Potential subchronic food safety of the stacked trait transgenic maize GH5112E-117C in Sprague-Dawley rats

Abstract

The food safety of stacked trait genetically modified (GM) maize GH5112E-117C containing insect-resistance gene Cry1Ah and glyphosate-resistant gene G2-aroA was evaluated in comparison to non-GM Hi-II maize fed to Sprague-Dawley rats during a 90-day subchronic feeding study. Three different dietary concentrations (12.5, 25 and 50 %, w/w) of the GM maize were used or its corresponding non-GM maize. No biologically significant differences in the animals’ clinical signs, body weights, food consumption, hematology, clinical chemistry, organ weights and histopathology were found between the stacked trait GM maize groups, and the non-GM maize groups. The results of the 90-day subchronic feeding study demonstrated that the stacked trait GM maize GH5112E-117C is as safe as the conventional non-GM maize Hi-II.

This is a preview of subscription content, access via your institution.

Fig. 1

Abbreviations

USDA:

United States Department of Agriculture

GM:

Genetically modified

Bt:

Bacillus thuringiensis

SPF:

Specific pathogen free

GMOs:

Genetically modified organisms

OECD:

Organization for Economic Cooperation and Development

EU:

European Union

References

  1. Appenzeller LM, Malley L, Mackenzie SA, Hoban D, Delaney B (2009) Subchronic feeding study with genetically modified stacked trait lepidopteran and coleopteran resistant (DAS-O15O7-1xDAS-59122-7) maize grain in Sprague-Dawley rats. Food Chem Toxicol 47:1512–1520

    CAS  Article  PubMed  Google Scholar 

  2. Barros E, Lezar S, Anttonen MJ, van Dijk JP, Rohlig RM, Kok EJ, Engel KH (2010) Comparison of two GM maize varieties with a near-isogenic non-GM variety using transcriptomics, proteomics and metabolomics. Plant Biotechnol J 8:436–451

    CAS  Article  PubMed  Google Scholar 

  3. Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–425

    CAS  Article  PubMed  Google Scholar 

  4. Cao GY, Liu YJ, Zhang SX, Yang XW, Chen RR, Zhang YW, Liu Y, Wang JH, Lin M, Wang GY (2012) A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. PLoS One 7(6):1–11

    Google Scholar 

  5. Chinese Standard 14924.3-2001 (2001) Mixed feed of experimental animals mice and rats. Standards Press of China, Beijing

    Google Scholar 

  6. Chinese Standard GB/T5009.3-2003 (2003) Inspection of grain and oilseeds: methods for determination of moisture. Standards Press of China, Beijing

    Google Scholar 

  7. Chinese Standard GB/T5009.4-2003 (2003) Inspection of grain and oilseeds: methods for determination of ash. Standards Press of China, Beijing

    Google Scholar 

  8. Chinese Standard GB/T5009.5-2003 (2003) Inspection of grain and oilseeds: methods for determination of crude protein. Standards Press of China, Beijing

    Google Scholar 

  9. Chinese Standard GB/T5009.6-2003 (2003) Inspection of grain and oilseeds: methods for determination of crude fat. Standards Press of China, Beijing

    Google Scholar 

  10. Chinese Standard GB/T5009.10-2003 (2003) Inspection of grain and oilseeds: methods for determination of crude fiber. Standards Press of China, Beijing

    Google Scholar 

  11. Chinese Standard GB/T5009.87-2003 (2003) Inspection of grain and oilseeds: methods for determination of phosphorus in foods. Standards Press of China, Beijing

    Google Scholar 

  12. Chinese Standard GB/T5009.92-2003 (2003) Inspection of grain and oilseeds: methods for determination of calcium in foods. Standards Press of China, Beijing

    Google Scholar 

  13. Coll A, Nadal A, Rossignol M, Puigdomenech P, Pla M (2011) Proteomic analysis of MON810 and comparable non-GM maize varieties grown in agricultural fields. Transgenic Res 20:939–949

    CAS  Article  PubMed  Google Scholar 

  14. 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 18:101–109

    Article  Google Scholar 

  15. Dun BQ, Wang XJ, Lu W, Chen M, Zhang W, Ping SZ, Wang ZX, Zhang BM, Lin M (2014) Development of highly glyphosate-tolerant tobacco by coexpression of glyphosate acetyltransferase gat and EPSPS G2-aroA genes. Crop J 2:164–169

    Article  Google Scholar 

  16. Green JM (2009) Evolution of glyphosate-resistant crop technology. Weed Sci 57:108–117

    CAS  Article  Google Scholar 

  17. Green JM (2012) The benefits of herbicide-resistant crops. Pest Manag Sci 68:1323–1331

    CAS  Article  PubMed  Google Scholar 

  18. James C (2010) Global status of commercialized biotech/GM crops: 2010. International Service for the Acquisition of Agri-biotech Applications (ISAAA), Ithaca

    Google Scholar 

  19. Kawahigashi H, Hirose S, Ohkawa H, Ohkawa Y (2007) Herbicide resistance of transgenic rice plants expressing human CYP1A1. Biotechnol Adv 25:75–84

    CAS  Article  PubMed  Google Scholar 

  20. Li XY, Li SY, Lang ZH, Zhang J, Zhu L, Huang DF (2013) Chloroplast-targeted expression of the codon-optimized truncated cry1Ah gene in transgenic tobacco confers a high level of protection against insects. Plant Cell Rep 32:1299–1308

    Article  PubMed  Google Scholar 

  21. Li XY, Lang ZH, Zhang J, He KL, Zhu L, Huang DF (2014) Acquisition of insect-resistant transgenic maize harboring a truncated cry1Ah gene via agrobacterium-mediated transformation. J Integr Agric 13:937–944

    CAS  Article  Google Scholar 

  22. McComas KA, Besley JC, Steinhardt J (2014) Factors influencing U.S. consumer support for genetic modification to prevent crop disease. Appetite 78:8–14

    Article  PubMed  Google Scholar 

  23. NY/T1102-2006 (2006) Safety assessment of genetically modified plant and derived products 90-day feeding test in rats. Standards Press of China, Beijing

    Google Scholar 

  24. OECD (1998) Repeated dose 90-day oral toxicity study in rodents. OECD Guideline for the Testing of Chemicals. Guideline 408. Organization for Economic Cooperation and Development (OECD), Paris

  25. Paul L, Angevin F, Collonnier C, Messean A (2012) Impact of gene stacking on gene flow: the case of maize. Transgenic Res 21:243–256

    CAS  Article  PubMed  Google Scholar 

  26. Qaim M (2009) The economics of genetically modified crops. Annu Rev Resour Econ 1:665–694

    Article  Google Scholar 

  27. Qi XZ, He XY, Luo YB, Li SY, Zou SY, Cao SS, Tang MZ, Delaney B, Xu WT, Huang KL (2012) Subchronic feeding study of stacked trait genetically-modified soybean (3O5423 × 40-3-2) in Sprague-Dawley rats. Food Chem Toxicol 50:3256–3263

    CAS  Article  PubMed  Google Scholar 

  28. Shin KS, Suh SC, Lim MH, Woo HJ, Lee JH, Kim HY, Cho HS (2013) Event-specific detection system of stacked genetically modified maize by using the multiplex-PCR technique. Food Sci Biotechnol 22:1763–1772

    CAS  Article  Google Scholar 

  29. Song Y, Liang CL, Wang W, Fang J, Sun NN, Jia XD, Li N (2014) Immunotoxicological evaluation of corn genetically modified with Bacillus thuringiensis Cry1Ah Gene by a 30-day feeding study in BALB/c Mice. PLoS One 9(2):1–11

    Google Scholar 

  30. Xue J, Liang GM, Crickmore N, Li HT, He KL, Song FP, Feng X, Huang DF, Zhang J (2008) Cloning and characterization of a novel Cry1A toxin from Bacillus thuringiensis with high toxicity to the Asian corn borer and other lepidopteran insects. FEMS Microbiol Lett 280:95–101

    CAS  Article  PubMed  Google Scholar 

  31. Zhu YX, He XY, Luo YB, Zou SY, Zhou X, Huang KL, Xu WT (2013) A 90-day feeding study of glyphosate-tolerant maize with the G2-aroA gene in Sprague-Dawley rats. Food Chem Toxicol 51:280–287

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Genetically Modified Organisms Breeding Major Projects of PR China Grant 2014ZX0801103B. The authors also give the best appreciation to the Beijing Origin Seed Technology Inc. (Beijing, China) for providing the GM maize GH5112E-117C and the near-isogenic non-GM maize Hi-II.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Xiaohong Mei.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Han, S., Zou, S., He, X. et al. Potential subchronic food safety of the stacked trait transgenic maize GH5112E-117C in Sprague-Dawley rats. Transgenic Res 25, 453–463 (2016). https://doi.org/10.1007/s11248-016-9944-6

Download citation

Keywords

  • Genetically modified maize
  • Cry1Ah
  • G2-aroA
  • Safety assessment