Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-24T04:57:19.677Z Has data issue: false hasContentIssue false

Bt-toxin uptake by the non-target herbivore, Myzus persicae (Hemiptera: Aphididae), feeding on transgenic oilseed rape in laboratory conditions

Published online by Cambridge University Press:  01 November 2010

G. Burgio*
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-entomologia, Alma Mater Studiorum Università di Bologna, viale Fanin, 42, Bologna, Italy
G. Dinelli
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-agronomia, Alma Mater Studiorum Università di Bologna, viale Fanin, 44, Bologna, Italy
I. Marotti
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-agronomia, Alma Mater Studiorum Università di Bologna, viale Fanin, 44, Bologna, Italy
M. Zurla
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-entomologia, Alma Mater Studiorum Università di Bologna, viale Fanin, 42, Bologna, Italy
S. Bosi
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-agronomia, Alma Mater Studiorum Università di Bologna, viale Fanin, 44, Bologna, Italy
A. Lanzoni
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali-entomologia, Alma Mater Studiorum Università di Bologna, viale Fanin, 42, Bologna, Italy
*
*Author for correspondence Fax: +39 051 2096281 E-mail: [email protected]

Abstract

The potential non-target effects of genetically modified crops are some of the more debated topics within applied biotechnologies in agriculture and environmental risk assessment. The objective of the present research was to study the potential Bt-toxin uptake by the non-target herbivore Myzus persicae Sulzer (Hemiptera: Aphididae) feeding on transgenic oilseed rape plants (Brassica napus cv. ‘Westar’ lines GT 2–4) expressing the Cry1Ac endotoxin. A specific aim was to replicate our previous experiment in controlled laboratory conditions to avoid or minimize the risk of contamination leading to potential false positive results. The toxin levels in vernalized (V) and not-vernalized (not-V) transgenic oilseed rape plants was also monitored to better clarify the role of physiological processes on Bt-toxin expression. Cry1Ac expression in not-V plants (mean concentration±SE=167.8±5.7 μg kg−1 FW) showed a pattern of large variability, in comparison with V plants whose expression (mean concentration±SE=227.7±1.9 μg kg−1 FW) was significantly more stable. Cry1Ac toxin was detected in three aphid samples reared on V plants with a mean toxin concentration±SE of 4.8±0.6 μg Kg−1 FW and in three out of six samples of aphids reared on not-V plants (mean toxin concentration±SE=7.1±1.2 μg kg−1 FW). The mean Bt-toxin concentration of all the positive aphid samples was 5.9±1.0 μg kg−1 FW. Our results confirmed the findings of our previous experiment and highlighted the potential for Cry1Ac toxin uptake by aphids feeding on transgenic oilseed rape plants.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andow, D.A., Löwei, G.L. & Arpaia, S. (2006) Ecological risk assessments for Bt crops. Nature Biotechnology 24, 749751.CrossRefGoogle ScholarPubMed
Arpaia, S. (2004) Workshop report – Monitoring/bioindicators. IOBC wprs Bulletin 27(3), 205208.Google Scholar
Burgio, G., Lanzoni, A., Accinelli, G., Dinelli, G., Bonetti, A., Marotti, I. & Ramilli, F. (2007) Evaluation of Bt-toxin uptake by the non-target herbivore, Myzus persicae (Hemiptera: Aphididae), feeding on transgenic oilseed rape. Bullettin of Entomoogical Research 97, 211215.CrossRefGoogle ScholarPubMed
Carozzi, N.B. & Koziel, M.G. (1997) Advances in Insect Control: The Role of Transgenic Plants. London, UK, Taylor & Francis.Google Scholar
Dong, H.Z. & Li, W.J. (2007) Variability of endotoxin expression in Bt transgenic cotton. Journal of Agronomy and Crop Science 193, 2129.CrossRefGoogle 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. Ecogical. Entomology 27, 441447.CrossRefGoogle Scholar
Fischhoff, D.A. (1996) Insect-resistant crops plants. pp. 214227 in Persley, G.J. (Ed) Biotechnology and Integrated Pest Management. Cambridge, UK, CAB Iinternational.Google Scholar
Groot, A.T. & Dicke, M. (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant Journal 31, 387406.CrossRefGoogle Scholar
Harper, B.K., Mabon, S.A., Leffel, S.M., Halfhill, M.D., Richards, H.A., Moyer, K.A. & Stewart, C.N. Jr (1999) Green fluorescent protein as a marker for expression of a second gene in transgenic plants. Nature Biotechnology 17, 11251129.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 agroecosystem. Molecular Ecology 14, 28152823.Google Scholar
Harwood, J.D., Samson, R.A. & Obrycki, J.J. (2007) Temporal detection of Cry1Ab-endotoxins in coccinellid predators from fields of Bacillus thuringiensis corn. Bulletin of Entomological Research 97, 643648.CrossRefGoogle ScholarPubMed
Head, G., Brown, C.R., Groth, M.E. & Duan, I.J. (2001) Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomologia Experimentalis et Applicata 99, 3745.CrossRefGoogle Scholar
Hilbeck, A., Jänsch, S., Meier, M. & Römbke, J. (2008) Analysis and validation of present ecotoxicological test methods and strategies for the risk assessment of genetically modified plants. Bonn, Germany, Bfn-Federal Agency for Nature Conservation. Available online at http://www.bfn.de/fileadmin/MDB/documents/service/skript236.pdf.Google Scholar
Hodek, I. & Honek, A. (1996) Ecology of Coccinellidae. Dordrecht, The Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Lancashire, P.D., Bleiholder, H., Van dem Boom, T., Langeluddecke, P., Staugs, R., Weer, E. & Witzenber, A. (1991) A uniform decimal code for growth stages of crops and weeds. Annals of Applied Biology 119, 561601.CrossRefGoogle Scholar
Lanzoni, A., Accinelli, G., Bazzocchi, G.G. & Burgio, G. (2004) Biological traits and life table of the exotic Harmonia axyridis compared to Hippodamia variegata, and Adalia bipunctata (Col.: Coccinellidae). Journal of Applied Entomology 128(4), 298306.CrossRefGoogle Scholar
Lawo, N.C., Wäckers, F.L. & Romeis, J. (2009) Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS ONE 4(3), e4804 (doi:10.1371/journal.pone.0004804).CrossRefGoogle Scholar
Lövei, G.L. & Arpaia, S. (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomologia Experimentalis et Applicata 114, 114.CrossRefGoogle Scholar
Lövei, G.L., Andow, D.A. & Arpaia, S. (2009) Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies. Environmental Entomology 38(2), 293306.Google Scholar
Lozzia, G.C., Furlanis, C., Manachini, B. & Rigamonti, I.E. (1998) Effects of Bt corn on Rhopalosiphum paid L. (Rhynchota: Aphidae) and on its predator Chrysoperla carnea Stephen (Neuroptera Chrysopidae). Bollettino di Zoologia Agraria e Bachicoltura 30, 153164.Google Scholar
Marvier, M., McCreedy, C., Regetz, J. & Kareiva, P. (2007) A meta-analysis of effects of Bt cotton and maize nontarget invertebrates. Science 316, 14751477.CrossRefGoogle ScholarPubMed
Obrist, L.B., Klein, H., Dutton, A. & Bigler, F. (2005) Effects of Bt maize on Frankliniella tenuicornis and exposure to prey-mediated Bt toxin. Entomologia experimentalis et applicata 115, 409416.CrossRefGoogle Scholar
Obrist, L.B., Dutton, A., Albajes, R. & Bigler, F. (2006) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecological Entomology 31, 134154.CrossRefGoogle Scholar
Olsen, K.M., Daly, J.C., Finnegan, E.J. & Mahon, R.J. (2005) Changes in Cry1Ac Bt transgenic cotton in response to two environmental factors: temperature and insect damage. Journal of Economic Entomology 98(4), 13821390.Google Scholar
Porcar, M., Grenier, A.-M., Federici, B. & Rahbé, Y. (2009) Effects of Bacillus thuringiensis δ-endotoxins on the pea aphid, Acyrthosiphon pisum. Applied and Environmental Microbiology 75, 48974900.CrossRefGoogle ScholarPubMed
Raps, A., Kehr, J., Gugerli, P., Moar, W.J., Bigler, F. & Hilbeck, A. (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Molecular Ecology 10, 525533.CrossRefGoogle ScholarPubMed
Romeis, J. (2004) Workshop report – Impact of GM crops on natural enemies. IOBC wprs Bulletin 27(3), 193–095.Google Scholar
Romeis, J. & Meissle, M. Non-target risk assessment of Bt crops – Cry protein uptake by aphids. Journal of Applied Entomology, in press (doi: 10.1111/j.1439-0418.2010.01546.x).Google Scholar
Romeis, J., Meissle, M. & Bigler, F. (2006) Transgenic crops expressing Bacillus thuringiensis and biological control. Nature Biotechnology 24, 6371.CrossRefGoogle ScholarPubMed
Schmidt, J.E.U., Braun, A.E., Whitehouse, L.P. & Hilbeck, A. (2009) Effects of Activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Archives of Environmental Contamination and Toxicology 56, 221228.CrossRefGoogle ScholarPubMed
Schuler, T.H., Clark, A.J., Clark, S.J., Poppy, G.M., Stewart, J.C.N. & Denholm, I. (2005) Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect. Bullettin of Entomological Research 95, 243247.CrossRefGoogle ScholarPubMed
Shelton, A.M., Naranjo, S.E., Romeis, J., Hellmich, R.L., Wolt, J.D., Federici, B.A., Albajes, R., Bigler, F., Burgess, E.P.J., Dively, G.P., Gatehouse, A.M.R., Malone, L.A., Roush, R., Sears, M. & Sehnal, F. (2009) Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies. Transgenic Research 18, 317322.CrossRefGoogle Scholar
Sorlini, C., Buiatti, M., Burgio, G., Cellini, F., Giovannelli, V., Lener, M., Massari, G., Perrino, P., Selva, E., Spagnoletti, A. & Staiano, G. (2005) La valutazione ambientale dell'emissione deliberata dell'ambiente di organismi geneticamente modificati. Proposta metodologica. Peschiera Borromeo (MI), Italy, Ministero dell'Ambiente e della Tutela del Territorio.Google Scholar
Torres, J.B., Ruberson, J.R. & Adang, M.J. (2006) Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: A tritrophic analysis. Agricultural and Forest Entomology 8, 191202.Google Scholar
Triltsch, H. (1999) Food remains in the guts of Coccinella septempunctata (Coleoptera Coccinellidae) adults and larvae. European Journal of Entomology 96, 355364.Google Scholar
Wu, G., Cui, H., Ye, G., Xia, Y., Sardana, R., Cheng, X., Li, Y., Altosaar, I. & Shu, Q. (2002) Inheritance and expression of the cry1Ab gene in Bt (Bacillus thuringiensis) transgenic rice. Theoretical and Applied Genetics 104, 727734.CrossRefGoogle ScholarPubMed
Zhang, G.-F., Wan, F.-H., Lövei, G.L., Liu, W.-X. & Guo, J.-Y. (2006) Transmission of Bt toxin to the predator Propylaea japonica (Coleoptera: Coccinellidae) through its aphid prey feeding on transgenic Bt cotton. Environmental Entomology 35, 143150.CrossRefGoogle Scholar