Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T21:00:56.340Z Has data issue: false hasContentIssue false
  • English
  • Français

Biosafety considerations for selectable and scorable markers used in cassava (Manihot esculenta Crantz) biotechnology

Published online by Cambridge University Press:  15 November 2005

William Petersen ,
Paul Umbeck ,
Karen Hokanson  and
Mark Halsey
William Petersen
Affiliation:
Umbeck & Associates, Madison, WI 53717, USA
Paul Umbeck
Affiliation:
Umbeck & Associates, Madison, WI 53717, USA
Karen Hokanson
Affiliation:
University of Minnesota, St Paul, MN 55108, USA
Mark Halsey
Affiliation:
Donald Danforth Plant Science Center, St Louis, MO 63132, USA

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Cassava is an important subsistence crop grown only in the tropics, and represents a major source of calories for many people in developing countries. Improvements in the areas of resistance to insects and viral diseases, enhanced nutritional qualities, reduced cyanogenic content and modified starch characteristics are urgently needed. Traditional breeding is hampered by the nature of the crop, which has a high degree of heterozygosity, irregular flowering, and poor seed set. Biotechnology has the potential to enhance crop improvement efforts, and genetic engineering techniques for cassava have thus been developed over the past decade. Selectable and scorable markers are critical to efficient transformation technology, and must be evaluated for biosafety, as well as efficiency and cost-effectiveness. In order to facilitate research planning and regulatory submission, the literature on biosafety aspects of the selectable and scorable markers currently used in cassava biotechnology is surveyed. The source, mode of action and current use of each marker gene is described. The potential for toxicity, allergenicity, pleiotropic effects, horizontal gene transfer, and the impact of these on food or feed safety and environmental safety is evaluated. Based on extensive information, the selectable marker genes nptII, hpt, bar/pat, and manA, and the scorable marker gene uidA, all have little risk in terms of biosafety. These appear to represent the safest options for use in cassava biotechnology available at this time.

Keywords

cassavabiotechnologytransgenicsselectable markersscorable markers
Type
Research Article
Information
Environmental Biosafety Research , Volume 4 , Issue 2 , April 2005 , pp. 89 - 102
Copyright
© ISBR, EDP Sciences, 2005

References

Advisory Committee on Releases to the Environment's (ACRE’s) response to concerns raised in written representations and submissions associated with the CHARDON LL public hearing and to statements made at ACRE’s open hearing relating to the safety assessment of T25 GM maize conducted under Directive 90/220/EEC. (2002) http://www.defra.gov.uk/environment/acre/advice/pdf/acre_advice20.pdf
Alonso J, Barredo JL, Diez B, Mellado E, Salto F, Garcia JL, Cortes E (1998) D- Amino-acid oxidase gene from Rhodotorula gracilis (Rhodosporidium toruloides) ATCC 26217. Microbiology 144: 1095–1101 CrossRef
Aragão FJL, Brasileiro ACM (2002) Positive, negative and marker-free strategies for transgenic plant selection. Braz. J. Plant Physiol. 14: 1–10
Astwood JD, Fuchs RL (1996) Allergenicity of foods derived from transgenic plants. In Wuthrich B, Ortolani C, eds, Highlights in Food Allergy, Monogr. Allergy 32: 105–120
Australia New Zealand Food Authority (2001) Food derived from insect protected (New Leaf®) Potato lines BT-06, ATBT04-06, ATBT04-31, ATBT04-36,and SPBT02-05; A Safety Assessment. Technical Report Series No. 11
Beck, E, Ludwig, G, Auerswald, EA, Reiss, B, Schaller, H (1982) Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn5. Gene 9: 327–336 CrossRef
Bevan, MW, Flavell, RB, Chilton, M-D (1983) A chimaeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304: 184–187 CrossRef
Brasileiro, ACM, Aragão, FJL (2001) Marker genes for in vitro selection of transgenic plants. J. Plant Biotechnol. 3: 113–121
Canadian Food Inspection Agency, Plant Health and Production Division, Decision Document DD98-28 (1998) Determination of the Safety of AgrEvo Canada Inc.'s Glufosinate Ammonium Herbicide-Tolerant Brassica rapa Canola Line HCR-1. http://www.inspection.gc.ca/english/plaveg/bio/dd/dd9828e.shtml
Canadian Food Inspection Agency, Plant Products Directorate Plant Biosafety Office, Decision Document DD2004-49 (2004) Determination of the Safety of Bayer CropScience's Herbicide Tolerant LibertyLink® Cotton Event LLcotton25 (Gossypium hirsutum L.). http://www.inspection.gc.ca/english/plaveg/bio/dd/dd0449e.shtml
Cellini, F, Chesson, A, Colquhoun, I, Constable, A, Davies, HV, Engel, KH, Gatehouse, AMR, Karenlampi, S, Kok, EJ, Leguay, J-J, Lehesranta, S, Noteborn, HPJM, Pedersen, J, Smith, M (2004) Unintended effects and their detection in genetically modified crops. Food Chem. Toxicol. 42: 1089–1125 CrossRef
Chalfie, M (1995) Green Fluorescent Protein. Photochem. Photobiol. 62: 651–656 CrossRef
Chalfie, M, Tu, Y, Euskirchen, G, Ward, WW, Prasher, DC (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802–805 CrossRef
Chavarriaga P (2005) Personal communication
Codex Alimentarius Commission Alinorm 03/34, Joint FAO/WHO Food Standard Programme Codex Alimentarius Commission, Twenty-fifth session, Rome Italy (2003) Report of the Third Session of the CODEX Ad Hoc Intergovernmental Task Force on Foods Derived From Biotechnology, Yokohama, Japan 4–8 March 2002. Appendix IV:57-60. http://www.codexalimentarius.net/download/report/46/Al0334ae.pdf
DeBlock, M, De Brower, D, Tenning, P (1989) Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in the transgenic plants. Plant Physiol. 91: 694–701 CrossRef
de Vetten, N, Wolters, AM, Raemakers, K, van der Meer, I, ter Stege, R, Heeres, E, Heeres, P, Visser, R (2003) A transformation method for obtaining marker-free plants of a cross-pollinating and vegetatively propagated crop. Nat. Biotechnol. 21: 439–442 CrossRef
Environmental Protection Agency (EPA) (1997) Phosphinothricin Acetyltransferase and the Genetic Material Necessary for Its Production in All Plants; Exemption from the Requirement of a Tolerance on All Raw Agricultural Commodities. Federal Register 62: 17717–17720
Environmental Protection Agency (EPA) (2004a) Hygromycin B phosphotransferase; exemption from the requirement of a tolerance. Federal Register 69: 18275–18278
Environmental Protection Agency (EPA) (2004b) Phosphomannose Isomerase and the Genetic Material Necessary for Its Production in All Plants; Exemption from the Requirement of a Tolerance. Federal Register 69: 26770–26775
Erikson O, Clapham D, Hertzberg M, Näsholm T (2003) D- Amino acid selectable markers. Online abstract at http://www.treebiotech2003.norrnod.se/s2_o.htm accessed 1/27/2005
Erikson, O, Hertzberg, M, Näsholm, T (2004) A conditional marker gene allowing both positive and negative selection in plants. Nat. Biotechnol. 22: 455–458 CrossRef
European Federation of Biotechnology (2001) Antibiotic resistance markers in genetically modified GM crops. Briefing Paper 10 http://www.efbweb.org/public/pubview.htm site access 12/16/2004
European Food Safety Authority (2004) Opinion of the Scientific Panel on Genetically Modified Organisms on the use of antibiotic resistance genes as marker genes in genetically modified plants (Question N EFSA-Q-2003-109) Opinion adopted on 2 April 2004 The EFSA Journal 48:1-18
Food and Drug Administration (1994) “Secondary Food Additives Permitted in Food for Human Consumption; Food Additives Permitted in Feed and Drinking Water of Animals; Aminoglycoside 3'-Phosphotransferase II; Final Rule.” Federal Register 59:26700-26711
Food and Drug Administration Center for Food Safety and Applied Nutrition Office of Premarket Approval (1998) Guidance for Industry: Use of Antibiotic Resistance Marker Genes in Transgenic Plants Draft Guidance. http://vm.cfsan.fda.gov/~dms/opa-armg.html
Food Standards Australia New Zealand (2002) Final assessment report application A436. Oil and linters derived from insect protected cotton containing event 15985. http://www.foodstandards.gov.au/standardsdevelopment/applications/applicationa436insectprotectedcotton/a436farexecsummary211633.cfm
Fraley, RT, Rogers, SG, Horsch, RB, Sanders, PR, Flick, JS, Adams, SP, Bittner, ML, Brand, LA, Fink, CL, Fry, JS, Gallupi, GR, Goldberg, SB, Hoffman, NL, Woo, SC (1983) Expression of bacterial genes in plant cells. Proc. Natl. Acad. Sci. (USA) 80: 4803–4807 CrossRef
Fregene M, Puonti-Kaerlas J (2002) Cassava Biotechnology. In Hillocks RJ, Thresh JM, Bellotti AC, eds, Cassava: Biology, Production and Utilization, CAB International, pp 179–207
Fuchs, RL, Ream, JE, Hammond, BG, Naylor, MW, Leimgruber, RM, Berberich, SA (1993) Safety assessment of the neomycin phosphotransferase II (NPTII) protein. Biotechnology 11: 1543–1547
Gilissen, LJW, Metz, PLJ, Stiekema, WJ, Nap, JP (1998) Biosafety of E. coli $\beta$ -glucuronidase (GUS) in plants. Transgenic Res. 7: 157–163 CrossRef
Goldsbrough A (2001) Methods for avoidance and removal of selectable marker genes in crop transformation systems. http://www.defra.gov.uk/environment/acre/uti/08.htm
González, AE, Schöpke, C, Taylor, NJ, Beachy, RN, Fauquet, CM (1998) Regeneration of transgenic cassava plants (Manihot esculenta Crantz) through Agrobacterium-mediated transformation of embryogenic suspension cultures. Plant Cell Rep. 17: 827–831
Gritz L, Davies J (1983) Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 25: 179–188 CrossRef
Hails, RS (2000) Genetically modified plants – The debate continues. Trends Ecol. Evol. 15: 14–18 CrossRef
Haseloff, J, Amos, B (1995) GFP in Plants. Trends Genet. 11: 328–329 CrossRef
Haslberger, AG (2003) Codex Guidelines for GM Foods Include the Analysis of Unintended Effects. Nat. Biotechnol. 21: 739–741 CrossRef
Herrera-Estrella, L, De Block, M, Messens, E, Hernalsteen, JP, Van Montagu, M, Schell, J (1983) Chimeric genes as dominant selectable markers in plant cells. EMBO J. 2: 987–995
Information Systems for Biotechnology, Field Test Releases in the U.S. Updated 12/22/2004 http://www.isb.vt.edu/cfdocs/fieldtests1.cfm accessed 12/27/2004
Jefferson, RA (1989) The GUS reporter gene system. Nature 342: 837–838 CrossRef
Jelenic, S (2003) Kanamycin Resistance Marker Gene in Transgenic Plants. Food Technol. Biotechnol. 41: 183–190
Jennings DL, Iglesias C (2002) Breeding for Crop Improvement. In Hillocks RJ, Thresh JM, Bellotti AC, eds, Cassava: Biology, Production and Utilization, CAB International, pp 149–166
Jones DD, Maryanski JH (1991) Safety considerations in the evaluation of transgenic plants for human food. In Levin MA, Straus HS, eds, Risk Assessment in Genetic Engineering, New York: McGraw-Hill, pp 64–82
Kärenlampi S (1996) Health Effects of Marker Genes in Genetically Engineered Food Plants. TemaNord 530. The Nordic Council of Ministers. Store Standstræde 18. DK-1255 Copenhagen K, pp 7–66
Kopertekh, L, Jüttner, G, Schiemann, J (2004) PVX-Cre-mediated marker gene elimination from transgenic plants. Plant Mol. Biol. 55: 491–500 CrossRef
Kuhstoss, S, Rao, RN (1983) Expression in Streptomyces ambofaciens of an Escherichia coli K-12 gene which confers resistance to hygromycin B. Gene 26: 295–299 CrossRefPubMed
Laminski, S, Gray, VM, Mycock, DJ, Blatch, GL, Groll, J, Rey, MEC (2002) Green fluorescent protein as a reporter of early transformation in Cassava (Manihot esculenta Crantz). South African J. Sci. 98: 301–303
Leboul J, Davies J (1982) Enzymatic modification of hygromycin B in Streptomyces hygroscopicus. J. Antibiot. 35: 527–528 CrossRef
Li, HQ, Sautter, C, Potrykus, I, Pounti-Kaerlas J (1996) Genetic transformation of cassava (Manihot esculenta Crantz). Nat. Biotechnol. 14: 736–740 CrossRef
Malpartida F, Zalacain M, Jimenez A, Davies J (1983) Molecular cloning and expression in Streptomyces lividans of a hygromycin B phosphotransferase gene from Streptomyces hygroscopicus. Biochem. Biophys. Res. Commun. 117: 6–12 CrossRef
Marker Genes Technologies, Inc., Live cell luciferase assay kit – Product Mo626 Product Information Sheet (0626-005). http://www.markergene.com/
Matthews P, Fieg S, Gubler F, McCallum G, McCarthy N, Thornton S, Wang M, Jacobsen J (1999) Transgene Segregation to Obtain Selectable Marker-Free Transformed Barley. Proceedings of the 9th Australian Barley Technical Symposium. http://www.regional.org.au/au/abts/1999/matthews. htm?PHPSESSID=ec4a0c42626ab4dc068f9be832936974#P0_0
Miki, B, McHugh, S (2004) Selectable marker genes in transgenic plants: applications, alternatives and biosafety. J. Biotechnol. 107: 193–232 CrossRef
Miles JS, Guest JR (1984) Nucleotide sequence and transcriptional start point of the phosphomannose isomerase gene (manA) of Escherichia coli. Gene 32: 41–48
Millar, AJ, Short, SR, Hiratsuka, K, Chua, NH, Kay, SA (1992) Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Mol. Biol. Rep. 10: 324–337 CrossRef
Monsanto Company web site: http://www.monsanto.com/monsanto/content/sci_tech/prod_safety/bollgard_II/pss.pdf August 2003 accessed 12/23/2004
Nap, JP, Bijvoet, J, Stiekema, WJ (1992) Biosafety of kanamycin-resistant transgenic plants. Transgenic Res. 1: 239–249 CrossRef
National Academy of Sciences (NAS) (2000) Genetically modified pest-protected plants: Science and regulation, Washington D.C.: National Academy Press
National Academy of Sciences (NAS) (2002) Environmental effects of transgenic plants, Washington D.C.: National Academy Press
OECD Environmental Health and Safety Publications Series on Harmonization of Regulatory Oversight in Biotechnology No. 11 (1999) Consensus Document on General Information Concerning the Genes and Their Enzymes that Confer Tolerance to Phosphinothricin Herbicide. http://www.olis.oecd.org/olis/1999doc.nsf/LinkTo/env-jm-mono(99)13
Office of the Gene Technology Regulator (2003) Risk Assessment and Risk Management Plan Application for license for dealings involving intentional release of a genetically modified organism into the environment. DIR 034/2003 Title: Field Trial of Genetically Modified Cotton (Gossypium hirsutum) Expressing an Insecticidal Gene (vip3A) http://www.ogtr.gov.au/pdf/ir/dir034.pdf
Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: Phylogeography of Manihot esculenta. Proc. Natl. Acad. Sci. (USA) 96: 5586–5591
Ouakfaoui S, Miki B (2005) The stability of the Arabidopsis transcriptome in transgenic plants expressing the marker genes nptII and uidA. Plant J. 41: 791–800 CrossRef
Ow, DW (2002) Recombinase-directed plant transformation for the post-genomic era. Plant Mol. Biol. 48: 183–200 CrossRef
Ow, DW, Wood, KV, DeLuca, M, De Wet, JR, Helinski, DR, Howell, SH (1986) Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants. Science 234: 856–859 CrossRef
Pang, S-Z, DeBoer, D, Wan, Y, Ye, G, Layton, JC, Neher, MK, Armstrong, CL, Fry, JE, Hinchee, MAW, Fromm, ME (1996) An improved Green Fluorescent Protein gene as a vital marker in plants. Plant Physiol. 112: 893–900 CrossRef
Pardo, JM, Malpartida, F, Rico, M, Jimenez, A (1985) Biochemical basis of resistance to hygromycin B in Streptomyces hygroscopicus – the producing organism. J. Gen. Microbiol. 131: 1289–1298
Privalle, LS (2002) Phosphomannose isomerase, a novel plant selection system: potential allergenicity assessment. Ann. N. Y. Acad. Sci. 964: 129–138 CrossRef
Privalle LS, Wright M, Reed J, Hansen G, Dawson J, Dunder EM, Chang Y-F, Powell ML, Meghji M (2000) Phosphomannose Isomerase, A Novel Selectable Plant Selection System: Mode of Action and Safety Assessment. In Fairbairn C, Scoles G, McHughen A, eds, Proceedings of the 6th International Symposium on The Biosafety of Genetically Modified Organisms, Saskatoon, Canada, University Extension Press, Univ. Saskatchewan, pp 171–178
Raemakers, CJJM, Sofiari, E, Taylor, N, Henshaw, G, Jacobsen, E, Visser, RGF (1996) Production of transgenic cassava (Manihot esculenta Crantz) plants by particle bombardment using luciferase activity as selection marker. Mol. Breed. 2: 339–349 CrossRef
Raemakers, CJJM, Sofiari, E, Jacobsen, E, Visser, RGF (1997) Regeneration and transformation of cassava. Euphytica 96: 153–161 CrossRef
Raemakers, K, Schreuder, M, Pereira, I, Munyikwa, T, Jacobsen, E, Visser, R (2001) Progress made in FEC transformation of cassava. Euphytica 120: 15–24 CrossRef
Rao RN, Allen NE, Hobbs JN Jr., Alborn WE Jr., Kirst HA, Paschal JW (1983) Genetic and enzymatic basis of hygromycin B resistance in Escherichia coli. Antimicrob. Agents Chemother. 24: 689–695 CrossRef
Redenbaugh, K, Hiatt, W, Martineau, B, Lindemann, J, Emlay, D (1994) Aminoglycoside 3'-phosphotransferase II (APH (3') II): Review of its safety and use in the production of genetically engineered plants. Food Biotechnol. 8: 137–165 CrossRef
Reed, J, Privalle, LS, Powell, ML, Meghji, M, Dawson, J, Dunder, E, Suttie, J, Wenke, A, Launis, K, Kramer, C, Chang, YF, Hansen, G, Wright, M (2001) Phosphomannose isomerase: An efficient selectable marker for plant transformation. In Vitro Cell. Dev. Biol. Plant 37: 127–132 CrossRef
Richards, HA, Han, CT, Hopkins, RG, Failla, ML, Ward, WW, Stewart, CN (2003) Safety assessment of recombinant green fluorescent protein orally administered to weaned rats. J. Nutr. 133: 1909–1912 CrossRef
Sarria, R, Torres, E, Angel, F, Chavarriaga, P, Roca, WM (2000) Transgenic plants of cassava (Manihot esculenta) with resistance to Basta obtained by Agrobacterium-mediated transformation. Plant Cell Rep. 19: 339–344 CrossRef
Schöpke, C, Taylor, N, Carcamo, R, Konan, NK, Marmey, P, Henshaw, GG, Beachy, RN, Fauquet, CM (1996) Regeneration of transgenic cassava plants (Manihot esculenta Crantz) from microbombarded embryogenic suspension cultures. Nat. Biotechnol. 14: 731–735 CrossRef
Siritunga, D, Sayre, RT (2003) Generation of cyanogen-free transgenic cassava. Planta 217: 367–373 CrossRef
Sjoblad, RD, McClintock, JT, Engler, R (1992) Toxicological considerations for protein components of biological pesticide products. Regul. Toxicol. Pharmacol. 15: 3–9 CrossRef
Smalla K, Borin S, Heuer H, Gebhard F, van Elsas JD, Nielsen K (2000) Horizontal transfer of antibiotic resistance genes from transgenic plants to bacteria – are there new data to fuel the debate? In Fairbairn C, Scoles G, McHughen A, eds, Proceedings of the 6th International Symposium on The biosafety of genetically modified organisms, Saskatoon, Canada, University Extension Press, Univ. Saskatchewan, pp 146–154
Stewart, CN, Richards, HA, Halfhill, MD (2000) Transgenic Plants and Biosafety: Science, Misconceptions and Public Perception. Biotechniques 29: 832–843
Taylor N (2005) Personal communication
Taylor, N, Chavarriaga, P, Raemakers, K, Siritunga, D, Zhang, P (2004) Development and application of transgenic technologies in cassava. Plant Mol. Biol. 56: 671–688 CrossRef
Taylor, SL, Lemanske, RF, Bush, RK, Busses, WW (1987) Food Allergens: Structure and Immunologic Properties. Ann. Allergy 59: 93–99
Thompson CJ, Movva NR, Tizard R, Crameri R, Davies JE, Lauwereys M, Botterman J (1987) Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J. 6: 2519–2523
Van den Eede G, Aarts H, Buhk H-J, Corthier G, Flint HJ, Hammes W, Jacobsen B, Midvedt T, Van der Vossen J, von Wright A, Wackernagel W, Wilcks A (2004). The relevance of gene transfer to the safety of food and feed derived from GM plants. Food Chem. Toxicol. 42: 1127–1156
Waldron C, Murphy EB, Roberts JL, Gustafson GD, Armour SL and Malcom SK (1985) Resistance to hygromycin B – a new marker for plant transformation studies. Plant
Mol. Biol. 5: 103–108
Westby A (2002) Cassava utilization, storage and small-scale processing. In Hillocks RJ, Thresh JM, Bellotti AC, eds, Cassava: Biology, Production and Utilization, CAB International, pp 281–300
Wohlleben W, Arnold W, Broer I, Hilleman D, Struach E, Puhler A (1988) Nucleotide sequence of the phosphinothricin N-acetyltransferase gene from Streptomyces viridochromogenes Tu494 and its expression in Nicotiana tabacum. Gene 70: 25–37 CrossRef
Wolfenbarger, LL, Phifer, PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290: 2088–2093 CrossRef
World Health Organization (1993) Health aspects of marker genes in genetically modified plants: report of a WHO workshop, WHO/FNU/FOS/93.6
Zhang, P, Legris, G, Coulin, P, Puonti-Kaerlas J (2000a) Production of stably transformed cassava plants via particle bombardment. Plant Cell Rep. 19: 939–945 CrossRef
Zhang, P, Potrykus, I, Puonti-Kaerlas J (2000b) Efficient production of transgenic cassava using negative and positive selection. Transgenic Res. 9: 405–415 CrossRef