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Plant Molecular Biology

, Volume 35, Issue 1–2, pp 231–240 | Cite as

Retrotransposons of rice: their regulation and use for genome analysis

  • Hirohiko Hirochika
Article

Abstract

Retrotransposons were extensively surveyed in rice using two molecular methods. The total copy number of retrotransposons in the rice genome was estimated to be about 1000 and 32 families were isolated, showing that retrotransposons are a major class of transposable elements in rice. Although these retrotransposons appear inactive during normal growth conditions, 5 out of 32 families were active under tissue culture conditions. The most active element, Tos17, was studied in detail. Its activity was show to be regulated mainly at the transcriptional level. The analysis of target sites of transposition indicated that activation of Tos17 is an important cause of tissue culture-induced mutations in rice. Tissue culture-induced activation of Tos17 was used to develop the site-selected mutagenesis system, in which mutants carrying a Tos17 insertion in the gene of interest can be identified among rice plants regenerated from tissue culture by the PCR using one primer for the ends of Tos17 and another for the gene of interest. This system will contribute to understanding the functions of rice genes whose sequences are being determined by the rice genome project.

insertion mutation retrotransposon rice somaclonal variation transposable elements transposon tagging 

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References

  1. 1.
    Bajaj YSP: Somaclonal variation: origin, induction, cryopreservation, and implications in plant breeding. In Bajaj YSP (ed) Somaclonal variation in crop, pp. 4–48. Springer-Verlag, Berlin (1991).Google Scholar
  2. 2.
    Ballinger DG, Benzer S: Targeted gene mutations in Drosophila. Proc Natl Acad Sci USA 86: 9402–9406 (1989).Google Scholar
  3. 3.
    Bancroft I, Dean C: Transposition pattern of the maize element Ds in Arabidopsis thaliana. Genetics 134: 1221–1229 (1993).Google Scholar
  4. 4.
    Bancroft I, Jones JDG, Dean C: Heterologous transposon tagging of the DRL1 locus in Arabidopsis. Plant Cell 5: 631–638 (1993).Google Scholar
  5. 5.
    Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP: Cloning and characterization of the maize An1 gene. Plant Cell 7: 75–84 (1995).Google Scholar
  6. 6.
    Bingham P, Zachar Z: Retrotransposons and the FB transposon from Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA, pp. 485–502. American Society for Microbiology, Washington, DC (1989).Google Scholar
  7. 7.
    Bingham PM, Levis R, Rubin G: Cloning of DNA sequences from the white locus of D. melonagaster by a novel and general method. Cell 25: 693–704 (1981).Google Scholar
  8. 8.
    Brettell RIS, Dennis ES, Scowcroft WR, Peacock WJ: Molecular analysis of a somaclonal mutant of maize alcohol dehydrogenase. Mol Gen Genet 202: 235–239 (1986).Google Scholar
  9. 9.
    Boeke JD: Transposable elements in Saccharomyces cerevisiae. In: Berg DE, Howe MM (eds) Mobile DNA, pp. 335–374. American Society for Microbiology, Washington, DC (1989).Google Scholar
  10. 10.
    Boeke JD, Garfinkel DJ, Styles CA, Fink GR: Ty elements transpose through an RNA intermediate. Cell 40: 491–500 (1985).Google Scholar
  11. 11.
    Bureau TE, White SE, Wessler SR: Transduction of a cellular gene by a plant retroelement. Cell 77: 479–480 (1994).Google Scholar
  12. 12.
    Casacuberta JM, Grandbastien MA: Characterization of LTR sequences involved in the protoplasts specific expression of the tobacco Tnt1 retrotransposon. Nucl Acids Res 21: 2087–2093 (1993).Google Scholar
  13. 13.
    Castle LA, Errampalli D, Atherton TL, Franzmann LH, Yoon ES, Meinke DW: Genetic and molecular characterization of embryonic mutants identified following seed transformation in Arabidopsis. Mol Gen Genet 241: 504–514 (1993).Google Scholar
  14. 14.
    Das L, Martienssen R: Site-selected transposon mutagenesis at the hfc109 locus in maize. Plant Cell 7: 287–294 (1995).Google Scholar
  15. 15.
    Dennis ES, Brettell RIS, Peacock WJ: A tissue culture induced Adh null mutant of maize results from a single base change. Mol Gen Genet 210: 181–183 (1987).Google Scholar
  16. 16.
    Doolittle RF, Feng D-F, Johnson MS, McClure MA: Origin and evolutionary relationships of retroviruses. Q Rev Biol 64, 1–30 (1989).Google Scholar
  17. 17.
    Echalier G: Drosophila retrotransposons: interactions with genome. Adv Virus Res 36: 33–103 (1989).Google Scholar
  18. 18.
    Evans DA, Sharp WR: Singlemutations in tomato plants regenerated from tissue culture. Science 221: 949–951 (1983).Google Scholar
  19. 19.
    Finnegan DJ: Eukaryotic transposable elements and genome evolution. Trends Genet 5: 103–107 (1989).Google Scholar
  20. 20.
    Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A: Ty1-copia group retrotransposons are ubiquitous and heterogenous in higher plants. Nucl Acids Res 20: 3639–3644 (1992).Google Scholar
  21. 21.
    Flavell AJ, Smith DB, Kumar A: Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet 231: 233–242 (1992).Google Scholar
  22. 22.
    Flavell AJ, Pearce SR, Kumar A: Plant transposable elements and the genome. Curr Opin Genet Dev 4: 838–844 (1994).Google Scholar
  23. 23.
    Fukuchi A, Nakamura A, Hirano H, Hirochika H, Kikuchi F: Linkage analysis for a semidwarfing gene sd-1 on chromosome 1. Rice Genetic Newsletter 9: 50–52 (1992).Google Scholar
  24. 24.
    Fukuchi A, Kikuchi F, Hirochika H: DNA fingerprinting of cultivated rice with rice retrotransposon probes. Jnp J Genet 68: 195–204 (1993).Google Scholar
  25. 25.
    Grandbastien, M-A: Retroelements in higher plants. Trends Genet. 8: 103–108 (1992).Google Scholar
  26. 26.
    Grandbastien M-A, Spielman A, Caboche M: Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337: 376–380 (1989).Google Scholar
  27. 27.
    Grandbastien M-A, Audeon C, Casacuberta JM, Grappin P, Lucas H, Moreau C, Pouteau S: Functional analysis of the tobacco Tnt1 retrotransposon. Genetica 93: 181–189 (1994).Google Scholar
  28. 28.
    Green MM: Mobile DNA elements and spontaneous gene mutation. In: Lambert ME, McDonald JF, Weinstein IB (eds) Eukaryotic Transposable Elements as Mutagenic Agents, pp. 41–50. Cold Spring Harbor Laboratory Press, New York (1988).Google Scholar
  29. 29.
    Haring MA, Rommens CMT, Nijkamp HJJ, Hille J: The use of transgenic plants to understand tranposition mechanisms and to develop transposon tagging strategies. Plant Mol Biol 16: 449–461 (1991).Google Scholar
  30. 30.
    Hirochika H: Activation of tobacco retrotransposons during tissue culture. EMBO J 12: 2521–2528 (1993).Google Scholar
  31. 31.
    Hirochika H: Activation of plant retrotransposons by stress. In: Oono K, Takaiwa F (eds) Modification of Gene Expression and Non-Mendelian Inheritance, pp. 15–21. National Institute of Agrobiological Resource, Tsukuba (1995).Google Scholar
  32. 32.
    Hirochika H, Fukuchi A: Transposable elements in rice plants. Jpn Agr Res Q 25: 230–237 (1992).Google Scholar
  33. 33.
    Hirochika H, Hirochika R: Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn J Genet 68: 35–46 (1993).Google Scholar
  34. 34.
    Hirochika H, Fukuchi A, Kikuchi F: Retrotransposon families in rice. Mol Gen Genet 233: 209–216 (1992).Google Scholar
  35. 35.
    Hirochika H, Otsuki H, Yoshikawa M, Otsuki Y, Sugimoto K, Takeda S: Autonomous transposition of the tobacco retrotransposon Tto1 in rice. Plant Cell 8: 725–734 (1996).Google Scholar
  36. 36.
    Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M: Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93: 7783–7788 (1996).Google Scholar
  37. 37.
    Hu W, Das OP, Messing J: Zeon-1, a member of a new maize retrotransposon family. Mol Gen Genet 248: 471–480 (1995).Google Scholar
  38. 38.
    Jin Y-K, Bennetzen JL: Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6: 1177–1186 (1994).Google Scholar
  39. 39.
    Johns MA, Mottinger J, Freeling M: A low copy number, copia-like transposon inmaize. EMBO J 4: 1093–1102 (1985).Google Scholar
  40. 40.
    Kaiser K, Goodwin SF: ‘site-selected’ transposonmutagenesis of Drosophila. Proc Natl Acad Sci USA 87: 1686–1690 (1990).Google Scholar
  41. 41.
    Koes R, Souer E, van Houwelingen A, Mur L, Spelt C, Quattrocchio F, Wing J, Oppedijk B, Ahmed S, Maes T, Gerats T, Hoogeveen P, Meesters M, Kloos D, Mol JN: Targeted gene inactivation in petunia by PCR-based dselection of transposon insertion mutants. Proc Natl Acad Sci USA 92: 8149–8153 (1995).Google Scholar
  42. 42.
    Konieczny A, Voytas DF, Cummings MP, Ausubel FM: A superfamily of Arabidopsis thaliana retrotransposons. Genetics 127: 801–809 (1991).Google Scholar
  43. 43.
    Kricker MC, Drake JW, Radman M: Duplication-targeted DNA methylation and mutagenesis in the evolution of eukaryotic chromosomes. Proc Natl Acad Sci USA 89: 1075–1079 (1992).Google Scholar
  44. 44.
    Larkin PJ, Scowcroft WR: Somaclonal variation: a novel source of variability from cell culture for plant improvement. Theor Appl Genet 60: 197–214 (1981).Google Scholar
  45. 45.
    Larkin PJ, Ryan SA, Brettell RIS, Scowcroft WR: Heritable somaclonal variation in wheat. Theor Appl Genet 67: 443–455 (1984).Google Scholar
  46. 46.
    Loake GJ, Faktor O, Lamb CJ, Dixon RA: Combination of H-box and G-box cis-elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc Natl Acad Sci USA 89: 9230–9234 (1992).Google Scholar
  47. 47.
    Lucas H, Feuerbach F, Kunert K, Grandbastien M-A, Caboche M: The tobacco retrotransposon Tnt1 transposes in Arabidopsis thaliana. EMBO J 14: 2364–2373 (1995).Google Scholar
  48. 48.
    Manninen I, Schulman AH: BARE-1, a copia-like retroelement in barley (Hordeum vulgareL.). Plant Mol Biol 22: 829–846 (1993).Google Scholar
  49. 49.
    McClintock B: The significance of responses of the genome to challenge. Science 226: 792–801 (1984).Google Scholar
  50. 50.
    Moore G, Cheung W, Schwazacher T, Flavell R: BIS 1, a major component of the cereal genome and a tool for studying genomic organization. Genomics 10: 469–476 (1991).Google Scholar
  51. 51.
    Motohashi R, Ohtsubo E, Ohtsubo H: Identification of Tnr3, a Suppressor-Mutator/Enhancer-like transposable element from rice. Mol Gen Genet 250: 148–152 (1996).Google Scholar
  52. 52.
    Mount SM, Rubin GM: Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol 5: 1630–1638 (1985).Google Scholar
  53. 53.
    Okagaki RJ, Wessler SR: Comparison of non-mutant and mutant waxy genes in rice and maize. Genetics 120: 1137–1143 (1988).Google Scholar
  54. 54.
    Pearce SR, Harrison G, Li D, Heslop-Harrison JS, Kumar A, Flavell AJ: The Ty1-copia group retrotransposons in Vicia species: copy number, sequence heterogeneity and chromosomal localisation. Mol Gen Genet 250: 305–315 (1996).Google Scholar
  55. 55.
    Pennisi E: From genes to genome biology. Science 272: 1736–1738 (1996).Google Scholar
  56. 56.
    Peschke VM, Phillips RL: Activation of themaize transposable element Suppressor-mutator Spm) in tissue culture. Theor Appl Genet 81: 90–97 (1991).Google Scholar
  57. 57.
    Peschke VM, Phillips RL, Gengenbach BG: Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238: 804–807 (1987).Google Scholar
  58. 58.
    Peterson PA: Transposable elements in maize: their role in creating plant genetic variability. Adv Agron 51: 79–123 (1993).Google Scholar
  59. 59.
    Pouteau S, Huttner E, Grandbastien MA, Caboche M: Specific expression of the tobacco Tnt1 retrotransposon in protoplats. EMBO J 10: 1911–1918 (1991).Google Scholar
  60. 60.
    Pouteau S, Grandbastien M-A, Boccara M: Microbial elicitors of plant defence responses activate transcription of a retrotransposon. Plant J 5: 535–542 (1994).Google Scholar
  61. 61.
    Purugganan MD, Wessler S: Molecular evolution of Magellan, a maize Ty3/gypsy-like retrotransposon. Proc Natl Acad Sci USA 91: 11674–11678 (1994).Google Scholar
  62. 62.
    Sasaki T, Song J, Koga-Ban Y, Matsui E, Fang F et al: Towards cataloguing all rice genes: large scale sequencing of randomly chosen cDNAs from a callus cDNA library. Plant J 6: 615–624 (1994).Google Scholar
  63. 63.
    Sentry JW, Smyth DR: An element with long terminal repeats and its variant arrangements in the genome of Lilium henryi. Mol Gen Genet 215: 349–354 (1989).Google Scholar
  64. 64.
    Shepard JF: Protoplasts as sources of disease resistance in plants. Annu Rev Phytopath 19: 145–166 (1981).Google Scholar
  65. 65.
    Sun Z-X, Zheng K-L: Somaclonal variation in rice. In: Bajaj YPS (ed) Somaclonal Variation in Crop Improvement I, pp. 288–315. Springer-Verlag, Berlin (1990).Google Scholar
  66. 66.
    Sundaresan V: Horizontal spread of transpososn mutagenesis: new uses for old elements. Trends Plant Sci 1: 184–190 (1996).Google Scholar
  67. 67.
    Toh H, Kikuno R, Hayashida H, Miyata T, Kugimiya W, Inouye S, Yuki S, Saigo K: Close structural resemblance between putative polymerase of a Drosophila transposable genetic element 17.6 and pol gene product of Molony murine leukemia virus. EMBO J 4: 1267–1272 (1985).Google Scholar
  68. 68.
    Varagona MJ, Purugganan M, Wessler SR: Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4: 811–820 (1992).Google Scholar
  69. 69.
    Yoytas DF, Boeke JD: Yeast retrotransposons and tRNAs. Trends Genet 9: 421–427 (1993).Google Scholar
  70. 70.
    Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR: Copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89: 7124–7128 (1992).Google Scholar
  71. 71.
    Wessler SR, Bureau TE, White SE: LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Devel 5: 814–821 (1995).Google Scholar
  72. 72.
    White SE, Habera LF, Wessler SR: Retrotransposons in the flanking regions of normal plant genes: a role of copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci USA 91: 11792–11796 (1994).Google Scholar
  73. 73.
    Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H: Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86: 6201–6205 (1989).Google Scholar
  74. 74.
    Xiong Y, Eickbush TH: Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9: 3353–3362 (1990).Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Hirohiko Hirochika
    • 1
  1. 1.Dept. of Molecular GeneticsNational Institute of Agrobiological ResourcesTsukuba, IbarakiJapan

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