Transgene excision in pollen using a codon optimized serine resolvase CinH-RS2 site-specific recombination system

Plant Molecular Biology

Volumn 75, Issue 6, 2011, Pages 621-631

  Moon, Hong S ^a   Abercrombie, Laura L ^a   Eda, Shigetoshi ^a   Blanvillain, Robert ^b,d   Thomson, James G ^c   Ow, David W ^b,e   Stewart, Jr ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b PLANT GENE EXPRESSION CENTER   (United States)

^c WESTERN REGIONAL RESEARCH CENTER   (United States)

^d CNRS   (France)

^e SOUTH CHINA INSTITUTE OF BOTANY   (China)

Author keywords

Biocontainment; CinH RS2; Flow cytometry; Green fluorescent protein (GFP); Pollen; Site specific recombination; Transgene excision

Indexed keywords

GREEN FLUORESCENT PROTEIN; RECOMBINASE;

ARTICLE; BIOSYNTHESIS; CODON; FLOW CYTOMETRY; GENETIC ENGINEERING; GENETICS; GERMINATION; METHODOLOGY; POLLEN; SOUTHERN BLOTTING; TOBACCO; TOMATO; TRANSGENE; TRANSGENIC PLANT;

BLOTTING, SOUTHERN; CODON; FLOW CYTOMETRY; GENETIC ENGINEERING; GERMINATION; GREEN FLUORESCENT PROTEINS; LYCOPERSICON ESCULENTUM; PLANTS, GENETICALLY MODIFIED; POLLEN; RECOMBINASES; TOBACCO; TRANSGENES;

LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

EID: 79952700417     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-011-9756-2     Document Type: Article

References (49)

1. Al-Ahmad H, Galili S, Gressel J (2004) Tandem constructs to mitigate transgene persistence: tobacco as a model. Mol Ecol 13: 697-710.
2. Al-Ahmad H, Dwyer J, Moloney M, Gressel J (2006) Mitigation of establishment of Brassica napus transgenes in volunteers using a tandem construct containing a selectively unfit gene. Plant Biotechnol J 4: 7-21.
3. Aono M, Wakiyama S, Nagatsu M, Nakajima N, Tamaoki M, Kubo A, Saji H (2006) Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan. Environ Biosafety Res 5: 77-87.
4. Beckie HJ, Warwick SI, Nair H, Séguin-Swartz G (2003) Gene flow in commercial fields of herbicide-resistant canola (Brassica napus). Ecol Appl 13: 1276-1294.
5. Brown T (2001) Southern blotting. Curr Protocols Mol Biol 2. 9. 1-2. 9. 20.
6. Chevre AM, Eber F, Darmency H, Fleury A, Picault H, Letan-neur JC, Renard M (2000) Assessment of interspecific hybridization between transgenic oilseed rape and wild radish under agronomic conditions. Theor Appl Genet 100: 1233-1239.
7. Dale EC, Ow DW (1990) Intra- and intermolecular site-specific recombination in plant cells mediated by bacteriophage P1 recombinase. Gene 91: 79-85.
8. Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nature Biotechnol 20: 581-586.
9. Daniell H, Datta R, Varma S, Gray S, Lee SB (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nature Biotechnol 16: 345-348.
10. Gray AJ, Raybould AF (1998) Crop genetics-reducing transgene escape routes. Nature 392: 653-654.
11. Grindley NDF, Whiteson KL, Rice PA (2006) Mechanisms of site-specific recombination. Annu Rev Biochem 75: 567-605.
12. Halfhill MD, Zhu B, Warwick SI, Raymer PL, Millwood RJ, Weissinger AK, Stewart CN Jr (2004) Hybridization and backcrossing between transgenic oilseed rape and two related weed species under field conditions. Environ Biosafety Res 3: 73-81.
13. Haygood R, Ives AR, Andow DA (2005) Population genetics of transgene containment. Ecol Lett 7: 213-220.
14. Horsh RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
15. Iamtham S, Day A (2000) Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat Biotechnol 18: 1172-1176.
16. Ingram J (2000) The separation distance required to ensure cross-pollination is below specified limits in non-seed crops of sugar beet, maize and oilseed rape. Plant Var and Seeds 13: 181-199.
17. Kempe K, Rubtsova M, Berger C, Kumlehn I, Schollmeier C, Gils M (2010) Transgene excision from wheat chromosomes by phage phiC31 integrase. Plant Mol Biol 72: 673-687.
18. Kholodii G (2001) The shuffling function of resolvases. Gene 269: 121-130.
19. Klippell A, Kanaar R, Kahmann R, Cozzarelli NR (1993) Analysis of strand exchange and DNA binding of enhancer-independent Gin recombinase mutants. EMBO J 12: 1047-1057.
20. Lloyd AM, Davis RW (1994) Functional expression of the yeast FLP/FRT site-specific recombination system in Nicotina tabacum. Mol Gen Genet 242: 653-657.
21. Luo K, Duan H, Zhao D, Zheng X, Deng W, Chen Y, Stewart CN Jr, McAvoy R, Jiang X, Wu Y, He A, Pei Y, Li Y (2007) 'GM-gene-deletor': fused loxP-FRT recognition sequences dramatically improve the efficiency of FLP or CRE recombinase on transgene excision from pollen and seed of tobacco plants. Plant Biotechnol J 5: 263-274.
22. Lyznik LA, Mitchell JC, Hirayama L, Hodges TK (1993) Activity of yeast FLP recombinase in maize and rice protoplasts. Nucleic Acids Res 21: 969-975.
23. Maeser S, Kahmann R (1991) The Gin recombinase of phage Mu can catalyze site-specific recombination in plant protoplasts. Mol Gen Genet 230: 170-176.
24. Maliga P (2004) Plastid transformation in higher plants. Annu Rev Plant Biol 55: 289-300.
25. Mariani C, DeBeuckeleer M, Trueltner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimeric ribonuclease gene. Nature 347: 737-741.
26. Moon HS, Li Y, Stewart CN Jr (2010) Keeping the genie in the bottle: transgene biocontainment by excision in pollen. Trends Biotechnol 28: 3-8.
27. Moon HS, Eda S, Saxton AM, Ow D, Stewart CN Jr (2011) An efficient and rapid transgenic pollen screening and detection method using a flow cytometry. Biotechnol J 6: 118-123.
28. Morris WF, Kareiva PM, Raymer PL (1994) Do barren zones and pollen traps reduce gene escape from transgenic crops? Ecol Appl 4: 157-165.
29. Nakagawa Y, Machida C, Machida Y, Toriyama K (2001) A system to induce the deletion of genomic sequences using R/RS site-specific recombination and the Ac transposon in transgenic rice plants. Theor Appl Genet 102: 1136-1141.
30. Onouchi H, Yokoi K, Machida C, Matsuzaki H, Oshima Y, Matsuoka K, Nakamura K, Machida Y (1991) Operation of an efficient site-specific recombination system of Zygosaccharomyces rouxii in tobacco cells. Nucleic Acids Res 19: 6373-6378.
31. Onouchi H, Nishihama R, Kudo M, Machida Y, Machida C (1995) Visualization of site-specific recombination catalyzed by a recombinase from Zygosaccharomyces rouxii in Arabidopsis thaliana. Mol Gen Genet 247: 653-660.
32. Petolino JF, Worden A, Curlee K, Connell J, Strange Moynahan TL, Larsen C, Russel S (2010) Zinc finger nuclease-mediated transgene deletion. Plant Mol Biol 73: 617-628.
33. Piñeyro-Nelson A, van Heerwaarden J, Perales HR, Serratos-Hernandez JA, Rangel A, Hufford MB, Gepts P, Garay-Arroyo A, Rivera-Bustamante R, Alvarez-Buylla ER (2009) Transgenes in Mexican maize: molecular evidence and methodological considerations for GMO detection in landrace populations. Mol Ecol 18: 750-761.
34. Rao MR, Moon HS, Schenk TMH, Becker D, Mazarei M, Stewart CN Jr (2010) FLP/FRT Recombination from yeast: application of a two gene cassette scheme as an inducible system in plants. Sensors 10: 8526-8535.
35. Ruf S, Hermann M, Berger IF, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids- high-level foreign protein expression in fruits. Nature Biotechnol 19: 870-875.
36. Sreekala C, Wu L, Gu K, Wang D, Tian D, Yin Z (2005) Excision of a selectable marker in transgenic rice (Oryza sativa L.) using a chemically regulated Cre/loxP system. Plant Cell Rep 24: 86-94.
37. Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques 14: 748-751.
38. Stewart CN Jr, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Rev Genet 4: 806-817.
39. Svab Z, Maliga P (2007) Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc Natl Acad Sci USA 104: 7003-7008.
40. Thomson JG, Ow DW (2006) Site-specific recombination systems for the genetic manipulation of eukaryotic genomes. Genesis 44: 465-476.
41. Thomson JG, Yau Y-Y, Blanvillain R, Chinquy D, Thilmony R, Ow DW (2009) ParA resolvase catalyzes site-specific excision of DNA from the Arabidopsis genome. Transgenic Res 18: 237-248.
42. Thomson JG, Chan R, Thilmony R, Yau Y-Y, Ow DW (2010) PhiC31 recombination system demonstrates heritable germinal transmission of site-specific excision from the Arabidopsis genome. BMC Biotechnol 10: 17.
43. Twell D, Yamaguchi J, McCormick S (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705-713.
44. Verweire D, Verleyen K, De Buck S, Claeys M, Angenon G (2007) Marker-free transgenic plants through genetically programmed auto-excision. Plant Physiol 145: 1220-1231.
45. Weinthal D, Tovkach A, Zeevi V, Tzfira T (2010) Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci 15: 308-321.
46. Whittington M (2006) Underground farming. http://www. associatedcontent. com/article/27102/underground_farming. html?cat=15. Accessed 24 Oct 2010.
47. Woo H-J, Cho H-S, Lim S-H, Shin K-S, Lee S-M, Lee K-J, Kim D-H, Cho Y-G (2009) Auto-excision of selectable marker genes from transgenic tobacco via a stress inducible FLP/FRT site-specific recombination system. Transgenic Res 18: 455-465.
48. Zhang Y, Li H, Quyang B, Lu Y, Ye Z (2006) Chemical-induced autoexcision of selectable markers in elite tomato plants transformed with a gene conferring resistance to lepidopteran insects. Biotechnol Lett 28: 1247-1253.
49. Zuo J, Niu Q-W, Møller SG, Chua N-H (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nature Biotechnol 19: 157-161.