Skip to main content
Log in

BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.)

  • Research Articles
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Retroviruses and retrotransposons make up the broad class of retroelements replicating and transposing via reverse transcriptase. Retroelements have recently been found to be ubiquitous in the plants. We report here the isolation, sequence and analysis of a retroelement from barley (Hordeum vulgare L.) with all the features of a copia-like retrotransposon. This is named BARE-1 (for BArley RetroElement 1), the first such element described for barley. BARE-1 is 12 088 bp, with long terminal repeats (LTRs) of 1829 bp containing perfect 6 bp inverted repeats at their ends and flanked by 4 bp direct repeats in the host DNA. Between the long terminal repeats is an internal domain with a derived amino acid sequence of 1285 residues, bearing homology to the gag, pro, int and rt domains of retroviruses and both plant and non-plant copia-like retrotransposons. Cultivated barley contains about 5000 elements in the genome similar to the BARE-1 putative gag domain, but ten-fold more hybridizing to rt or LTR probes. The particular BARE-1 element reported here appears to be inactive, as the putative protein-coding domain is interrupted by four stop codons and a frameshift. In addition, the 3′ LTR is 4% divergent from the 5′ LTR and contains a 3135 bp insertion. Nevertheless, we have recently detected transcripts hybridizing to BARE-1 on northern blots, presumably from active copies. Analysis of BARE-1 expression and function in barley is currently underway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215: 403–410 (1990).

    PubMed  Google Scholar 

  2. Barber AM, Hizi A, Maizel JVJr, Hughes SH: HIV-1 reverse transcriptase: Structure predictions for the polymerase domain. AIDS Res Hum Retroviruses 6: 1061–1072 (1990).

    PubMed  Google Scholar 

  3. Bennett MD, Smith JB: Nuclear DNA amounts in angiosperms. Phil Trans R Soc Lond B 274: 228–274 (1976).

    Google Scholar 

  4. Berg JM: Potential metal-binding domains in nucleic acid binding proteins. Science 232: 485–487 (1986).

    PubMed  Google Scholar 

  5. Blundell TL, Cooper JB, Šali A, Zhu Z-Y: Comparisons of the sequences, 3-D structures and mechanisms of pepsin-like and retroviral aspartic proteinases. In: Dunn BM (ed) Structure and Function of the Aspartic Proteinases, pp. 443–453. Plenum Press, New York (1991).

    Google Scholar 

  6. Boeke JD, Corces VG: Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43: 403–434 (1989).

    Article  PubMed  Google Scholar 

  7. Bucher P, Trifonov EN: Compilation and analysis of eukaryotic POL II promoter sequences. Nucl Acids Res 14: 10009–10026 (1986).

    PubMed  Google Scholar 

  8. Clare J, Farabaugh P: Nucleotide sequence of yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci USA 82: 2829–2833 (1985).

    PubMed  Google Scholar 

  9. Covey SN: Amino acid homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus. Nucl Acids Res 14: 623–633 (1986).

    PubMed  Google Scholar 

  10. Davies JF, Hostomska Z, Hostomsky Z, Jordan SR, Matthews DA: Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science 252: 88–95 (1991).

    PubMed  Google Scholar 

  11. Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1: 19–21 (1983).

    Google Scholar 

  12. Devereux JR, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for VAX and Convex systems. Nucl Acids Res 12: 387–395 (1984).

    PubMed  Google Scholar 

  13. Doolittle RF, Feng D-F, Johnson MS, McClure MA: Origins and evolutionary relationships of retroviruses. Quart Rev Biol 64: 1–30 (1989).

    Article  PubMed  Google Scholar 

  14. Emori Y, Shiba T, Kanaya S, Inouye S, Yuki S, Saigo K: The nucleotide sequences of copia and copia-related RNA in Drosophila virus-like particles. Nature 315: 773–776 (1985).

    PubMed  Google Scholar 

  15. Feng DF, Doolittle RF: Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25: 351–360 (1987).

    PubMed  Google Scholar 

  16. Finnegan DJ: Eukaryotic transposable elements and genome evolution. Trends Genet 5: 103–107 (1989).

    Article  PubMed  Google Scholar 

  17. Flavell AJ, Smith DB, Kumar A: Extreme heterogeneity of Tyl-copia group retrotransposons in plants. Mol Gen Genet 231: 233–242 (1992).

    PubMed  Google Scholar 

  18. Flavell RB, Rimpau J, Smith DB: Repeated sequence DNA relationships in four cereal genomes. Chromosoma 63: 205–222 (1977).

    Article  Google Scholar 

  19. Georgiev GP: Mobile genetic elements in animal cells and their biological significance. Eur J Biochem 145: 203–220 (1984).

    PubMed  Google Scholar 

  20. Ghosh HP, Ghosh K, Simsek M, RajBhandary UL: Nucleotide sequence of wheat germ cytoplasmic initiator methionine transfer ribonucleic acid. Nucl Acids Res 10: 3241–3247 (1982).

    PubMed  Google Scholar 

  21. Gojobori T, Yokoyama S: Rates of evolution of the retroviral oncogene of Moloney murine sarcoma virus and its cellular homologues. Proc Natl Acad Sci USA 82: 4198–4201 (1985).

    PubMed  Google Scholar 

  22. Grandbastien M-A: Retroelements in higher plants. Trends Genet 8: 103–108 (1992).

    PubMed  Google Scholar 

  23. Grandbastien M-A, Spielmann A, Caboche M: Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337: 376–380 (1989).

    PubMed  Google Scholar 

  24. Grandgenett DP, Mumm SR: Unraveling retrovirus integration. Cell 60: 3–4 (1990).

    Article  PubMed  Google Scholar 

  25. Gribskov M, Burgess RR: Sigma factors from E. coli, B. subtilis, phage SP01, and phage T4 are homologous proteins. Nucl Acids Res 14: 6745–6763 (1986).

    PubMed  Google Scholar 

  26. Guidet F, Rogowsky P, Taylor C, Song W, Langridge P: Cloning and characterization of a new rye-specific repeated sequence. Genome 34: 81–87 (1991).

    Google Scholar 

  27. Hansen L, vonWettstein-Knowles P: The barley genes Ac11 and Ac13 encoding acyl carrier proteins I and III are located on different chromosomes. Mol Gen Genet 229: 467–478 (1991).

    Article  PubMed  Google Scholar 

  28. Hansen LJ, Chalker DL, Sandmeyer SB: Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol 8: 5245–5256 (1988).

    PubMed  Google Scholar 

  29. Harberd NP, Flavell RB, Thompson RD: Identification of a transposon-like insertion in a Glu-1 allele of wheat. Mol Gen Genet 209: 326–332 (1987).

    Article  Google Scholar 

  30. Hartshorne TA, Blumberg H, Young ET: Sequence homology of the yeast regulatory protein ADR1 with Xenopus transcription factor TFIIIA. Nature 320: 283–287 (1986).

    PubMed  Google Scholar 

  31. Hirochika H, Fukuchi F, Hirochika R: Retrotransposons are ubiquitous in plants. In: Molecular Biology of Plant Growth and Development (Proc Third Int Congr Plant Mol Biol, Tucson, USA), Abst. 1758 (1991).

  32. Inouye M, Inouye S: Retroelements in bacteria. Trends Biochem Sci 16: 18–21 (1991).

    Article  PubMed  Google Scholar 

  33. Inouye M, Inouye S: msDNA and bacterial reverse transcriptase. Annu Rev Microbiol 45: 163–186 (1991).

    Article  PubMed  Google Scholar 

  34. Jin Y-K, Bennetzen JL: Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc Natl Acad Sci USA 86: 6235–6239 (1989).

    PubMed  Google Scholar 

  35. Johns MA, Babcock MS, Fuerstenberg SM, Fuerstenberg SI, Freeling M, Simpson RB: An unusually compact retrotransposon in maize. Plant Mol Biol 12: 633–642 (1989).

    Google Scholar 

  36. Johnson MS, McClure MA, Feng D-F, Gray J, Doolittle RF: Computer analysis of retroviral pol genes: Assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci USA 83: 7648–7652 (1986).

    PubMed  Google Scholar 

  37. Joshi CP: An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acids Res 15: 6643–6653 (1987).

    PubMed  Google Scholar 

  38. Konieczny A, Voytas DF, Cummings MP, Ausubel F: A superfamily of Arabidopsis thaliana retrotransposons. Genetics 127: 801–809 (1991).

    PubMed  Google Scholar 

  39. Kozak M: Selection of initiation sites by eucaryotic ribosomes: effect of inserting AUG triplets upstream from the coding sequence for preproinsulin. Nucl Acids Res 12: 3873–3893 (1984).

    PubMed  Google Scholar 

  40. Kyte J, Doolittle RP: A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132 (1982).

    PubMed  Google Scholar 

  41. Lapatto R, Blundell T, Hemmings A, Overington J, Wilderspin A, Wood S, Merson JR, Whittle PJ, Danley DE, Geoghegan KF, Hawrylik SJ, Lee SE, Scheld KG, Hobart PM: X-ray analysis of HIV-1 proteinase at 2.7 Å resolution confirms structural homology among retroviral enzymes. Nature 342: 299–302 (1989).

    Article  PubMed  Google Scholar 

  42. Larder BA, Purifoy DJM, Powell KL, Darby G: Site-specific mutagenesis of AIDS virus reverse transcriptase. Nature 327: 716–717 (1987).

    Article  PubMed  Google Scholar 

  43. Lee D, Ellis THN, Turner L, Hellens RP, Cleary WG: A copia-like element in Pisum demonstrates the uses of dispersed repeated sequences in genetic analysis. Plant Mol Biol 15: 707–722 (1990).

    Google Scholar 

  44. Lim D, Maas WK: Reverse transcriptase in bacteria. Mol Microbiol 3: 1141–1144 (1989).

    PubMed  Google Scholar 

  45. Lucas H, Moore G, Murphy G, Flavell RB: Inverted repeats in the long-terminal repeats of the wheat retrotransposon Wis 2–1A. Mol Biol Evol 9: 716–728 (1992).

    PubMed  Google Scholar 

  46. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  47. Marlor RL, Parkhurst SM, Corces VG: The Drosophila melanogaster Gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6: 1129–1134 (1986).

    PubMed  Google Scholar 

  48. McClintock B: The significance of responses of the genome to challenge. Science 226: 792–801 (1984).

    Google Scholar 

  49. McClure MA, Johnson MS, Feng D-F, Doolittle RF: Sequence comparisons of retroviral proteins: Relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85: 2469–2473 (1988).

    PubMed  Google Scholar 

  50. McIntyre CL, Clarke BC, Appels R: Amplification and dispersion of repeated DNA sequences in the Triticeae. Plant Syst Evol 160: 39–59 (1988).

    Google Scholar 

  51. Miller J, McLachlan AD, Klug A: Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4: 1609–1614 (1985).

    Google Scholar 

  52. Mogen BD, MacDonald MH, Graybosch R, Hunt AG: Upstream sequences other than AAUAAA are required for efficient messenger RNA 3′-end formation in plants. Plant Cell 2: 1261–1272 (1990).

    Article  PubMed  Google Scholar 

  53. Moore G, Cheung W, Schwarzacher T, Flavell R: BIS 1, a major component of the cereal genome and a tool for studying genomic organization. Genomics 10: 469–476 (1991).

    PubMed  Google Scholar 

  54. Moore G, Lucas H, Batty N, Flavell R: A family of retrotransposons and associated genomic variation in wheat. Genomics 10: 461–468 (1991).

    PubMed  Google Scholar 

  55. 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).

    PubMed  Google Scholar 

  56. Needleman SB, Wunsch CD: A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48: 443–453 (1970).

    PubMed  Google Scholar 

  57. Pearl LH, Taylor WR: A structural model for the retroviral proteases. Nature 329: 351–354 (1987).

    Article  PubMed  Google Scholar 

  58. Pouteau S, Huttner E, Grandbastien MA, Caboche M: Specific expression of the tobacco Tnt 1 retrotransposon in protoplasts. EMBO J 10: 1911–1918 (1991).

    PubMed  Google Scholar 

  59. Pouteau S, Spielmann A, Meyer C, Grandbastien M-A, Caboche M: Effects of Tnt1 tobacco retrotransposon insertion on target gene transcription. Mol Gen Genet 228: 233–239 (1991).

    Article  PubMed  Google Scholar 

  60. Prats AC, Sarih L, Gabus C, Litvak S, Keith G, Darlix JL: Small finger protein of avian and murine retroviruses has nucleic acid annealing activity and positions the replication primer tRNA onto genomic RNA. EMBO J 7: 1777–1783 (1988).

    PubMed  Google Scholar 

  61. Qu R, Bhattacharyya M, Laco GS, deKochko A, Rao BLS, Kaniewska MB, Elmer JS, Rochester DE, Smith CE, Beachy RN: Characterization of the genome of rice tungro bacilliform virus: Comparison with Commelina yellow mottle virus and caulimoviruses. Virology 185: 354–364 (1991).

    Article  PubMed  Google Scholar 

  62. Roberts JD, Bebenek K, Kunkel TA: The accuracy of reverse transcriptase from HIV-1. Science 242: 1171–1173 (1988).

    PubMed  Google Scholar 

  63. Roeder GS, Farabaugh PJ, Chaleff DT, Fink GR: The origins of gene instability in yeast. Science 209: 1375–1380 (1980).

    PubMed  Google Scholar 

  64. Rogowski PM, Manning S, Liu J-Y, Langridge P: The R173 family of rye-specific repetitive DNA sequences: a structural analysis. Genome 34: 88–95 (1991).

    Google Scholar 

  65. Rogowsky PM, Liu J-Y, Manning S, Taylor C, Langridge P: Structural heterogeneity in the R173 family of ryespecific repetitive DNA sequences. Plant Mol Biol 20: 95–112 (1992).

    Google Scholar 

  66. Runeberg-Roos P, Törmäkangas K, Östman A: Primary structure of a barley-grain aspartic proteinase. Eur J Biochem 202: 1021–1027 (1991).

    PubMed  Google Scholar 

  67. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  68. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  69. Schnorr KM, Juricek M, Culley D, Kleinhofs A: Analysis of barley nitrate reductase cDNA and genomic clones. Mol Gen Genet 227: 411–416 (1991).

    Article  PubMed  Google Scholar 

  70. Schödel D, Weimer T, Will H, Sprengel R: Amino acid similarity between retroviral and E. coli RNase H and hepadnaviral gene products. AIDS Res Hum Retroviruses 4: 9–11 (1988).

    Google Scholar 

  71. Schuster W, Brennicke A: Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: is genetic information transferred between organelles via RNA? EMBO J 6: 2857–2863 (1987).

    PubMed  Google Scholar 

  72. Skalka AM: Retroviral proteases: first glimpses at the anatomy of a processing machine. Cell 56: 911–913 (1989).

    Article  PubMed  Google Scholar 

  73. Smyth DR, Kalitsis P, Joseph JL, Sentry JW: Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc Natl Acad Sci USA 86: 5015–5019 (1989).

    PubMed  Google Scholar 

  74. Steinhauer DA, Holland JJ: Direct method for quantitation of extreme polymerase error frequencies at selected single base sites in viral RNA. J Virol 57: 219–228 (1986).

    PubMed  Google Scholar 

  75. Tang J, Wong RNS: Evolution in the structure and function of aspartic proteinases. J Cell Biochem 33: 53–63 (1987).

    PubMed  Google Scholar 

  76. Temin HW: Structure, variation and synthesis of retrovirus long terminal repeat. Cell 27: 1–3 (1981).

    Article  PubMed  Google Scholar 

  77. Varmus HE: Retroviruses. In: Shapiro JA (ed) Mobile Genetic Elements, pp. 411–503. Academic Press, New York (1983).

    Google Scholar 

  78. Voytas DF, Ausubel FM: A copia-like transposable element family in Arabidopsis thaliana. Nature 336: 242–244 (1988).

    Article  PubMed  Google Scholar 

  79. Voytas DF, Konieczny A, Cummings MP, Ausubel FM: The structure, distribution and evolution of the Ta1 retrotransposable element family of Arabidopsis thaliana. Genetics 126: 713–721 (1990).

    PubMed  Google Scholar 

  80. Voytas DF, Cummings M, Konieczny A, Ausubel FM, Rodermel SR: copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89: 7124–7128 (1992).

    PubMed  Google Scholar 

  81. Warmington JR, Waring RB, Newlon CS, Indge KJ, Oliver SG: Nucleotide sequence characterization of Ty 1–17, a class II transposon from yeast. Nucl Acids Res 13: 6679–6693 (1985).

    PubMed  Google Scholar 

  82. Wellink J, vanKammen A: Proteases involved in the processing of viral polyproteins. Arch Virol 98: 1–26 (1988).

    PubMed  Google Scholar 

  83. Wilke CM, Adams J: Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics 131: 31–42 (1992).

    PubMed  Google Scholar 

  84. Xiong Y, Eickbush TH: Origin and evolution of retroelements based upon their novel reverse transcriptase sequences. EMBO J 9: 3353–3362 (1992).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Manninen, I., Schulman, A.H. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol Biol 22, 829–846 (1993). https://doi.org/10.1007/BF00027369

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00027369

Key words

Navigation