Transgenic crops expressing Bacillus thuringiensis toxins and biological control

Romeis, Jörg; Meissle, Michael; Bigler, Franz

doi:10.1038/nbt1180

Cited by 722Insect Resistance and GeneticsGenetically Modified Organisms ResearchInsect-Plant Interactions and Control

Transgenic crops expressing Bacillus thuringiensis toxins and biological control

Romeis, Jörg, Meissle, Michael, Bigler, Franz·2006·Nature Biotechnology

DOI 10.1038/nbt1180

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Abstract

The area devoted to growing transgenic plants expressing insecticidal Cry proteins derived from Bacillus thuringiensis (Bt) is increasing worldwide. A major concern with the adoption of Bt crops is their potential impact on nontarget organisms including biological control organisms. Regulatory frameworks should advocate a step-wise (tiered) approach to assess possible nontarget effects of Bt crops. Laboratory and glasshouse studies have revealed effects on natural enemies only when Bt-susceptible, sublethally damaged herbivores were used as prey or host, with no indication of direct toxic effects. Field studies have confirmed that the abundance and activity of parasitoids and predators are similar in Bt and non-Bt crops. In contrast, applications of conventional insecticides have usually resulted in negative impacts on biological control organisms. Because Bt-transgenic varieties can lead to substantial reductions in insecticide use in some crops, they can contribute to integrated pest management systems with a strong biological control component.

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Reduced numbers of target pests, reduced nutritional quality of the remaining ones, and lack of host-derived or induced attractant cues may particularly affect parasitoids specialized to target pests, such as M. cingulum or Tachinidae [34, 47].
“Reduced numbers of target pests, reduced nutritional quality of the remaining ones, and lack of host-derived or induced attractant cues may particularly affect parasitoids specialized to target pests, such as M. cingulum or Tachinidae [34, 47].”
From Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review (2022) · cites this paper as [47]
Numerous laboratory studies have demonstrated that Cry1- and Cry2-class Bt proteins are specific to Lepidoptera and Cry3-class proteins to Chrysomelidae.
“numerous non-target laboratory studies with a wide range of taxa using purified Bt proteins, plant material, or prey that had consumed Bt proteins have demonstrated the specificity of Cry1- and Cry2-class proteins to Lepidoptera and Cry3-class proteins to Chrysomelidae (Coleoptera) [47, 61–63].”
From Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review (2022) · cites this paper as [47]
This can lead to adverse effects on the natural enemy that are related to reduced quality of the prey/host rather than to the insecticidal protein itself.
“This can lead to adverse effects on the natural enemy that are related to the reduced quality of the prey/host rather than to the insecticidal protein itself (Fig. 3) (Naranjo, 2009;Romeis et al., 2006).”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as Romeis et al., 2006

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Select Nontarget Arthropod Abundance in Transgenic and Nontransgenic Field Crops in Ohio
Jasinski, J. R., Eisley, J. B., Young, C. E., Kovach, J., & Willson, H. R. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.2.407 · Cited by 65 · see citing works
Effects of transgenic cry1Ab rice pollen on fitness of Propylea japonica (Thunberg)
Bai, Y., Jiang, M., & Cheng, J. A. (2005) · Journal of Pest Science · doi:10.1007/s10340-004-0078-x · Cited by 63 · see citing works
Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae)
Meissle, M., Vojtech, E., & Poppy, G. M. (2005) · Transgenic Research · doi:10.1007/s11248-004-6458-4 · Cited by 63 · see citing works
Self-citation
Impacts of Developing on Bt Maize-Intoxicated Hosts on Fitness Parameters of a Stem Borer Parasitoid
Bernal, J. S., Griset, J. G., & Gillogly, P. O. (2002) · Journal of Entomological Science · doi:10.18474/0749-8004-37.1.27 · Cited by 59 · see citing works
Biodiversity and structure of ground beetle assemblages (Coleoptera Carabidae) in Bt corn and its effects on non target insects.
Lozzia, G. C. (1999) · Cited by 55 · see citing works
Effect ofBacillus thuringiensisTransgenic Corn for Lepidopteran Control on Nontarget Arthropods
Daly, T., & Buntin, G. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1292 · Cited by 55 · see citing works
Predaceous Arthropods and Lepidopteran Pests on Conventional, Bollgard, and Bollgard Ii Cotton Under Untreated and Disrupted Conditions
Hagerty, A. M., Kilpatrick, A. L., Turnipseed, S. G., Sullivan, M. J., & Bridges, W. C. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.1.105 · Cited by 54 · see citing works
Interaction of Resistant Plants and Wasp Parasitoids of Tobacco Budworm (Lepidoptera: Noctuidae)
Johnson, M. T. (1997) · Environmental Entomology · doi:10.1093/ee/26.2.207 · Cited by 53 · see citing works
Unexpected Effects of Different Potato Resistance Factors to the Colorado Potato Beetle (Coleoptera: Chrysomelidae) on the Potato Aphid (Homoptera: Aphididae)
Ashouri, A., Michaud, D., & Cloutier, C. (2001) · Environmental Entomology · doi:10.1603/0046-225x-30.3.524 · Cited by 51 · see citing works
Influence of Bacillus thuringiensis- Transgenic and Nectariless Cotton on Insect Populations with Emphasis on the Tarnished Plant Bug (Heteroptera: Miridae)
Hardee, D. D., & Bryan, W. W. (1997) · Journal of Economic Entomology · doi:10.1093/jee/90.2.663 · Cited by 50 · see citing works
Field Evaluation of Transgenic Tobacco Containing a Bacillus thuringiensis Insecticidal Protein Gene
Warren, G. W., Carozzi, N. B., Desai, N., & Koziel, M. G. (1992) · Journal of Economic Entomology · doi:10.1093/jee/85.5.1651 · Cited by 49 · see citing works
Utility of Ground Beetle Species in Field Tests of Potential Nontarget Effects of Bt Crops
Lopez, M. D., Prasifka, J. R., Bruck, D. J., & Lewis, L. C. (2005) · Environmental Entomology · doi:10.1603/0046-225x(2005)034[1317:uogbsi]2.0.co;2 · Cited by 48 · see citing works
Principles for regulatory testing and interpretation of semi-field and field studies with non-target arthropods
Candolfi, M. P., Bigler, F., Campbell, P., Heimbach, U., Schmuck, R., Angeli, G., Bakker, F. M., Brown, K., Carli, G., Dinter, A., et al. (2000) · Journal of Pest Science · doi:10.1007/bf02956449 · Cited by 47 · see citing works
Self-citation
The effects of transgenic cotton, Gossypium hirsutum L., containing Bacillus thuringiensis toxin genes for the control of the pink bollworm, Pectinophora gossypiella (Saunders) and other arthropods
Flint, H. M., Henneberry, T. J., Wilson, F. D., Holguín, E. S., Parks, N. J., & Buehler, R. E. (1995) · Cited by 47 · see citing works
Development of European corn borer larvae on Event 176 Bt corn: influence on survival and fitness
Siegfried, B. D., Zoerb, A. C., & Spencer, T. (2001) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2001.00843.x · Cited by 44 · see citing works
Effect of Bt corn leaf suspension on food consumption by Chilo partellus and life history parameters of its parasitoid Cotesia flavipes under laboratory conditions
Prütz, G., & Dettner, K. (2004) · Entomologia Experimentalis et Applicata · doi:10.1111/j.0013-8703.2004.00166.x · Cited by 44 · see citing works
Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages
Meissle, M., & Lang, A. (2005) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2004.12.007 · Cited by 44 · see citing works
Self-citation
Dusky Sap Beetles (Coleoptera: Nitidulidae) and Other Kernel Damaging Insects in Bt and Non-Bt Sweet Corn in Illinois
Dowd, P. F. (2000) · Journal of Economic Entomology · doi:10.1603/0022-0493-93.6.1714 · Cited by 42 · see citing works
Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes
Ashouri, A., Michaud, D., & Cloutier, C. (2001) · BioControl · doi:10.1023/a:1014123712776 · Cited by 41 · see citing works
Longevity of phytophagous heteropteran predators feeding on transgenic Btt‐potato plants
Armer, C. A., Berry, R. E., & Kogan, M. (2000) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2000.00672.x · Cited by 40 · see citing works
Effects of Transgenic Bacillus thuringiensis Potato and Conventional Insecticides for Colorado Potato Beetle (Coleoptera: Chrysomelidae) Management on the Abundance of Ground-Dwelling Arthropods in Oregon Potato Ecosystems
Duan, J. J., Head, G., Jensen, A. S., & Reed, G. L. (2004) · Environmental Entomology · doi:10.1603/0046-225x-33.2.275 · Cited by 40 · see citing works
Influence of pesticide applications on pest and predatory arthropods associated with transgenicBt cotton and nontransgenic cotton plants
Men, X., Ge, F., Edwards, C. A., & Yardım, E. N. (2004) · Phytoparasitica · doi:10.1007/bf02979819 · Cited by 37 · see citing works
Long-Term Assessment of the Effects of TransgenicBtCotton on the Function of the Natural Enemy Community
Naranjo, S. E. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1211 · Cited by 35 · see citing works
Spring aphid-parasitoid (Hom., Aphididae, Hym., Braconidae) associations and interactions in a Mediterranean arable crop ecosystem, including Bt maize
Pons, X., & Star�, P. (2003) · Journal of Pest Science · doi:10.1007/s10340-003-0003-8 · Cited by 33 · see citing works
Impact of TransgenicBacillus thuringiensisCorn and Crop Phenology on Five Nontarget Arthropods
Pilcher, C. D., Rice, M. E., & Obrycki, J. J. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1302 · Cited by 33 · see citing works
Transgenic Resistance to the Colorado Potato Beetle in Bt-expressing Eggplant Fields
Acciarri, N., Vitelli, G., Arpaia, S., Mennella, G., Sunseri, F., & Rotino, G. L. (2000) · HortScience · doi:10.21273/hortsci.35.4.722 · Cited by 32 · see citing works
Effects of transgenic Cry1A+CpTI cotton and Cry1Ac toxin on the parasitoid, Campoketis chlorideae (Hymenoptera: Ichneumonidae)
Liu, X., SUN, C.-G., & Zhang, Q. (2005) · Insect Science · doi:10.1111/j.1744-7917.2005.00012.x · Cited by 30 · see citing works
Season-Long Abundance of Generalist Predators in Transgenic versus Nontransgenic Potato Fields2
Riddick, E. W., Dively, G. P., & Barbosa, P. (2000) · Journal of Entomological Science · doi:10.18474/0749-8004-35.4.349 · Cited by 29 · see citing works
The effects of six species of aphids on some life history parameters of the ladybird Propylea quatuordecimpunctata (Coleoptera: Coccinellidae)
Kalushkov, P., & Hodek, I. (2005) · European Journal of Entomology · doi:10.14411/eje.2005.064 · Cited by 29 · see citing works
Field Evaluation of the Impact of Corn Rootworm (Coleoptera: Chrysomelidae)–ProtectedBtCorn on Foliage-Dwelling Arthropods
Bhatti, M. A., Duan, J., Head, G. P., Jiang, C., McKee, M. J., Nickson, T. E., Pilcher, C. L., & Pilcher, C. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1336 · Cited by 28 · see citing works
Field Evaluation of the Impact of Corn Rootworm (Coleoptera: Chrysomelidae)–ProtectedBtCorn on Ground-Dwelling Invertebrates
Bhatti, M. A., Duan, J. J., Head, G., Jiang, C., McKee, M. J., Nickson, T. E., Pilcher, C., & Pilcher, C. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1325 · Cited by 23 · see citing works
Development of Spodoptera exigua and Helicoverpa zea (Lepidoptera: Noctuidae) on Transgenic Cotton Containing CrylAc Insecticidal Protein
Ashfaq, M., Young, S. Y., & McNew, R. W. (2000) · Journal of Entomological Science · doi:10.18474/0749-8004-35.4.360 · Cited by 20 · see citing works
Simulated Effects of Transgenic Bt Crops on Specialist Parasitoids of Target Pests
Sisterson, M. S., & Tabashnik, B. E. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.4.733 · Cited by 20 · see citing works
Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect
Schuler, T. H., Clark, A. J., Clark, S. J., Poppy, G. M., Stewart, C. N., & Denholm, I. (2005) · Bulletin of Entomological Research · doi:10.1079/ber2004356 · Cited by 19 · see citing works
Insects, Spiders and Mites
JEPSON, P. C. (1997) · doi:10.1002/9781444313512.ch15 · Cited by 17 · see citing works
Insect Populations on Bacillus thuringiensis Transgenic Sweet Corn
Hassell, R. L., & Shepard, B. M. (2002) · Journal of Entomological Science · doi:10.18474/0749-8004-37.4.285 · Cited by 15 · see citing works
Genetically modified potatoes expressing Cry 3A protein do not affect aphidophagous coccinellids
Kalushkov, P., & Nedvěd, O. (2005) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2005.00987.x · Cited by 14 · see citing works
Bollworm (Helicoverpa armigera (Hubner), Lepidoptera : Noctuidae) occurrences in Bt- and non-Bt-cotton fields, Marble Hall, Mpumalanga, South Africa
Mellet, M., Schoeman, A. S., Broodryk, S. W., & Hofs, J.-L. (2004) · Agritrop (Cirad) · Cited by 11 · see citing works
GM Pest-resistant Crops: Assessing Environmental Impacts on Non-target Organisms
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Effects of transgenic corn on Lydella thompsoni Herting (Diptera:Tachinidae) parasitoid of Ostrinia nubilalis Hb. (Lepidoptera Crambidae)
Manachini, B. (2003) · Cited by 11 · see citing works
Spider web survey or whole plant visual sampling? Impact assessment ofBtcorn on non-target predatory insects with two concurrent methods
Tóth, F., Árpás, K., Szekeres, D., Kádár, F., Szentkirályi, F., Szénási, Á., & Kiss, J. G. (2004) · Environmental Biosafety Research · doi:10.1051/ebr:2005006 · Cited by 6 · see citing works

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Insect pathogens as biological control agents: Back to the future
Lacey, L. A., Grzywacz, D., Shapiro‐Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2015.07.009 · Cited by 1,603 · see citing works
Wildlife Ecotoxicology of Pesticides: Can We Track Effects to the Population Level and Beyond?
Köhler, H.-R., & Triebskorn, R. (2013) · Science · doi:10.1126/science.1237591 · Cited by 911 · see citing works
Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services
Lu, Y., Wu, K., Jiang, Y., Guo, Y., & Desneux, N. (2012) · Nature · doi:10.1038/nature11153 · Cited by 805 · see citing works
Biological control and sustainable food production
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Self-citation
Role of Receptors in Bacillus thuringiensis Crystal Toxin Activity
Pigott, C. R., & Ellar, D. J. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00034-06 · Cited by 694 · see citing works
Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China
Lu, Y., Wu, K., Jiang, Y., Xia, B., Li, P., Feng, H., Wyckhuys, K. A. G., & Guo, Y. (2010) · Science · doi:10.1126/science.1187881 · Cited by 664 · see citing works
Assessment of risk of insect-resistant transgenic crops to nontarget arthropods
Romeis, J., Bartsch, D. K., Bigler, F., Candolfi, M. P., Gielkens, M. M. C., Hartley, S. E., Hellmich, R. L., Huesing, J. E., JEPSON, P. C., Layton, R. J., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1381 · Cited by 501 · see citing works
Self-citation
A Meta-Analysis of Effects of Bt Cotton and Maize on Nontarget Invertebrates
Marvier, M., McCreedy, C., Regetz, J., & Kareiva, P. (2007) · Science · doi:10.1126/science.1139208 · Cited by 445 · see citing works
Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms
Orozco-Mosqueda, M. D. C., Rocha-Granados, M. D. C., Glick, B. R., & Santoyo, G. (2018) · Microbiological Research · doi:10.1016/j.micres.2018.01.005 · Cited by 381 · see citing works
Restoring a maize root signal that attracts insect-killing nematodes to control a major pest
Degenhardt, J., Hiltpold, I., Köllner, T. G., Frey, M., Gierl, A., Gershenzon, J., Hibbard, B. E., Ellersieck, M. R., & Turlings, T. C. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906365106 · Cited by 360 · see citing works
Bt Crop Effects on Functional Guilds of Non-Target Arthropods: A Meta-Analysis
Wolfenbarger, L. L., Naranjo, S. E., Lundgren, J. G., Bitzer, R. J., & Watrud, L. S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002118 · Cited by 324 · see citing works
Pests, pesticide use and alternative options in European maize production: current status and future prospects
Meissle, M., Mouron, P., Musa, T., Bigler, F., Pons, X., Vasileiadis, V. P., Otto, S., Antichi, D., Kiss, J., Pálinkás, Z., et al. (2010) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2009.01491.x · Cited by 321 · see citing works
Self-citation
Evolutionary ecology of insect adaptation to Bt crops
Carrière, Y., Crowder, D. W., & Tabashnik, B. E. (2010) · Evolutionary Applications · doi:10.1111/j.1752-4571.2010.00129.x · Cited by 318 · see citing works
Integration of Insect-Resistant Genetically Modified Crops within IPM Programs
Kennedy, G. G. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_1 · Cited by 292 · see citing works
Insect-Resistant Genetically Modified Rice in China: From Research to Commercialization
Chen, M., Shelton, A. M., & Yè, G. (2010) · Annual Review of Entomology · doi:10.1146/annurev-ento-120709-144810 · Cited by 290 · see citing works
Recent developments and future prospects in insect pest control in transgenic crops
Christou, P., Capell, T., Kohli, A., Gatehouse, J. A., & Gatehouse, A. M. R. (2006) · Trends in Plant Science · doi:10.1016/j.tplants.2006.04.001 · Cited by 289 · see citing works
Impacts of Bt crops on non-target invertebrates and insecticide use patterns.
Naranjo, S. E. (2009) · CABI Reviews · doi:10.1079/pavsnnr20094011 · Cited by 252 · see citing works
Regional pest suppression associated with widespread Bt maize adoption benefits vegetable growers
Dively, G. P., Venugopal, P. D., Bean, D., Whalen, J., Holmstrom, K., Kuhar, T. P., Doughty, H. B., Patton, T., Cissel, W., & Hutchison, W. D. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720692115 · Cited by 239 · see citing works
Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants
Romeis, J., Hellmich, R. L., Candolfi, M. P., Carstens, K., de Schrijver, A., Gatehouse, A. M. R., Herman, R. A., Huesing, J. E., McLean, M. A., Raybould, A. F., et al. (2010) · Transgenic Research · doi:10.1007/s11248-010-9446-x · Cited by 232 · see citing works
Self-citation
Genetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
Self-citation
The second green revolution? Production of plant-based biodegradable plastics
Mooney, B. (2009) · Biochemical Journal · doi:10.1042/bj20081769 · Cited by 229 · see citing works
Genetically Engineered Crops: From Idea to Product
Prado, J. R., Segers, G. C., Voelker, T. A., Carson, D., Dobert, R. C., Phillips, J., Cook, K. A., Cornejo, C., Monken, J., Grapes, L., et al. (2014) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050213-040039 · Cited by 194 · see citing works
Impacts of Bt Transgenic Cotton on Integrated Pest Management
Naranjo, S. E. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf102939c · Cited by 186 · see citing works
Microbial and viral chitinases: Attractive biopesticides for integrated pest management
Berini, F., Katz, C., Gruzdev, N., Casartelli, M., Tettamanti, G., & Marinelli, F. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.01.002 · Cited by 170 · see citing works
Transgenic Insecticidal Crops and Natural Enemies: A Detailed Review of Laboratory Studies
Lövei, G. L., Andow, D. A., & Arpaia, S. (2009) · Environmental Entomology · doi:10.1603/022.038.0201 · Cited by 166 · see citing works
Ecological Impacts of Genetically Modified Crops: Ten Years of Field Research and Commercial Cultivation
Sanvido, O., Romeis, J., & Bigler, F. (2007) · Springer eBooks · doi:10.1007/10_2007_048 · Cited by 163 · see citing works
Self-citation
Budding trends in integrated pest management using advanced micro- and nano-materials: Challenges and perspectives
Khandelwal, N., Barbole, R. S., Banerjee, S. S., Chate, G. P., Biradar, A. V., Khandare, J. J., & Giri, A. P. (2016) · Journal of Environmental Management · doi:10.1016/j.jenvman.2016.09.071 · Cited by 152 · see citing works
Current status and potential of conservation biological control for agriculture in the developing world
Wyckhuys, K. A. G., Lu, Y., Morales, H., Vázquez, L. L., Legaspi, J. C., Eliopoulos, P. A., & Hernández‐Pelegrín, L. (2012) · Biological Control · doi:10.1016/j.biocontrol.2012.11.010 · Cited by 148 · see citing works
Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields
Obrist, L. B., Dutton, A. C., Albajes, R., & Bigler, F. (2006) · Ecological Entomology · doi:10.1111/j.0307-6946.2006.00762.x · Cited by 148 · see citing works
Self-citation
RNAi-Based Insecticidal Crops: Potential Effects on Nontarget Species
Lundgren, J. G., & Duan, J. J. (2013) · BioScience · doi:10.1525/bio.2013.63.8.8 · Cited by 143 · see citing works
Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops
Raybould, A. F. (2006) · Environmental Biosafety Research · doi:10.1051/ebr:2007004 · Cited by 143 · see citing works
Screening of Brazilian Bacillus thuringiensis isolates active against Spodoptera frugiperda, Plutella xylostella and Anticarsia gemmatalis
Monnerat, R. G., Batista, A. C., Medeiros, P. T., Martins, E. S., Melatti, V. M., Praça, L. B., Dumas, V. F., Morinaga, C., Demo, C., Gomes, A. C. M. M., et al. (2006) · Biological Control · doi:10.1016/j.biocontrol.2006.11.008 · Cited by 142 · see citing works
Bacterial Entomopathogens
Jurat‐Fuentes, J. L., & Jackson, T. A. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-384984-7.00008-7 · Cited by 137 · see citing works
Food biotechnology and education
Sengooba, T., Grumet, R., Hancock, J. F., Zawedde, B. M., Kitandu, L., Weebadde, C. K., Karembu, M., Kenya, E., Meredia, K., Nampala, P., et al. (2009) · Electronic Journal of Biotechnology · doi:10.2225/vol12-issue1-fulltext-6 · Cited by 132 · see citing works
No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa
Comas, C., Lumbierres, B., Pons, X., & Albajes, R. (2014) · Transgenic Research · doi:10.1007/s11248-013-9737-0 · Cited by 129 · see citing works
Extrapolating non-target risk of Bt crops from laboratory to field
Duan, J. J., Lundgren, J. G., Naranjo, S., & Marvier, M. (2010) · Biology Letters · doi:10.1098/rsbl.2009.0612 · Cited by 127 · see citing works
Integration of Plant Defense Traits with Biological Control of Arthropod Pests: Challenges and Opportunities
Peterson, J. A., Ode, P. J., Oliveira-Hofman, C., & Harwood, J. D. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01794 · Cited by 126 · see citing works
Biopesticides: Where We Stand?
Mishra, J., Tewari, S., Singh, S., & Arora, N. K. (2014) · Springer eBooks · doi:10.1007/978-81-322-2068-8_2 · Cited by 123 · see citing works
Advanced Technologies for Managing Insect Pests
Ishaaya, I., Palli, S. R., & Horowitz, A. R. (2012) · Springer eBooks · doi:10.1007/978-94-007-4497-4 · Cited by 119 · see citing works
Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops
Romeis, J., Raybould, A. F., Bigler, F., Candolfi, M. P., Hellmich, R. L., Huesing, J. E., & Shelton, A. M. (2012) · Chemosphere · doi:10.1016/j.chemosphere.2012.09.035 · Cited by 119 · see citing works
Self-citation
Low susceptibility of Spodoptera cosmioides, Spodoptera eridania and Spodoptera frugiperda (Lepidoptera: Noctuidae) to genetically-modified soybean expressing Cry1Ac protein
Bernardi, O., Sorgatto, R. J., Barbosa, A. D., Domingues, F. A., Dourado, P. M., Carvalho, R. A., Martinelli, S., Head, G., & Omoto, C. (2014) · Crop Protection · doi:10.1016/j.cropro.2014.01.001 · Cited by 118 · see citing works
Metabolomics – A robust bioanalytical approach for the discovery of the modes-of-action of pesticides: A review
Aliferis, K. A., & Jabaji, S. (2011) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2011.03.004 · Cited by 118 · see citing works
The development and status of Bt rice in China
Li, Y., Hallerman, E. M., Liu, Q., Wu, K., & Peng, Y. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12464 · Cited by 117 · see citing works
Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops
Raybould, A. F. (2007) · Plant Science · doi:10.1016/j.plantsci.2007.09.003 · Cited by 116 · see citing works
Genetic Transformation of Sugarcane, Current Status and Future Prospects
Budeguer, F., Enrique, R., Perera, M. F., Racedo, J., Castagnaro, A. P., Noguera, A. S., & Welin, B. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.768609 · Cited by 115 · see citing works
Antibiotic and pesticide susceptibility and the Anthropocene operating space
Living with Resistance project, Jørgensen, P. S., Aktipis, A., Brown, Z. S., Carrière, Y., Downes, S. J., Dunn, R. R., Epstein, G., Frisvold, G. B., Hawthorne, D. J., et al. (2018) · Nature Sustainability · doi:10.1038/s41893-018-0164-3 · Cited by 114 · see citing works
High Susceptibility of Bt Maize to Aphids Enhances the Performance of Parasitoids of Lepidopteran Pests
Faria, C. A., WÄCKERS, F. L., Pritchard, J., Barrett, D. A., & Turlings, T. C. J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000600 · Cited by 114 · see citing works
Recombinant protease inhibitors for herbivore pest control: a multitrophic perspective
Schlüter, U., Benchabane, M., Munger, A., Kiggundu, A., Vorster, J., Goulet, M., Cloutier, C., & Michaud, D. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq166 · Cited by 113 · see citing works
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Authors: Romeis, J., Meissle, M., & Bigler, F.
Affiliations: Agroscope (CH)
Corresponding author: Romeis, Jörg
ORCID: Romeis, Jörg
Meissle, Michael
Venue: Nature Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2006-01-01
Volume: 24
Issue: 1
Pages: 63-71
ISSN: 0733-222X (ISSN-L)
1087-0156
1546-1696
DOI: 10.1038/nbt1180
OpenAlex: W2043034823
Cited by: 719
References: 123
Citations by year: 2026: 13 · 2025: 14 · 2024: 12 · 2023: 16 · 2022: 30 · 2021: 21 · 2020: 31 · 2019: 21 · 2018: 27 · 2017: 21 · 2016: 38 · 2015: 36 · 2014: 48 · 2013: 40 · 2012: 48
FWCI: 5.02
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Biotechnology (publishedVersion)
PubMed (publishedVersion)
Funders: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords: genetically modified crops, Bacillus thuringiensis, Cry proteins, insecticidal proteins, biological control, non-target effects, parasitoids, predators, natural enemies, insecticide reduction, integrated pest management, regulatory evaluation
MeSH terms: Bacillus thuringiensis, Bacterial Proteins, Consumer Product Safety, Insecticide Resistance, Pest Control, Biological, Risk Factors, Risk Assessment, Plants, Genetically Modified

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Transgenic crops expressing Bacillus thuringiensis toxins and biological control

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