rice lines MSA and MSB on non-target pests Nilaparvata lugens and Sogatella fucifera. Acta Entomologica Sinica, 46, 697 - 704. (in Chinese).
19. Gao, X.W., Peng, L.N. and Liang, D.Y. (2006a) Factors causing the outbreak of brown planthopper, Nilaparvata lugens Stal in China in 2005. Plant Protection, 32(2), 23 - 24. (in Chinese).
20. Gao, Y.L., Fu, Q., Wang, F., Lai, F.X., Luo, J., Peng, Y.F. and Zhang, Z.T. (2006b) Effects of transgenic cry1Ac+CpTI rice on survival and field composition of Chilo suppressalis and Sesamia inferens. Chinese Journal of Rice Science, 20, 543 - 548. (in Chinese).
21. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars-integrating pest genetics and ecology. Annual Review of Entomology, 43, 701 - 726.
22. Han, L.Z., Wu, K.M., Peng, Y.F. and Guo, Y.Y. (2006a) Advances in ecological safety of insect-resistant rice. Chinese Journal of Applied and Environmental Biology, 12(3), 431 - 436. (in Chinese).
23. Han, L.Z., Wu, K.M., Peng, Y.F., Wang, F. and Guo, Y.Y. (2006b) Evaluation of transgenic rice expressing Cry1Ac and CpTI against Chilo suppressalis and its intrapopulation variation in susceptibility to Cry1Ac. Environmental Entomology, 35, 1453 - 1459.
24. High, S.M., Cohen, M.B., Shu, Q.Y. and Altosaar, I. (2004) Achieving successful deployment of Bt rice. Trends in Plant Science, 9, 286 - 292.
25. Hu, Y.Q., Li, Y.R., Zheng, Y., Hu, X.B., Zhang, M.J. and Li, B. J. (2005) Insecticidal activity of transgenic rice expressing CpTI or CpTI+Bt to Chilo suppressalis Walker. Journal of Fujian Agriculture and Forestry University (Nature Science Edition), 34, 185 - 188. (in Chinese).
26. Huang, J.K., Hu, R.F., Rozelle, S. and Pray, C. (2005) Insect-resistant GM rice in farmers' fields: Assessing productivity and health effects in China. Science, 308, 688 - 690.
27. Huang, J.K., Rozelle, S., Pray, C. and Wang, Q.F. (2002) Plant biotechnology in China. Science, 295, 674 - 677.
28. James, C. (2005) Executive summary: Global Status of Commercialized Biotech/GM Crops: 2005. ISAAA Briefs, No. 34, ISAAA: Ithaca, NY.
29. Janmaat, A.F. and Myers, J. (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage looper, Trichoplusia ni. Proceedings of the Royal Society B: Biological Sciences, 270, 2263 - 2270.
30. Jiang, X.H., Zhang, Q.H., Hu, S.M., Xie, S.J. and Xu, S.G. (2001) The status of pesticide resistance of rice stalk borer in Zhejiang Province and their management tactics. Plant Protection Technology and Extension, 21(3), 27 - 29. (in Chinese).
31. Jiang, Y.H., Fu, Q., Cheng, J.A., Ye, G.Y., Bai, Y.Y. and Zhang, Z.T. (2004) Effects of transgenic Bt rice on the biological characteristics of Apanteles chilonis (Munakata) (Hymenoptera: Braconidae). Acta Entomologica Sinica, 47, 124 - 129. (in Chinese).
32. Jiang, Y.H., Fu, Q., Cheng, J.A., Zhu, Z.R., Jiang, M.X. and Zhang, Z.T. (2005a) Effect of transgenic sck+cry1Ac rice on the survival and growth of Chilo suppressalis (Walker) and its parasitoid Apanteles chilonis (Munakata)(Hymenoptera: Braconidae). Acta Entomologica Sinica, 48, 554 - 560. (in Chinese).
33. Jiang, W.H., Han, Z.J. and Hao, M.L. (2005b) Primary study on resistance of rice stem borer (Chilo suppressalis) to fipronil. Chinese Journal of Rice Science, 19, 577 - 579. (in Chinese).
34. Kain, W.C., Zhao, J.-Z., Janmaat, A.F., Myers, J., Shelton, A.M. and Wang, P. (2004) Inheritance of resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper (Lepidoptera: Noctuidae). Journal of Economic Entomology, 97, 2073 - 2078.
35. Khush, G.S. (1995) Breaking the yield frontier of rice. GeoJournal, 35, 329 - 332.
36. Khush, G.S. (1997) Origin, dispersal, cultivation and variation of rice. Plant Molecular Biology, 35, 25 - 34.
37. Li, D.H., Fu, Q., Wang, F., Yao, Q., Lai, F.X., Wu, J.C. and Zhang, Z.T. (2004) Resistance of transgenic rice containing both sck and cry1Ac genes against Chilo suppressalis and Cnaphalocrocis medinalis. Chinese Journal of Rice Science, 18, 43 - 47. (in Chinese).
38. Li, X.F., Han, Z.J., Chen, C.K., Li, G.Q. and Wang, Y.C. (2001) Monitoring for resistance of rice stem borer (Chilo suppressalis Walker) to 4 conventional insecticides. Journal of Nanjing Agricultural University, 24, 43 - 46. (in Chinese).
39. Li, Y.R., Hu, Y.Q., Zheng, Y., Hu, X.B., Zhang, M.J. and Li, B. J. (2005) Field evaluation of the resistance of transgenic rice expressing CpTI or CpTI+Bt to lepidopterous pests. Journal of Fujian Agriculture and Forestry University (Nature Science Editon), 34, 182 - 185. (in Chinese).
40. Liu, Y.F., Su, J., You, M.S., Wang, Q., Hu, S.Q., Liu, W.H., Zhao, S.X. and Wang, F. (2005a) Effect of transgenic pest-resistant rice on pest insect communities in paddy fields. Acta Entomologica Sinica, 48, 544 - 553. (in Chinese).
41. Liu, Y.F., Wang, F., You, M.S., Wang, Q., Hu, S.Q., Liu, W.H. and Zhao, S.X. (2005b) Resistance of cry1Ac+SCK transgenic rice and its filial generation to the rice leaf roller Cnaphalocrocis medinalis. Scientia Agricultura Sinica, 38, 725 - 729. (in Chinese).
42. Liu, Z.C., Ye, G.Y. and Hu, C. (2004) Effects of Bacillus thuringiensis transgenic rice and chemical insecticides on arthropod communities in paddy-fields. Chinese Journal of Applied Ecology, 15, 2309 - 2314. (in Chinese).
43. Liu, Z.C., Ye, G.Y., Hu, C. and Datta, S.K. (2003a) Impact of transgenic indica rice with a fused gene of cry1Ab/cry1Ac on the rice paddy arthropod community. Acta Entomologica Sinica, 46, 454 - 465. (in Chinese).
44. Liu, Z.C., Ye, G.Y., Fu, Q., Zhang, Z.T. and Hu, C. (2003b) Indirect impact assessment of transgenic rice with cry1Ab gene on predations by the wolf spider, Pirata subpiraticus. Chinese Journal of Rice Science, 17, 175 - 178.
45. Meng, F.X., Wu, K.M., Gao, X.W., Peng, Y.F. and Guo, Y.Y. (2003) Geographic variation in susceptibility of Chilo suppressalis (Lepidoptera: Pyralidae) to Bacillus thuringiensis toxins in China. Journal of Economic Entomology, 96, 1383 - 1842.
46. Naranjo, S.E., Head, G. and Dively, G.P. (2005) Field studies assessing arthropod non-target effects in Bt transgenic crops: Introduction. Environmental Entomology, 34, 1178 - 1180.
47. Pathak, M.D. and Khan, Z.R. (1994) Insect Pests of Rice. International Rice Research Institute, Manila, The Philippines.
48. Peng, Y., Chen, C.K., Han, Z.J. and Wang, Y.C. (2001) Resistance measurement of Chilo suppressalis from Jiangsu province and its resistance mechanism to methamidophos. Acta Phytophylacica Sinica, 28, 173 - 177. (in Chinese).
49. Qaim, M. and Zilberman, D. (2003) Yield effects of genetically modified crops in developing countries. Science, 299, 900 - 902.
50. Qu, M.J., Han, Z.J., Xu, X.J. and Yue, L.N. (2003) Triazophos resistance mechanisms in the rice stem borer (Chilo suppressalis Walker). Pesticide Biochemistry and Physiology, 77, 99 - 105.
51. Romeis, J., Meissle, M. and Bigler, F. (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology, 24, 63 - 71.
52. Rose, R.I. (2006) Tier-based testing for effects of proteinaceous insecticidal plant-incorporated protectants on non-target arthropods in the context of regulatory risk assessments. IOBC/WPRS Bulletin, 29, 145 - 252.
53. Roush, R.T. (1998) Two-toxin strategies for management of insect resistant transgenic crops: Can pyramiding succeed where pesticide mixtures have not Philosophical Transactions of the Royal Society B: Biological Sciences, 353, 1777 - 1786.
54. Savary, S., Willocquet, L., Elazegui, F.S., Castilla, N.P. and Teng, P.S. (2000) Rice pest constraints in tropical Asia: quantification of yield losses due to rice pests in a range of production situations. Plant Disease, 84, 357 - 369.
55. Shelton, A.M., Robertson, J.L., Tang, J.D., Perez, C., Eigenbrode, S.D., Preisler, H.K., Wilsey, W.T. and Cooley, R.J. (1993) Resistance of diamondback moth to Bacillus thuringiensis subspecies in the field. Journal of Economic Entomology, 86, 697 - 705.
56. Shelton, A.M. and Sears, M.K. (2001) The monarch butterfly controversy: Scientific interpretations of a phenomenon. The Plant Journal, 27, 483 - 488.
57. Shelton, A.M., Zhao, J.-Z. and Roush R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annual Review of Entomology, 47, 845 - 881.
58. Sheng, C.F., Wang, H.T., Gao, L.D. and Xuan, W.J. (2003) The occurrence status, damage cost estimate and control strategies of stem borers in China. Plant Protection, 29, 37 - 39. (in Chinese).
59. Shu, Q.Y., Ye, G.Y., Cui, H.R., Cheng, X.Y., Xiang, Y.B., Wu, D. X., Gao, M.W., Xia, Y.W., Hu, C., Sardana, R. and Altosaar, I. (2000) Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran rice pest species. Molecular Breeding, 6, 433 - 439.
60. Tabashnik, B.E., Cushing, N.L., Finson, N. and Johnson, M.W. (1990) Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology, 83, 1671 - 1676.
61. Tabashnik, B.E., Carrière, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M. and Zhao, J.-Z. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology, 96, 1031 - 1038.
62. Tabashnik, B.E., Dennehy, T.J. and Carrière, Y. (2005) Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences of United States of America, 102, 15389 - 15393.
63. Tanaka, K., Endo, S. and Kazano, H. (2000) Toxicity of insecticides to predators of rice planthoppers: Spiders, the mirid bug and the dryinid wasp. Applied Entomology and Zoology, 35, 177 - 187.
64. Tu, J.M., Datta, K., Alam, M.F., Fan, Y., Khush, G.S. and Datta, S.K. (1998) Expression and function of a hybrid Bt toxin gene in transgenic rice conferring resistance to insect pest. Plant Biotechnology, 15, 195 - 203.
65. Tu, J.M., Zhang, G.A., Datta, K., Xu, C.G., He, Y.Q., Zhang, Q. F., Khush, G.S. and Datta, S.K. (2000) Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensisδ-endotoxin. Nature Biotechnology, 18, 1101 - 1104.
66. US EPA (1998) Final Report of the Subpanel on Bacillus thuringiensis (Bt) Plant-Pesticides and Resistance Management, Meeting held on February 9-10, 1998. Available at: http://www.epa.gov/scipoly/sap/meetings/1998/february/finalfeb.pdf.
67. US EPA (2001) Biopesticides Registration Action Document-Bacillus thuringiensis Plant-Incorporated Protectants. Available at: http://www.epa.gov/pesticides/biopesticides/pips/bt_brad.htm.
68. Wang, A.J., Yao, F.Y., Wen, F.J., Zhu, C.X., Li, G.X., Yang, L., Zhu, Q.S. and Zhang H.R. (2002a) Obtaining of transgenic rice plants resistant to both stem borer and Bacterial blight disease from Bt and Xa21 genes transforming. Acta Agronomica Sinica, 28, 857 - 860. (in Chinese).
69. Wang, F. (2000) Progress and prospects in the development of transgenic rice breeding. Fujian Journal of Agricultual Sciences, 15 (Suppl.), 141 - 144. (in Chinese).
70. Wang, Y.C., Fan, J.Q. and Tian, X.Z. (1994) Studies on the resurgent question of plant-hoppers induced by deltamethrin and methamidophos. Entomology Knowledge, 31, 257 - 262. (in Chinese).
71. Wang, Z.H., Shu, Q.Y., Cui, H.R., Xu, M.K., Xie, X.B. and Xia, Y.W. (2002b) The effect of Bt transgenic rice flour on the development of silkworm larvae and the sub-microstructure of its midgut. Scientica Agricultura Sinica, 35, 714 - 718. (in Chinese).
72. Wang, Z.H., Shu, Q.Y., Ye, G.Y., Cui, H.R., Wu, D.X., Altosaar, I. and Xia, Y.W. (2002c) Genetic analysis of resistance of Bt rice to stripe stem borer (Chilo supperssalis). Euphytica, 123, 379 - 386.
73. Wang, Z.H., Shu, Q.Y., Cui, H.R., Ye, G.Y., Wu, D.X., Gao, M. W., Xia, Y.W., Cheng, X.Y. and Altosaar, I. (2000) Resistance of progenies of crosses between Bt transgenic rice and conventional rice varieties to stripe stem borer Chlio suppressalis. Acta Agronomica Sinica, 26, 310 - 314. (in Chinese).
74. Wu, J.C., Xu, J.X., Yuan, S.Z., Liu, J.L., Jiang, Y.H. and Xu, J. F. (2001) Pesticide-induced susceptibility of rice to brown planthopper Nilaparvata lugens. Entomologia Experimentalis et Applicata, 100, 119 - 126.
75. Yao, F.Y., Zhu, C.X., Li, G.X. and Wen, F.J. (2002) Identification of Bt rice resistance to stripe stem borer and genetic analysis of transgenes. Scientia Agricultura Sinica, 35, 142 - 145. (in Chinese).
76. Ye, G.Y., Shu, Q.Y., Cui, H.R., Gao, M.W., Xia, Y.W., Cheng, X.Y. and Altosaar, I. (2000) A leaf-section bioassay for evaluating rice stem borer resistance in transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner. Bulletin of Entomological Research, 90, 179 - 182.
77. Ye, G.Y., Shu, Q.Y., Yao, H.W., Cui, H.R., Cheng, X.Y., Hu, C., Xia, Y.W., Gao, M.W. and Altosaar, I. (2001a) Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. Journal of Economic Entomology, 94, 270 - 276.
78. Ye, G.Y., Tu, J.M., Hu, C., Datta, K. and Datta, S.K. (2001b) Transgenic non-Bt with fused Bt gene cry1Ab/cry1Ac from Bacillus thuringiensis is resistant against four lepidopteran species under field conditions. Plant Biotechnology, 18, 125 - 133.
79. Ye, G.Y., Yao, H.W., Shu, Q.Y., Cheng, X.Y., Hu, C., Xia, Y.W., Gao, M.W. and Altosaar, I. (2003) High levels of stable resistance in transgenic rice with a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to rice leaffolder, Cnaphalocrocis medinalis (Guenée) under field conditions. Crop Protection, 22, 171 - 178.
80. Zhao, H.Y., Zhang, Y.J., Wu, K.M., Zhao, K.J., Peng, Y.F. and Guo, Y.Y. (2004) Expression of Cry1Ac/CpTI transgenic rice and its resistance in different stages to Chilo suppressalis. Journal of Agricultural Biotechnology, 12, 76 - 79.
81. Zhao, J.-Z., Cao, J., Li, Y.X., Collins, H.L., Roush, R.T., Earle, E.D. and Shelton, A.M. (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nature Biotechnology, 21, 1493 - 1497.
82. Zhao, J.-Z., Cao, J., Collins, H.L., Bates, S.L., Roush, R.T., Earle, E.D. and Shelton, A.M. (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proceedings of the National Academy of Sciences of United States of America, 102, 8426 - 8430.
83. Zhao, J.-Z. and Rui, C.H. (2004) Insect resistance management for transgenic Bt cotton. Transgenic Cotton (English Edition), (ed. S.R. Jia), pp. 184 - 204. Science Press, Beijing.
84. Zhou, X., Cheng, J.A., Hu, Y. and Lou, Y.G. (2004) Effects of transgenic Bt rice on the population development of Nephotettix cincticeps. Chinese Journal of Rice Science, 19, 74 - 78. (in Chinese).
85. Zhu, C.X., Hu, A.Q., Wen, F.J., Zheng, C.C. and Zhang, J. (1999) Production of insect-resistant rice plants transformed with cry1Ab and pinII genes. Journal of Agricultural Biotechnology, 7, 259 - 266. (in Chinese).
86. Zhu, Z. (2001) Research and development of highly insect-resistant transgenic rice. Bulletin of the Chinese Academy of Sciences, 5, 353 - 358. (in Chinese).