Site-specific T-DNA integration in Arabidopsis thaliana mediated by the combined action of CRE recombinase and φc31 integrase

Plant Journal

Volumn 75, Issue 1, 2013, Pages 172-184

  De Paepe, Annelies ^a,b   De Buck, Sylvie ^a,b   Nolf, Jonah ^a,b   Van Lerberge, Els ^a,b   Depicker, Ann ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

C31 integrase; Arabidopsis; CRE recombinase; gene stacking; site specific integration; T DNA; technical advance

Indexed keywords

ARABIDOPSIS; CRE RECOMBINASE; INTEGRASE; SITE-SPECIFIC; T-DNA; TECHNICAL ADVANCES;

DNA; GENES; INTEGRATION; PLANTS (BOTANY);

POLYMERASE CHAIN REACTION;

BACTERIAL DNA; CRE RECOMBINASE; INTEGRASE; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE TARGETING; GENE VECTOR; GENETIC RECOMBINATION; GENETICS; METABOLISM; PLANT GENOME; TRANSGENIC PLANT;

ARABIDOPSIS; DNA, BACTERIAL; GENE TARGETING; GENETIC VECTORS; GENOME, PLANT; INTEGRASES; MUTAGENESIS, INSERTIONAL; PLANTS, GENETICALLY MODIFIED; RECOMBINATION, GENETIC;

AGROBACTERIUM; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84879205542     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12202     Document Type: Article

References (64)

1. Akbudak, M.A., and, Srivastava, V., (2011) Improved FLP recombinase, FLPe, efficiently removes marker gene from transgene locus developed by Cre-lox mediated site-specific gene integration in rice. Mol. Biotechnol. 49, 82-89.
2. Arumugam, N., Gupta, V., Jagannath, A., Mukhopadhyay, A., Pradhan, A.K., Burma, P.K., and, Pental, D., (2007) A passage through in vitro culture leads to efficient production of marker-free transgenic plants in Brassica juncea using the Cre-loxP system. Transgenic Res. 16, 703-712.
3. Britt, A.B., and, May, G.D., (2003) Re-engineering plant gene targeting. Trends Plant Sci. 8, 90-95.
4. Cheng, M., Fry, J.E., Pang, S., Zhou, H., Hironaka, C.M., Duncan, D.R., Conner, T.W., and, Wan, Y., (1997) Genetic transformation of wheat mediated by Agrobacterium tumefaciens. Plant Physiol. 115, 971-980.
5. Christian, M., Cermak, T., Doyle, E.L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A.J., and, Voytas, D.F., (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 186, 757-761.
6. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
7. Dafhnis-Calas, F., Xu, Z., Haines, S., Malla, S.K., Smith, M.C.M., and, Brown, W.R.A., (2005) Iterative in vivo assembly of large and complex transgenes by combining the activities of φC31 integrase and Cre recombinase. Nucleic Acids Res. 33, e189.
8. Dale, E.C., and, Ow, D.W., (1990) Intra- and intermolecular site-specific recombination in plant cells mediated by bacteriophage P1 recombinase. Gene, 91, 79-85.
9. De Buck, S., Jacobs, A., Van Montagu, M., and, Depicker, A., (1998) Agrobacterium tumefaciens transformation and cotransformation frequencies of Arabidopsis thaliana root explants and tobacco protoplasts. Mol. Plant-Microbe Interact. 11, 449-457.
10. De Buck, S., Jacobs, A., Van Montagu, M., and, Depicker, A., (1999) The DNA sequences of T-DNA junctions suggest that complex T-DNA loci are formed by a recombination process resembling T-DNA integration. Plant J. 20, 295-304.
11. De Buck, S., De Wilde, C., Van Montagu, M., and, Depicker, A., (2000) Determination of the T-DNA transfer and the T-DNA integration frequencies upon cocultivation of Arabidopsis thaliana root explants. Mol. Plant-Microbe Interact. 13, 658-665.
12. De Buck, S., Van Montagu, M., and, Depicker, A., (2001) Transgene silencing of invertedly repeated transgenes is released upon deletion of one of the transgenes involved. Plant Mol. Biol. 46, 433-445.
13. De Buck, S., Peck, I., De Wilde, C., Marjanac, G., Nolf, J., De Paepe, A., and, Depicker, A., (2007) Generation of single-copy T-DNA transformants in Arabidopsis by the CRE/loxP recombination-mediated resolution system. Plant Physiol. 145, 1171-1182.
14. De Buck, S., Podevin, N., Nolf, J., Jacobs, A., and, Depicker, A., (2009) The T-DNA integration pattern in Arabidopsis transformants is highly determined by the transformed target cell. Plant J. 60, 134-145.
15. De Loose, M., Danthinne, X., Van Bockstaele, E., Van Montagu, M., and, Depicker, A., (1995) Different 5' leader sequences modulate β-glucuronidase accumulation levels in transgenic Nicotiana tabacum plants. Euphytica, 85, 209-216.
16. De Neve, M., De Buck, S., Jacobs, A., Van Montagu, M., and, Depicker, A., (1997) T-DNA integration patterns in co-transformed plant cells suggest that T-DNA repeats originate from co-integration of separate T-DNAs. Plant J. 11, 15-29.
17. De Paepe, A., De Buck, S., Hoorelbeke, K., Nolf, J., Peck, I., and, Depicker, A., (2009) High frequency of single-copy T-DNA transformants produced by floral dip in CRE-expressing Arabidopsis plants. Plant J. 59, 517-527.
18. De Paepe, A., De Buck, S., Nolf, J., and, Depicker, A., (2012) High frequency of single-copy T-DNA transformants produced after floral dip in CRE-expressing Arabidopsis plants. In Transgenic Plants: Methods and Protocols (, Dunwell, J.M., and, Wetten, A.C., eds). New York, NY: Humana Press, pp. 317-333.
19. Fauser, F., Roth, N., Pacher, M., Ilg, G., Sánchez- Fernández, R., Biesgen, C., and, Puchta, H., (2012) In planta gene targeting. Proc. Natl Acad. Sci. USA, 109, 7535-7540.
20. Gao, H., Smith, J., and, Yang, M., et al. (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J. 61, 176-187.
21. Gils, M., Marillonnet, S., Werner, S., Grützner, R., Giritch, A., Engler, C., Schachschneider, R., Klimyuk, V., and, Gleba, Y., (2008) A novel hybrid seed system for plants. Plant Biotechnol. J. 6, 226-235.
22. Hanin, M., and, Paszkowski, J., (2003) Plant genome modification by homologous recombination. Curr. Opin. Plant Biol. 6, 157-162.
23. Hobbs, S.L.A., Warkentin, T.D., and, DeLong, C.M.O., (1993) Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol. Biol. 21, 17-26.
24. Iida, S., and, Terada, R., (2004) A tale of two integrations, transgene and T-DNA: gene targeting by homologous recombination in rice. Curr. Opin. Biotechnol. 15, 132-138.
25. Jones, J.D.G., Gilbert, D.E., Grady, K.L., and, Jorgensen, R.A., (1987) T-DNA structure and gene expression in petunia plants transformed by Agrobacterium tumefaciens C58 derivates. Mol. Gen. Genet. 207, 478-485.
26. Kapusi, E., Kempe, K., Rubtsova, M., Kumlehn, J., and, Gils, M., (2012) PhiC31 integrase-mediated site-specific recombination in barley. PLoS ONE 7, e45353.
27. Kempe, K., Rubtsova, M., Berger, C., Kumlehn, J., Schollmeier, C., and, Gils, M., (2010) Transgene excision from wheat chromosomes by phage phiC31 integrase. Plant Mol. Biol. 72, 673-687.
28. Kilby, N.J., Davies, G.J., Snaith, M.R., and, Murray, J.A.H., (1995) FLP recombinase in transgenic plants: constitutive activity in stably transformed tobacco and generation of marked cell clones in Arabidopsis. Plant J. 8, 637-652.
29. Kittiwongwattana, C., Lutz, K., Clark, M., and, Maliga, P., (2007) Plastid marker gene excision by the phiC31 phage site-specific recombinase. Plant Mol. Biol. 64, 137-143.
30. Li, Z., Xing, A., Moon, B.P., McCardell, R.P., Mills, K., and, Falco, S.C., (2009) Site-specific integration of transgenes in soybean via recombinase-mediated DNA cassette exchange. Plant Physiol. 151, 1087-1095.
31. Lutz, K.A., Corneille, S., Azhagiri, A.K., Svab, Z., and, Maliga, P., (2004) A novel approach to plastid transformation utilizes the phiC31 phage integrase. Plant J. 37, 906-913.
32. Lyznik, L.A., Mitchell, J.C., Hirayama, L., and, Hodges, T.K., (1993) Activity of yeast FLP recombinase in maize and rice protoplasts. Nucleic Acids Res. 21, 969-975.
33. Marjanac, G., De Paepe, A., Peck, I., Jacobs, A., De Buck, S., and, Depicker, A., (2008) Evaluation of CRE-mediated excision approaches in Arabidopsis thaliana. Transgenic Res. 17, 239-250.
34. Matzke, A.J.M., and, Matzke, M.A., (1998) Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1, 142-148.
35. Matzke, M.A., Mette, M.F., and, Matzke, A.J.M., (2000) Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol. Biol. 43, 401-415.
36. Muskens, M.W.M., Vissers, A.P.A., Mol, J.N.M., and, Kooter, J.M., (2000) Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing. Plant Mol. Biol. 43, 243-260.
37. Nandy, S., and, Srivastava, V., (2012) Marker-free site-specific gene integration in rice based on the use of two recombination systems. Plant Biotechnol. J. 10, 904-912.
38. Odell, J., Caimi, P., Sauer, B., and, Russell, S., (1990) Site-directed recombination in the genome of transgenic tobacco. Mol. Gen. Genet. 223, 369-378.
39. Onouchi, H., Yokoi, K., Machida, C., Matsuzaki, H., Oshima, Y., Matsuoka, K., Nakamura, K., and, Machida, Y., (1991) Operation of an efficient site-specific recombination system of Zygosaccharomyces rouxii in tobacco cells. Nucleic Acids Res. 19, 6373-6378.
40. Onouchi, H., Nishihama, R., Kudo, M., Machida, Y., and, Machida, C., (1995) Visualization of site-specific recombination catalyzed by a recombinase from Zygosaccharomyces rouxii in Arabidopsis thaliana. Mol. Gen. Genet. 247, 653-660.
41. Ow, D.W., (2002) Recombinase-directed plant transformation for the post-genomic era. Plant Mol. Biol. 48, 183-200.
42. Ow, D.W., (2011) Recombinase-mediated gene stacking as a transformation operating system. J. Integr. Plant Biol. 53, 512-519.
43. Puchta, H., (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J. Exp. Bot. 56, 1-14.
44. Rubtsova, M., Kempe, K., Gils, A., Ismagul, A., Weyen, J., and, Gils, M., (2008) Expression of active Streptomyces phage phiC31 integrase in transgenic wheat plants. Plant Cell Rep. 27, 1821-1831.
45. Russell, S.H., Hoopes, J.L., and, Odell, J.T., (1992) Directed excision of a transgene from the plant genome. Mol. Gen. Genet. 234, 49-59.
46. Shukla, V.K., Doyon, Y., and, Miller, J.C., et al. (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature, 459, 437-441.
47. Smith, M.C.M., Brown, W.R.A., McEwan, A.R., and, Rowley, P.A., (2010) Site-specific recombination by φC31 integrase and other large serine recombinases. Biochem. Soc. Trans. 38, 388-394.
48. Srivastava, V., and, Ow, D.W., (2001) Single-copy primary transformants of maize obtained through the co-introduction of a recombinase-expressing construct. Plant Mol. Biol. 46, 561-566.
49. Srivastava, V., and, Ow, D.W., (2003) Rare instances of Cre-mediated deletion product maintained in transgenic wheat. Plant Mol. Biol. 52, 661-668.
50. Thomson, J.G., Chan, R., Thilmony, R., Yau, Y.-Y., and, Ow, D.W., (2010) PhiC31 recombination system demonstrates heritable germinal transmission of site-specific excision from the Arabidopsis genome. BMC Biotechnol. 10, 17.
51. Thomson, J.G., Chan, R., Smith, J., Thilmony, R., Yau, Y.-Y., Wang, Y., and, Ow, D.W., (2012) The Bxb1 recombination system demonstrates heritable transmission of site-specific excision in Arabidopsis. BMC Biotechnol. 12, 9.
52. Thorpe, H.M., and, Smith, M.C.M., (1998) In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc. Natl Acad. Sci. USA, 95, 5505-5510.
53. Townsend, J.A., Wright, D.A., Winfrey, R.J., Fu, F., Maeder, M.L., Joung, J.K., and, Voytas, D.F., (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 459, 442-445.
54. Tuteja, N., Verma, S., Sahoo, R.K., Raveendar, S., and, Reddy, I.N.B.L., (2012) Recent advances in development of marker-free transgenic plants: regulation and biosafety concern. J. Biosci. 37, 167-197.
55. Tzfira, T., Weinthal, D., Marton, I., Zeevi, V., Zuker, A., and, Vainstein, A., (2012) Genome modifications in plant cells by custom-made restriction enzymes. Plant Biotechnol. J. 10, 373-389.
56. Van Ex, F., Verweire, D., Claeys, M., Depicker, A., and, Angenon, G., (2009) Evaluation of seven promoters to achieve germline directed Cre-lox recombination in Arabidopsis thaliana. Plant Cell Rep. 28, 1509-1520.
57. Verdaguer, B., de Kochko, A., Fux, C.I., Beachy, R.N., and, Fauquet, C., (1998) Functional organization of the cassava vein mosaic virus (CsVMV) promoter. Plant Mol. Biol. 37, 1055-1067.
58. Vergunst, A.C., Jansen, L.E.T., and, Hooykaas, P.J.J., (1998) Site-specific integration of Agrobacterium T-DNA in Arabidopsis thaliana mediated by Cre recombinase. Nucleic Acids Res. 26, 2729-2734.
59. Wang, M.-B., and, Waterhouse, P.M., (2000) High-efficiency silencing of a β-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol. Biol. 43, 67-82.
60. Wang, Y., Yau, Y.-Y., Perkins-Balding, D., and, Thomson, J.G., (2011) Recombinase technology: applications and possibilities. Plant Cell Rep. 30, 267-285.
61. Xu, Z., Lee, N.C.O., Dafhnis-Calas, F., Malla, S., Smith, M.C.M., and, Brown, W.R.A., (2008) Site-specific recombination in Schizosaccharomyces pombe and systematic assembly of a 400kb transgene array in mammalian cells using the integrase of Streptomyces phage φBT1. Nucleic Acids Res. 36, e9.
62. Yang, M., Djukanovic, V., Stagg, J., Lenderts, B., Bidney, D., Falco, S.C., and, Lyznik, L.A., (2009) Targeted mutagenesis in the progeny of maize transgenic plants. Plant Mol. Biol. 70, 669-679.
63. Yau, Y.-Y., Wang, Y., Thomson, J.G., and, Ow, D.W., (2011) Method for Bxb1-mediated site-specific integration in planta. In Plant Chromosome Engineering (, Birchler, J.A., ed.). New York, NY: Springer, pp. 147-166.
64. Zhang, Y., Zhang, F., Li, X., Baller, J.A., Qi, Y., Starker, C.G., Bogdanove, A.J., and, Voytas, D.F., (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161, 20-27.