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Environmental Chemistry Letters

, Volume 13, Issue 3, pp 239–249 | Cite as

Safe use of Cry genes in genetically modified crops

  • M. Rahman
  • Muhammad Zaman
  • Tayyaba Shaheen
  • Samra Irem
  • Yusuf Zafar
Review

Abstract

Genomic technologies have been used to improve cultivated crop species. For example, Bt genes such as Cry1Ac, Cry2Ab, Cry1F and Cry3Bb1 are derived from Bacillus thuringiensis, a soil bacterium. Such genes provide protection against lepidopteran insect pests. Bt genes have been introduced in corn, cotton, soybean, rice, potato and canola. Genetically modified (GM)-cotton, containing the Cry1Ac gene, was released for cultivation in the mid-1990s in the USA and later in 28 countries including China and India. Potential harmful effects of the Bt-crops on non-targets were assessed before release into the environment. Most commonly, cultivation of the Bt-crops was found safe. Safety was tested using various experiments including: the insertional impact of transgene and its regulatory elements on plant phenotype and agronomic performance; effect on non-target organisms; and nutritional impacts on multiple experimental models, albeit the studies were conducted for limited durations. However, skeptics always claim for conducting extensive clinical as well as field trials and also cast doubt on methods and procedures of calculating the ecological risks. This debate got further momentum especially after the publication of reports on substantial reduction in monarch butterfly caterpillars when exposed to Bt-maize pollen—though later nullified—and detection of traces of transgene in various tissues of experimental animals. It is generally accepted that procedures, methods and protocols for evaluating the potential risks of GM-crops and foods should be standardized for building confidence of all stakeholders. Efforts should be exerted in deploying genes of interest, marker genes and regulatory sequences invoking no or little issues of potential risks to the ecosystem.

Keywords

GM-crops Bt-crops Cry genes Risk assessment Safety evaluation Genotoxicity Blood biochemistry Allergic response Non-target organisms Mammals Birds Human 

Abbreviations

GM

Genetically modified

GE

Genetically engineered

Bt

Bacillus thuringiensis

NTOs

Non-target organisms

PIPs

Plant-incorporated protectants

CaMV35S

Cauliflower mosaic virus 35S promoter

GFP gene

Green fluorescent protein gene

nptII gene

Neomycin phosphotransferase gene

IgE

Immunoglobulin E

IgG

Immunoglobulin G

ELISA

Enzyme-linked immunosorbent assay

PCR

Polymerase chain reaction

MBC

Biomass carbon

MBN

Biomass nitrogen

Notes

Acknowledgments

We are extremely grateful to the funding agency Pakistan Science Foundation for providing funds through a project “Exploration of Cotton Germplasm Potential Against Drought Stress Using Genomic Approaches”—Project No. PSF/NSLP/P-NIBGE (19).

References

  1. Bannon G, Fu TJ, Kimber I, Hinton DM (2003) Protein digestibility and relevance to allergenicity. Environ Health Perspect 111:1122–1124CrossRefGoogle Scholar
  2. Barriere Y, Verite R, Brunschwig P, Surault F, Emile JC (2001) Feeding value of corn silage estimated with sheep and dairy cows is not altered by genetic incorporation of Bt1376 resistance to Ostrinia nubilalis. J Dairy Sci 84:1863–1871CrossRefGoogle Scholar
  3. Bashir K, Husnain T, Fatima T, Riaz N, Makhdoom R, Riazuddin S (2005) Novel indica basmati line (B-370) expressing two unrelated genes of Bacillus Thuringiensis is highly resistant to two lepidopteron insects in the field. Crop Prot 24:870–879CrossRefGoogle Scholar
  4. Bernstein JA, Bernstein IL, Bucchini L, Goldman LR, Hamilton RG, Lehrer S, Rubin C (2003) Clinical and laboratory investigation of allergy to genetically modified foods. Environ Health Perspect 111:1114–1121CrossRefGoogle Scholar
  5. Chen H, Lin Y (2013) Promise and issues of genetically modified crops. Curr Opin Plant Biol 16:255CrossRefGoogle Scholar
  6. Chen M, Ye GY, Liu ZC, Yao HW, Chen XX, Shen ZC, Hu C, Datta SK (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(1):127–134CrossRefGoogle Scholar
  7. Chowdhury EH, Kuribara H, Hino A, Sultana P, Mikami O, Shimada N, Guruge KS, Saito M, Nakajima Y (2003) Detection of corn intrinsic and recombinant DNA fragments Cry1Ab protein in the gastrointestinal contents of pigs fed genetically modified corn Bt11. J Anim Sci 81:2546–2551Google Scholar
  8. Conner AJ, Jacobs JME (1999) Genetic engineering of crops as potential source of genetic hazard in the human diet. Mutat Res 443:223–234CrossRefGoogle Scholar
  9. De Schrijver A, Devos Y, van den Bulcke M, Cadot P, De Loose M, Reheul D, Sneyers M (2007) Risk assessment of GM stacked events obtained from crosses between GM events. Trends Food Sci Technol 18:101–109CrossRefGoogle Scholar
  10. de Vries J, Meier P, Wackernagel W (2001) The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiol Lett 195:211–215CrossRefGoogle Scholar
  11. Donkin SS, Velez JC, Totten AK, Stanisiewski EP, Hartnell GF (2003) Effects of feeding silage and grain from glyphosate-tolerant or insect-protected corn hybrids on feed intake, ruminal digestion, and milk production in dairy cattle. J Dairy Sci 86:1780–1788CrossRefGoogle Scholar
  12. FAO/WHO (2001) Evaluation of allergenicity of genetically modified foods report of a joint FAO/WHO expert consultation on foods derived from biotechnology, 22–15 January 2001, Rome Italy. Food and Agriculture Organisation of the United Nations, Rome http://www.fao.org/es/esn/allergygm.pdf
  13. Flachowsky G, Chesson A, Aulrich K (2005) Animal nutrition with feeds from genetically modified plants. Arch Anim Nutr 59:1–40CrossRefGoogle Scholar
  14. Framond AJ, Bevan MW, Barton KA, Flavell F, Chilton MD (1983) Mini-Ti plasmid and a chimeric gene construct: new approaches to plant gene vector construction. Adv Gene Technol Mol Genet Plants Anim Miami Winter Symp 20:159–170CrossRefGoogle Scholar
  15. Germolec DR, Kimber I, Goldman L, Selgrade M (2003) Key issues for the assessment of the allergenic potential of genetically modified foods: breakout group reports. Environ Health Perspect 11:1131–1139Google Scholar
  16. Gupta VVSR, Roberts GN, Neate SM, McClure SG, Crisp P, Watson SK (2002) Impact of Bt-cotton on biological processes in Australian soils. In: Akhurst RJ, Beard CE, Hughes PA (Eds.) Proceedings of the fourth Pacific Rim conference on the biotechnology of Bacillus thuringiensis and its environmental impacts. CSIRO, Australia, pp 191–194Google Scholar
  17. Head G, Surber JB, Watson JA, Martin JW, Duan JJ (2002) No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollgard) use. Environ Entomol 31:30–36CrossRefGoogle Scholar
  18. Hellmich RL, Hellmich KA (2012) Use and impact of Bt maize. Nat Educ Knowl 3(5):4Google Scholar
  19. Ho MW, Ryan A, Cummins J (2000) Hazards of transgenic plants containing the cauliflower mosaic virus promoter. Microb Ecol Health Dis 12(3):189–198CrossRefGoogle Scholar
  20. Hodgson J (2000) Scientists avert new GMO crisis. Nat Biotechnol 18:13CrossRefGoogle Scholar
  21. Huang J, Mi JW, Lin H, Wang Z, Chen R, Hu R, Rozelle S, Pray CE (2010) A decade of Bt cotton in Chinese fields: assessing the direct effects and indirect externalities of Bt cotton adoption in China. Sci China Life Sci 53:981–991CrossRefGoogle Scholar
  22. Huesing J, English L (2004) The impact of Bt crops on the developing world. AgBioForum 7(1&2):84–95Google Scholar
  23. Hutchison WD, Burkness EC, Mitchell PD, Moon RD, Leslie TW, Fleischer SJ, Abrahamson M, Hamilton KL, Steffey KL, Gray ME, Hellmich RL, Kaster LV, Hunt TE, Wright RJ, Pecinovsky K, Rabaey TL, Flood BR, Raun ES (2010) Area wide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330:222–225CrossRefGoogle Scholar
  24. Jagadish CT, Indira R, Vandana S (2012) Effect of Bt-transgenic cotton on soil biological health. Appl Biol Res 14(1):5–23Google Scholar
  25. James C (2014) Global status of commercialized biotech/GM crops. ISAAA, Ithaca, NYGoogle Scholar
  26. Jennings JC, Albee LD, Kolwyck DC, Surber JB, Taylor ML, Hartnell GF, Lirette RP, Glenn Monsanto KC (2003a) Attempts to detect transgenic and endogenous plant DNA and transgenic protein in muscle from broilers fed yieldgard corn borer corn. Poult Sci 82:371–380CrossRefGoogle Scholar
  27. Jennings JC, Kolwyck DC, Kays SB, Whetsell AJ, Suber JB, Cromwell GL, Lirette RP, Glenn KC (2003b) Determining whether transgenic and endogenous plant DNA and transgenic protein are detectable in muscle from swine fed roundup ready soybean meal. J Anim Sci 81:1447–1455Google Scholar
  28. Jiang J, Linscombe SD, Wang J, Oard JH (2000) Field evaluation of transgenic rice (Oryza sativa L.) produced by agrobacterium and particle bombardment methods. In: Plant and animal genome VIII conference (9–12 January 2000, Town and County Hotel, San Diego, CA; Abstr)Google Scholar
  29. Kaeppler Shawn M, Kaeppler Heidi F, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188CrossRefGoogle Scholar
  30. Karihaloo JL, Kumar PA (2009) Bt cotton in India—a status report, 2nd edn. Asia-Pacific consortium on agricultural biotechnology (APCoAB), New DelhiGoogle Scholar
  31. Kuiper HA, Kleter GA, Noteborn HPMJ, Kok EJ (2001) Assessment of the food safety issues related to genetically modified foods. Plant J 27:503–528CrossRefGoogle Scholar
  32. Kuiper HA, Konig A, Kleter GA, Hammes WP, Knudsen I (2004) Concluding remarks. Food Chem Toxicol 42:1195–1202CrossRefGoogle Scholar
  33. Magaña-Gómez JA, de la Barca AMC (2009) Risk assessment of genetically modified crops for nutrition and health. Nutr Rev 67:1–16CrossRefGoogle Scholar
  34. Mal P, Manjunatha AV, Bauer S, Ahmed MN (2011) Technical efficiency and environmental impact of Bt cotton and non-Bt cotton in north India. AgBioForum 14(3):164–170Google Scholar
  35. Matzke MA, Mette MF, Matzke AJM (2000) Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol Biol 43:401–415CrossRefGoogle Scholar
  36. Mendelsohn M, Kough J, Vaituzis Z, Matthewset K (2003) Are Bt crops safe? Nat Biotechnol 21:1003–1009CrossRefGoogle Scholar
  37. Mendelsohn M, Kough J, Vaituzis Z, Matthews K (2004) Are Bt crops safe? AgBioForum 7(1&2):30Google Scholar
  38. Messeguer J (2003) Gene flow assessment in transgenic plants. Plant Cell Tissue Organ 73:201–212CrossRefGoogle Scholar
  39. Metcalfe DD (2003) Introduction: what are the issues in addressing the allergenic potential of genetically modified foods? Environ Health Perspect 11:1110–1113Google Scholar
  40. Murray SR, Butler RC, Hardacre AK, Timmerman-Vaughan (2007) Use of quantitative real-time PCR to estimate maize endogenous DNA degradation after cooking and extrusion or in food products. J Agric Food Chem 55:2231–2239CrossRefGoogle Scholar
  41. Nordlee JA, Taylor SL, Townsend JA, Thomas LA, Bush RK (1996) Identification of a Brazil nut allergen in transgenic soybeans. N Engl J Med 334:688–692CrossRefGoogle Scholar
  42. Noteborn HPJM, Kuiper HA (1994) Safety assessment strategies for genetically modified plant products case study: Bacillus thuringiensis-toxin tomato. In: Jones DD (ed) proceeding of 3rd international symposium on the biosafety results of field tests of genetically modified plants and microorganisms. University of California, Division of Agriculture and Natural Resources, Oakland, CA, pp 199–207Google Scholar
  43. Oosterhuis DM, Jernstedt J (1999) Morphology and anatomy of cotton plant. In: Smith CW, Cothren JT (eds) Cotton: origin, history, technology and production. Willie, Darvers, pp 170–206Google Scholar
  44. Pakistan National Biosafety Rules (2005)Google Scholar
  45. Palm CJ, Donegan KK, Harris D, Seidler RJ (1994) Quantification in soil of Bacillus thuringiensis var kurstaki d-endotoxin from transgenic plants. Mol Ecol 3:145–151CrossRefGoogle Scholar
  46. Paparini A, Romano-Spica V (2004) Public health issues related with the consumption of food obtained from genetically modified organisms. Biotechnol Annu Rev 10:85–122CrossRefGoogle Scholar
  47. Paparini A, Romano-Spica V (2006) Gene transfer and cauliflower mosaic virus promoter 35S activity in mammalian cells. J Environ Sci Health 41:437–449CrossRefGoogle Scholar
  48. Perlak FJ, Oppenhuizen M, Gustafson K, Voth R, Sivasupramaniam S, Heering D, Carey B, Ihrig RA, Roberts JK (2001) Development and commercial use of Bollgard® cotton in the USA: early promises versus today’s reality. Plant J 27(6):489–501CrossRefGoogle Scholar
  49. Pilcher CD, Rice ME, Obrycki JJ (2005) Impact of transgenic Bacillus thuringiensis corn and crop phenology on five nontarget arthropods. Environ Entomol 34:1302–1316CrossRefGoogle Scholar
  50. Poehlman JM (1994) Breeding field crops, 3rd edn. Iowa State University Press, AmesGoogle Scholar
  51. Prado JR, Segers G, Voelker T, Carson D, Dobert R, Phillips J, Cook K, Cornejo C, Monken J, Grapes L (2014) Genetically engineered crops: from idea to product. Annu Rev Plant Biol 65:769–790CrossRefGoogle Scholar
  52. Pray C, Naseem A (2007) Supplying crop biotechnology to the poor: opportunities and constraints. J Dev Stud 43(1):192–217CrossRefGoogle Scholar
  53. Prescott VE, Hogan SP (2006) Genetically modified plants and food hypersensitivity diseases: usage and implications of experimental models for risk assessment. Pharmacol Therap 111:374–383. http://www.isaaa.org/resources/publications/pocketk/6/default.asp
  54. Prescott VE, Campbell PM, Moore A, Mattes J, Rothenberg ME, Foster PS, Higgins TJV, Hogan SP (2005) Transgenic expression of bean alpha-amylase inhibitor in peas results in altered structure and immunogenicity. J Agric Food Chem 53:9023–9030Google Scholar
  55. Pusztai A (2001) Genetically modified foods: are they a risk to human/animal health? Action Bioscience. http://www.ask-force.org/web/Pusztai/Pusztai-GM-Foods-Risk-Human-Animal-Health-2001.pdf
  56. Pusztai A, Bardocz S, Ewen SWB (2003) Genetically modified foods: potential human health effects. In: D’Mello JPF (ed) Food safety: contaminants and toxins. CAB International, Wallingford, pp 347–372CrossRefGoogle Scholar
  57. Rahman M, Rashid H, Shahid AA, Bashir K, Husnain T, Riazuddin S (2007) Insect resistance and risk assessment studies of advanced generations of basmati rice expressing two genes of Bacillus thuringiensis. Electron J Biotechnol 10(2):241–251CrossRefGoogle Scholar
  58. Rahman M, Shaheen T, Ashraf M, Zafar Y (2012) Bridging genomic and classical breeding approaches for improving crop productivity. In: Ashraf M et al (eds) Crop production for agricultural improvement, vol 1. Springer, The Netherlands, pp 19–41Google Scholar
  59. Rahman M, Shaheen T, Irem S, Zafar Y (2015) Biosafety risk of genetically modified crops containing Cry genes. In: Lichtfouse E et al (eds) CO2 sequestration, biofuels and depollution. Environmental chemistry for a sustainable World 5. Springer, The Netherlands, pp 307–334Google Scholar
  60. Richards HA, Chung-Ting Han RG, Hopkins ML, Failla WW, Ward CN, Stewart CN Jr (2003) Safety assessment of recombinant green fluorescent protein orally administered to weaned rats nutrient interactions and toxicity. J Nutr 133:1909–1912Google Scholar
  61. Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens MM, Hartley SE, Hellmich RL, Huesing JE, Jepson PC, Layton R, Quemada H, Raybould A, Rose RI, Schiemann J, Sears MK, Shelton AM, Sweet J, Vaituzis Z, Wolt JD (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208CrossRefGoogle Scholar
  62. Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9:283–300CrossRefGoogle Scholar
  63. Saxena D, Flores S, Stotzky G (1999) Insecticidal toxin in root exudates from Bt corn. Nature 402:480Google Scholar
  64. Sayanova O, Smith MA, Lapinskas P, Stobart AK, Dobson G, Christie WW (1997) Expression of a borage desaturase cDNA containing an N-terminal cytochrome b5 domain results in the accumulation of high levels of delta6-desaturated fatty acids in transgenic tobacco. Proc Natl Acad Sci USA 94:4211–4216CrossRefGoogle Scholar
  65. Sims SR, Holden LR (1996) Insect bioassay for determining soil degradation of Bacillus thuringiensis subsp. kurstaki CryIA(b) protein in corn tissue. Environ Entomol 25:659–664CrossRefGoogle Scholar
  66. Singh NP, McCoy MT, Tice RR, Shneider EL (1988) A simple technique for quantification of low level of DNA damage in individual cells. Exp Cell Res 715:184–194CrossRefGoogle Scholar
  67. Singh AK, Mehta AK, Sridhara S, Gaur SN, Singh BP, Sarma PU, Arora N (2006) Allergenicity assessment of transgenic mustard (Brassica juncea) expressing bacterial cod A gene. Allergy 61:491–497CrossRefGoogle Scholar
  68. Stotzky G (2000) Persistence and biological activity in soil of insecticidal proteins from Bacillus thuringiensis and of bacterial DNA bound on clays and humic acids. J Environ Qual 29:691–705CrossRefGoogle Scholar
  69. Subedi KD, Ma BL (2007) Dry matter and nitrogen partitioning patterns in Bt and non-Bt near-isoline maize hybrids. Crop Sci 47:1186–1192CrossRefGoogle Scholar
  70. Subramanian A, Qaim M (2010) The impact of Bt cotton on poor households in rural India. J Dev Stud 46:295–311CrossRefGoogle Scholar
  71. Tabashnik BE (2010) Communal benefits of transgenic corn. Science 330:189–190CrossRefGoogle Scholar
  72. Tapp H, Stotzky G (1998) Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol Biochem 30:471–476CrossRefGoogle Scholar
  73. Taylor SL, Hefle SL (2002) Genetically engineered foods: implications for food allergy. Curr Opin Allergy Clin Immunol 2:249–252CrossRefGoogle Scholar
  74. Tice RR, Agurell E, Andeson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicity testing. Environ Mol Mutagen 35:206–221CrossRefGoogle Scholar
  75. Tryphonas H, Arvanitakis G, Vavasour E, Bondy G (2003) Animal models to detect allergenicity to foods and genetically modified products: workshop summary. Environ Health Perspect 11:221–222CrossRefGoogle Scholar
  76. Wu G, Cu HR, Shu Q, Xia YW, Xiang YB, Gao MW, Cheng X, Altosaar (2000) Stripped stem borer (Chilo suppressalis) resistant transgenic rice with a cry1Ab gene from Bt (Bacillus thuringiensis) and its rapid screening. J Zhejiang Univ 19:15–18Google Scholar
  77. Xu-Chongren MY, Chang S (2001) Research on biosafety of transgenic Bt cotton. College of life sciences. Beijing University, BeijingGoogle Scholar
  78. Yanni SF, Whaen JK, Ma BL (2011) Field-grown Bt and non-Bt corn: yield, chemical composition, and decomposition. Agron J 103:486–493CrossRefGoogle Scholar
  79. Yonemochi C, Fujisaki H, Harada C, Kusama T, Hanazumi M (2002) Evaluation of transgenic event CBH 351 (StarLink) corn in broiler chicks. Anim Sci J 73:221–228CrossRefGoogle Scholar
  80. Zaman M (2015). Efficacy and impact of GM (Bt) cotton in ecosystem. Ph.D. thesis, QA University, IslamabadGoogle Scholar
  81. Zaman M, Mirza MS, Irem S, Zafar Y, Rahman M (2015) A temporal expression of Cry1Ac protein in cotton plant and its impact on soil health. Int J Agric Biol 17:280–288Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • M. Rahman
    • 1
  • Muhammad Zaman
    • 1
  • Tayyaba Shaheen
    • 2
  • Samra Irem
    • 1
  • Yusuf Zafar
    • 1
  1. 1.Plant Genomics and Molecular Breeding LabNational Institute for Biotechnology and Genetic Engineering (NIBGE)FaisalabadPakistan
  2. 2.Department of Bioinformatics and BiotechnologyGovernment College UniversityFaisalabadPakistan

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