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Prospects of applying a combination of DNA transposition and site-specific recombination in plants: a strategy for gene identification and cloning

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Abstract

The concept of gene identification and cloning using insertional mutagenesis is well established. Many genes have been isolated using T-DNA transformation or transposable elements. Maize transposable elements have been introduced into heterologous plant species for tagging experiments. The behaviour of these elements in heterologous hosts shows many similarities with transposon behaviour in Zea mays. Site-specific recombination systems from lower organisms have also been shown to function efficiently in plant cells. Combining transposon and site-specific recombination systems in plants would create the possibility to induce chromosomal deletions. This ‘transposition-deletion’ system could allow the screening of large segments of the genome for interesting genes and may also permit the cloning of the DNA corresponding to the deleted material by the same site-specific recombination reaction in vitro. This methodology may provide a unique means to construct libraries of large DNA clones derived from defined parts of the genome, the phenotypic contribution of which is displayed by the mutant carrying the deletion.

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References

  1. Aarts MGM, Dirkse WG, Stiekema WJ, Pereira A: Transposon tagging of a male sterility gene in Arabidopsis. Nature: 363: 715–717 (1993).

    Google Scholar 

  2. Adams DE, Bliska JB, Cozzarelli NR: Cre-lox recombination in Escherichia coli cells. Mechanistic differences from the in vitro reaction. J Mol Biol 226: 661–673 (1992).

    Google Scholar 

  3. Arondel V, Lemieux B, Hwang I, Gibson S, Goodman HM, Sommerville CR: Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis. Science 258: 1353–1355 (1992).

    Google Scholar 

  4. Baker B, Coupland G, Federoff NV, Starlinger P, Schell J: Phenotypic assay for excision of the maize controlling element Ac in tobacco. EMBO J 6: 1547–1554 (1987).

    Google Scholar 

  5. Bancroft I, Jones JDG, Dean C: Heterologous transposon tagging of the DRL1 locus in Arabidopsis. Plant Cell 5: 631–638 (1993).

    Google Scholar 

  6. Bayley CC, Morgan M, Dale EC, Ow DW: Exchange of gene activity in transgenic plants catalysed by the Cre-lox site-specific recombination system. Plant Mol Biol 18: 353–361 (1992).

    Google Scholar 

  7. Chang C, Meyerowitz EM: Plant genome studies: restriction fragment length polymorphism and chromosome mapping information. Curr Opin Biotecnol 2: 178–183 (1991).

    Google Scholar 

  8. Chuck G, Robbins T, Nijjar C, Ralston E, Courtney-Gutterson N, Dooner HK: Tagging and cloning of a petunia flower color gene with the maize transposable element Activator. Plant Cell 5: 371–378 (1993).

    Google Scholar 

  9. Coen ES, Robins PT, Almeida J, Hudson A, Carpenter R: Consequences and mechanisms of transposition in Antirrhinum majus. In: Berg DE, Howe MM (eds) Mobile DNA, pp. 413–436. American Society for Microbiology, Washington DC (1989).

    Google Scholar 

  10. Craig N: The mechanism of conservative site-specific recombination, Annu Rev Genet 22: 77–105 (1988).

    Google Scholar 

  11. Dale EC, Ow DW: Intra- and intermolecular site-specific recombination in plant cells mediated by bacteriophage P1 recombinase. Gene 91: 79–85 (1990).

    Google Scholar 

  12. Dale EC, Ow DW: Gene transfer with subsequent removal of the selection gene from the host genome. Proc Natl Acad Sci USA 88: 10 588–10 562 (1991).

    Google Scholar 

  13. Dale EC, Ow DW: Mutations in the Cre/lox recombination site enhance the stability of recombination products: applications for gene targeting in plants. J Cell Biochem, Suppl 16F: 206 (1992).

    Google Scholar 

  14. Depicker A, Herman L, Jacobs A, Schell J, VanMontagu M: Frequencies of simultaneous transformation with different T-DNA's and their relevance to the Agrobacterium/plant cell interaction. Mol Gen Genet 201: 477–484 (1985).

    Google Scholar 

  15. Dooner HK, Belachew A: Transposition pattern of the maize element Ac from the bz-m 2 (Ac) allele. Genetics 122: 447–457 (1989).

    Google Scholar 

  16. Dooner HK, Keller J, Harper E, Ralston E: Variable patterns of transposition of the maize element Activator in tobacco. Plant Cell 3: 473–482 (1991).

    Google Scholar 

  17. Doring HP: Tagging genes with maize transposable elements: an overview. Maydica 34: 73–88 (1989).

    Google Scholar 

  18. Fedoroff N: Maize transposable elements. In: Berg DE, Howe MM (eds) Mobile DNA, pp. 375–411, American Society for Microbiology, Washington DC (1989).

    Google Scholar 

  19. Feldmann KA: T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J 1: 71–82 (1991).

    Google Scholar 

  20. Fukushige S, Sauer B: Genomic targeting with a positiveselection lox integration vector allows highly reproducible gene expression in mammalian cells. Proc Natl Acad Sci USA 89: 7905–7909 (1992).

    Google Scholar 

  21. Giovannoni JJ, Wing RA, Ganal MW, Tanksley SD: Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucl Acids Res 19: 6553–6558 (1991).

    Google Scholar 

  22. Giraudet J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM: Isolation of the Arabidopsis AB13 gene by positional cloning. Plant Cell 4: 1251–1261 (1992).

    Google Scholar 

  23. Golic KG, Lindquist S: The FLP recombinase of yeast catalyses site-specific recombination in the Drosophila genome. Cell 59: 499–509 (1989).

    Google Scholar 

  24. Greenblatt IM: A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, Modulator, in maize. Genetics 108: 417–485 (1984).

    Google Scholar 

  25. Hamilton BA, Palazzolo MJ, Chang JH, Vijayraghavan K, Mayeda CA, Whitney MA, Meyerowitz EM: Large scale screen for transposon insertions into cloned genes. Proc Natl Acad Sci USA 88: 2731–2735 (1991).

    Google Scholar 

  26. Haring MA, Rommens CMT, Nijkamp HJJ, Hille J: The use of transgenic plants to understand transposition mechanisms and to develop transposon tagging strategies. Plant Mol Biol 16: 449–461 (1991).

    Google Scholar 

  27. Hille J, Rudenko G, van derBiezen E, Blok K, Overduin B, Rommens C, Nijkamp J, vanHaaren M: Transposon induced chromosomal rearrangements. In: Molecular Biology of Tomato: Fundamental Advances in Crop Improvement, Chap. 10, pp. 93–106. Technomic Publishing Co., Yoder JI (ed) Lancaster, PA (1993).

    Google Scholar 

  28. Hwang I, Kohchi T, Hauge BM, Goodman HG, Schmidt R, Cnops G, Dean C, Gibson S, Iba K, Lemieux B, Arondel V, Danhoff L, Somerville C: Identification and map position of YAC clones comprising one-third of the Arabidopsis genome, Plant J 1: 367–374 (1991).

    Google Scholar 

  29. Johal GS, Briggs SP: Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987 (1992).

    Google Scholar 

  30. Jones JDG, Carland F, Lim E, Ralston E, Dooner HK: Preferential transposition of the maize element Activator to linked chromosomal locations in tobacco. Plant Cell 2: 701–707 (1990).

    Google Scholar 

  31. Kamalay JC, Goldberg RB: Regulation of structural gene expression in tobacco. Cell 19: 935–946 (1980).

    Google Scholar 

  32. Koncz C, Nemeth K, Redei GP, Schell J: T-DNA insertional mutagenesis in Arabidopsis. Plant Mol Biol 20: 963–976 (1992).

    Google Scholar 

  33. Khush GS, Rick CM: Cytogenetic analysis of the tomato genome by means of induced deficiencies. Chromosoma 23: 452–484 (1968).

    Google Scholar 

  34. Lakso M, Sauer B, Mosinger B, Lee EJ, Manning RW, Yu SH, Mulder KL, Westphal H: Targeted oncogene activation by site-specific recombination in transgenic mice. Proc Natl Acad Sci USA 89: 6232–6236 (1992).

    Google Scholar 

  35. Lichtenstein C, Barrena E: Prospects for reverse genetics in plants using recombination. Plant Mol Biol 21: V-XII (1993).

    Google Scholar 

  36. Lisitsyn N, Lisitsyn N, Wigler M: Cloning the diferences between two complex genomes. Science 259: 946–951 (1993).

    Google Scholar 

  37. Lyznik LA, Mitchell JC, Hirayama L, Hodges TK: Activity of yeast FLP recombinase in maize and rice protoplasts. Nucl Acids Res 21: 969–975 (1993).

    Google Scholar 

  38. Maeser S, Kahmann R: The Gin recombinase of phage Mu can catalyse site-specific recombination in plant protoplasts. Mol Gen Genet 230: 170–176 (1991).

    Google Scholar 

  39. Martin GB, Williams JGK, Tanksley SD: Rapid identification of markers linked to a Pseudomonas resistance gene in tomato by using random primers and near-isogenic lines. Proc Natl Acad Sci USA 88: 2336–2340 (1991).

    Google Scholar 

  40. Matsuzaki H, Nakajima R, Nishiyama J, Araki H, Oshima Y: Chromosome engineering in Saccharomyces cerevisiae by using a site-specific recombination system of a yeast plasmid. J Bact 172: 610–618 (1990).

    Google Scholar 

  41. Morris AC, Schanb TL, James AA: FLP-mediated recombination in the vector mosquito Aedes aegypti. Nucl Acids Res 19: 5895–5900 (1991).

    Google Scholar 

  42. Nam HG, Giraudat J, denBoer B, Moonan F, Loos WDB, Hauge BM, Goodman HM: Restriction fragment length polymorphism linkage map of Arabidopsis thaliana. Plant Cell 1: 699–705 (1989).

    Google Scholar 

  43. Odell J, Caimi P, Sauer B, Russel S: Site-directed recombination in the genome of transgenic tobacco. Mol Gen Genet 223: 369–378 (1990).

    Google Scholar 

  44. Offringa R, deGroot MJA, Haagsman HJ, Does MJ, van denElzen PJM, Hooykaas PJJ: Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation. EMBO J 9: 3077–3084 (1990).

    Google Scholar 

  45. O'Gorman S, Fox DT, Wahl GM: Recombinase-mediated gene activation and site-specific integration in mammalian cells. Science 251: 1351–1355 (1991).

    Google Scholar 

  46. Onouchi H, Yokoi K, Machida C, Matsuzaki H, Oshima Y, Matsuoka K, Nakamura K, Machida Y: Operation of an efficient site-specific recombination system of Zygosaccharomyces rouxii in tobacco cells. Nucl Acids Res 19: 6373–6378 (1991).

    Google Scholar 

  47. Orban PC, Chui D, Marth JD: Tissue- and site-specific DNA recombination in transgenic mice. Proc Natl Acad Sci USA 89: 6861–6865 (1992).

    Google Scholar 

  48. Osborne BI, Corr CA, Prince JP, Hehl R, Tanksley SD, McCormick S, Baker B: Ac transposition from a T-DNA can generate linked and unlinked clusters of insertions in the tomato genome. Genetics 129: 833–844 (1991).

    Google Scholar 

  49. Paszkowski J, Baur M, Bogucki A, Potrykus I: Gene targetting in plants. EMBO J 7: 4021–4026 (1988).

    Google Scholar 

  50. Qin M, Bayley C, Ow DW: Cre-lox mediated site-specific recombination between plant chromosomes: a novel approach for generating chromosomal translocations. J of Cell Biochem, Supplement 16F: 210 (1992).

  51. Rommens CMT, Haaren MJJv, Buchel AS, Mol JMN, Tunen AJv, Nijkamp HJJ, Hille J: Transactivation of Ds by Ac-transposase gene fusions in tobacco. Mol Gen Genet 231: 433–441 (1992).

    Google Scholar 

  52. Rommens CMT, Rudenko GN, Dijkwel PP, vanHaaren MJJ, Ouwerkerk PBF, Blok KM, Nijkamp HJJ, Hille J: Characterization of the Ac/Ds behaviour in transgenic tomato plants using plasmid rescue. Plant Mol Biol 20: 61–70 (1992).

    Google Scholar 

  53. Rommens CMT, Munyikwa TRI, Overduin B, Nijkamp HJJ, Hille J: Transposition pattern of a modified Ds element in tomato. Plant Mol Biol 21: 1109–1119 (1993).

    Google Scholar 

  54. Russell SH, Hoopes JL, Odell JT: Directed excision of a transgene from the plant genome. Mol Gen Genet 234: 49–59 (1992).

    Google Scholar 

  55. Sauer B: Functional expression of the cre-lox site-specific recombination system in the yeast Saccharomyces cerevisiae. Mol Cell Biol 7: 2087–2096 (1987).

    Google Scholar 

  56. Sauer B, Henderson N: Cre-stimulated recombination at loxP-containing DNA sequences placed into the mammalian genome. Nucl Acids Res 17: 147–161 (1989).

    Google Scholar 

  57. Scofield SR, Harrison K, Nurrish SJ, Jones JDG: Promoter fusions to the Activator transposase gene cause distinct patterns of dissociation excision in tobacco cotyledons. Plant Cell 4: 573–582 (1992).

    Google Scholar 

  58. Sun TP, Goodman HM, Ausubel FM: Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4: 119–128 (1992).

    Google Scholar 

  59. Tanksley SD, Ganal MW, Prince JP, deVicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND: High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141–1160 (1992).

    Google Scholar 

  60. Vincentz M, Cabouche M: Constitutive expression of nitrate reductase allows normal growth and development of Nicotiana plumbaginifolia plants. EMBO J 10: 1027–1035 (1991).

    Google Scholar 

  61. Walden R, Hayashi H, Schell J: T-DNA as a gene tag. Plant J 1: 281–288 (1991).

    Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, Institute for Molecular Biological Sciences, Biocentrum Amsterdam, De Boelelaan 1087, 1081 HV, Amsterdam, Netherlands

    Mark J. J. van Haaren

  2. Plant Gene Expression Center, U.S., Department of Agriculture, 800 Buchanan Street, 94710, Albany, CA, USA

    David W. Ow

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  1. Mark J. J. van Haaren
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  2. David W. Ow
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van Haaren, M.J.J., Ow, D.W. Prospects of applying a combination of DNA transposition and site-specific recombination in plants: a strategy for gene identification and cloning. Plant Mol Biol 23, 525–533 (1993). https://doi.org/10.1007/BF00019300

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