Evaluating the Potential for Adverse Interactions Within Genetically Engineered Breeding Stacks

Task Force #9

Plant Physiology. 2013;161:1587-1594

Abstract: Crops containing a single transgenic event are subjected to extensive safety assessments before authorization. These assessments evaluate the resulting phenotype for food and feed safety, cognizant that the phenotype is the result of interactions of the transgenes and their products with the tens of thousands of endogenous genes and their products. Genetically engineered (GE) stacks (also known as stacked or combined events) are produced by combining two or more single transgenic events by conventional breeding. The potential for interactions between the products of the events in a GE stack that impact food and feed safety can be evaluated in the context of conventional breeding of non-GE plants. Conventional breeding recombines tens of thousands of genes and alleles in the genome, and does so with a long history of safety. The numerous interactions between the products of endogenous genes are largely unknown and therefore currently do not lend themselves to experimental testing. In contrast, the functions of transgenes are known in great detail relative to endogenous genes, so such evaluation can be based on testable hypotheses concerning possible interactions between single events in a stack. Since interactions between events and the endogenous genes were evaluated for single events, safety assessment of GE stacks should focus on potential interactions between the products of the transgenes. Guiding questions are provided for consideration in formulating hypotheses regarding food and feed safety issues resulting from interactions between the products of combined events, and examples are included to aid in clarifying the use of these questions.

To download this article, click here.

References

• Ames BN, Profet M, Gold LS (1990) Dietary pesticides (99.99% all natural). Proc Natl Acad Sci USA 87: 7777–7781 LINK
• Anonymous (1970) Name of potato variety Lenape withdrawn. Am J Potato Res 47: 103 LINK
• 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. ASULGC, Washington, DC. LINK
• Auger DL, Gray AD, Ream TS, Kato A, Coe EH Jr, Birchler JA (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169: 389–397 LINK
• Beier RC (1990) Natural pesticides and bioactive components in foods. In GW Ware, ed, Reviews of Environmental Contamination and Toxicology. Springer-Verlag, New York and Heidelberg, pp 47–137
• Berkley SF, Hightower AW, Beier RC, Fleming DW, Brokopp CD, Ivie GW, Broome CV (1986) Dermatitis in grocery workers associated with high natural concentrations of furanocoumarins in celery. Ann Intern Med 105: 351–355 LINK
• Buchanan B, Gruissem W, Jones R (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Biologists
• Canadian Food Inspection Agency, Feed Division (2006) Regulation of Novel Feeds. http://www.inspection.gc.ca/english/anima/feebet/bio/regulatione.shtml (last accessed December 2010) LINK
• Cellini F, Chesson A, Colquhoun I, Constable A, Davies HV, Engel KH, Gatehouse AM, Kärenlampi S, Kok EJ, Leguay JJ, Lehesranta S, Noteborn HP, Pedersen J, Smith M (2004) Unintended effects and their detection in genetically modified crops. Food Chem Toxicol 42: 1089–1125 LINK
• 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) from Foods Derived from Modern Biotechnology, FAO/WHO, Rome, pp. 1–5, 7–33. LINK
• Council of the European Union (2002) Council Directive 2002/53/EC of 13 June 2002 on the common catalogue of varieties of agricultural plant species. Off J Eur Union L2. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2002:193:0001:0011: EN:PDF (last accessed 2011 April 5) LINK
• Delaney B, Astwood JD, Cunny H, Eichen Conn R, Herouet-Guicheney C, MacIntosh S, Meyer Linda S, Privalle L, Gao, Y, Mattson J (2008) Evaluation of protein safety in the context of agricultural biotechnology. Food Chem Toxicol 46: S71–S97 LINK
• D’Mello JPF, Duffus CM, Duffus JH, eds (1991) Toxic Substances in Crop Plants. Royal Society of Chemistry, Cambridge, UK
• Drewnowski A, Gomez-Carneros C (2000) Bitter taste, phytonutrients, and the consumer: a review. Am J Clin Nutr 72: 1424–1435 LINK
• 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. ESCOP, Washington, DC LINK
• Finkelstein E, Afek U, Gross E, Aharoni N, Rosenberg L., Halevy S. 1994. An outbreak of phytophotodermatitis due to celery. Int J Dermatol 33: 116–118. LINK
• [FAO/WHO] Food and Agriculture Organization of the United Nations and the World Health Organization (1996) joint FAO/WHO Expert Consultation on Biotechnology and Food Safety, FAO, Rome, Italy. ftp://ftp.fao.org/es/esn/food/biotechnology.pdf LINK
• [FAO/WHO] Food and Agriculture Organization of the United Nations and the World Health Organization (2000) Safety of genetically modified foods of plant origin: Report of a joint FAO/WHO Expert Consultation on Foods Derived from Biotechnology. WHO, Geneva Switzerland. http://www.who.int/foodsafety/publications/biotech/en/ec_june2000_en.pdf LINK
• Groszmann, M, Greaves IK, Albertyn ZI, Scofield GN, Peacock WJ, Dennis ES (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc. Natl. Acad. Sci. 108: 2617–2622 LINK
• Hannah LC (2005) Starch synthesis in the maize endosperm. Maydica 50: 497–506 LINK
• Hannah LC (2007) Starch formation in the maize endosperm. In O-A Olsen, ed, Endosperm, Developmental and Molecular Biology. Springer Books, New York, pp 179–194
• Hannah LC, James M (2008) The complexities of starch biosynthesis in cereal endosperms. Curr Opin Biotechnol 19: 160–165 LINK
• Health Canada Food Directorate (2006) Guidelines for the safety assessment of novel foods, http://www.novelfoods.gc.ca (last accessed December 2010) LINK
• Herrington ME (1983) Intense bitterness in commercial zucchini. Cucurbit Genetics Cooperative Report 6:75–76 LINK
• Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12: 427–432 LINK
• [ILSI] International Life Sciences Institute (2006) Crop Composition Database. Version 3.0. http://www.cropcomposition.org (last accessed 2011 March 31) LINK
• Jadav SJ, Sharma RP, Salunkhe DK (1981) Naturally occurring toxic alkaloids in foods. In CRC Critical Reviews in Toxicology, p. 21–104 LINK
• James C (2010) Global Status of Commercialized Biotech/GM Crops: 2010. ISAAA Brief No. 42. ISAAA: Ithaca, NY LINK
• Keurentjes JJ, Fu J, de Vos CH, Lommen A, Hall RD, Bino RJ, van der Plas LH, Jansen RC, Vreugdenhil D, Koornneef M (2006) The genetics of plant metabolism. Nat Genet 38: 842–849 LINK
• Kuiper HA, Kleter GA, Noteborn HP, Kok EJ (2001) Assessment of the food safety issues related to genetically modified foods. Plant J 27: 503–528 LINK
• Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, Wang J (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42: 1027–1030 LINK
• Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, et al (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42: 1053–1059 LINK
• Laurila J, Laakso I, Valkonen JPT, Hiltunen R, Pehu E (1996) Formation of parental-type and novel glycoalkaloids in somatic hybrids between Solanum brevidens and S. tuberosum. Plant Science 118: 145–155 LINK
• Metcalfe, DD Astwood, JD, Townsend, R, Sampson, HA, Taylor, SL, Fuchs, RL (1996) Assessment of the allergenic potential of foods derived from genetically engineered Crop Plants. Critical Reviews in Food Science and Nutrition 36(S): S165-S186. LINK
• Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, Bak S (2008) Beta-glucosidases as detonators of plant chemical defense. Phytochemistry 69: 1795–1813 LINK
• Parrott W, Chassy B, Ligon J, Meyer L, Petrick J, Zhou J, Herman R, Delaney B, Levine M (2010) Application of food and feed safety assessment principles to evaluate transgenic approaches to gene modulation in crops. Food Chem Toxicol 48: 1773–1790 LINK
• Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189–195. LINK
• Que Q, Chilton M-D, de Fontes CM, He C, Nuccio M, Zhu T, Wu Y, Chen JS, Shi L (2010) Trait stacking in transgenic crops: Challenges and opportunities. GM Crops 1: 220–229 LINK
• Ridley WP, Shillito RD, Coats I, Steiner H-Y, Shawgo M, Phillips A, Dussold P, Kurtyka L (2004) Development of the International Life Sciences Institute Crop Composition Database. J Food Comp Anal 17: 423–438 LINK
• Rymal KS, Chambliss OL, Bond MD, Smith DA (1984) Squash containing toxic cucurbitacin compounds occuring in California and Alabama. Journal of Food Protection 47: 270–271. LINK
• Seligman PJ, Mathias CG, O’Malley MA, Beier RC, Fehrs LJ, Serrill WS, Halperin WE (1987) Phytophotodermatitis from celery among grocery store workers. Arch Dermatol. 123: 1478–1482 LINK
• Springer NM, Ying K, Fu Y, Ji T, Yeh CT, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H, Iniguez AL, Barbazuk WB, Jeddeloh JA, Nettleton D, Schnable PS (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 5: e1000734. LINK
• Stevens MA (1974) Breeding for safety in vegetables and fruits. In CH Hanson, ed, The Effect of FDA Regulations (GRAS) on Plant Breeding and Processing. Crop Science Society of America, Madison, WI, pp 47–63 LINK
• Stewart A (2009) Wicked Plants: The Weed that Killed Lincoln’s Mother and Other Botanical Atrocities. Algonquin Books, Chapel Hill, NC LINK
• Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103: 6805–6810 LINK
• Thomas K, MacIntosh S, Bannon G, Herouet-Guicheney C, Holsapple M, Ladics G, McClain S, Vieths S, Woolhiser M, Privalle L (2009) Scientific advancement of novel protein allergenicity evaluation: an overview of work from the HESI Protein Allergenicity Technical Committee (2000–2008). Food Chem Toxicol 47: 1041–1050 LINK
• US Food and Drug Administration (1992) Guidance to industry for foods derived from new plant varieties. Fed Regist 57: 22984 LINK
• Weber N, Halpin C, Hannah, LC, Jez, JM, Kough, J. and Parrott W. (2012) Crop Genome Plasticity and Its Relevance to Food and Feed Safety of Genetically Engineered Breeding Stacks. Plant Physiol, 160: 1842–1853 LINK