, Volume 18, Issue 2, pp 230–238 | Cite as

Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator

  • Mao Chen
  • Gong-yin Ye
  • Zhi-cheng Liu
  • Qi Fang
  • Cui Hu
  • Yu-fa Peng
  • Anthony M. Shelton


Lessons from organophosphorus pesticides, which could be bioaccumulated in non-target organisms at different trophic levels and caused unexpected negative impacts, necessitate a study of the possibility of biotransfer and bioaccumulation of Bacillus thuringiensis (Bt) insecticidal toxin(s) expressed in Bt plants. Using ELISA, we evaluated the transfer of Cry1Ab toxin in a food chain of Bt rice (KMD1 and KMD2), the target insect, Cnaphalocrocis medinalis, and its predator, Pirata subpiraticus. Cry1Ab was detected in C. medinalis and P. subpiraticus. However, the concentration of Cry1Ab detected from C. medinalis and P. subpiraticus did not increase as feeding or preying time increased. A binding study of Cry1Ab to the brush border membrane vesicle of C. medinalis and P. subpiraticus indicated that P. subpiraticus does not have binding receptors in its midgut to Cry1Ab, while C. medinalis does. Survivorship and fecundity of P. subpiraticus preying on Bt rice-fed C. medinalis were not significantly different from those preying on non-Bt rice-fed C. medinalis. Developmental time of P. subpiraticus was significantly longer when it preyed on Bt rice-fed C. medinalis than on non-Bt rice-fed prey. However, a 3-year field trial indicated that Bt rice did not significantly affect the density of P. subpiraticus.


Bt rice Non-target effect Bioaccumulation Tritrophic interactions Ecological risk assessment 



We thank Dr. I. Altosaar (University of Ottawa) for providing activated Cry1Ab toxin and Dr. D. B. Zhang (College of Agriculture and Biology, Shanghai Jiaotong University, China) for providing the monoclonal antibody of Cry1Ab. Financial supports from the National Program on Key Basic Research Projects (973 Program, 2007CB109202), the Ministry of Science and Technology of China, the National Natural Science Foundation of China (39970507) and the Special Foundation for the Winner of National Excellent Doctoral Dissertation, the Ministry of Education of China (199944) are gratefully acknowledged.


  1. Bernal JS, Griset JG, Gillogly PO (2002) Impacts of developing on Bt maize-intoxicated hosts on fitness parameters of a stem borer parasitoid. J Entomol Sci 37:27–40Google Scholar
  2. Carino FO, Kenmore PE, Dyck VA (1979) The Farmcop suction sampler for hoppers and predators in flooded rice fields. Int Rice Res Newsl 4:21–22Google Scholar
  3. Chen M, Ye GY, Lu XM, Hu C, Peng YF, Shu QY, Illimar A (2005) Biotransfer and bioaccumulation of Cry1Ab insecticidal protein in rice plant-brown planthopper-wolf spider food chain. Acta Entomol Sin 48:208–213Google Scholar
  4. Chen M, Zhao JZ, Ye GY, Fu Q, Shelton AM (2006) Impact of insect-resistant transgenic rice on target insect pests and non-target arthropods in China. Insect Sci 13:409–420. doi: 10.1111/j.1744-7917.2006.00110.x CrossRefGoogle Scholar
  5. Cheng X, Sardana R, Kaplan H, Altosaar I (1998) Agrobacterium-transformed rice plants expressing synthetic cry1A(b) and cry1A(c) genes are highly toxic to yellow stem borer and striped stem borer. Proc Natl Acad Sci USA 95:2767–2772. doi: 10.1073/pnas.95.6.2767 CrossRefGoogle Scholar
  6. Cohen M, Chen M, Bentur JS, Heong KL, Ye GY (2008) Bt rice in Asia: potential benefits, impact, and sustainability. In: Romeis J, Shelton AM, Kennedy G (eds) Integration of insect-resistant GM crops within IPM programs. Springer, Dordrecht, pp 223–248CrossRefGoogle Scholar
  7. D’Adamo R, Pelosi S, Trotta P, Sansone G (1997) Bioaccumulation and biomagnification of polycyclic aromatic hydrocarbons in aquatic organisms. Mar Chem 56:45–49. doi: 10.1016/S0304-4203(96)00042-4 CrossRefGoogle Scholar
  8. FAO (2007) FAOSTAT <> accessed September 1, 2007
  9. Ferry N, Edwards MG, Mulligan EA, Emami K, Petrova A, Frantescu M, Davison GM, Gatehouse AMR (2003) Engineering resistance to insect pests. In: Christou P, Klee H (eds) Handbook of plant biotechnology. Wiley, Chichester, pp 373–394Google Scholar
  10. Forcada C, Akcácer EM, Garcerá NDM, Tato A, Martínez R (1999) Resistance to Bacillus thruingiensis cry1Ac toxin in three strains of Heliothis virescens: proteolytic and SEM study of the larval midgut. Arch Insect Biochem Physiol 42:51–63. doi:10.1002/(SICI)1520-6327(199909)42:1<51::AID-ARCH6>3.0.CO;2-6CrossRefGoogle Scholar
  11. High SM, Cohen MB, Shu QY, Altosaar I (2004) Achieving successful deployment of Bt rice. Trends Plant Sci 9:286–292. doi: 10.1016/j.tplants.2004.04.002 CrossRefGoogle Scholar
  12. Huang JK, Hu RF, Rozelle S, Pray C (2005) Insect-resistant GM rice in farmers’ fields: assessing productivity and health effects in China. Science 308:688–690. doi: 10.1126/science.1108972 CrossRefGoogle Scholar
  13. James C (2007) Global status of commercialized biotech/GM crops: 2007. ISAAA briefs, no. 37, ISAAA: Ithaca, NYGoogle Scholar
  14. Liao CY, Trowell SC, Akhurst R (2005) Purification and characterization of Cry1Ac toxin binding proteins from the brush border membrane of Helicoverpa armigera midgut. Curr Microbiol 51:367–371. doi: 10.1007/s00284-005-0051-9 CrossRefGoogle Scholar
  15. Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316:1475–1477. doi: 10.1126/science.1139208 CrossRefGoogle Scholar
  16. Matteson PC (2000) Insect pest management in tropical Asian irrigated rice. Annu Rev Entomol 45:549–574. doi: 10.1146/annurev.ento.45.1.549 CrossRefGoogle Scholar
  17. McShaffrey D (1995) Leaders in environmental activism-trophic levels. pp 1–6. Accessed January 20, 2008
  18. Norusis M (2005) SPSS 13.0 advanced statistical procedure companion. Prentice Hall, Upper Saddle River, pp 103–122Google Scholar
  19. Obrist LB, Dutton A, Albajes R, Bigler F (2006) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:143–154. doi: 10.1111/j.0307-6946.2006.00762.x CrossRefGoogle Scholar
  20. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71. doi: 10.1038/nbt1180 CrossRefGoogle Scholar
  21. Romeis J, Bartsch D, Bigler F, Candolfi M, Gielkens MMC, Hartley SE et al (2008) Non-target arthropod risk assessment of insect-resistant GM crops. Nat Biotechnol 26:203–208. doi: 10.1038/nbt1381 CrossRefGoogle Scholar
  22. Serrano R, Hernández F, López FJ, Peña JB (1997a) Bioconcentration, depuration and chronic toxicity of the organophosphorus pesticide chlorpyrifos in the marine molluse Mytilus edulis. Arch Environ Contam Toxicol 33:47–52. doi: 10.1007/s002449900222 CrossRefGoogle Scholar
  23. Serrano R, Hernández F, López FJ, Peña JB (1997b) Study on bioconcentration of chlorpyrifos, chlorfenvinfos and methidathion in Mytilus galloprovincialis. Relationships with physicochemical properties and biotransformation. Bull Environ Contam Toxicol 59:968–975. doi: 10.1007/s001289900577 CrossRefGoogle Scholar
  24. Shelton AM, Zhao JZ, Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu Rev Entomol 47:845–881. doi: 10.1146/annurev.ento.47.091201.145309 CrossRefGoogle Scholar
  25. Sheng CF, Wang HT, Gao LD, Xuan JW (2003) The occurrence status, damage cost estimate and control strategies of stem borers in China. Plant Prot 29:37–39Google Scholar
  26. Shu QY, Ye GY, Cui HR, Xiang YB, Gao MW (1998) Development of transgenic Bacillus thuringiensis rice resistant to rice stem borers and leaf folders. J Zhejiang Agric Uni 24:579–580Google Scholar
  27. Wang YQ, Johnston S (2007) The status of GM rice R&D in China. Nat Biotechnol 25:717–718. doi: 10.1038/nbt0707-717 CrossRefGoogle Scholar
  28. Wolfersberger MG, Luethy P, Maurer A, Parenti P, Sacchi VF, Giordana B, Hanozet GM (1987) Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp Biochem Physiol 86A:301–308. doi: 10.1016/0300-9629(87)90334-3 CrossRefGoogle Scholar
  29. Xiang YB, Cheng X, Liang Z, Shu QY, Ye GY, Gao MW, Altosaar I (1999) Agrobacterium-mediated transformation of insecticidal Bacillus thuringiensis cry1Ab and cry1Ac genes and their expression in rice. Chin J Biotechnol 15:494–500Google Scholar
  30. Ye GY, Shu QY, Cui HR, Gao MW, Xia YW, Cheng XY, Altosaar I (2000) A leaf-section bioassay for evaluating rice stem borer resistance in transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner. Bull Entomol Res 90:179–182. doi: 10.1017/S0007485300000298 CrossRefGoogle Scholar
  31. Ye GY, Shu QY, Yao HW, Cui HR, Cheng XY, Hu C, Xia YW, Gao MW, Altosaar I (2001) Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. J Econ Entomol 94:270–276CrossRefGoogle Scholar
  32. Ye GY, Yao HW, Shu QY, Cheng XY, Hu C, Xia YW, Gao MW, Altosaar I (2003) High levels of stable resistance in transgenic rice with a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to rice leaffolder, Cnaphalocrocis medinalis (Guenée) under field conditions. Crop Prot 22:171–178. doi: 10.1016/S0261-2194(02)00142-4 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Mao Chen
    • 1
    • 2
  • Gong-yin Ye
    • 1
  • Zhi-cheng Liu
    • 3
  • Qi Fang
    • 1
  • Cui Hu
    • 1
  • Yu-fa Peng
    • 4
  • Anthony M. Shelton
    • 2
  1. 1.State Key Laboratory of Rice Biology, Institute of Insect SciencesZhejiang UniversityHangzhouChina
  2. 2.Department of EntomologyCornell University, New York State Agricultural Experiment StationGenevaUSA
  3. 3.College of Agriculture and BiologyShanghai Jiaotong UniversityShanghaiChina
  4. 4.State Key Laboratory for Biology of Plant Diseases and Insect pests, Institute of Plant ProtectionChinese Academy of Agricultural SciencesBeijingChina

Personalised recommendations