Editor’s Choice: Evaluating the Potential for Adverse Interactions within Genetically Engineered Breeding Stacks
Open accessAbstract
Plant breeding has a long history of developing varieties with desirable traits in response to the needs of both growers and consumers. Although the bases for most of these traits are not known genetically or biochemically, conventional breeding combines these multiple traits to create new hybrids and stable varieties that are safe and not generally subject to safety assessment. With the advent of genetic engineering, a tool for incorporating additional traits has become available to plant breeders. The safe application of genetic engineering to food and feed crops is widely acknowledged as a useful tool in addressing global agricultural challenges, including population growth and climate change. As used here, the term genetically engineered (GE) stack refers to a plant in which two or more transgenic events (i.e. single-locus insertions) that have been separately assessed for safety have been combined by conventional breeding (Table I). In recent years, increasing numbers of GE stacks have been planted, the first of which offered combinations of insect and herbicide tolerance genes to combat a wider range of pests and weeds than covered by the single events (Que et al., 2010; James, 2011). Two main questions arise when considering the food and feed safety of GE stacks: (1) does incorporation of more than one event increase genomic instability, and (2) can potential interactions between the products of the combined events impact safety? A related paper considered the stacking of events in light of the plasticity of plant genomes and concluded that enhanced genetic instability from a transgene or from common sequences in two or more transgenes is remote (Weber et al., 2012). This paper addresses the second question of potential interactions between events and their products combined in a stack, reviews the basic principles of plant breeding and its history of safe use, and extends these principles to the feed and food safety of events combined through the same processes used in conventional breeding of non-GE plants. Potential environmental impacts are outside the scope of food and feed safety. The new varieties developed through modern biotechnology are identified by a number of terms, including genetically modified (GM), GE, transgenic, biotech, recombinant, and plants with novel traits. The term GE is used here as defined by Weber et al. (2012). For these reasons, the term GE is preferred over the term GM. There are many methods encompassed by the general term conventional breeding, including wide crosses and selection, mutagenesis, and somaclonal variation. When the parental species are not closely related, the cross may be facilitated by embryo rescue, somatic hybridization, or x-ray-induced translocations. The term interaction, as used in this paper, refers to an effect, such as a new or modified metabolic activity, resulting from a combination of transgenes. An example of an interaction is protein-protein binding resulting in a novel effect only seen with a specific combination of proteins, for instance, protein cofactors or subunits for the same enzymatic complex or subcellular metabolic binding reaction. Examples can also include a direct metabolic interaction that would inhibit or activate components in a metabolic pathway shared by the proteins newly combined in the GE stack or components of independent metabolic pathways that indirectly interact by way of a common metabolite. Thus, interactions within GE stacks generally refer to the metabolic or physiochemical interplay between the products of transgenes or between the product of one transgene and the second gene, rather than between the two genes themselves. Conventional breeding has a long history of safe use despite the presence of antinutritional factors, toxins, and allergens in crops. There is no evidence that a random genomic change in a crop has resulted in a novel food or feed safety issue (Weber et al., 2012). Historically, humans have selected desirable traits that arise from the crop’s genomic plasticity and interactions between genes. As breeding became more advanced, new methods were applied to select and combine desired traits, which also modify the genome as a consequence. Plants produce a multitude of metabolites that provide various functions. These include signaling activities in response to environmental stress or attack from plant pathogens and pests. Some metabolites have beneficial effects, while others are toxic when fed at high levels to sensitive animal species (Ames et al., 1990). Although particular metabolites tend to be specific to some plant families, there are metabolites of concern in a number of common food and feed crops, including apple (Malus domestica), apricot (Prunus armeniaca), Brassica spp., celery (Apium graveolens), cucumber (Cucumis sativus), lima bean (Phaseolus lunatus), potato (Solanum tuberosum), cherry (Prunus avium or Prunus cerasus), and sorghum (Sorghum bicolor; Beier, 1990; D’Mello et al., 19
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There is no evidence that the insertion of a transgene from a non-toxic source into a GM crop has any greater propensity to result in the de novo generation of novel toxic compounds than does the range of conventional plant breeding techniques that currently require no toxicity testing.
“Furthermore, there is no evidence that the insertion of a transgene from a non-toxic source into a GM crop has any greater propensity to result in the de novo generation of novel toxic compounds than does the range of conventional plant breeding techniques that currently require no toxicity testing (Steiner et al. 2013).”
From The use of whole food animal studies in the safety assessment of genetically modified crops: Limitations and recommendations (2013) · cites this paper as Steiner et al. 2013
Such possibilities can be readily examined using sensitive analytical techniques and are used in plant breeding to monitor levels of naturally occurring toxins that are identified in OECD consensus documents for specific crops.
“Fortunately such possibilities can be readily examined using sensitive analytical techniques and are used in plant breeding to monitor levels of naturally occurring toxins that are identified in OECD consensus documents for specific crops (Steiner et al., 2013).”
From The use of whole food animal studies in the safety assessment of genetically modified crops: Limitations and recommendations (2013) · cites this paper as Steiner et al., 2013
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Cites
Biochemistry & molecular biology of plants
(2001) · Choice Reviews Online · doi:10.5860/choice.38-3895 · Cited by 2,980 · see citing works
Genome sequence and analysis of the tuber crop potato
Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P., Zhang, G., Guzman, F., Torres, M., Lozano, R., et al. (2011) · Nature · doi:10.1038/nature10158 · Cited by 2,050 · see citing works
Bitter taste, phytonutrients, and the consumer: a review
Drewnowski, A., & Gomez-Carneros, C. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/72.6.1424 · Cited by 1,366 · see citing works
Lam, H., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F., Li, M., He, W., Qin, N., Wang, B., et al. (2010) · Nature Genetics · doi:10.1038/ng.715 · Cited by 1,051 · see citing works
Assessment of the food safety issues related to genetically modified foods
Kuiper, H. A., Kleter, G. A., Noteborn, H. P. J. M., & Kok, E. J. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01119.x · Cited by 557 · see citing works
β-Glucosidases as detonators of plant chemical defense
Morant, A. V., Jørgensen, K., Jørgensen, C., Paquette, S. M., Sánchez‐Pérez, R., Møller, B. L., & Bak, S. (2008) · Phytochemistry · doi:10.1016/j.phytochem.2008.03.006 · Cited by 550 · see citing works
Springer, N. M., Ying, K., Fu, Y., Ji, T., Yeh, C., Jia, Y., Wu, W., Richmond, T., Kitzman, J. O., Rosenbaum, H., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000734 · Cited by 538 · see citing works
The genetics of plant metabolism
Keurentjes, J. J. B., Fu, J., de Vos, C. H. R., Lommen, A., Hall, R. D., Bino, R. J., van der Plas, L. H. W., Jansen, R. C., Vreugdenhil, D., & Koornneef, M. (2006) · Nature Genetics · doi:10.1038/ng1815 · Cited by 499 · see citing works
Genome-wide patterns of genetic variation among elite maize inbred lines
Lai, J., Li, R., Xu, X., Jin, W., Xu, M., Zhao, H., Xiang, Z., Song, W., Ying, K., Zhang, M., et al. (2010) · Nature Genetics · doi:10.1038/ng.684 · Cited by 470 · see citing works
Assessment of the allergenic potential of foods derived from genetically engineered crop plants*
Metcalfe, D. D., Astwood, J. D., Townsend, R., Sampson, H. A., Taylor, S. L., & Fuchs, R. L. (1996) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408399609527763 · Cited by 435 · see citing works
Swanson-Wagner, R. A., Jia, Y., DeCook, R. R., Borsuk, L. A., Nettleton, D. S., & Schnable, P. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510430103 · Cited by 424 · see citing works
Unintended effects and their detection in genetically modified crops
Cellini, F., Chesson, A., Colquhoun, I., Constable, A., Davies, H. V., Engel, K. H., Gatehouse, A. M. R., Kärenlampi, S., Kok, E. J., Leguay, J.-J., et al. (2004) · Food and Chemical Toxicology · doi:10.1016/j.fct.2004.02.003 · Cited by 397 · see citing works
Dietary pesticides (99.99% all natural).
Ames, B. N., Profet, M., & Gold, L. S. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.19.7777 · Cited by 395 · see citing works
Towards the molecular basis of heterosis
Hochholdinger, F., & Hoecker, N. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.08.005 · Cited by 373 · see citing works
Groszmann, M., Greaves, I. K., Albertyn, Z., Scofield, G. N., Peacock, W. J., & Dennis, E. S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019217108 · Cited by 306 · see citing works
Toxic Substances in Crop Plants
D’Mello, J. P. F., DUFFUS, C. M., & Duffus, J. H. (1991) · Woodhead Publishing Limited eBooks · doi:10.1533/9781845698454 · Cited by 270 · see citing works
Nonadditive Gene Expression in Diploid and Triploid Hybrids of Maize
Auger, D. L., Gray, A. D., Ream, T. S., Kato, A., Coe, E. H., & Birchler, J. A. (2004) · Genetics · doi:10.1534/genetics.104.032987 · Cited by 217 · see citing works
Naturally Occurring Toxic Alkaloids in Foods
JADHAV, S. J., Sharma, R. P., & Salunkhe, D. K. (1981) · Critical Reviews in Toxicology · doi:10.3109/10408448109059562 · Cited by 200 · see citing works
Trait stacking in transgenic crops: Challenges and opportunities
Que, Q., Chilton, M.-D. M., de Fontes, C. M., He, C., Nuccio, M., Zhu, T., Wu, Y., Chen, J. S., & Shi, L. (2010) · GM Crops · doi:10.4161/gmcr.1.4.13439 · Cited by 191 · see citing works
The complexities of starch biosynthesis in cereal endosperms
Hannah, L. C., & James, M. (2008) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2008.02.013 · Cited by 191 · see citing works
Self-citationEvaluation of protein safety in the context of agricultural biotechnology
Delaney, B., Astwood, J. D., CUNNY, H. C., Conn, R. E., Hérouet-Guicheney, C., Macintosh, S. C., Meyer, L. S., Privalle, L., Gao, Y., Mattsson, J. L., et al. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2008.01.045 · Cited by 177 · see citing works
Natural Pesticides and Bioactive Components in Foods
Beier, R. C. (1990) · Reviews of Environmental Contamination and Toxicology · doi:10.1007/978-1-4612-3366-4_2 · Cited by 167 · see citing works
The Complexities of Starch Biosynthesis in Cereal Endosperms
Hannah, L. C., & Greene, T. W. (2008) · Biotechnology in agriculture and forestry · doi:10.1007/978-3-540-68922-5_20 · Cited by 134 · see citing works
Self-citationParrott, W. A., Chassy, B. M., Ligon, J., Meyer, L. S., Petrick, J. S., Zhou, J., Herman, R. A., Delaney, B., & Levine, M. J. (2010) · Food and Chemical Toxicology · doi:10.1016/j.fct.2010.04.017 · Cited by 102 · see citing works
Self-citationPhytophotodermatitis From Celery Among Grocery Store Workers
Seligman, P. J. (1987) · Archives of Dermatology · doi:10.1001/archderm.1987.01660350078017 · Cited by 81 · see citing works
Development of the International Life Sciences Institute Crop Composition Database
Ridley, W. P., Shillito, R. D., Coats, I., Steiner, H., Shawgo, M., Phillips, A., Dussold, P., & Kurtyka, L. (2004) · Journal of Food Composition and Analysis · doi:10.1016/j.jfca.2004.03.006 · Cited by 79 · see citing works
Self-citationWeber, N., Halpin, C., Hannah, L. C., Jez, J. M., Kough, J., & Parrott, W. (2012) · Plant Physiology · doi:10.1104/pp.112.204271 · Cited by 78 · see citing works
Self-citationBERKLEY, S. F., Hightower, A. W., BEIER, R. C., FLEMING, D. W., BROKOPP, C. D., IVIE, G. W., & BROOME, C. V. (1986) · Annals of Internal Medicine · doi:10.7326/0003-4819-105-3-351 · Cited by 72 · see citing works
Laurila, J., Laakso, I., Valkonen, J. P. T., Hiltunen, R., & Pehu, E. (1996) · Plant Science · doi:10.1016/0168-9452(96)04435-4 · Cited by 52 · see citing works
Squash Containing Toxic Cucurbitacin Compounds Occurring in California and Alabama
Rymal, K. S., Chambliss, O. L., Bond, M., & Smith, D. A. (1984) · Journal of Food Protection · doi:10.4315/0362-028x-47.4.270 · Cited by 40 · see citing works
AN OUTBREAK OF PHYTOPHOTODERMATITIS DUE TO CELERY
Finkelstein, E., Afek, U., Gross, E. M., Aharoni, N., Rosenberg, L. A., & Halevy, S. (1994) · International Journal of Dermatology · doi:10.1111/j.1365-4362.1994.tb01539.x · Cited by 37 · see citing works
Thomas, K., MacIntosh, S., Bannon, G. A., Hérouet-Guicheney, C., Holsapple, M. P., Ladics, G. S., McClain, S., Vieths, S., Woolhiser, M. R., & Privalle, L. (2009) · Food and Chemical Toxicology · doi:10.1016/j.fct.2009.02.001 · Cited by 34 · see citing works
Starch Formation in the Cereal Endosperm
Hannah, L. C. (2007) · Springer eBooks · doi:10.1007/7089_2007_116 · Cited by 26 · see citing works
Self-citationBreeding for Safety in Vegetables and Fruits
Stevens, M. A. (1974) · CSSA special publication - Crop Science Society of America · doi:10.2135/cssaspecpub5.c5 · Cited by 2 · see citing works
Flagged first, then by citations
2 of the 36 references couldn’t be matched to a known paper.
Research works printed but not linked: 12
- Anonymous (1970) Name of potato variety Lenape withdrawn. Am J Potato Res 47: 103 [Google Scholar]
- Association of State Universities and Land Grant Colleges (1972) Statement of Responsibilities and Policies Relating to the Development, Release, and Multiplication of Publicly Developed Varieties of Seed-Propagated Crops: A Policy Statement of the Experiment Station Committee on Organization and Policy of the Experiment Station Section of the Association of State Universities and Land Grant Colleges, and the Agricultural Research Service and the Soil Conservation Service of the United States Department of Agriculture. Association of State Universities and Land Grant Colleges, Washington, DC [Google Scholar]
- Codex Alimentarius Commission (2009) Principles for the risk analysis of foods derived from modern biotechnology (CAC/GL 44-2003) and guideline for the conduct of food safety assessment of foods derived from recombinant-DNA plants (CAC/GL 45-2003). In Foods Derived from Modern Biotechnology, Ed 2 Food and Agriculture Organization/World Health Organization, Rome, pp 1–5, 7–33 [Google Scholar]
- Council of the European Union (2002) Council Directive 2002/53/EC of June 13, 2002 on the common catalogue of varieties of agricultural plant species. Off J Eur Commun L193: 1–11 [Google Scholar]
- Experiment Station Committee on Organization and Policy (2006) 540.79 ESCOP policy statement for developing and releasing improved plants. In Title 190: National Plant Materials Manual. Experiment Station Committee on Organization and Policy, Washington, DC [Google Scholar]
- FAO/WHO (1996) Joint FAO/WHO Expert Consultation on Biotechnology and Food Safety. Food and Agriculture Organization, Rome [Google Scholar]
- FAO/WHO (2000) Safety of Genetically Modified Foods of Plant Origin: Report of a Joint FAO/WHO Expert Consultation on Foods Derived from Biotechnology. World Health Organization, Geneva [Google Scholar]
- Hannah LC. (2005) Starch synthesis in the maize endosperm. Maydica 50: 497–506 [Google Scholar]
- Herrington ME. (1983) Intense bitterness in commercial zucchini. Cucurbit Genet Coop Rep 6: 75–76 [Google Scholar]
- James C. (2011) Global Status of Commercialized Biotech/GM Crops: 2011. ISAAA Brief No. 43. International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY [Google Scholar]
- Stewart A. (2009) Wicked Plants: The Weed that Killed Lincoln’s Mother and Other Botanical Atrocities. Algonquin Books, Chapel Hill, NC [Google Scholar]
- U.S. Food and Drug Administration (1992) Guidance to industry for foods derived from new plant varieties. Fed Regist 57: 22984 [Google Scholar]
Cited by
Sorted by citations
The food and environmental safety of Bt crops
Koch, M. S., Ward, J., Levine, S. L., Baum, J. A., Vicini, J. L., & Hammond, B. G. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00283 · Cited by 228 · see citing works
Genetic basis and detection of unintended effects in genetically modified crop plants
Ladics, G. S., Bartholomaeus, A., Bregitzer, P., Doerrer, N. G., Gray, A. J., Holzhauser, T., Jordan, M. C., Keese, P. K., Kok, E. J., Macdonald, P., et al. (2015) · Transgenic Research · doi:10.1007/s11248-015-9867-7 · Cited by 153 · see citing works
Self-citationSchnell, J., Steele, M., Bean, J., Neuspiel, M., Girard, C., Dormann, N., Pearson, C., Savoie, A., Bourbonnière, L., & Macdonald, P. (2014) · Transgenic Research · doi:10.1007/s11248-014-9843-7 · Cited by 142 · see citing works
Kaiser, N. R., Douches, D. S., Dhingra, A., Glenn, K. C., Herzig, P. R., Stowe, E. C., & Swarup, S. (2020) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2020.03.042 · Cited by 113 · see citing works
Toxicological evaluation of proteins introduced into food crops
Hammond, B., Kough, J., Herouet-Guicheney, C., Jez, J. M., & on behalf of the ILSI International Food Biotechnology Committee Task Force on the Use of Mammalian Toxicology Studies in the Safety Assessment of GM Foods (2013) · Critical Reviews in Toxicology · doi:10.3109/10408444.2013.842956 · Cited by 110 · see citing works
Self-citationNovel features and considerations for ERA and regulation of crops produced by genome editing
Duensing, N., Sprink, T., Parrott, W. A., Fedorova, M., Lema, M. A., Wolt, J. D., & Bartsch, D. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00079 · Cited by 106 · see citing works
Self-citationGlenn, K. C., Alsop, B., Bell, E., Goley, M. E., Jenkinson, J. E., Liu, B., Martin, C. E., Parrott, W. A., Souder, C., Sparks, O. C., et al. (2017) · Crop Science · doi:10.2135/cropsci2017.03.0199 · Cited by 82 · see citing works
Self-citationGenetic Variation and Unintended Risk in the Context of Old and New Breeding Techniques
Singer, S. D., Laurie, J. D., Bilichak, A., Kumar, S., & Singh, J. (2021) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2021.1883826 · Cited by 77 · see citing works
A risk-based approach to the regulation of genetically engineered organisms
Conko, G., Kershen, D. L., Miller, H. I., & Parrott, W. A. (2016) · Nature Biotechnology · doi:10.1038/nbt.3568 · Cited by 68 · see citing works
Self-citationBartholomaeus, A., Parrott, W., Bondy, G., Walker, K., & on behalf of the ILSI International Food Biotechnology Committee Task Force on the Use of Mammalian Toxicology Studies in the Safety Assessment of GM Foods (2013) · Critical Reviews in Toxicology · doi:10.3109/10408444.2013.842955 · Cited by 59 · see citing works
“…evidence that the insertion of a transgene from a non-toxic source into a GM crop has any greater propensity to result in the de novo generation of novel toxic compounds than does the range of conventional plant breeding techniques that currently require no toxicity testing (Steiner et al. 2013).”
BackgroundSelf-citationWang, X., Zhang, X., Yang, J., & Wang, Z. (2018) · The Plant Journal · doi:10.1111/tpj.13825 · Cited by 50 · see citing works
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Strauss, S. H., & Sax, J. K. (2016) · Nature Biotechnology · doi:10.1038/nbt.3541 · Cited by 37 · see citing works
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Kramer, C. M., Brune, P., McDonald, J., Nesbitt, M., Sauve-Ciencewicki, A., & Storck-Weyhermüller, S. (2016) · Plant Biotechnology Journal · doi:10.1111/pbi.12551 · Cited by 25 · see citing works
Rocca, E., & Andersen, F. (2017) · Life Sciences Society and Policy · doi:10.1186/s40504-017-0057-7 · Cited by 25 · see citing works
Molinari, M. D. C., Fuganti‐Pagliarini, R., Florentino, L. H., Lima, R. N., Arraes, F. B. M., Abbad, S. V., de Farias, M. P., Mertz-Henning, L. M., Rech, E. L., Nepomuceno, A. L., et al. (2024) · Interdisciplinary biotechnological advances · doi:10.1007/978-981-99-9338-3_2 · Cited by 24 · see citing works
Taylor, M. L., Bickel, A. D., Mannion, R. M., Bell, E., & Harrigan, G. G. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.7b03844 · Cited by 20 · see citing works
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Andersen, F., & Rocca, E. (2020) · Studies in History and Philosophy of Science Part C Studies in History and Philosophy of Biological and Biomedical Sciences · doi:10.1016/j.shpsc.2020.101335 · Cited by 17 · see citing works
Sherp, A. M., Lee, S. G., Schraft, E. K., & Jez, J. M. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004975 · Cited by 15 · see citing works
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Wang, X., Zhang, X., Yang, J., Liu, X., Song, Y., & Wang, Z. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1956-y · Cited by 14 · see citing works
Bell, E., Nakai, S., & Burzio, L. A. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b02317 · Cited by 14 · see citing works
Single-Event Transgene Product Levels Predict Levels in Genetically Modified Breeding Stacks
Gampala, S. S., Fast, B. J., Richey, K. A., Gao, Z., Hill, R. C., Wulfkuhle, B., Shan, G., Bradfisch, G. A., & Herman, R. A. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.7b03098 · Cited by 13 · see citing works
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Clawson, E. L., Perrett, J. J., Cheng, L. L., Ahmad, A., Stojšin, D., McGowan, Y., Díaz, O. H., Asim, M., Vertuan, H., Quddusi, M., et al. (2019) · Crop Science · doi:10.2135/cropsci2018.12.0758 · Cited by 11 · see citing works
Assuring the Food Safety of Crops Developed through Breeding
Lemke, S. L., Tao, X., & Kushner, G. J. (2022) · ACS Agricultural Science & Technology · doi:10.1021/acsagscitech.2c00268 · Cited by 9 · see citing works
Slewinski, T. L., Turner, S., Paciorek, T., Brower‐Toland, B., & Shyu, C. (2025) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiaf378 · Cited by 7 · see citing works
Bartholomaeus, A., Batista, J. C., Burachik, M., & Parrott, W. A. (2015) · GM crops & food · doi:10.1080/21645698.2015.1011886 · Cited by 7 · see citing works
Self-citationGoodwin, L., Hunst, P., Burzio, L. A., Rowe, L., Money, S., & Chakravarthy, S. (2021) · Journal of Regulatory Science · doi:10.21423/jrs-v09i1goodwin · Cited by 7 · see citing works
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Tagliabue, G. M. (2018) · Life Sciences Society and Policy · doi:10.1186/s40504-018-0089-7 · Cited by 5 · see citing works
José, M., Vertuan, H., Soares, D. J., de Sordi, D., Bellini, L. F., Kotsubo, R. M., & Berger, G. U. (2020) · PLoS ONE · doi:10.1371/journal.pone.0231733 · Cited by 5 · see citing works
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Chemical Composition of Food Products from Genetically Modified Organisms
van Rijssen, W. J., & Morris, E. J. (2014) · Springer eBooks · doi:10.1007/978-3-642-41609-5_24-1 · Cited by 1 · see citing works
Rodríguez, H. D. S., Duarte, D. A. B., Chaparro-Giraldo, A., & Acosta, O. (2022) · Agronomía Colombiana · doi:10.15446/agron.colomb.v40n2.98948 · Cited by 1 · see citing works
A Risk-Based Approach to the Regulation of Genetically Engineered PlantsPreprint
Conko, G., Miller, H. I., & Parrott, W. A. (2016) · SSRN Electronic Journal · doi:10.2139/ssrn.2971485
Self-citationSul, S.-Y., Suh, S., Park, S.-B., & Kim, H. (2021) · Food Science and Biotechnology · doi:10.1007/s10068-021-01004-9 · Cited by 1 · see citing works
Chemical Composition of Food Products from Genetically Modified Organisms
van Rijssen, W. J., & Morris, E. J. (2015) · Springer eBooks · doi:10.1007/978-3-642-36605-5_24
Sun, Y., Chen, H., Chen, Z., Wang, C., Qin, L., Lin, X., Yicong, C., Zhou, D., Ouyang, L., Zhu, C., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1660011/v1
Sun, Y., Chen, H., Chen, Z., Wang, C., Qin, L., Lin, X., Cai, Y., Zhou, D., Ouyang, L., Zhu, C., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1660011/v2
Sun, Y., Chen, H., Chen, Z., Wang, C., Li, B., Lin, X., Cai, Y., Zhou, D., Ouyang, L., Zhu, C., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1660011/v3
Translocation of Insecticidal Bt Protein in Transgrafted Plants
Ando, A., Ohkubo, H., Maki, H., Nishiuchi, T., Ogawa, T., Mochizuki, T., Ohta, D., Kodama, H., & Miyahara, T. (2025) · BioTech · doi:10.3390/biotech14030064
- Authors
- Steiner, H.-Y., Halpin, C., Jez, J. M., Kough, J., Parrott, W., Underhill, L., Weber, N., & Hannah, L. C.
- Affiliations
- Herbicides, Arysta Life Science, Cary, North Carolina 27513
- James Hutton Institute (GB)
- Washington University in St. Louis (US)
- Environmental Protection Agency (US)
- University of Georgia (US)
- Health Canada (CA)
- Pioneer Hi-Bred (US)
- University of Florida (US)
- Venue
- Plant Physiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-03-04
- Volume
- 161
- Issue
- 4
- Pages
- 1587-1594
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC3613440
- OpenAlex
- W2063273303
- Cited by
- 46
- References
- 36
- Citations by year
- 2025: 4 · 2024: 1 · 2023: 2 · 2022: 6 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 7 · 2016: 4 · 2015: 4 · 2014: 2 · 2013: 2
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- PLANT PHYSIOLOGY (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
- Life Sciences › Agricultural and Biological Sciences › Food Science › Agricultural safety and regulations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Animal Genetics and Reproduction
- Keywords
- food safety, feed safety, genomic instability, conventional breeding, genetically modified crops, transgene stability, history of plant breeding, somaclonal variation, mutagenesis, somatic hybridization, embryo rescue, wide crosses
- MeSH terms
- Breeding, Genetic Engineering, Plants, Plants, Genetically Modified, Food Safety
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