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Does cotton bollworm show cross-resistance to the Bacillus thuringiensis toxins Cry1Ac and Cry2Ab? A mini review |
MA Jihong1,2,3, TIAN Changyan1,*(), LYU Guanghui3, MAI Wenxuan1 |
1 State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China 2 University of Chinese Academy of Sciences, Beijing 100049, China 3 College of Resources and Environment Science, Xinjiang University, Urumqi 830046, China |
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Abstract Since 1996, transgenic Bacillus thuringiensis (Bt) cotton has been commercially grown in numerous countries in an effort to stem the losses caused by key lepidopteran pests. However, the development of pest resistance to Bt toxins has jeopardized the continued utilization of Bt cotton. As a strategy designed to circumvent the development of resistance, Bt cotton varieties expressing two or more toxins targeting the same pest have been introduced. Nevertheless, from the perspective of long-term planting of Bt cotton, the potential risk of cross-resistance to these Bt toxins is a threat that cannot be ignored. In this paper, we review current research (including that based on the analysis of protein binding sites and resistance genes) on the resistance of cotton bollworm (Helicoverpa armigera) to the Bt toxins Cry1Ac and Cry2Ab and the interrelationship between these toxins. On the basis of existing evidence, we assume that the actions of Cry1Ac and Cry2Ab against cotton bollworm are not completely independent, and then propose the ''resistance-associated gene mutation potential hypothesis''. Although the mechanisms underlying the resistance of pests to Bt toxins are yet to be comprehensively elucidated, this hypothesis could undoubtedly have important implications for adopting ''pyramid'' strategy in the future. Further research is recommended to devise strategies to retard the development of H. armigera resistance to Bt cotton, either using different Bt toxins or their various combinations.
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Received: 21 May 2019
Published: 10 March 2020
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Corresponding Authors:
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About author: *Corresponding author: TIAN Changyan (E-mail: tianchy@ms.xjb.ac.cn) |
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[1] |
Akhurst R J, James W, Bird L J, et al. 2003. Resistance to the Cry1Ac δ-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology, 96(4): 1290-1299.
doi: 10.1603/0022-0493-96.4.1290
pmid: 14503603
|
|
|
[2] |
Albernaz K C, Merlin B L, Martinell S, et al. 2013. Baseline susceptibility to Cry1Ac insecticidal protein in Heliothis virescens (Lepidoptera: Noctuidae) populations in Brazil. Journal of Economic Entomology, 106(4): 1819-1824.
doi: 10.1603/EC12222
|
|
|
[3] |
Allah B, Rao A Q, Shahid A A, et al. 2009. Insect resistance and risk assessment studies in advance lines of Bt cotton harboring Cry1Ac and Cry2A genes. American-Eurasian Journal of Agricultural and Environmental Science, 6(1): 1-11.
|
|
|
[4] |
Alvi A H, Sayyed A H, Naeem M, et al. 2012. Field evolved resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis toxin Cry1Ac in Pakistan. PloS ONE, 7(10): e47309, doi: 10.1371/journal.pone.0047309.
doi: 10.1371/journal.pone.0047309
pmid: 23077589
|
|
|
[5] |
Bravo A, Soberón M. 2008. How to cope with insect resistance to Bt toxins? Trends in Biotechnology, 26(10): 573-579.
doi: 10.1016/j.tibtech.2008.06.005
|
|
|
[6] |
Brevault T, Heuberger S, Zhang M, et al. 2013. Potential shortfall of pyramided transgenic cotton for insect resistance management. Proceed of the National Academy of Sciences of the United States of America, 110(15): 5806-5811.
doi: 10.1073/pnas.1216719110
pmid: 23530245
|
|
|
[7] |
Brvault T, Prudent P, Vaissayre M, et al. 2009. Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry1Ac and Cry2Ab2 insecticidal proteins in four countries of the West African cotton belt. Journal of Economic Entomology, 102(6): 2301-2309.
doi: 10.1603/029.102.0636
pmid: 20069861
|
|
|
[8] |
Caccia S, Hernandez-Rodriguez C S, Mahon R J, et al. 2010. Binding site alteration is responsible for field-isolated resistance to Bacillus thuringiensis Cry2A insecticidal proteins in two Helicoverpa species. PloS ONE, 5(4): e9975, doi: 10.1371/journal.pone.0009975.
doi: 10.1371/journal.pone.0009975
pmid: 20376312
|
|
|
[9] |
Carrière Y, Degain B A, Unnithan G C, et al. 2018. Effects of seasonal changes in cotton plants on the evolution of resistance to pyramided cotton producing the Bt toxins Cry1Ac and Cry1F in Helicoverpa zea. Pest Management Science, 74(3): 627-637.
doi: 10.1002/ps.4746
pmid: 28967711
|
|
|
[10] |
Cui L, Wang Q Q, Qi H L, et al. 2018. Resistance selection of indoxacarb in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): Cross-resistance, biochemical mechanisms and associated fitness costs. Pest Management Science, 74(11): 2636-2644.
doi: 10.1002/ps.5056
pmid: 29707889
|
|
|
[11] |
Denholm I, Rowland M W. 1992. Tactics for managing pesticide resistance in arthropods: Theory and practice. Annual Review of Entomology, 37(1): 91-112.
doi: 10.1146/annurev.en.37.010192.000515
pmid: 1539942
|
|
|
[12] |
Downes S J, Mahon R, Olsen K. 2007. Monitoring and adaptive resistance management in Australia for Bt-cotton: Current status and future challenges. Journal of Invertebrate Pathology, 95(3): 208-213.
doi: 10.1016/j.jip.2007.03.010
pmid: 17470372
|
|
|
[13] |
Downes S J, Kriticos D J, Parry H, et al. 2017. A perspective on management of Helicoverpa armigera: transgenic Bt cotton, IPM, and landscapes. Pest Management Science, 73(3): 485-492.
doi: 10.1002/ps.4461
pmid: 27753247
|
|
|
[14] |
Fleming D, Musser F, Reisig D, et al. 2018. Effects of transgenic Bacillus thuringiensis cotton on insecticide use, heliothine counts, plant damage, and cotton yield: A meta-analysis, 1996-2015. PLoS ONE, 13(7): e0200131, doi: 10.1371/journal.pone.0200131.
doi: 10.1371/journal.pone.0200131
pmid: 30024919
|
|
|
[15] |
Gould F, Anderson A, Jones A, et al. 1997. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Sciences of the United States of America, 94(8): 3519-3523.
|
|
|
[16] |
Gould F. 2000. Testing Bt refuge strategies in the field. Nature Biotechnology, 18(3): 266-267.
doi: 10.1038/73693
pmid: 10700135
|
|
|
[17] |
Gujar G T, Kalia V, Bunker G K, et al. 2010. Impact of different levels of non-Bt cotton refuges on pest populations, bollworm damage, and Bt cotton production. Journal of Asia-Pacific Entomology, 13(4): 249-253.
doi: 10.1016/j.aspen.2010.06.004
|
|
|
[18] |
Hernandez-Rodriguez C S, Hernandez-Martinez P, van R J, et al. 2013. Shared midgut binding sites for Cry1A. 105, Cry1Aa, Cry1Ab, Cry1Ac and Cry1Fa proteins from Bacillus thuringiensis in two important corn pests, Ostrinia nubilalis and Spodoptera frugiperda. PloS ONE, 8(7): e68164, doi: 10.1371/journal.pone.0068164.
doi: 10.1371/journal.pone.0068164
pmid: 23861865
|
|
|
[19] |
ISAAA (International Service for the Acquisition of Agri-biotech Applications). 2018. Global development of biotechnology/genetically modified crops in 2017. China Biotechnology, 38(6): 1-8. (in Chinese)
|
|
|
[20] |
Jin L, Wei Y Y, Zhang L, et al. 2013. Dominant resistance to Bt cotton and minor cross-resistance to Bt toxin Cry2Ab in cotton bollworm from China. Evolutionary Applications, 6(8): 1222-1235.
doi: 10.1111/eva.12099
|
|
|
[21] |
Kain W, Song X Z, Janmaat A F, et al. 2015. Resistance of Trichoplusia ni populations selected by Bacillus thuringiensis sprays to cotton plants expressing pyramided Bacillus thuringiensis toxins Cry1Ac and Cry2Ab. Applied and Environmental Microbiology, 81(5): 1884-1890.
doi: 10.1128/AEM.03382-14
pmid: 25480752
|
|
|
[22] |
Kaur P, Dilawari V K. 2011. Inheritance of resistance to Bacillus thuringiensis Cry1Ac toxin in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) from India. Pest Management Science, 67(10): 1294-1302.
doi: 10.1002/ps.2185
|
|
|
[23] |
Kranthi S, Dhawad C S, Naidu S, et al. 2009. Susceptibility of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) to the Bacillus thuringiensis toxin Cry2Ab before and after the introduction of Bollgard-II. Crop Protection, 28(5): 371-375.
doi: 10.1016/j.cropro.2008.12.001
|
|
|
[24] |
Li Y M. 2009. Study on molecular genetic mechanism of resistance to Bt toxin Cry1Ac in Helicoberpa armigera (Hubner). PhD Dissertation. Harbin: Northeast Agricultural University, 52-53. (in Chinese)
|
|
|
[25] |
Li Y X, Greenberg S M, Liu T X. 2006. Effects of Bt cotton expressing Cry1Ac and Cry2Ab and non-Bt cotton on behavior, survival and development of Trichoplusia ni (Lepidoptera: Noctuidae). Crop Protection, 25(9): 940-948.
doi: 10.1016/j.cropro.2005.12.007
|
|
|
[26] |
Liang G M, Wu K M, Yu H K, et al. 2008. Changes of inheritance mode and fitness in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) along with its resistance evolution to Cry1Ac toxin. Journal of Invertebrate Pathology, 97(2): 142-149.
doi: 10.1016/j.jip.2007.09.007
pmid: 17950749
|
|
|
[27] |
Liu C, Zhang D D, Wang Z Y, et al. 2018. Resistance, and cross-resistance, of Helicoverpa armigera to different Bt proteins. Chinese Journal of Applied Entomology, 55(1): 55-60. (in Chinese)
|
|
|
[28] |
Liu L P, Gao M J, Yang S, et al. 2017. Resistance to Bacillus thuringiensis toxin Cry2Ab and survival on single-toxin and pyramided cotton in cotton bollworm from China. Evolutionary Applications, 10(2): 170-179.
doi: 10.1111/eva.12438
pmid: 28127393
|
|
|
[29] |
Luo S D. 2007. The investigation of resistance risk on Bt-Cry1Ac-resistant Helicoberpa armigera (Lepidoptrea: Noctuidae) to Cry2Ab. PhD Dissertation. Beijing: Chinese Academy of Agricultural Sciences, 71-72. (in Chinese)
|
|
|
[30] |
Luttrell R G, Fitt G P, Ramalho F S, et al. 1994. Cotton pest management: Part 1. A worldwide perspective. Annual Review of Entomology, 39: 517-526.
doi: 10.1146/annurev.en.39.010194.002505
|
|
|
[31] |
Mcgaughey W H, Whalon M E. 1992. Managing insect resistance to Bacillus thuringiensis toxins. Science, 258(5087): 1451-1455.
doi: 10.1126/science.258.5087.1451
pmid: 17755107
|
|
|
[32] |
Melo A L D, Soccol V T, Soccol C R. 2014. Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Critical Reviews in Biotechnology, 36(2): 317-326.
doi: 10.3109/07388551.2014.960793
pmid: 25264571
|
|
|
[33] |
Nair R, Kalia V, Aggarwal K K, et al. 2010. Inheritance of Cry1Ac resistance and associated biological traits in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology, 104(1): 31-38.
doi: 10.1016/j.jip.2010.01.004
pmid: 20097203
|
|
|
[34] |
Niu L, Ma Y, Mannakkara A, et al. 2013. Impact of single and stacked insect-resistant Bt-cotton on the honey bee and silkworm. PLoS ONE, 8(9): e72988, doi: 10.1371/journal.pone.0072988.
doi: 10.1371/journal.pone.0072988
pmid: 24039838
|
|
|
[35] |
Peterson B, Bezuidenhout C C, van den Berg J. 2017. An overview of mechanisms of cry toxin resistance in lepidopteran insects. Journal of Economic Entomology, 110(2): 362-377.
doi: 10.1093/jee/tow310
pmid: 28334065
|
|
|
[36] |
Pray C, Ma D M, Huang J K, et al. 2001. Impact of Bt cotton in China. World Development, 29(5): 813-825.
doi: 10.1016/S0305-750X(01)00010-9
|
|
|
[37] |
Qaim M. 2009. The economics of genetically modified crops. Annual Review of Resource Economics, 1: 665-693.
doi: 10.1146/annurev.resource.050708.144203
|
|
|
[38] |
Qiao F B, Huang J K, Wang X B. 2017. Fifteen years of Bt cotton in China: Results from household surveys. World Development, 98: 351-359.
doi: 10.1016/j.worlddev.2017.05.006
|
|
|
[39] |
Reisig D D, Huseth A S, Bacheler J S, et al. 2018. Long-term empirical and observational evidence of practical Helicoverpa zea resistance to cotton with pyramided Bt toxins. Journal of Economic Entomology, 111(4): 1824-1833.
doi: 10.1093/jee/toy106
pmid: 29668958
|
|
|
[40] |
Sanahuja G, Banakar R, Twyman R M, et al. 2011. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnology Journal, 9(3): 283-300.
doi: 10.1111/j.1467-7652.2011.00595.x
|
|
|
[41] |
Shabbir M Z, Quan Y D, Wang Z Y, et al. 2018. Characterization of the Cry1Ah resistance in Asian corn Borer and its cross-resistance to other Bacillus thuringiensis toxins. Scientific Reports, 8: 234, doi: 10.1038/s41598-017-18586-2.
doi: 10.1038/s41598-017-18586-2
pmid: 29321568
|
|
|
[42] |
Sivasupramaniam S, Head G P, English L, et al. 2007. A global approach to resistance monitoring. Journal of Invertebrate Pathology, 95(3): 224-226.
doi: 10.1016/j.jip.2007.03.013
pmid: 17467005
|
|
|
[43] |
Shivendra S K, Deepthi K. 2016. Agricultural biotechnology and crop productivity: macro-level evidences on contribution of Bt cotton in India. Current Science, 110(3): 311-319.
doi: 10.18520/cs/v110/i3/311-319
|
|
|
[44] |
Subramanian A, Qaim M. 2010. The impact of Bt cotton on poor households in rural India. Journal of Development Studies, 46(2): 295-311.
doi: 10.1080/00220380903002954
|
|
|
[45] |
Sushmita K, Ramesh B, Pattanayak D, et al. 2016. Gene pyramiding: A strategy for insect resistance management in Bt transgenic crops. Indian Journal of Biotechnology, 15: 283-291.
|
|
|
[46] |
Tabashnik B E. 1994. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology, 39: 47-79.
doi: 10.1146/annurev.en.39.010194.000403
|
|
|
[47] |
Tabashnik B E, Dennehy T J, Sims M A, et al. 2002. Control of resistant pink bollworm (Pectinophora gossypiella) by transgenic cotton that produces Bacillus thivingiensis toxin Cry2Ab. Applied & Evironmental Microbiology, 68(8): 3790-3794.
doi: 10.1128/aem.68.8.3790-3794.2002
pmid: 12147473
|
|
|
[48] |
Tabashnik B E, van Rensburg J B J, Carrière Y. 2009a. Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology, 102(6): 2011-2025.
doi: 10.1603/029.102.0601
pmid: 20069826
|
|
|
[49] |
Tabashnik B E, Unnithan G C, Masson L, et al. 2009b. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America, 106(29): 11889-11894.
|
|
|
[50] |
Tay W T, Mahon R J, Heckel D G, et al. 2015. Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily a protein. PLoS Genetics, 11(11): e1005534, doi: 10.1371/journal.pgen.1005534.
doi: 10.1371/journal.pgen.1005534
pmid: 26583651
|
|
|
[51] |
Wang J N, Dai X F. 2009. Resistance for Helicoverpa armigera against the transgenic Bt cotton and its management strategy. Molecular Plant Breeding, 7(1): 117-124. (in Chinese)
|
|
|
[52] |
Wang Y Q, Wang Y D, Wang Z Y, et al. 2016. Genetic basis of Cry1F-resistance in a laboratory selected Asian corn borer strain and its cross-resistance to other Bacillus thuringiensis toxins. PLoS ONE, 11(8): e0161189, doi: 10.1371/journal.pone.0161189.
doi: 10.1371/journal.pone.0161189
pmid: 27518813
|
|
|
[53] |
Wei J Z, Guo Y Y, Gao X W, et al. 2012. Evaluation of the toxicity of Cry1Fa to the Cry1Ac-resistant cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Acta Entomologica sinica, 55(10): 1154-1160. (in Chinese)
|
|
|
[54] |
Wei J Z, Guo Y Y, Liang G M, et al. 2015. Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Scientific Reports, 5: 7714, doi: 10.1038/srep07714.
doi: 10.1038/srep07714
pmid: 25586723
|
|
|
[55] |
Wei J Z. 2016. The roles of receptors in the mechanism of cross-resistance between Cry1Ac and Cry2Ab in cotton bollworm. PhD Dissertation. Beijing: Chinese Academy of Agricultural Sciences. (in Chinese)
|
|
|
[56] |
Wei J Z, Liang G M, Wang B J, et al. 2016. Activation of Bt protoxin Cry1Ac in resistant and susceptible cotton bollworm. PLoS ONE, 11(6): e0156560, doi: 10.1371/journal.pone.0156560.
doi: 10.1371/journal.pone.0156560
pmid: 27257885
|
|
|
[57] |
Welch K L, Unnithan G C, Degain B A, et al. 2015. Cross-resistance to toxins used in pyramided Bt crops and resistance to Bt sprays in Helicoverpa zea. Journal of Invertebrate Pathology, 132: 149-156.
doi: 10.1016/j.jip.2015.10.003
pmid: 26458274
|
|
|
[58] |
Williams S, Friedrich L, Dincher S, et al. 1992. Chemical regulation of Bacillus thuringiensis ∂-endotoxin expression in transgenic plants. Bio/Technology, 10(5): 540-543.
|
|
|
[59] |
Wilson L J, Whitehouse M E A, Herron G A. 2018. The management of insect pests in Australian Cotton: An evolving story. Annual Review of Entomology, 63(1): 215-237.
doi: 10.1146/annurev-ento-020117-043432
pmid: 29324044
|
|
|
[60] |
Wu K M, Liang G M, Guo Y Y. 1997. Phoxim resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) in China. Journal of Economic Entomology, 90(4): 868-872.
doi: 10.1093/jee/90.4.868
|
|
|
[61] |
Wu K M, Guo Y Y, Lv N. 1999. Geographic variation in susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis insecticidal protein in China. Journal of Economic Entomology, 92(2): 273-278.
doi: 10.1093/jee/92.2.273
|
|
|
[62] |
Wu K M, Guo Y Y. 2005. The evolution of cotton pest management practices in China. Annual Review of Entomology, 50(1): 31-52.
doi: 10.1146/annurev.ento.50.071803.130349
|
|
|
[63] |
Xiao Y T, Dai Q, Hu R Q, et al. 2017. A single point mutation resulting in cadherin mislocalization underpins Resistance against Bacillus thuringiensis toxin in cotton bollworm. Journal of Biological Chemistry, 292(7): 2933-2943.
doi: 10.1074/jbc.M116.768671
pmid: 28082675
|
|
|
[64] |
Xu X J. 2005. Biochemical and molecular mechanisms of resistance to Cry1Ac-endotoxin of Bacillus thuringensis in Helicoverpa armigera (Hubner). PhD Dissertation. Nanjing: Nanjing Agricultural University, 97. (in Chinese)
|
|
|
[65] |
Xu Y L, Wang Z Y, He K L, et al. 2006. The mechanism of insect resistance to Bt toxin and the resistance management tactics. Acta Phytophylacica Sinica, 33(4): 437-444. (in Chinese)
|
|
|
[66] |
Yang Y J. 2010. Identification and detection of mutated cadherin alleles associated with Cry1Ac resistance in Helicoverpa armigera (Hübner). PhD Dissertation. Nanjing: Nanjing Agricultural University. (in Chinese)
|
|
|
[67] |
Yin W. 2012. Baseline toxicity of Cry2Ab and identification of midgut Cry2Ab-binding proteins and midgut juice proteins of Helicoverpa armigera. MSc Thesis. Nanjing: Nanjing Agricultural University: 36-37. (in Chinese)
|
|
|
[68] |
Yu L Y. 2004. Inheritance mode and cross resistance pattern of a Cry1Ac-resistant strain or Helicoverpa armigera (Hübner). MSc Thesis. Nanjing: Nanjing Agricultural University. (in Chinese)
|
|
|
[69] |
Zhao J. 2012. Frequency and inheritance of resistance alleles to Cry1Ac and Cry2Ab in Jiangpu and Anyang populations of Helicoverpa armigera. PhD Dissertation. Nanjing: Nanjing Agricultural University. (in Chinese)
|
|
|
[70] |
Zhao Z Y, Li Y H, Xiao Y T, et al. 2016. Distribution and metabolism of Bt-Cry1Ac toxin in tissues and organs of the cotton bollworm, Helicoverpa armigera. Toxins, 8(7): 212, doi: 10.3390/toxins8070212.
doi: 10.3390/toxins8070212
pmid: 27399776
|
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