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The transfer of Bt insecticidal protein to higher tropic levels via a transgenic cotton, then beet armyworm (Lepidoptera: Noctuidae) and their natural enemies

Published online by Cambridge University Press:  10 October 2013

Chun-Xia Chen
Affiliation:
School of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
Erzhong Wu
Affiliation:
School of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
Yi-Zhong Yang*
Affiliation:
School of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
Hong-Hua Su
Affiliation:
School of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
*
1Corresponding author (e-mail: yzyang@yzu.edu.cn).

Abstract

In order to determine the transference of Bacillus thuringiensis Berliner (Bacillaceae) (Bt) insecticidal protein in the food chain, enzyme-linked immunosorbent assay was used to detect Bt insecticidal protein levels in transgenic Bt cotton (GK12, New variety 33B and SGK321), Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) fed on the Bt cotton varieties, and two natural enemies of S. exigua, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Microplitis pallidipes Szépligeti (Hymenoptera: Braconidae). The results showed that Bt insecticidal protein was found not only in cotton leaves, but also in the body and excrement of S. exigua and the bodies of both C. carnea and M. pallidipes. Bt toxin was detected in S. exigua larvae of all the examined instars (second, third, fourth, and fifth) that fed on transgenic cotton varieties and the Bt toxin level was the highest in the body of the second instar. In addition, the Bt toxin content in the excrement of the second instar was lower than that in the older ones. After the natural enemies C. carnea and M. pallidipes preyed/parasitised the S. exigua larvae that fed on transgenic cotton, Bt toxin was found in both the predator and parasite. This research indicates that Bt protein can be transferred through the food chain and to natural enemies of various predatory habits.

Résumé

Afin de déterminer la possibilité de transfert de la protéine insecticide de Bacillus thuringiensis Berliner (Bacillaceae) (Bt) dans la chaîne alimentaire, nous avons utilisé des dosages d'immunosorption liée à enzyme (ELISA) pour mesurer les concentrations de la protéine insecticide Bt dans du coton transgénique Bt (GK12, NuCTN 33B et SGK321), dans des Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) nourris de ces variétés de coton-Bt et dans deux ennemis naturels de S. exigua, soit Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) et Microplitis pallidipes Szépligeti (Hymenoptera: Braconidae). Nous avons trouvé la protéine insecticide Bt non seulement dans les feuilles de coton, mais aussi dans le corps et les excréments de S. exigua, ainsi que dans les corps de C. carnea et de M. pallidipes. La toxine Bt peut être décelée chez les larves de S. exigua de tous les stades examinés (2e, 3e, 4e et 5e) nourries des variétés de coton transgénique et la concentration de toxine Bt est maximale dans le corps des larves de 2e stade. De plus, le contenu en toxine Bt des excréments des larves de 2e stade est inférieur à celui des larves plus âgées. Après que les ennemis naturels C. carnea et M. pallidipes se soient nourris de larves de S. exigua alimentées de coton transgénique ou les aient parasitées, la toxine Bt se retrouve tant chez le prédateur que chez le parasite. Notre travail indique que la protéine Bt peut être transmise à travers la chaîne alimentaire et passer aux ennemis naturels présentant divers comportements prédateurs.

Type
Physiology, Biochemistry, Development and Genetics
Copyright
Copyright © Entomological Society of Canada 2013 

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Footnotes

Subject editor: Kevin Floate

References

Álvarez-Alfageme, F., Ferry, N., Castañera, P., Ortego, F., Gatehouse, A.M.R. 2008. Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Research, 17: 943954.CrossRefGoogle ScholarPubMed
Chen, M., Ye, G.Y., Liu, Z.C., Fang, Q., Hu, C., Peng, Y.E., et al. 2009. Analysis of Cry1Ab toxin accumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology, 18: 230238.Google Scholar
Chen, M., Ye, G.Y., Lu, X.M., Hu, C., Peng, Y.F., Su, Q.Y., et al. 2005. Transfer and accumulation of Cry1Ab insecticidal protein in rice plant-brown planthopper-wolf spider food chain. Acta Entomologica Sinica, 48: 208213.Google Scholar
Chen, M., Zhao, J.Z., Collins, H.L., Earle, E.D., Cao, J., Shelton, A.M. 2008. A critical assessment of the effects of Bt transgenic plants on parasitoids. PLoS One, 3: e2284. doi:10.1371/journal.pone.0002284. Google Scholar
Chen, Y. 2007. The transmission and location of Cry1A protein in the food chain from transgenic cotton to resistant Helicoverpa armigera and its natural enemy Microplitis mediator Haliday. Chinese Academy of Agriculture Sciences, Beijing, China, Master's degree dissertation. 245–269.Google Scholar
Dutton, A., Klein, H., Romeis, J., Bigler, F. 2002. Uptake of Bt toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea . Ecological Entomology, 27: 441447.CrossRefGoogle Scholar
Ferry, N., Mulligan, E.A., Majerus, M.E.N., Gatehouse, A.M.R. 2007. Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target, beetles. Transgenic Research, 16: 795812.Google Scholar
Ferry, N., Mulligan, E.A., Majerus, M.E.N., Stewart, C.N., Tabashnik, B.E., Port, G.R., et al. 2006. Prey-mediated effects of transgenic canola on a beneficial, non-target, carabid beetle. Transgenic Research, 15: 501514.CrossRefGoogle ScholarPubMed
Harwood, J.D., Wallin, W.G., Obrycki, J.J. 2005. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agro-ecosystem. Molecular Ecology, 14: 28152823.Google Scholar
Jiang, Y.H., Fu, Q., Cheng, J.A., Zhu, Z.R., Jiang, M.X., Ye, G.Y., et al. 2004. Dynamics of Cry1Ab protein from transgenic Bt rice in herbivores and their predators. Acta Entomologica Sinica, 47: 124129.Google Scholar
Li, F.F., Ye, G.Y., Wu, Q., Peng, Y.F., Chen, X.X. 2007. Arthropod abundance and diversity in Bt and non-Bt rice fields. Environmental Entomology, 36: 646654.Google Scholar
Li, S., Li, T., Yang, C., He, J., Yang, H., Wang, X. 2001. The artificial diet and the mass rearing method of Spodoptera exigua . Chinese Bulletin Entomology, 38: 383386.Google Scholar
Liu, Y.Q. Jiang, X.F. 2002. The biological control of Spodoptera exigua (Hb.). Plant Protection, 28: 5456.Google Scholar
Qu, Z.G., Wang, J.Y., Zhu, L.Y. 2005. Effects of parasitism by Microplitis tuberculifer on food consumption and development of Spodoptera exigua larvae. Acta Agriculturae Boreali Sinica, 20: 9396.Google Scholar
Shi, X.L., Yang, Y.Z., Cai, J.H., Zhang, X.L., Shi, M.J. 2009. Bt toxic protein expression in insect-resistant transgenic corns and its transfer to and accumulation in Ostrinia furnacalis . Chinese Applied Ecology, 20: 27732777.Google ScholarPubMed
Steel, R.G.D. Torrie, J.H. 1980. Principles and procedure of statistics. McGraw-Hill, New York, United States of America.Google Scholar
Tang, Q. Feng, M. 2002. DPS data processing system for practical statistics. Science Press, Beijing, China.Google Scholar
Tian, J.C., Liu, Z.C., Yao, H.W., Ye, G.Y., Peng, Y.F. 2008. Impact of transgenic rice with a cry1Ab gene on parasitoid sub-community structure and the dominant population dynamics of parasitoid wasps in rice paddy. Environmental Entomology, 30: 17.Google Scholar
Torres, J.B. Ruberson, J.R. 2006. Interactions of Bt-cotton and the omnivorous big-eyed bug Geocoris punctipes (Say), a key predator in cotton fields. Biological Control, 39: 4757.Google Scholar
Torres, J.B. Ruberson, J.R. 2008. Interactions of Bacillus thuringiensis CrylAc toxin in genetically engineered cotton with predatory heteropterans. Transgenic Research, 17: 345354.Google Scholar
Vojtech, E., Meissle, M., Poppy, G.M. 2005. Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesta marginiventris (Hymenoptera: Braconidae). Transgenic Research, 14: 133144.Google Scholar
Xia, J.Y., Cui, J.J., Chang, R.Q. 2000. A resistance research of transgenic cotton varieties to Spodoptera exigua . China Cotton, 27: 1011.Google Scholar
Zhang, G.F., Wan, F.H., Guo, J.Y., Hou, M.L. 2004. Expression of Bt toxin in transgenic Bt cotton and its transmission through pests Helicoverpa armigera and Aphis gossypii to natural enemy Propylaea japonica in cotton plots. Acta Entomologica Sinica, 47: 334341.Google Scholar
Zhang, G.F., Wan, F.H., Liu, W.X. 2006. Early instar response to plant-delivered Bt-toxin in a herbivore (Spodoptera litura) and a predator (Propylaea japonica). Crop Protection, 25: 527533.Google Scholar
Zhang, X.L., Chen, P., Chen, C.F., Yang, Y.Z. 2007. Effect of the transgenic Bt cotton on laboratory population increasing of the beet armyworm Spodoptera exigua Hübner. Acta Phytophylacica Sinica, 34: 391395.Google Scholar
Zhang, X.S., Li, S.G., Xu, C.R., Zhao, J.Z., Zhao, K.J. 2000. Bacillus thuringiensis insecticidal protein levels in different tissue and growing period of transgenic cotton determination using ELISA. Acta Scientiarum Naturalium Universitatis Pekinensis, 36: 478484.Google Scholar
Zhou, W.R., Liu, Z.L., Chen, W., Qiu, S.B. 1980. Use of powdered feed for raising Chinese green lacewing imagines. Plant Protection, 16: 23.Google Scholar