摘要
从1997年,中国开始种植转Bt基因抗虫棉,2013年成为第二大转Bt基因抗虫棉种植国,种植面积达到420万公顷。转Bt基因抗虫棉的种植,有效地控制了棉铃虫的为害,但长期种植抗虫棉也带来棉铃虫对Bt毒蛋白产生抗性的风险。本研究利用生态学、昆虫毒理学和分子生物技术,对中棉所41、中棉所79和Bollgard Ⅱ等三种类型转基因抗虫棉的抗虫性及外源杀虫蛋白的表达量进行研究,并于2012-2013年对黄河流域棉区棉铃虫的抗性发展动态进行系统监测,同时对棉铃虫抗性相关基因钙粘蛋白的变异情况了进行了研究。主要研究结果如下:
1.2012-2013年,对中棉所41、中棉所79和Bollgard Ⅱ等三种类型抗虫棉的抗虫性进行研究。三种类型转基因棉花均具有较好的抗虫性,但品种间和生育时期间的抗虫性存在差异。在苗期,三种类型抗虫棉抗虫效果都高于其他时期,中棉所41的抗虫效果最好,在2012年和2013年棉铃虫死亡率分别为87.98%和75.48%;在蕾期,Bollgard Ⅱ的抗虫效果最好,在2012年和2013年棉铃虫死亡率分别为49.56%和54.47%;在铃期,2012年Bollgard Ⅱ的抗虫效果最好,棉铃虫死亡率为39.51%,而2013年,中棉所41的抗虫效果最好,棉铃虫死亡率为47.68%。棉铃虫低龄幼虫对转基因棉花叶片敏感,取食转基因棉花叶片后,未死亡的棉铃虫低龄幼虫取食和消化均受到抑制,取食5天后,Bollgard Ⅱ叶片上的棉铃虫平均体重最大。以上结果说明,抗虫棉的抗虫效果存在发育时期、年度和品种间差异,这些差异能直接影响田间棉铃虫种群的抗性发展。
2.转Bt基因抗虫棉主要通过表达Bt杀虫蛋白来抵御铃虫,Bt蛋白的表达量与抗虫性密切相关。为了研究中棉所41、中棉所79和Bollgard Ⅱ在大田生长季中Bt蛋白表达量变化情况,于2012-2013年对大田种植的三种棉花不同生长阶段Bt蛋白进行定量检测。在整个生长季,不同类型的转基因棉花中的Cry1Ac蛋白的表达量存在显著地差异(P<0.05)。CrylAc蛋白在棉花叶片中的表达量显著高于蕾和铃中,蛋白表达量随棉花的生长逐渐降低,这与它们的抗虫性变化趋势一致。在Bollgard Ⅱ中,整个生长季Cry2Ab蛋白的表达量显著高于CyrlAc蛋白;Cry2Ab蛋白在蕾和铃中的表达量显著高于叶片。Bollgard Ⅱ中Cry2Ab蛋白的表达量和CrylAc蛋白的表达量没有明显的相关性,试验数据表明在整个棉花生长季Cry2Ab蛋白的高表达没有减少CrylAc蛋白的表达量。以上结果说明外源杀虫蛋白的表达量与棉花的抗虫效果呈正相关,通过检测棉花外源杀虫蛋白的含量,可以推断出该品种的抗虫效果。
3.2012-2013连续两年对中棉所41、中棉所79和Bollgard Ⅱ等3种类型转基因棉花和广泛应用的常规棉品种中棉所49的纤维品质进行了检测。结果显示这3种转基因棉花质量性状与中棉所49相比,除纤维强度和马克隆值外,没有明显的差异。所以种植这3种转基因抗虫棉不会影响棉花的纤维品质。外源基因对棉花纤维品质是否具有影响还需进一步研究。
4.为了实时监测黄河流域棉区在长期种植转Bt基因抗虫棉后,田间棉铃虫种群的抗性发展动态,本研究对黄河流域棉区田间棉铃虫种群的抗性基因频率进行测定。在2010-2013年,分别从河南、河北、山东棉田采集棉铃虫成虫。使用含有1.Oμg/ml Cry1Ac蛋白的人工饲料,在室内对单雌家系F1/F2代抗性水平进行测定。2010年共对河南、山东、河北的58,43和12个家系成功进行生物测定;2011年共对河南、山东、河北的48,25和26个家系成功进行生物测定;2012年共对河南、山东、河北的96,36和17个家系成功进行生物测定;2013年共对河南、山东、河北的342,146和40个家系成功进行生物测定。总体而言,黄河流域棉区棉铃虫抗性仍处于较低的水平,2010—2013年三省抗性基因频率无明显的差异(2010:χ2=0.0001<χ20.052=5.99;2011:χ2=0.0001<χ20.052=5.99;2012:χ2=0.0001<χ20.052=5.99;2013:χ2=0.0001<χ20.052=5.99)。2010-2013年,棉铃虫F1代平均相对发育级别没有明显的上升。但为防止棉铃虫对Bt抗性升高,有必要种植转复合Bt基因抗虫棉花并结合其他防治策略来防治棉铃虫。
5.本研究对采自于田间的棉铃虫抗性基因缺失突变情况进行了研究,以发展从分子水平监测棉铃虫抗性的方法。本研究期望筛选出田间抗性个体,但在2012-2013年没有检测到抗性个体。这一结果也符合田间棉铃虫种群抗性基因频率较低的监测结果。对4类在Bt饲料上发育级别不同的棉铃虫家系钙粘蛋白基因的全长序列进行克隆测序,钙粘蛋白全长5190bp,编码1730个aa,所有4类棉铃虫钙粘蛋白基因与NCBI注册的钙粘蛋白长度一致,没有发生缺失的情况。序列比对结果显示,4类棉铃虫钙粘蛋白氨基酸序列间存在突变位点。
In China transgenic Bt(Bacillus thuringiensis) cotton has been broadly planted since1997, which makes the China second largest Bt cotton growing country with planting area of4.2million hectares in2013. For the control of H. armigera (Hubner)(Lepidoptera:Nocruidae) the planting of transgenic Bt cotton has been extensively successful and competent tool. Although, the cultivation of Bt crops on large-scale may be the source of evolution in pest resistance to Bt toxin. Therefore, the main object of this study was biosafety of transgenic Bt cotton after continuous cultivation of Bt cotton in Yellow River cotton growing region of China during2012-2013and appropriate understanding the evolution of resistance of H. armigera to Bt cotton. The present scientifically studies helps to understand the efficacy of different transgenic Bt cotton, expression level of Bt insecticidal proteins and their effect on the survival of H. armigera. Also in this study, we estimate the frequency of Cryl Ac resistance genes in H. armigera populations with logical monitoring and find variation in cadherin gene related with resistance in H. armigera. As well as this study will help to improve the biosafety Bt cotton crops. The main conclusions of the study were as follows:
1. During three growing stages of Bt cotton, larval mortality of H. armigera were calculated on cotton leaf tissue of three transgenic Bt cotton varieties after five days of trail in2012and2013. The result indicates that transgenic Bt cotton are resistant to H. armigera during early stage of cotton but as plant grow up the mortality is declining with cotton crop age. The highest mortality%was recorded during seedling stage and less mortality%during boll stage of CCRI41and Bollgard Ⅱ but in CCR179the less mortality%was recorded in bud stage during2012-2013. During seedling stage, the higher mortality%was recorded in CCRI4187.97%and75.48%in2012-2013respectively. During bud stage, the maximum mortality%was recorded in Bollgard Ⅱ49.56%and54.47%in2012-2013, in boll stage; the highest mortality%was recorded39.51%in Bollgard Ⅱ in2012and highest mortality was recorded in CCRI4147.68%in2013. The data showed that bollworms were more susceptible to Bollgard Ⅱ and CCRI41than CCRI79. The average weight of each insect also calculated after five days of feeding on three transgenic Bt cotton varieties. The result indicates that Bt toxins which are present in the transgenic Bt cotton reduced the growth and development of the H. armigera larvae. Among all transgenic Bt cotton varieties the highest average of weight was recorded in Bollgard Ⅱ. These results suggested that differences in mortality%between developmental stages of Bt cotton in two years can directly affect the development of resistance in populations of H. armigera.
2. B. thuringiensis produced insecticidal protein CrylAc which is an important natural biological agent for the control of H. armigera considered as one of the most important economic insect pests in many parts of the world. To quantify the expression level of CrylAc and Cry2Ab during different growth stages of cotton plant, three Bt cotton varieties CCRI41(Bt+CpTI), CCRI79(CrylAc) and Bollgard II (CrylAc+Cry2Ab) were planted in2012and2013. For the quantification of the CrylAc and Cry2Ab content Envirologix Qualiplate kit for CrylAc and Cry2Ab were used. The Result showed some clear significant differences in the amount of CrylAc protein present in various plant parts of transgenic Bt cotton throughout the growing season (P<0.05). The expression levels of CrylAc proteins in the leaves of transgenic Bt cotton was significantly higher than buds and bolls but gradually decreasing as plant grew. Result showed that in Bt cotton CCRI41(5/+CpTI) which is toxic to H. armigera the CrylAc and CpTI proteins together have synergistic effect which enhances the level of Cry lAc Protein. In2012, measure the level of Cry2Ab, result showed that in Bollgard II the Cry2Ab present at much higher level throughout the season in the plant compared with CrylAc. Data showed that at the same time in fruiting bodies the expression level of Cry2Ab is higher but the expression level of Cry2Ab was lower in leaves, in Bollgard II expression level of the two Cry proteins found to be different from one another. However, data proved that in Bollgard II both proteins were present throughout the season and the addition of Cry2Ab had no deleterious effect on levels of CrylAc. These results recommend that expression levels of insecticidal proteins are linked with the cotton growth.
3. During2012and2013, the cotton fiber quality characters were tested to recognize the effect of different transgenic Bt cotton on the lint. Result shows that the fiber quality characters of transgenic cotton varieties were not significantly affected when compared with conventional non Bt variety. But in2013, fiber strength and micronaire are significantly affected. Finally it is concluded that there was no significant effect of transgenic Bt cotton on the fiber quality of cotton during2012and2013. To know the effect of transgenic Bt cotton on fiber qualities further research work will be carry on in future.
4. For the biosafety and continuous cultivation of Bt cotton in Yellow River region of China, the most important to gain a timely understanding the evolution of resistance of H. armigera to Bt toxin and estimate the frequency of alleles conferring resistance to CrylAc toxin in field populations of H. armigera. Adult female moths of H. armigera were collected from Henan Province, Shandong Province and Hebei Province in2010-2013. The female moths trapped in the field used for screening through bioassay test of F1and F2generations. The females moths reared on a diet containing1.0μg/ml CrylAc to estimate the frequency of resistance alleles. In2010, totals58,43and12isofemale lines tested for the F1generation bioassay, total48,25and26isofemale lines for the F1generation bioassay in2011, total of96,36and17isofemale lines for the F1generation in2012, and342,146and40isofemale were screened out during2013from Henan, Shandong and Hebei Provinces respectively. Yellow River region is the largest growing region of cotton in China, result shows that resistance gene frequency was still very low, fluctuating and it did not increase significantly from2010to2013in Henan Province, Shandong Province and Hebei Province(2010:χ2=0.0001<χ200.052=5.99;2011:χ2=0.0001<χ20.053=5.99;2012:=0.0001<χ20.0052=5.99;2013:χ2=0.0001<χ20.0052=5.99).Result shows that in F, tests the relative average development rating (RADR) of H. armigera larvae had no substantial increase in Cry1Ac tolerance during the four years period. In H. armigera to keep away from further increases in Bt resistance frequency, it is necessary to introduce Bt cotton expressing several Bt toxins and put together this technology with other strategy for management of H. armigera.
5. To identify the CrylAc binding protein in H. armigera, characterized the deletion mutation of field collected strain; which significantly monitor the changes in the frequency of resistance gene. We tried to identify the mutant in field populations of H. armigera, but no mutant was found in moths collected in2012-2013. This result is constant with the existing low gene frequency of Bt resistance in field population of H. armigera. The results shows sequencing of four types of H. armigera, the full length of H. armigera were5190bp that encoding1730Amino Acid proteins of the same length with bollworm cadherin sequence in NCBI registered bollworm cadherin (CAD accession AF519180.2). Sequences are of the same length and all sequences have no deletion mutations. Sequence alignments showed that amino acid sequences of four groups were different.
引文
1. Adamczyk Jr. J. J., Hardee D.D., Adams L.C., Sumerford D.V., Correlating differences in larval survival and development of bollwonns (Lepidoptera:Noctuidae)and fall armywonns (Lepidoptera: Noctuidae) to differential expression of CrylA(c) a-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton. Journal of Economic Entomology, 2001a,94:284-290.
2. Adamczyk Jr. J.J., Sumerford D.V. Potential factors impacting season-long expression of CrylAc in 13 commercial varieties of Bollgard (?) cotton. Journal of Insect Science,2001b,13:1-6.
3. Akhurst R.J., James W., Bird L.J., Beard C., Resistance to the CrylAc deltaendotoxin of Bacillus thuringiensis in the cotton bollworm Helicoverpa armigera (Lepidoptera:Noctuidae). Journal of Economic Entomology,2003,96:1290-1299.
4. Akin D.S., Stewart S.D., Knighten K.S., Field efficacy of cotton expressing two insecticidal proteins of Bacillus thuringiensis. In:Dugger, P.A., Richter D., (Eds.), Proceedings of the Beltwide Cotton Conference, National Cotton Council, Memphis, USA,2001, vol.2. pp.1041-1043.
5. Ali A., Abdulai A., The adoption of genetically modified cotton and poverty reduction in Pakistan. Journal of Agricultural Economics,2010,61:175-192.
6. Alstad D.N. and Andow D.A., Implementing management of insect resistance to transgenic crops. AgBiotech News Informat,1996,8:177-181.
7. Andow D.A., Alstad D.N., F2 screen for rare resistance alleles. Journal of Economic Entomology, 1998,91:572-578.
8. Andow D.A., Olson D.M., Hellmich R.L., Alstad D.N., Hutchison W.D., Frequency of resistance to Bacillus thuringiensis toxin CrylAb in an Iowa population of European corn borer (Lepidopeta: Crambidae). Journal of Economic Entomology,2000,93:26-30.
9. Bagla P., Hardy cotton-munching pests are latest blow to GM crops. Science,2010, 327(5972):1439.
10. Bambawale, O.M.,Singh A., Sharrma O.P., Bhosle B.B., Lavekar R.C, Dhandapani A., Kanwar V., Tanwar R.K., Rathod K.S., Patange N.R., Pawar V.M., Performance of δ-cotton (MECH-162) under integrated pest management in farmers' participatory field trial in Nanded district, Central India. Current Science,2003,86:1628-1633.
11. Bird L.J., Akhurst R.J., Variation in susceptibility of Helicoverpa armigera (Hubner) and Helicoverpa punctigera (Wallengren) (Lepidoptera:Noctuidae) in Australia to two Bacillus thuringiensis toxins. Journa of Invertebrate Pathology,2007,94:84-94.
12. Blanco C.A., Perera O.P., Gould F., Sumerford D.V., Hernandez G, Abel C.A., Andow D.A., An empirical test of the F2 screen for detection of Bacillus thuringiensis-resistance alleles in tobacco budworm (Lepidoptera:Noctuidae). Journal of Economic Entomology,2008,101:1406-1414.
13. Boonserm P., Davis P., Ellar D.J., Li J., Crystal Structure of the Mosquito larvicidal Toxin Cry4Ba and Its biological implications. Journal Mol. Biol,2005,348:363-382.
14. Boonserm P., Mo M., Angsuthanasombat Ch., Lescar J., Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-A resolution. Journal of Bacteriology,2006,188:3391-3401.
15. Boulter D., Gatehouse A.M.R., Hilder V., Use of cowpea trypsin inhibitor (CpTI) to protect plants against insect predation. Biotechnol Adv,1989,7:489-497.
16. Bravo, A., Phylogenetic relationships of Bacillus thuringiensis α-endotoxin family proteins and their functional domains. Journal of Bacteriology,1997,179:2793-2801.
17. Bravo A., Gill S.S., Soberon M., Bacillus thuringiensis Mechanisms and Use In:Comprehensive Molecular Insect Science. Elsevier BV,2005,6:175-206.
18. Bravo, A., Gill, S.S., Soberon, M., Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon,2007,49:423-435.
19. Bravo A., Go'mez I., Conde J., un~oz-Garay C., Sa'nchez J., Miranda R., Zhuang M., Gill S.S., Sobero'n M., Oligomerization triggers binding of a Bacillus thuringiensis CrylAb pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta,2004,1667:38-46.
20. Bravo A., Likitvivatanavong S., Gill S.S., Soberon M., Bacillus thuringiensis:A story of a successful bioinsecticide. Insect Biochemistry and Molecular Biology,2011,41:423-431.
21. Bravo A., Soberon M., How to cope with resistance to Bt toxins? Trends Biotechnol,2008,26: 573-579.
22. Bruce M.J., Gatsi R., Crickmore N., Sayyed A.H., Mechanisms of resistance to Bacillus thuringiensis in the Diamondback Moth. Biopestic Int,2007,3(1):1-12.
23. Burd A.D., Gould R, Bradley J.R., Van Duyn J.W., Moar W.J., Estimated frequency of non-recessive Bt resistance genes in bollworm, Helicoverpa zea (Bolddie) (Lepidoptera:Noctuidae) in eastern North Carolina. Journal of Economic Entomology,2003,96:137-142.
24. Carpenter J.E., Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nature Biotechnology,2010,28:319-321.
25. Chandrasheka K., Guja, G.T., Development and mechanisms of resistance to Bacillus thuringiensis endotoxin CrylAc in the American bollworm, Helicoverpa armigera (Hu" bner). Indian J. Exp. Biol,2004,42:164-173.
26. Chandrashekar K., Kumari A., Kalia V., Gujar GT., Baseline susceptibility of the American bollworm, Helicoverpa armigera (Hu" bner) to Bacillus thuringiensis Berl. var. kurstaki and its endotoxins in India. Cuirent Science,2005,88:167-175.
27. Chaufaux J., Muller-cohn J., Buisson C., Sanchis V., Lereclus D. Pasteur N., Inheritance of resistance to the Bacillus thuringiensis CrylA(c) toxin in Spodoptera littoralos (Lepidoptera: Noctuidae). Journal of Economic Entomology,1997,90:873-878.
28. Clive J., Global status of commercialized biotech/GM crops:2007. ISAAA brief no.37. ISAAA, Ithaca,2007.
29. Cohen S., Dym O., Albeck S., Ben-Dov E., Cahan R, Firer M., Zaritsky A., High-resolution crystal of activated Cyt2Ba monomer from Bacillus thuringiensis subs. Israelensis. J. Mol. Biol.,2008, 380:820-827.
30. Cooke F.T. JR., Scott W.P., Martin S. W., Parvin D. W., The Economics of Bt Cotton in the Mississippi Delta 1997-2000. Proc. Beltwide Cotton Conf., National Cotton Council,2001, 1:175-177.
31. Cooper D.J., The application of a model to achieve predicted mortality in a field trial using Bacillus thuringiensis to control Heliothispunctiger. Entomol. Exp Appl.1984,36:253-259.
32. Creech J.B.,2000Mississippi Cotton Variety Trials Preliminary Data. Mississippi Agricultural and Forestry Experiment Station Cotton Improvement,2001. (Online) Available at http://www.mstate.edu/dept/drec/cip/default.htm
33. Cui J.J., Effects and mechanisms of the transgenic CrylAc+CpTI (cowpea trypsin inhibitor) cotton on insect communities. Ph.D. Dissertation, Chinese Academy of Agricultural Sciences,2003, p 2
34. Culpepper A.S., York A.C., Weed Management in Glyphosate-Tolerant Cotton. Journal of Cotton Science,1998,4:174-185.
35. Daly J. C. Fitt G. P., Efficacy of Bt-cotton plants in Australia-What is going on? In Proceedings World Cotton ResearchConference-2 (eds. Gillham, F. and Petridis, P.), Thessaloniki, Greece,1998, pp.675-678.
36. Dang H.T., Gunning R.., Evidence of the shift in susceptibility to Bacillus thuringiensis delta-endotoxin CrylAc in Australian Helicoverpa armigera (Lepidoptera:Noctuidae). Res. Pest Manage. Newslett,2002,11:44-48.
37. Dankocsik C., Donovan W.P., Jany C.S., Activation of a cryptic crystal protein gene of Bacillus thuringiensis subsp. kurstaki by gene fusion and determination of the crystal protein insecticidal specificity. Mol. Microbiol,1990,4:2087-2094.
38. Dong H.Z., Li W.J., Variability of endotoxin expression in Bt transgenic cotton. J. Agron. Crop Sci. 2007,193:21-29.
39. 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. Evolutionary Applications,2003,574-584.
40. Downes S., Mahon R., Olsen K., Monitoring and adaptive resistance management in Australia for Bt-cotton:current status and future challenges. Journal of Invertebrate Pathology,2007,95: 208-213.
41. Estela A., Escriche B., Ferre J., Interaction of Bacillus thuringiensis toxins with larval midgut binding sites of Helicoverpa armigera (Lepidoptera:Noctuidae). Applied and Environmental Microbiology,2004,70:1378-1384.
42. Ethridge M. D., Hequet, E. F., Fibre properties and textile performance of transgenic cotton versus parent varieties. In:Proc. of the Beltwide Cotton Conf., National Cotton Council of America,2000, 1:488-494.
43. Fabrick J.A., Jech L.F., Henneberry T.J., Novel pink bollworm resistance to the Bt toxin Cry-lAc: effects on mating, oviposition, larval development and survival. J Insect Sci,2009,9(24):1-8.
44. Faircloth J.C., Edmisten K., Wells R., Stewart A., Planting cotton cultivar mixtures to enhance fiber quality. Journal Cotton Sci.,2003,7:51-56.
45. Feitelson J.S., Payne J., Kim L., Bacillus thuringiensis:Insects and beyond, Bio:Technology,1992, 10:271-275.
46. Feng H.Q., Wu K.M., Cheng D.F., Guo Y.Y., Radar observations of the autumn migration of the beet armyworm Spodoptera exigua (Lepidoptera:Noctuidae)and other moths in northern China. Bulletin of Entomological Research,2003,93,115-124.
47. Feng H.Q., Wu x.F, Wu B., Wu K.M., Seasonal migration of Helicoverpa armigera (Lepidoptera: Noctuidae) over the Bohai Sea. Journal of Economic Entomology,2009,102,95-104.
48. Finnegan E.J., Llewellyn D.J., Fitt G.P., What's happening to the expression of the insect protection in field grown Ingard cotton? In Proceedings of the Ninth Australian Cotton Conference, The Cotton Research and Development Corporation, Conrad, Australia,1998, pp.291-297.
49. Fitt G. P., Efficacy of Ingard cotton-patterns and consequences. In Proceedings of the Ninth Australian Cotton Conference, The Cotton Research and Development Corporation, Conrad, Australia,1998, pp.233-245.
50. Fitt GP., An Australian approach to IPM in cotton:integrating new technologies to minimize insecticide dependence. Crop Protect,2000,19:793-800.
51. Fitt GP., mares C.L., Llewellyn D.J., Field evaluation and potential ecological impact of transgenic cotton (Gossypium hirsutum) in Australia. Biocontrol Science and Technology,1994,4:535-548.
52. Fitt G.P., Wilson L.J., Genetic engineering in IPM:Bt cotton. In:Kennedy, G, Sutton, T. (Eds.), Emerging technologies for integrated pest management:concepts, research and implementation. APS Press, USA,2000, pp.108-125.
53. Forrester N., Cahill M., Bird L., Layland J., Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera:Noctuidae) in Australia. Bulletin Entomological Research Supplement Series,1993,1:120-132.
54. Gahan L.J., Gould F, Heckel D.G, Identification of a gene associated with Bt resistance in Heliothis virescens. Science,2001,293:857-860.
55. Gahan L., Gould F, Lopez J., Micinski S., Heckel D., A polymerase chain reaction screen of field populations of Heliothis virescens for a retrotransposon insertion conferring resistance to Bacillus thuringiensis toxin. J. Econ. Entomol.2001',100:187-194.
56. Gahan L.J., Pauchet Y., Vogel H., Hecke, D.G, An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis CrylAc toxin. PLoS Genetics,2010; 6(12):e 1001248. Doi:10.1371/journal.pgen.1001248.
57. Gao Y.L., An J.J., Liu C.x., Wu K.M., Monitoring of Bt resistance from field collected Helicoverpa armigera populations in northern China. Southwest Entomology,2010a,35:399-402.
58. Gao Y.L., Feng H.Q., Wu K.M., Regulation of the seasonal population patterns of Helicoverpa armigera moths by Bt cotton planting. Transgenic Research,2010b,19:557-562.
59. Gao Y.L., Wu K.M., Gould F., Frequency of Bt resistance alleles in H. armigera during 2006-2008 in Northern China. Environmental Entomology,2009,38:1336-1342.
60. Gassmann A.J., Carriere Y., Tabashnik B.E. Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol,2009,54:147-163.
61. Go'mez I., Sa'nchez J., Miranda R., Bravo A., Sobero'n M., Cadherin-like receptor binding facilitates proteolytic cleavage of helix a-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis CrylAb toxin. FEBSLett,2002,513:242-246.
62. Go'mez I., Pardo-Lo'pez L., Mun-oz-Garay C, Fernandez L.E., Pe'rez C., Sa'nchez J., Sobero'n M., Bravo A., Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis. Peptides,2007,28:169-173.
63. Gong Y.J., Wang C.L., Yang Y.H., Wu S.W., Wu YD., Characterization of resistance to Bacillus thuringiensis toxin CrylAc in Plutella xylostella from China. J Invertebr Pathol,2010, 104(2):90-96.
64. Gore J., Leonard B.R., Adamczyk J.J. Bolrworm (Lepidoptera:Noctuidae) survival on'Bollgard' and'Bollgard II'cotton flowerbud and flower components. Journal of Economic Entomology, 2001,94:1445-1451.
65. Gore J., Leonard B.R., Church G.E., Cook D.R., Behavior of bollworm (Lepidoptera:Noctuidae) larvae on genetically engineered cotton. Journal of Economic Entomology 2002,95:763-769.
66. Gould F., Sustainability of transgenic insecticidal cultivars:integrating pest genetics and ecology. Ann. Rev. Entomol.1998,43,701-726.
67. Gould F., Anderson A., Jones A., Sumerford D., Heckel, D.J., Lopez J., Micinski C.,Leonard R., Laster M., Initial frequency of alleles for resistance to Bacillus thuringiensis toxin in field populations of Heliothis virescens. Proc. Natl. Acad.Sci. USA,1997,94,3519-3523.
68. Gould F, Anderson A., Reynolds A., Bumgarner L., Moar W., Selection and genetic analysis of a Heliothis virescens(Lepidoptera:Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. Journal of Economic Entomology,1995,88:1545-1559.
69. Greenplate J.T., Mullins J.W., Perm S.R., Dahm A., Reich B.J., Osborn J.A., Ruschke L., Shappley Z.W., Partial characterization of cotton plants expressing rwotoxin proteins from Bacillus thuringiensis:relative toxin contribution, toxin interaction, and resistance management. Journal of Applied Entomology,2003,127:340-347.
70. Greenplate J.T., Quantification of. Bacillus thuringiensis insect control protein CrylAc over time in Bollgard cotton fruit and terminals.J. Econ. Entomol,1999,92:1377-1383.
71. Greenplate J.T., Penn S.R., Mullins J.W., Oppenhuizen M., Seasonal CrylAc levels in DP50B:the "Bollgard_ basis" for Bollgard II. In:Dugger P. and Richter D. (Eds.), Proceedings, the Beltwide Cotton Conference, National Cotton Council of America, Memphis,2000a, pp.1039-1040.
72. Greenplate J.T., Penn S.R., Shappley Z., Oppenhuizen M., Mann J., Reich B., Osborn J., Bollgard II efficacy:quantification of total lepidopteran activity in a 2-gene product. In:Dugger P. and Richter D. (eds.), Proceedings, Beltwide Cotton Conference, National Cotton Council of America, Memphis,2000b, pp.1041-1043.
73. Guo S.D., Cui H.Z., xia L.Q., Wu D.L., Ni W.Ch., Zhang Zh.L., Zhang B.L., xu Y.J., Development of bivalent insect-resistant transgenic cotton plants. Sci. Agric. Sin,1999,32:1-7.
74. Guo S., Ye S., Liu Y., Wei L., xue J., Wu H., Song F., Zhang J., Wu x., Huang D., Rao Z., Crystal structure of Bacillus thuringiensis Cry8Eal:An insecticidal toxin toxic to underground pests, the larvae of Holotrichia parallela. Journal of structural Biology,2009,168(2):259-266.
75. Gujar GT., Heliothis/Helicoverpa resistance to Bacillus thuringiensis resistance:management strategies. In:Sharma, H.C. (Ed.), Heliothis/Helicoverpa Management, Emerging Trends and Strategies for Future Research. Oxford & IBH Publ. Co. Pvt. Ltd., New Delhi,2005, pp.275-288.
76. Gujar G.T., Kumari A., Kalia V., Chandrashekar K., Spatial and temporal variation in susceptibility of the American bollworm Helicoverpa armigera (Hu"bner) to Bacillus thuringiensis var. kurstaki in India. Curr. Sci.2000,78:995-1001.
77. Gujar GT., Mittal A., Kumari A., Kalia V., Host crops influence on the susceptibility of the American Bollworm, Helicoverpa armigera (Hu" bner) (Noctuidae:Lepidoptera) to Bacillus thuringiensis Berliner var. kurstaki HD-73. Entomol. Exp. Appl,2004,113:165-173.
78. Haider M.Z., Ellar D.J., Mechanism of action of Bacillus thuringiensis insecticidal Π-endotoxin: interaction with phospholipid vesicles. Biochim BiophysActa Biomembr,1989,978(2):216-222.
79. Halcomb J.L., Benedict J.H., Cook B., Ring D. R., Survival and growth of bollworm and tobacco budworm on non-transgenic and transgenic cotton expressing a Cryl A insecticidal protein. Environ. Entomol,2000,25,250-255.
80. Heckel D.G, The complex genetic basis of resistance to Bacillus thuringiensis toxin in insects. Biocontrol Science Technology,1994,4:405-417.
81. Heckel D.G, Gahan L.J., Baxter S.W., Zhao J.Z., Shelton A.M., Gould F., Tabashnik B.E., The diversity of Bt resistance genes in species of Lepidoptera. JInvertebr Pathol,2007,95(3):192-197.
82. Heinicke C., Grove W.A., Labor markets, regional diversity, and cotton harvest mechanization in the post-World War II United States. Social Sci. Hist,2005,29:269-297.
83. Herrero S., Gechev T., Bakker P.L., Moar W.J., de Maagd R.A., Bacillus thuringiensis CrylCa-resistant Spodoptera exigua lacks expression of one of four Aminopeptidase N genes. BMC Genomics,2005,24:6-96.
84. Hilder V.A., Boulter D., Genetic engineering of crop plants for insect resisitance. A critical review. Crop Prot,1999,18:177-191.
85. Hilder V.A., Gatehouse A.M.R., Sheerman S.E., Barker R.F., Boulter D., A novel mechanism of insect resistance engineered into tobacco, Nature,1987,333:160-163.
86. Hofte H., Whiteley H.R., Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev, 1987,53:242-255.
87. Holloway J.W., Dang H., Monitoring susceptibility to Bt toxins in Australian Helicoverpa species. In:Proceedings of the 10th Australian Cotton Conference. Australian Cotton Cooperative Research Centre, Brisbane,2000, pp.189-194.
88. Holt, H.E., Season-long monitoring of transgenic cotton plants-Development of an assay for the quantification of Bacillus thuringiensis insecticidal crystal protein. In Proceedings of the Ninth Australian Cotton Conference, The Cotton Research and Development Corporation, Conrad, Australia,1998, pp.331-335.
89. Hovav R., Udall J.A., Hovav E., Rapp R., Flagel L., Wendel J.F., A majority of cotton genes are expressed in single celled fiber. Planta,2008,227:319-329.
90. Hsu H.H., Gale F., Regional shifts in China's cotton production and use. Cotton and wool situation outlook 2001. Economic Research Service, USDA,2001, pp.19-25.
91. Huang F., Leonard B.R., Moore S.H., Cook D.R., Baldwin J., Tindall K.V., Lee D.R., Allele frequency of resistance to Bacillus thuringiensis Cry lab corn in Louisiana populations of sugarcane borer (Lepidoptera:Crambidae). Journal of Economic Entomology,2008,101,492-498.
92. Huang J., Hu R., Rozelle S., Pray C., Insect-resistant GM rice in farmers'fields:assessing productivity and health effects in China. Science,2005,308:688-690.
93. Humphrey J., Commodities, diversification and poverty reduction. In:Sarris A., Hallam D. (Eds.), Agricultural commodity markets and trade:new approaches to analyzing market structure and instability. FAO-ONU, Roma, Italy,2006, p.380-401.
94. Ibargutxi M.A., Estela A., Ferre J., Caballero P., Bacillus thuringiensis toxins for the control of the cotton pest Earias insulana (Boisd.) (Lepidoptera:Noctuidae). Applied and Environmental Microbiology,2006,72,437-442.
95. ICAC, Genetically Engineered Cotton in the World-2002. International Cotton Advisory Committee, the ICAC Recorder,2002,20(4), pp.8-12.
96. Jackson R.E., Bradley J.R., Burd A.D., Van Duyn J.W., Field and greenhouse performance of bollworm on Bollgard-Ⅱ genotypes. In:Dugger, P.A., Richter, D. (Eds.), Proceedings of the Beltwide Cotton Conference. National Cotton Council, Memphis, USA,2002, pp.1048-1051.
97. Jackson R.E., Gould F., Bradley L., Van Duyn J., Genetic variation for resistance to Bacillus thuringiensis toxin in Helicoverpa zea (Lepidoptera:Noctuidae) in eastern North Carolina. Journal of Economic Entomology,2006,99:1790-1797.
98. Jalali S.K., Mohan K.S., Singh S.P., Manjunath T.M., Lalitha Y, Baseline susceptibility of the old-world bollworm Helicoverpa armigera (Hu" bner) (Lepidoptera:Noctuidae) populations from India to Bacillus thuringiensis CrylAc insecticidal proteins. Crop Prot.2004,23:53-59.
99. James C., Global Status of Commercialized Biotech/GM Crops:2013. ISAAA Brief No.46. ISAAA: Ithaca, NY,2013.
100. James C., Krattiger A. F., Global Review of the Field Testing and Commercialization of Transgenic Plants,1986 to 1995:The First Decade of Crop Biotechnology. ISAAA Briefs No.1. ISAAA: Ithaca, NY,1996, pp.31.
101. Janmaat A.F., Myers J.H., Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Tricoplusia ni. Proc.R. Soc. Lond. B,2003,270: 2263-2270.
102. John B., Cotton:Market setting, Trade policies and issues development prospects group. The World Bank,1818 h street, NW, Washington, D.C.2004.
103. Jordan A.G, Wakelyn P.J., May O.L., Transgenic cotton and fiber quality.16th Annual EFS System Conference,2003,9-11 June, Greenville, SC.
104. Jurat-Fuentes J.L., Gahan L.J., Gould F.L., Heckel D.G, Adang M.J., The HevCaLP protein mediates binding specificity of the CrylA class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry,2004,43:14299-14305.
105. Kalia V., Kumari A., Mittal A., Singh B.P., Nair R., Gujar G.T., Temporal variation in susceptibility of the American bollworm, Helicoverpa armigera to Bacillus thuringiensis(Bt) var. Kurstaki HD-73or its CrylAc toxin or Bt cotton. Pestic. Res. J,2006,18:47-50.
106. Knowles B.H., Ellar D.J., Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis δ-endotoxins with different insect specificity. Biochim Biophys Acta Gen Subj,1987,924(3):509-518.
107. Kranthi K., Jadhav D., Kranthi S., Wanjari R., Ali S., Russell D., Insecticide resistance in five major insect pests of cotton in India.Crop Protect.,2002,21,449-460.
108. Kranthi K.R., Kranthi S., Ali S., Banerjee S.K., Resistance to CrylAc d-endotoxinof Bacillus thuringiensis in a laboratory selected strain of Helicoverpa armigera (Hubner). Curr. Sci,2000,78, 1001-1004.
109. Kranthi K.R., Kranthi S., Wanjari R.R., Baseline susceptibility of Cryl toxins to Helicoverpa armigera (Hubner) (Lepidoptera:Noctuidae) in India. Int. J. Pest Manage,200147:141-145.
110. Kranthi K.R., Naidu S., Dhawa, C.S., Tatwawadi A., Mate K., Patil E., Bharose A.A., Behere G.T., Wadaskar R.M., Kranthi S., Temporal and intra-plant variability of CrylAc expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera (Hubner) (Noctuidae:Lepidoptera). Curr. Sci.2005,89,291-298.
111.Krishna V.V., Qaim M., Estimating the adoption of Bt eggplant in India:who benefits from public-private partnership? Food Policy,2007,32:523-543.
112. Kumar, Udayasuriyan V., Sangeetha, P., Bharathi, M., Analysis of Cry2A proteins encoded by genes from indigenous isolates of Bacillus thuringiensis for toxicity against Helicoverpa armigera. Curr. Sci,2004,86:566-570.
113. Lambert B., Peferoen M., Insecticidal promise of Bacillus thuringiensis. Facts and mysteries about a successful biopesticide, BioScience,1992,42,112-122.
114. Layton M.B.,2000. Cotton Insect Situation. Miss. State Univ. Ext. Serv. Leaf.13.
115. Li G.P., Feng H.Q., Gao Y.L., Wyckhuys Kris A., Wu K.M., Frequency of Bt resistance alleles in Helicoverpa armigera in the xinjiang cotton planting region of China. Environmental Entomology, 2010,39:1698-1704.
116. Li G.P., Wu K.M., Gould F., Feng H.Q., He Y.Z., Guo Y.Y., Bt toxin resistance gene frequencies in Helicoverpa armigera populations from the Yellow River cotton farming region of China. Entomologia Experimental et Applicata,2004,112:135-143.
117. Li G.P., Wu K.M., Gould F., Wang J.K., Miao J., Gao x.W., Guo Y.Y., Increasing tolerance to CrylAc cotton from cotton bollworm, Helicoverpa armigera, was confirmed in Bt cotton farming area of China. Ecol. Entomol,2007,32:366-375.
118. Liang G, Tan W., Guo Y, Study on screening and inheritance mode of resistance to Bt transgenic cotton in cotton bollworm. Acta Entomologica Sinica,2000,43:57-62.
119. Liao C.Y., Heckel D.G, Akhurst R., Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera:Noctuidae), major pests of cotton. Journal of Invertebrate Pathology,2002,80:55-63.
120. Liu F., xu Z., Chang J., Chen J., Meng F., Zhu Y.C., Shen J., Resistance allele frequency to Bt cotton in field populations of Helicoverpa armigera (Lepidoptera:Noctuidae) in China. Journal of Economic Entomology,2008,101:933-943.
121. Liu R, xu Z., Zhu Y.C., Huang F., Wang Y., Li H., Gao C., Zhou W., Shen J., Evidence of field evolved resistance to Cry 1 Ac-expressing Bt cotton in Helicoverpa anmigera(Lepidoptera: Noctuidae) in northern China. Pest Management Science,2010,66:155-161.
122. Luo S.D., Wu K.M., Tian Y, Liang GM., Feng x., Zhang J., Guo Y.Y, Crossresistance studies of Cryl Ac-resistant strains of Helicoverpa armigera (Lepidoptera:Noctuidae) to Cry2Ab. Journal of Economic Entomology,2007,100:909-915.
123. Luttrell R., Wan L., Knighten K., Variation in susceptibility of Noctuid (Lepidoptera) larvae attacking cotton and soyabean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. J. Econ. Entomol,1999,92:21-32.
124. Luttrell R.G., Mink J.S., Damage of Cotton fruiting structure by the fall armyworm, Spodoptera frugiperda (Lepidoptera:Noctuidae). J. Cotton Sci,1999,3:35-44.
125. Mahon R.J., Olsen K.M., Downes S., Addison S., Frequency of alleles conferring resistance to the Bt toxins CrylAc and Cry2Ab in Australian populations of Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology,2007,100:1844-1853.
126. McCaffery A.R., Resistance to insecticides in Heliothine lepidoptera:a global view. Philos. Trans. R. Soc. Lond. Ser. B,1998,353:1735-1750.
127. McCaffery, A.R., Resistance to insecticides in Heliothine Lepidoptera:a global view. In:Denholm, I., Pickett, J.A., Devonshire, A.L. (Eds.), Insecticide Resistance from Mechanisms to Management. CABI and the Royal Society, London, UK,1999, pp.59-74.
128. McGaughey W., Whalon M., Managing insect resistance toBacillus thuringiensis toxins. Science, 1992,258:1451-1455.
129. Morin S., Biggs R.W., Shriver L., Ellers-Kirk C, Higginson D., Holley D.,GahanHeckel D.G, Carriere Y, Dennehy T.J., Brown J.K., Tabashnik B.E., Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Nat. Acad. Sci. USA,2003,100: 5004-5009.
130. Morse R.J., Yamamoto T., Stroud R.M., Structure of Cry2Aa suggests an unexpected receptor binding epitope. Structure,2001,9:409-417.
131. Morse S., Bennett R., Ismael Y., Environmental impact of genetically modified cotton in South Africa. Agriculture Ecosystems & Environment,2006,117:277-289.
132. Olsen K., Daly J., Holt H., Finnegan E., Season-long variation in expression of the Cry 1 Ac gene and efficacy of Bacillus thuringiensis toxin in transgenic cotton against Helicoverpa armigera (Lepidoptera:Noctuidae). J. Econ. Entomol.2005,98:1007-1017.
133. Parker C.D. Luttrell R.G., Interplant movement of Heliothis virescens (Lepidoptera:Noctuidae) larvae in pure and mixed plantings of cotton with and without expression of the Cry 1 Ac a-endotoxin protein of Bacillus thuringiensis Berliner. Journal of Economic Entomology,1999,92: 837-845.
134. Pereira E.J.G, Lang B.A., Storer N.P., Siegfried B.D., Selection for Cry1F resistance in the European corn borer and cross-resistance to other Cry toxins. Entomol Exp Appl,2008, 126(2):115-121.
135. Pereira E.J.G, Siqueira H.A.A., Zhuang M., Storer N.P., Siegfried B.D, Measurements of Cry1F binding and activity of luminal gut proteases in susceptible and Cry1F resistant Ostrinia nubilalis larvae (Lepidoptera:Crambidae). J InvertebrPathol,2010,103(1):1-7.
136. Pigott C.R., Ellar D.J., Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev.2007,71:255-281.
137. Qaim M., The economics of genetically modified crops. Annual Review of Resource Economics, 2009,1:665-693.
138. Qaim M., de Janvry A., Bt cotton and pesticide use in Argentina:economic and environmental effects. Environment and Development Economics,2005,10:179-200.
139. Queensland, Insects:understanding Helicoverpa ecology and biology in southern Queensland: know the enemy to manage it better Dept. of Primary Industries and Fisheries (Brisbane),2005.
140. Rausell C., Pardo-Lopez L., Sanchez J., Munoz-Garay C., Morera C., Soberon M., Bravo A., Unfolding events in the water-soluble monomeric Cryl Ab toxin during transition to oligomeric pre-pore and membrane-inserted pore channel. JBiol Chem,2004,279(53):55168-55175.
141. Rajagopal R., Arora N., Sivakumar S., Rao N.GV., Nimbalkar S.A., Bhatnagar R.K., Resistance of Helicoverpa armigera to Cryl Ac toxin from Bacillus thuringiensis is due to improper processing of the protoxin. Biochem J,2009,419:309-316.
142. Rashid B., Khan GA., Husnain T., Riazuddin S., Field Evaluation and Fiber Analysis of Transgenic Cotton. Journal of Crop Sci. Biotech.2009,12 (3):135-141.
143. Romeis J., Meissle M., Bigler F., Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnol,2006,24:63-71.
144. Roush R., Bt-transgenic crops:just another pretty insecticide or a chance for a new start in resistance management? Pesticide Science,1997,51:328-334.
145. Sachs E.S., Benedict J.H., Stelly D.M., Taylor J.F., Altman D.W., Berberich S.A., Davis S.K., Expression and segregation of genes encoding CrylA insecticidal proteins in cotton. Crop Sci. 1998,38:1-11.
146. 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.
147. Sayyed A.H., Raymond B., Ibiza-Palacios M.S., Escriche B., Wright D.J., Genetic and biochemical characterization of field-evolved resistance to Bacillus thuringiensis toxin Cry 1 Ac in the diamondback moth, Plutella xylostella. Appl Environ Microbiol,2004,70(12):7010-7017.
148. Sayyed A.H., Moores G, Crickmore N., Wright D.J., Cross-resistance between a Bacillus thuringiensis Cry toxin and non-Bt insecticides in the diamondback moth. Pest Manag Sci,2008, 64(8):813-819.
149. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H., Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev,1998,62:775-806.
150. Shelton A.M., Zhao J.Z., Rough R.T., Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol.,2002,47:845-881.
151. Sims S.B., Greenplate J.T., Stone T.B., Caprio M.A., Gould F.L., Monitoring strategies for early detection of Lepidoptera resistance to Bacillus thuringiensis insecticidal proteins. In:Brown T.M. (Ed.), Molecular Genetics and Evolution of Pesticide Resistance. ACS Symposium Series, No.645, American Society, Washington, DC,1999, pp.229-242.
152. Sisterson M.S., Biggs R.W., Olson C., Carriere Y., Dennehy T.J., Tabashink B.E., Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environ. Entomol,2004,33:921-929.
153. Soberon M., Gill S.S., Bravo A., Signaling versus punching hole:howdo Bacillus thuringiensis toxins kill insect midgut cells? Cell Mol. Life Sci,2009,66:1337-1349.
154. 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 fi-ugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ.Entomol,2010,103:1031-1038.
155. Stone R., China plans $3.5 billion GM crops initiative. Science,2008,321:1279.
156. Stewart S.D., Adamczyk J.J.Jr., Knighten K.S., Davis F.M., Impact of Bt cottons expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. J. Econ. Entomol.2001,94:752-760.
157. Stewart S.D., Knighten K.S., Efficacy of Bt cottonexpressing two insecticidal proteins of Bacillus thuringiensis Berliner on selected catterpillar pests, In:Dugger P., Richter D., (eds.). Proceedings, 2000 Beltwide Cotton Conference. National Cotton Council, Memphis, TN,2000, p.1043-1048.
158. Subramanian A, Qaim M., Village-wide effects of agricultural biotechnology:the case of Bt cotton in India. World Development,2009,37:256-267.
159. Subramanian A., Qaim M., The impact of Bt cotton on poor households in rural India. Journal of Development Studies,2010,46:295-311.
160. Tabashnik B.E., Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology, 1994,39:47-79.
161. Tabashnik B.E., Carriere Y., Insect resistance to genetically modified crops. In:Gatehouse A., Ferry N. (Eds.), Environmental Impact of Genetically Modified and Novel Crops. CABI, Wallingford, UK,2009a, pp.74-100.
162. Tabashnik B.E., Cushing N.L., Finson N. Johnson M.W., Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera:Plutellidae). Journal of Economic Entomology,1990,83:1671-1676.
163. Tabashnik B.E., Gassmann A.J., Crowder D.W., Carriere Y., Insect resistance to Bt crops:evidence versus theory. Nat. Biotechnol.2008,26,199-202.
164. Tabashnik B.E., Liu Y.B., Malvar T., Heckel D.G., Masson L., Ferre J., Insect resistance to Bacillus thuringiensis:uniform or diverse? Philos Trans R Soc B Biol Sci,1998,353(1376):1751-1756.
165. Tabashnik B.E., Schwartz J.M., Finson N. Johnson M.W., Inheritance of resistance to Bacillus thuringiensis in diamond backmoth (Lepidoptera:Plutellidae). Journal of Economic Entomology, 1992,85:1046-1055.
166. 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., Yelich A.J., Ellers-Kirk C, Harpold V.S., Li x., Carrier, Y, Supressing resistance to Bt cotton with sterile insect releases. Nat. Biotechnol.2010,28:1304-1309.
167. Tabashnik B.E., van Rensburg J.B.J., Carriere Y, Field evolved insect resistance to Bt crop: definition, theory and data. J. Econ. Entomol,2009b,102:2011-2025.
168. UNEP, A country study on the cotton sector in China In:Integrated assessment of trade liberalization and trade related policies. United Nation Environment Programme (UNEP), New York and Geneva pp.1-6,2002.
169. Van Jaarsveld M.J., Basson N.C.J., Marais P., Synthetic pyrethroid resistance in field strains of Helicoverpa armigera (Hubner) (Lepidoptera:Noctuidae) in South Africa. Afr. Plant Protect,1998, 4,15-18.
170. 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.
171. Vaeck M., Reynaerts A., Hofte H., Jansens S., Beuckeleer M.D., Dean C., Zabeau M., Leemans J., Transgenic plants protected from insect attack. Nature,1987,328:33-37.
172. Vassal J.M., Brevault T., Achaleke J., Menozzi P., Genetic structure of the polyphagous pest Helicoverpa armigera (Lepidoptera:Noctuidae) across the sub-Saharan cotton belt. Commun. Agric. Appl. Biol Sci,2008,73,433-437.
173. Wakelyn P.J., May O.L., Menchey E.K., Cotton and Biotechnology. CRC Handbook of Plant Biotechnology. Christou P., Klee H., (Ed.). John Wiley & Sons, Ltd Chichester, West Sussex, UK, 2002, Chapter 57.
174. Walters F.S., deFontes Ch. M., Hart H., Warren GW., Chen J.S., Lepidopteranactive variable-region sequence imparts coleopteran activity in eCry3.1Ab, an engineered Bacillus thuringiensis hybrid insecticidal protein. Appl. Environ. Microbiol,2010,76:3082-3088.
175. Wang GR., Liang GM., Wu K.M., Guo Y.Y., Gene cloning and sequencing of aminopeptidase N3, a putative receptor for Bacillus thuringiensis insecticidal CrylAc toxin in Helicoverpa amigera (Lepidoptera:Noctuidae). Eur J Entomol,2005a,102:13-19.
176. Wang G, Wu K., Liang G, Guo Y, Gene cloning and expression of cadherin in midgut of Helicoverpa armigera and its Cryl A binding region. Science in China Series, C:Life Science,2005, 48:346-356.
177. Williams S., Friedrich L., Dincher S., Carozzi N., Kessmann H., Ward E., Ryals J., Chemical regulation of Bacillus thuringiensis delta-endotoxin expression in transgenic plants, Biotechnology,1993,7,194-200.
178. Wossink A., Denaux Z.S., Environmental and cost efficiency of pesticide use in transgenic and conventional cotton production. Agricultural Systems,2006,90:312-328.
179. Wu K.M., No refuge for insect pests. Nat. Biotechnol.2010,28:1273-1275.
180. Wu K.M., Guo Y.Y., The coordinated development and analysis of contributing factors of cotton bollworm resistance to insecticides in round-Bohai bayregion. Acta Phytophyl.Sin,2000,27, 173-178.
181. Wu K.M., Guo Y.Y., The evolution of cotton pest management practices in China. Annual Review of Entomology,2005,50,31-52.
182. 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 northern China. Journal of Economic Entomology,2002,95:832-837.
183. Wu K., Guo Y, Head G., Resistance monitoring of. Helicoverpa armigera (Lepidoptera:Noctuidae) to Bt insecticidal protein during 2001-2004 in China. J. Econ. Entomol,2006,99 (3):893-898.
184. Wu K., Guo Y, Lv N., Greenplate J. T., Deaton R., Efficacy of transgenic cotton containing a CrylAc gene from Bacillus thuringiensis against Helicovevrpa armigera (Lepidoptera:Noctuidae) in northern China. J. Econ. Entom.,2003,96:1322-1328.
185. Xia J.Y, Wang R.H., Wen S.Q., Wang Y H., A preliminary study on the role of Transgenic Bt cotton in integrated bollworm management. China Cotton,1995,22(8):8-11.
186. Xie R., Zhang M., Ross L.S., Gomez I., Oltean D.I., Bravo A., Soberon M., Gill S.S., Single amino acid mutations in the cadherin receptor from Heliothis virescens affects its toxin binding ability to CrylA toxins. J. Biol. Chem.2005,280:8416-8425.
187. Xu G, Wang G.R., Wu K.M., Guo Y.Y., Gene analysis among different geographical populations of Helicoverpa armigera (Hiibner) by restriction fragment length polymorphisms. Cotton Science 2002,14:352-355.
188. Xu L., Wang Z., Zhang J., He K., Ferry N., Gatehouse A.M.R., Cross-resistance of Cryl Ab selected Asian corn borer to other Cry toxins. JAppl Entomol,2010,134(5):429-438.
189. Xu x., Yu L., Wu Y, Disruption of a cadherin gene associated with resistance to CrylAc delta-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol,2005, 71:948-954.
190. Xu Z., Liu F., Chen J., Huang F., Andow D.A., Wang Y, Zhu Y.C., Shen J., Using an F2 screen to monitor frequency of resistance alleles to Bt cotton in field populations of Helicoverpa armigera (Hubner) (Lepidoptera:Noctuidae). Pest Manag. Sci.2009,65:391-397.
191. Yajun H., Wangzhen G., xinlian S., Tianzhen Z., Molecular cloning and characterization of a cytosolic glutamine synthetase gene, a Wber strength-associated gene in cotton. Planta,2008,228: 473-483.
192. Yang Y., Chen H., Wu Y, Yang Y, Wu S., Mutated cadherin alleles from a field population of Helicoverpa armigera confers resistance to Bacillus thuringiensis toxin Cry1Ac. Appl. Environ. Microbiol.2007,73:6939-6944.
193. Zhang J.H., Wang C.Z., Qin J.D. Guo S.D., Feeding behavior of Helicoverpa armigera larvae on insect-resistant transgenic cotton and non-transgenic cotton. Journal of Applied Entomology,2004, 128:218-225.
194. Zhang S., Cheng H., GAO Y, Wang G, Liang G, Wu K., Mutation of anaminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochern. Mol. Biol,2009,39:421-429.
195. Zhang x., Candas M., Griko N.B., Taussig R., Bulla Jr. L.A., A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the CrylAb toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. U.S.A.2006,103:9897-9902.
196. Zhao J.Z., Cao J., Collins H.L., Bates S.L., Rousch R.T., Earle E.D., Shelton A.M., Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to transgenic plants. Proc. Natl. Acad. Sci,2005,102 (24):8426-8430.
197. Zhao J.Z., Li Y.x., Collins H.L., Shelton A.M., Examination of the F2 screen forrare resistance alleles to Bacillus thuringiensis toxins in the diamondback moth (Lepidoptera:Plutellidae). J. Econ. Entomol,2002,95,14-21.
198. Zhao J.Z., Lu M.G., Fan x.L., xia F.Z., Interaction between Helicoverpa armigera and transgenic Bt cotton in North China. Scientia Agricultura Sinica,1998,31(5):1-6.
199. Zhou L., Fang Y, Yang J., Investigation on artificial diet in Heliothis armigera. Acta Entomol. Sin, 1981,24:108-110.
200. Zhao x., Tidsell C, A comparative economic study of China's and Australia's cotton production. Economic theory, application and issues,2009, working papers No.53, The University of Queensland.