Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens

Abstract

In this study, the non-target effects of Bt rice “KMD2” expressing a Cry1Ab protein on the performance of the brown planthopper (BPH), Nilaparvata lugens, over multiple generations were evaluated under laboratory and field conditions. In the laboratory, BPH was reared to observe the impact of the Bt rice as compared to its parental non-Bt cultivar Xiushui 11, while the population dynamics and oviposition performance of BPH were investigated in the field. The survival of BPH nymphs fed Bt and non-Bt rice did not differ significantly. The nymph developmental duration of BPH was significantly delayed by the Bt rice by comparison with the non-Bt rice for the 1st and 2nd but not the 4th generation. Most importantly, the fecundity of BPH on the Bt rice was significantly decreased in every generation when compared with the non-Bt rice. In the field investigations, the population density of BPH nymphs was significantly lower in the Bt rice field. However, the temporal pattern of population dynamics of BPH adults was similar between the Bt and non-Bt rice, presumably due to migratory interference of the adults. In the Bt rice field, the percentage of tillers with eggs and the number of eggs per tiller were also significantly lower from tillering to mature stage. Additionally, Cry1Ab protein could not be detected in guts from single BPH adults. In general, our results suggest that the Bt rice “KMD2” could not stimulate an outbreak of BPH.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Akhtar ZR, Tian JC, Chen Y, Fang Q, Hu C, Chen M, Peng YF, Ye GY (2010) Impacts of six Bt rice lines on nontarget rice feeding thrips under laboratory and field conditions. Environ Entomol 39(2):715–726

  2. Bae SH, Pathak MD (1970) Life history of Nilaparvata lugens (Homoptera: Delphacidae) and susceptibility of rice varieties to its attacks. Ann Entomol Soc Am 63(1):149–155

  3. Bai YY, Jiang MX, Cheng JA, Wang D (2006) Effects of CrylAb toxin on Propylea japonica (Thunberg) (Coleoptera: Coccinellidae) through its prey, Nilaparvata lugens Stål (Homoptera: Delphacidae), feeding on transgenic Bt rice. Environ Entomol 35(4):1130–1136

  4. Bashir K, Husnain T, Fatima T, Latif Z, Mehdi SA, Riazuddin S (2004) Field evaluation and risk assessment of transgenic indica basmati rice. Mol Breed 13(4):301–312

  5. Bernal CC, Aguda RM, Cohen MB (2002) Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol Exp Appl 102(1):21–28

  6. Breitler JC, Vassal JM, Catala MD, Meynard D, Marfa V, Mele E, Royer M, Murillo I, San Segundo B, Guiderdoni E, Messeguer J (2004) Bt rice harbouring cry genes controlled by a constitutive or wound-inducible promoter: protection and transgene expression under Mediterranean field conditions. Plant Biotechnol J 2(5):417–430

  7. Chatterjee PB (1978) Occurrence of brown planthopper on rice in West Bengal, India. Int Rice Res Newsletter 3(2):12

  8. Chen M, Ye GY, Hu C, Datta SK (2003a) Effects of transgenic Bt indica rice on the feeding and oviposition behavior of the brown planthopper, Nilaparvata lugens. Acta Phytophyl Sin 30(4):365–370

  9. Chen M, Ye GY, Hu C, Tu J, Datta SK (2003b) Effect of transgenic Bt rice on dispersal of planthoppers and leafhoppers as well as their egg parasitic wasp. J Zhejiang Univ (Agric Life Sci) 29(1):29–33

  10. Chen M, Ye GY, Yao HW, Hu C, Shu QR (2004) Evaluation of the impact of insect-resistant transgenic rice on the feeding and oviposition behavior of its non-target insect, the brown planthopper, Nilaparvata lugens (Homptera: Delphacidae). Sci Agric Sinica 37(2):222–226

  11. Chen M, Ye GY, Lu XM, Hu C, Peng YF, Shu QR, Altosaar I (2005) Biotransfer and bioaccumulation of Cry1Ab insecticidal protein in rice plant—brown planthopper—wolf spider food chain. Acta Entomol Sin 48(2):208–213

  12. Chen M, Ye GY, Liu ZC, Yao HW, Chen XX, Shen SZ, 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):127–134

  13. Chen M, Liu ZC, Ye GY, Shen ZC, Hu C, Peng YF, Altosaar I, Shelton AM (2007) Impacts of transgenic cry1Ab rice on non-target planthoppers and their main predator Cyrtorhinus lividipennis (Hemiptera: Miridae)—A case study of the compatibility of Bt rice with biological control. Biol Control 42(2):242–250

  14. Chen H, Mang G, Zhang QF, Lin YJ (2008) Effect of transgenic Bacillus thuringiensis rice lines on mortality and feeding behavior of rice stem borers (Lepidoptera: Crambidae). J Econ Entomol 101(1):182–189

  15. Cheng XY, Sardana R, Kaplan H, Altosaar I (1998) Agrobacterium-transformed rice plants expressing synthetic cryIA(b) and cryIA(c) genes are highly toxic to striped stem borer and yellow stem borer. Proc Natl Acad Sci USA 95(6):2767–2772

  16. Cheng XN, Wu JC, Ma F (2003) Brown planthopper: occurrence and control. China Agricultural Press, Beijing

  17. Cohen MB, Chen M, Bentur JS, Heong KL, Ye GY (2008) Bt rice in Asia: potential benefits, impact, and sustainability. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM systems. Springer, New York, pp 223–248

  18. Eizaguirre M, Albajes R, Lopez C, Eras J, Lumbierres B, Pons X (2006) Six years after the commercial introduction of Bt maize in Spain: field evaluation, impact and future prospects. Transgenic Res 15(1):1–12

  19. Faria CA, Wackers FL, Pritchard J, Barrett DA, Turlings TCJ (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of Lepidopteran pests. PLoS ONE 2(7):e600

  20. Fu Q, Wang F, Li DH, Yao Q, Lai FX, Zhang ZT (2003) Efects of insect-resistant transgenic rice lines MSA and MSB on non-target pests Nilaparvata lugens and Sogatella furcifera. Acta Entomol Sin 46(6):697–704

  21. Heinrichs EA, Medrano FG, Rapuas HR (eds) (1985) Genetic evaluation for insect resistance in rice. International rice research institute, Los Baños, Philippines

  22. Jiao Z, Si XX, Li GK, Zhang ZM, Xu XP (2010) Unintended compositional changes in transgenic rice seeds (Oryza sativa L.) studied by spectral and chromatographic analysis coupled with chemometrics methods. J Agr Food Chem 58 (3):1746–1754

  23. Joost PH, Riley DG (2004) Sampling techniques for thrips (Thysanoptera: Thripidae) in preflowering tomato. J Econ Entomol 97(4):1450–1454

  24. Kanaoka A, Yamaguchi R, Konno T (1996) Effect of buprofezin on oviposition of brown planthopper, Nilaparvata lugens, at sub-lethal dose. J Pesticide Sci 21(2):153–157

  25. Keymanesh K, Darvishi MH, Sardari S (2009) Metabolome comparison of transgenic and non-transgenic rice by statistical analysis of FTIR and NMR spectra. Rice Sci 16:119–123

  26. Lawo NC, Romeis J (2008) Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea. Biol Control 44(3):389–398

  27. Li FF, Ye GY, Wu Q, Peng YF, Chen XX (2007) Arthropod abundance and diversity in Bt and non-Bt rice fields. Environ Entomol 36(3):646–654

  28. Liu YF, He L, Wang Q, Hu SQ, Liu WH, Chen KG (2007) Effects of and ecological safety insect-resistant Cry1Ac/sck transgenic rice on key non-target pests in paddy fields. Sci Agric Sin 40(6):1181–1189

  29. Lu YH, Wu KM, Jiang YY, Xia B, Li P, Feng HQ, Wyckhuys KAG, Guo YY (2010) Mirid bug outbreaks in multiple crops correlated with fiide-scale adoption of Bt Cotton in China. Science 328(5982):1151–1154

  30. Ministry of Agriculture of the People’s Republic of China (MAPRC) (2009) The second list of approval agricultural genetically modified organisms’ safety certificates in 2009. http://www.stee.agri.gov.cn/biosafety/spxx/P020091127591594596689.pdf

  31. Minkenberg OPJM, Tatar M, Rosenheim JA (1992) Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65(1):134–142

  32. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutr Nat Res 4(11):23. http://www.cababstractsplus.org/cabreviews

  33. Riaz N, Husnain T, Fatima T, Makhdoom R, Bashir K, Masson L, Altosaar I, Riazuddin S (2006) Development of Indica Basmati rice harboring two insecticidal genes for sustainable resistance against lepidopteran insects. S Afr J Bot 72(2):217–223

  34. Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens MMC, 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(2):203–208

  35. SAS institute (2001) PROC user’s manual, 6th edn. SAS Institute, Cary, NC

  36. Sogawa K (1982) The rice brown planthopper—feeding physiology and host plant interactions. Annu Rev Entomol 27:49–73

  37. Sogawa K, Zhang H, Yang XJ, Liu GJ (2003) Whitebacked planthopper resistance in China rice varieties. Chin J Rice Sci 17(17):47–52

  38. Tan H, Ye GY, Shen ZC, Peng YF, Hu C (2006) Effects of transgenic indica rice expressing a gene of cry1Ab with insect resistance on the development and reproduction of nontarget pest, Sogatella furcifera (Homoptera: Delphacidae). Acta Phytophyl Sin 33:251–256

  39. Wada T, Ito K, Takahashi A, Tang J (2007) Variation of pre-ovipositional period in the brown planthopper, Nilaparvata lugens, collected in tropical, subtropical and temperate Asia. J Appl Entomol 131(9–10):698–703

  40. Wang YM, Zhang GA, Du JP, Wang MC, Liu BA (2010) Influence of transgenic hybrid rice expressing a fused gene derived from cry1Ab and cry1Ac on primary insect pests and rice yield. Crop Prot 29(2):128–133

  41. Ye XD, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287(5451):303–305

  42. 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(1):271–276

  43. Ye GY, Yao HW, Shu QY, Cheng X, Hu C, Xia YW, Gao MW, Altosaar I (2003) High levels of stable resistance in transgenic rice with a cry1Ab gene from Bacillus thuringiensis Berliner to rice leaffolder, Cnaphalocrocis medinalis (Guenée) under field conditions. Crop Prot 22(1):171–178

  44. Ye RJ, Huang HQ, Yang Z, Chen TY, Liu L, Li XH, Chen H, Lin YJ (2009) Development of insect-resistant transgenic rice with Cry1C*-free endosperm. Pest Manag Sci 65(9):1015–1020

  45. Zaidi MA, Ye GY, Yao HW, You TH, Loit E, Dean DH, Riazuddin S, Altosaar I (2009) Transgenic rice plants expressing a modified cry1Ca1 gene are resistant to Spodoptera litura and Chilo suppressalis. Mol Biotechnol 43(3):232–242

  46. Zhou X, Cheng JA, Hu Y, Lou YG (2005) Effect s of transgenic Bt Rice on the population development of Nephotettix cincticeps. Chin J Rice Sci 19(1):74–78

Download references

Acknowledgments

We greatly thank Prof. I. Altosaar (University of Ottawa, Canada) for providing a synthetic cry1Ab gene for developing the Bt rice line “KMD2”. We greatly appreciated Dr. J. Romeis (Agroscope Reckenholz-Tänikon Research Station ART, Switzerland) for critically revising the manuscript and for valuable comments. Financial support from the National Program on Key Basic Research Projects (973 Program, 2007CB109202), the Ministry of Science and Technology of China, and the National Natural Science Foundation of China (30671377), as well as the Special Research Projects for Developing Transgenic Plants (2008ZX08011-01), are gratefully acknowledged.

Author information

Correspondence to Gong-Yin Ye.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chen, Y., Tian, J., Wang, W. et al. Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens . Transgenic Res 21, 279–291 (2012). https://doi.org/10.1007/s11248-011-9530-x

Download citation

Keywords

  • Bt rice
  • Cry1Ab protein
  • Nilaparvata lugens
  • Safety assessment
  • Non-target effect