Streamlining Data Requirements for the Environmental Risk Assessment of Genetically Modified (GM) Crops for Cultivation Approvals
DOI:
https://doi.org/10.21423/JRS-V09I1ANDERSONKeywords:
environmental risk assessment, genetically modified plant, problem formulation, data requirements, cultivationAbstract
Genetically modified (GM) crops have been cultivated safely for more than 25 years, and the framework for conducting an environmental risk assessment (ERA) is well-established. Currently, there is alignment of broadly-stated protection goals across global jurisdictions; however, there is a lack of consistency for the data that are required by regulators. Risk assessors have over 25 years of collective experience assessing the environmental safety of GM crops and have conducted hundreds of ERAs to evaluate GM crop safety. This experience provides a scientific basis to help determine which data informs the ERA, and which data does not inform the safety assessment. The goals of this paper are to: 1) define the process for identifying potential pathways to harm based on robust problem formulation; 2) provide an overview of data that inform the science-based ERA for cultivation approval; 3) provide examples of data that are routinely or occasionally required but do not inform the ERA; and 4) make recommendations for harmonization of global ERA data requirements. Refinement and harmonization of data requirements across global regulatory authorities will add transparency and predictability to the ERA of GM crops globally, while ensuring that each country's protection goals are respected.
doi: 10.21423/jrs-v09i1anderson
References
Albright, V. C., III., Wong, C. R., Hellmich, R. L., & Coats, J. R. (2017). Dissipation of double‐stranded RNA in aquatic microcosms. Environmental Toxicology and Chemistry, 36(5), 1249-1253. https://www.doi.org/10.1002/etc.3648
Alix, A., Bakker, F., Barrett, K., Bruhl, C. A., Coulson, M., Hoy, S., Jansen, J-P., Jepson, P. C., Lewis, G., Neumann, P., Sussenbach, D., & van Vliet, P. J. (2012, January). ESCORT 3: Linking Non-Target Arthropod Testing and Risk Assessment with Protection Goals. CRC SETAC Press.
Anderson, J. A., Gipmans, M., Hurst, S., Layton, R., Nehra, N., Pickett, J., Shah, D. M., Souza, T. L. P. O., & Tripathi, L. (2016). Emerging Agricultural Biotechnologies for Sustainable Agriculture and Food Security. Journal of Agricultural and Food Chemistry, 64(2), 383-393. https://www.doi.org/10.1021/acs.jafc.5b04543
Bachman, P. M., Burns, A., Chakravarthy, S., Goodwin, L., Privalle, L., Song, S., Storer, N., & Anderson, J. (2021). Data Transportability for Studies Performed to Support an Environmental Risk Assessment for Genetically Modified (GM) Crops. Journal of Regulatory Science, 9(1), 38-44. doi: XXX
Baker, H. G. (1965). Characteristics and Modes of Origin of Weeds. In H. G. Baker, G. L. Stebbins (Eds.). Genetics of Colonizing Species (p. 147-172). Academic Press.
Baker, H. G. (1974). The Evolution of Weeds. Annual Review of Ecology and Systematics, 5(1), 1-24. https://www.doi.org/10.1146/annurev.es.05.110174.000245
Biotechnology Regulatory Services & Biopesticides and Pollution Prevention Division. (2007). White Paper on Tier-Based Testing for the Effects of Proteinaceous Insecticidal Plant-Incorporated Protectants on Non-Target Arthropods for Regulatory Risk Assessments. United States Department of Agriculture Animal Plant Health Inspection Service, United States Environmental Protection Agency. Retrieved from https://www.epa.gov/sites/production/files/2015-09/documents/tier-based-testing.pdf
Brink, K., Anitha, S. C., Beatty, M. K., Anderson, J. A., Lyon, M., Weaver, J., & Dietrich, N. (2019). Comparison of Southern-by-Sequencing (SbSTM) technology and Southern Blot Analysis for Molecular Characterization of Genetically Modified Crops. Journal of Regulatory Science, 7, 1-14. https://www.doi.org/10.21423/jrs-v07brink
Brune, P., Chakravarthy, S., Graser, G., Mathesius, C., McClain, S., Petrick, J. S., Sauve-Ciencewicki, A., Schafer, B., Silvanovich, A., Brink, K., Burgin, K.,Bushey, D., Cheever, M. L., Edrington, T., Fu, H., Habex, V., Herman, R., Islamovic, E., Lipscomb, E. A., Motyka, S., Privalle, L., Ranjan, R., Roper, J., Song, P., Tilton, G., Zhang, J., Waters, S., Ramos, A., Culler, A. H., Hunst, P., Gast, R., Mahadeo, D., & Goodwin, L. (2021). Core and supplementary studies to assess the safety of genetically modified (GM) plants used for food and feed. Journal of Regulatory Science, 9(1), 45-60. doi: XXX
Cade, R., Burgin, K., Schilling, K., Lee, T-J., Ngam, P., Devitt, N., & Fajardo, D. (2018). Evaluation of Whole Genome Sequencing and an Insertion Site Characterization Method for Molecular Characterization of GM Maize. Journal of Regulatory Science, 6(1), 1-14. https://www.doi.org/10.21423/jrs-v06n01p001
Canadian Food Inspection Agency. (1994). The Biology of Zea mays (L.) (Maize). Retrieved from https://www.inspection.gc.ca/plant-varieties/plants-with-novel-traits/applicants/directive-94-08/biology-documents/zea-mays-l-/eng/1330985739405/1330985818367
Clark, B. W., Phillips, T. A., & Coats, J. R. (2005). Environmental Fate and Effects of Bacillus thuringiensis (Bt) Proteins from Transgenic Crops: a Review. Journal of Agricultural and Food Chemistry, 53(12), 4643-4653. https://www.doi.org/10.1021/jf040442k
Codex Alimentarius Commission. (2009). Foods derived from modern biotechnology, Second edition. Food and Agriculture Organization of the United Nations and World Health Organization, Rome. Retrieved from http://www.fao.org/3/a-a1554e.pdf
Cong, B., Maxwell, C., Luck, S., Vespestad, D., Richard, K., Mickelson, J., & Zhong, C. (2015). Genotypic and Environmental Impact on Natural Variation of Nutrient Composition in 50 Non Genetically Modified Commercial Maize Hybrids in North America. Journal of Agricultural and Food Chemistry, 63(22), 5321-5334. https://www.doi.org/10.1021/acs.jafc.5b01764
CropLife International. (2017). Plant Biotechnology Pipeline. Retrieved from https://croplife.org/wp-content/uploads/2017/09/CropLifePlantBiotechPipeline2017_V5.pdf
CropLife International. (n.d.). Agricultural Innovation. Retrieved from https://croplife.org/agricultural-innovation/
de Vries, J., & Wackernagel, W. (2005). Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant and Soil, 266(1), 91-104. https://www.doi.org/10.1007/s11104-005-4783-x
Delaney, B., Astwood, J. D., Cunny, H., Conn, R. E., Herouet-Guicheney, C., MacIntosh, S., Meyer, L. S., Privalle, L., Gao, Y., Mattsson, J., & Levine, M. (2008). Evaluation of protein safety in the context of agricultural biotechnology. Food and Chemical Toxicology, 46(Suppl 2), S71-S97. https://www.doi.org/10.1016/j.fct.2008.01.045
Devos, Y., Romeis, J., Luttik, R., Maggiore, A., Perry, J. N., Schoonjans, R., Streissl, F., Tarazona, J. V., & Brock, T. C. M. (2015). Optimising environmental risk assessments: Accounting for ecosystem services helps to translate broad policy protection goals into specific operational ones for environmental risk assessments. EMBO Reports, 16(9), 1060-1063. https://www.doi.org/10.15252/embr.201540874
Dubelman, S., Fischer, J., Zapata, F., Huizinga, K., Jiang, C., Uffman, J., Levine, S., & Carson, D. (2014). Environmental Fate of Double-Stranded RNA in Agricultural Soils. PLoS One, 9(3), e93155. https://www.doi.org/10.1371/journal.pone.0093155
EFSA Panel on Genetically Modified Organisms. (2011). Guidance for risk assessment of food and feed from genetically modified plants. EFSA Journal, 9(5). https://www.doi.org/10.2903/j.efsa.2011.2150
Fischer, J. R., Zapata, F., Dubelman, S., Mueller, G. M., Jensen, P. D., & Levine, S. L. (2016). Characterizing a novel and sensitive method to measure dsRNA in soil. Chemosphere, 161, 319-324. https://www.doi.org/10.1016/j.chemosphere.2016.07.014
Fischer, J. R., Zapata, F., Dubelman, S., Mueller, G. M., Uffman, J. P., Jiang, C., Jensen, P. D., & Levine, S. L. (2017). Aquatic fate of a double‐stranded RNA in a sediment-water system following an over-water application. Environmental Toxicology and Chemistry, 36(3), 727-734. https://www.doi.org/10.1002/etc.3585
Garcia-Alonso, M., & Raybould, A. (2014). Protection goals in environmental risk assessment: a practical approach. Transgenic Research, 23(6), 945-956. https://www.doi.org/10.1007/s11248-013-9760-1
Glenn, K. C., Alsop, B., Bell, E., Goley, M., Jenkinson, J., Liu, B., Martin, C., Parrott, W., Souder, C., Sparks, O., Urquhart, W., Ward, J. M., & Vicini, J. L. (2017). Bringing New Plant Varieties to Market: Plant Breeding and Selection Practices Advance Beneficial Characteristics while Minimizing Unintended Changes. Crop Science, 57(6), 2906-2921. https://www.doi.org/10.2135/cropsci2017.03.0199
Guttikonda, S. K., Marri, P., Mammadov, J., Ye, L., Soe, K., Richey, K., Cruse, J., Zhuang, M., Gao, Z., Evans, C., Rounsley, S., & Kumpatla, S. P. (2016). Molecular Characterization of Transgenic Events Using Next Generation Sequencing Approach. PLoS One, 11(2), e0149515. https://www.doi.org/10.1371/journal.pone.0149515
Herman, R. A., Wolt, J. D., & Halliday, W. R. (2002). Rapid degradation of the Cry1F insecticidal crystal protein in soil. Journal of Agricultural and Food Chemistry, 50(24), 7076-7078. https://www.doi.org/10.1021/jf025630u
bibitem{icoz2008} Icoz, I., & Stotzky, G. (2008). Fate and effects of insect-resistant Bt crops in soil ecosystems. emph{Soil Biology and Biochemistry, 40}(3), 559-586. https://www.doi.org/10.1016/j.soilbio.2007.11.002
ILSI Research Foundation. (2014). Low-Level Presence in Seed: A Science Based Approach to Expedited Environmental Risk Assessment [Workshop]. Presented at the Center for Environmental Risk Assessment (CERA), Washington, D.C.
International Service for the Acquisition of Agri-biotech Applications. (2018). Global Status of Commercialized Biotech/GM Crops: 2018 (Brief 54). International Service for the Acquisition of Agri-biotech Applications. Retrieved from https://www.isaaa.org/resources/publications/briefs/54/executivesummary/pdf/B54-ExecSum-English.pdf
Keese, P. (2008). Risks from GMOs due to Horizontal Gene Transfer. Environmental Biosafety Research, 7(3), 123-149. https://www.doi.org/10.1051/ebr:2008014
Kovalic, D., Garnaat, C., Guo, L., Yan, Y., Groat, J., Silvanovich, A., Ralston, L., Huang, M., Tian, Q., Christian, A., Cheikh, N., Hjelle, J., Padgette, S., & Bannon, G. (2012). The Use of Next Generation Sequencing and Junction Sequence Analysis Bioinformatics to Achieve Molecular Characterization of Crops Improved Through Modern Biotechnology. The Plant Genome, 5(3), 149-163. https://www.doi.org/10.3835/plantgenome2012.10.0026
Marchetti, E., Accinelli, C., Talame, V., & Epifani, R. (2007). Persistence of Cry toxins and cry genes from genetically modified plants in two agricultural soils. Agronomy for Sustainable Development, 27, 231-236. https://www.doi.org/10.1051/agro:2007010
Mendelsohn, M., Kough, J., Vaituzis, Z., & Matthews, K. (2003). Are Bt crops safe? Nature Biotechnology, 21(9), 1003-1009. https://www.doi.org/10.1038/nbt0903-1003
Organisation for Economic Co-operation and Development. (2000). Series on Harmonization of Regulatory Oversight in Biotechnology, No. 15. Consensus document on the biology of Glycine max (L.) Merr. (Soybean), ENV/JM/MONO(2000)9, 1-22. Retrieved from https://www.oecd.org/env/ehs/biotrack/46815668.pdf
Organisation for Economic Co-operation and Development. (2003). Series on Harmonisation of Regulatory Oversight in Biotechnology, No. 27. Consensus Document on the Biology of Zea mays subsp. mays (Maize), ENV/JM/MONO(2003)11, 1-49. Retrieved from https://www.oecd.org/env/ehs/biotrack/46815758.pdf
Organisation for Economic Co-operation and Development. (2008). Series on Harmonisation of Regulatory Oversight in Biotechnology, No. 45. Consensus document on the biology of Cotton (Gossypium spp.), ENV/JM/MONO(2008)33, 1-64. Retrieved from https://www.oecd.org/env/ehs/biotrack/46815918.pdf
Organisation for Economic Co-operation and Development. (2012). Series on Harmonisation of Regulatory Oversight in Biotechnology, No. 54. Consensus document on the biology of Brassica crops (Brassica spp.), ENV/JM/MONO(2012)41, 1-142. Retrieved from http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2012)41&doclanguage=en
Parker, K. M., Borrero, V. B., van Leeuwen, D. M., Lever, M. A., Mateescu, B., & Sander, M. (2019). Environmental Fate of RNA Interference Pesticides: Adsorption and Degradation of Double-Stranded RNA Molecules in Agricultural Soils. Environmental Science & Technology, 53(6), 3027-3036. https://www.doi.org/10.1021/acs.est.8b05576
Raybould, A. (2006). Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops. Environmental Biosafety Research, 5(3), 119-125. https://www.doi.org/10.1051/ebr:2007004
Roberts, A. (2011). Information tools for environmental risk assessment of low level presence - an introduction to the reviews of the environmental safety of proteins used in genetically engineered plants. Environmental Biosafety Research, 10(1), 1-3. https://www.doi.org/10.1051/ebr/2012005
Roberts, A., Devos, Y., Raybould, A., Bigelow, P., & Gray, A. (2014). Environmental risk assessment of GE plants under low-exposure conditions. Transgenic Research, 23(6), 971-983. https://www.doi.org/10.1007/s11248-013-9762-z
Romeis, J., Bartsch, D., Bigler, F., Candolfi, M. P., Gielkens, M. M., Hartley, S. E., Hellmich, R. L., Huesing, J. E., Jepson, P. C., Layton, R., Quemada, H., Raybould, A., Rose, R. I., Schiemann, J., Sears, M. K., Shelton, A. M., Sweet, J., Vaituzis, Z., & Wolt, J. D. (2008). Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nature Biotechnology, 26(2), 203-208. https://www.doi.org/10.1038/nbt1381
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., Shelton, A. M., & Waggoner, A. (2011). Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Research, 20(1), 1-22. https://www.doi.org/10.1007/s11248-010-9446-x
Romeis, J., & Meissle, M. (2011). Non‐target risk assessment of Bt crops - Cry protein uptake by aphids. Journal of Applied Entomology, 135(1‐2), 1-6. https://www.doi.org/10.1111/j.1439-0418.2010.01546.x
Romeis, J., Raybould, A., Bigler, F., Candolfi, M. P., Hellmich, R. L., Huesing, J. E., & Shelton, A. M. (2013). Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops. Chemosphere, 90(3), 901-909. https://www.doi.org/10.1016/j.chemosphere.2012.09.035
Sanvido, O., Romeis, J., Gathmann, A., Gielkens, M., Raybould, A., & Bigler, F. (2012). Evaluating environmental risks of genetically modified crops: ecological harm criteria for regulatory decision-making. Environmental Science & Policy, 15}(1), 82-91. https://www.doi.org/10.1016/j.envsci.2011.08.006
Schellenberger, U., Oral, J., Rosen, B. A., Wei, J-Z., Zhu, G., Xie, W., McDonald, M. J., Cerf, D. C., Diehn, S. H., Crane, V. C., Sandahl, G. A., Zhao, J-Z., Nowatzki, T. M., Sethi, A., Liu, L., Pan, Z., Wang, Y., Lu, A. L., Wu, G., & Liu, L. (2016). A selective insecticidal protein from Pseudomonas for controlling corn rootworms. Science, 354(6312), 634-637. https://www.doi.org/10.1126/science.aaf6056
Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J. A., Feitelson, J., Zeigler, D. R., & Dean, D. (1998). Bacillus thuringiensis and Its Pesticidal Crystal Proteins. Microbiology and Molecular Biology Reviews, 62(3), 775-806. https://www.doi.org/10.1128/MMBR.62.3.775-806.1998
Shan, G., Embrey, S. K., Herman, R. A., & McCormick, R. (2014). Cry1F Protein Not Detected in Soil After Three Years of Transgenic Bt Corn (1507 Corn) Use. Environmental Entomology, 37(1), 255-262. https://www.doi.org/10.1603/0046-225X(2008)37[255:CPNDIS]2.0.CO;2
Shaw, R. H. (1988). Climate Requirement. In G. Sprague & J. W. Dudley (Eds.), Corn and Corn Improvement (Volume 18, Third Edition, pp. 609-638). American Society of Agronomy, Inc., Crop Science Society of America, Inc., Soil Science Society of America, Inc. https://www.doi.org/10.2134/agronmonogr18.3ed.c10
Shelton, A. M. (2010). The long road to commercialization of Bt brinjal (eggplant) in India. Crop Protection, 29(5), 412-414. https://www.doi.org/10.1016/j.cropro.2010.02.016
Stotzky, G. (2005). Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants. Plant and Soil, 266(1), 77-89. https://www.doi.org/10.1007/s11104-005-5945-6
Tripathi, L., Tripathi, J. N., & Tushemereirwe, W. K. (2004). Strategies for resistance to bacterial wilt disease of bananas through genetic engineering. African Journal of Biotechnology, 3(12), 688-692.
U.S. Environmental Protection Agency. (1998). Guidelines for Ecological Risk Assessment, EPA/630/R-95/002F. Retrieved from https://www.epa.gov/sites/production/files/2014-11/documents/eco_risk_assessment1998.pdf
Van Frankenhuyzen, K. (2009). Insecticidal activity of Bacillus thuringiensis crystal proteins. Journal of Invertebrate Pathology, 101(1), 1-16. https://www.doi.org/10.1016/j.jip.2009.02.009
Waltz, E. (2015). USDA approves next-generation GM potato. Nature Biotechnology, 33, 12-13. https://www.doi.org/10.1038/nbt0115-12
Wolt, J. D., Keese, P., Raybould, A., Fitzpatrick, J. W., Burachik, M., Gray, A., Olin, S. S., Schiemann, J., Sears, M., & Wu, F. (2010). Problem formulation in the environmental risk assessment for genetically modified plants. Transgenic Research, 19(3), 425-436. https://www.doi.org/10.1007/s11248-009-9321-9
World Health Organization & Food and Agriculture Organization of the United Nations. (1991). Strategies for assessing the safety of foods produced by biotechnology: report of a joint FAO/WHO consultation [held in Geneva from 5 to 10 November 1990]. Retrieved from https://apps.who.int/iris/bitstream/handle/10665/41465/9241561459-eng.pdf?sequence=1&isAllowed=y
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