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Structure, functionality, and evolution of the BARE-1 retrotransposon of barley

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Abstract

The BARE-1 retrotransposon is a major, active component of the genome of barley (Hordeum vulgareL.) and other Hordeum species. Copia-like in its organization, it consists of 1.8-kb long terminal repeats bounding an internal domain of 5275bp which encodes a predicted polyprotein of 1301 residues. The polyprotein contains the key residues, structural motifs, and conserved regions associated with retroviral and retrotransposon GAG, aspartic proteinase, integrase, reverse transcriptase, and RNaseH polypeptides. BARE-1 is actively transcribed and translated. As part of our effort to understand the evolution and function of BARE-1, we have examined its copy number and localization. Full-length members of the BARE-1 family constitute 2.8% of the barley genome. Globally, they are dispersed throughout the genome, excepting the centromeric, telomeric, and NOR regions. Locally, BARE-1 occurs more commonly in repetitive DNA than in coding regions, forming clusters of nested insertions. Both barley and other Hordeum genomes contain a high proportion of BARE-1 solo LTRs. New techniques have been developed which exploit the insertion site polymorphism generated by -1 integration to produce molecular markers for breeding, biodiversity, and mapping applications.

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References

  • Bennetzen, J.L., 1996. The contributions of retroelements to plant genome organization, function and evolution. Trends Microb. 4: 347–353.

    Article  CAS  Google Scholar 

  • Bevan, M., I. Brancroft, E. Bent, K. Love, H. Goodman et al., 1998. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391: 485–488.

    Article  PubMed  CAS  Google Scholar 

  • Boeke, J.D. & V.G. Corces, 1989. Transcription and reverse transcription of retrotransposons. Ann. Rev. Microbiol. 43: 403–434.

    Article  CAS  Google Scholar 

  • Boeke, J.D. & K.B. Chapman, 1991. Retrotransposition mechanisms. Curr. Opin. Cell Biol. 3: 502–507.

    Article  PubMed  CAS  Google Scholar 

  • Chavanne, F., D.X. Zhang, M.F. Liaud & R. Cerff, 1998. Structure and evolution of Cyclops: a novel giant retrotransposon of the Ty3/Gypsy family highly amplified in pea and other legume species. Plant Mol. Biol. 37: 363–375.

    Article  PubMed  CAS  Google Scholar 

  • Chen, M., P. SanMiguel & J.L. Bennetzen, 1998. Sequence organization and conservation in sh2/a1-homologous regions of sorghum and rice. Genetics 148: 435–443.

    PubMed  CAS  Google Scholar 

  • Day, A.M., M. Schimer-Rahire, M.R. Kuchka, S.P. Mayfield & J.D. Rochaix, 1988. A transposon with an unusual arrangement of long terminal repeats in the green alga Chlamydomonas reinhardtii. EMBO J. 7: 1917–1927.

    PubMed  CAS  Google Scholar 

  • Deragon, J.M., B.S. Landry, T. Pelissier, S. Tutois, S. Tourmente & G. Picard, 1994. An analysis of retroposition in plants of SINEs from Brassica napus. J. Mol. Evol. 39: 378–386.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, T.H.N., S.J. Poyser, M.R. Knox, A.V. Vershinin & M.J. Ambrose, 1998. Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. Mol. Gen. Genet. 260: 9–19.

    PubMed  CAS  Google Scholar 

  • Faustinella, F., H. Kwon, F. Serrano, J.W. Belmont, C.T. Caskey et al., 1994. A new family of murine retroviral vectors with extended multiple cloning sites for gene insertion. Hum. Gene Ther. 5: 307–312.

    PubMed  CAS  Google Scholar 

  • Flavell, A.J., D.B. Smith & A. Kumar, 1992. Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol. Gen. Genet. 231: 233–242.

    PubMed  CAS  Google Scholar 

  • Flavell, A.J., M.R. Knox, S.R. Pearce & T.H.N. Ellis, 1998. Retrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis. Plant J. 16: 643–650.

    Article  PubMed  CAS  Google Scholar 

  • Goff, S.P., 1990. Retroviral reverse transcriptase: synthesis, structure and function. J. Acquire. Immune Defic. Syn. Dr. 3: 817–831.

    CAS  Google Scholar 

  • Grandbastien, M.A., 1992. Retroelements in higher plants. Trends Genet. 8: 103–108.

    PubMed  CAS  Google Scholar 

  • Gribbon, B.M., S.R. Pearce, R. Kalendar, A.H. Schulman, L. Paulin, P. Jack, A. Kumar & A.J. Flavell, 1999. Phylogeny and transpositional activity of Ty-copia group retrotransposons in cereal genomes. Mol. Gen. Genet. 261: 883–891.

    Article  PubMed  CAS  Google Scholar 

  • Heyman, T., B. Agouti, S. Riant, D.X. Wilhelm & M.L. Wilhelm, 1995. Plus-strand DNA synthesis of yeast retrotransposon Ty1 is initiated at two sites: PPT1 next to the 3′ and PPT2 within the pol gene. PPT1 is sufficient for Ty1 transposition. J. Mol. Biol. 253: 291–303.

    Article  PubMed  CAS  Google Scholar 

  • Hirochika, H., 1993. Activation of tobacco retrotransposons during tissue culture. EMBO J. 12: 2521–2528.

    PubMed  CAS  Google Scholar 

  • Hirochika, H. & R. Hirochika, 1993. Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn. J. Genet. 68: 35–46.

    Article  PubMed  CAS  Google Scholar 

  • Hirochika, H., K. Sugimoto, Y. Otsuki, H. Tsugawa & M. Kanda, 1996. Autonomous transposition of the tobacco retrotransposon Tto1 in rice. Plant Cell 8: 725–734.

    Article  PubMed  CAS  Google Scholar 

  • Jääskeläinen, M., A.H. Mykkänen, T. Arna, C. Vicient, A. Suoniemi, R. Kalendar, H. Savilahti & A.H. Schulman, 1999. Retrotransposon BARE-1: expression of encoded proteins and formation of virus-like particles in barley cells. Plant J. 20: 413–422.

    Article  PubMed  Google Scholar 

  • Jordan, I.K. & J.F. McDonald, 1999. Tempo and mode of Ty element evolution in Saccharomyces cerevisiae. Genetics 151: 1341–1351.

    PubMed  CAS  Google Scholar 

  • Joseph, J.L., J.W. Sentry & D.R. Smyth, 1990. Interspecies distribution of abundant DNA sequences in Lilium. J. Mol. Evol. 30: 146–154.

    Article  CAS  Google Scholar 

  • Kalendar, R., T. Grob, M. Regina, A. Suoniemi & A.H. Schulman, 1999. IRAP and REMAP: Two new retrotransposon-based DNA fingerprinting techniques. Theor. Appl. Genet. 98: 704–711.

    Article  CAS  Google Scholar 

  • Kankaanpää, J., L. Mannonen & A.H. Schulman, 1996. The genome sizes of Hordeum species show considerable variation. Genome 39: 730–735.

    Google Scholar 

  • Kim, A., C. Terzian, P. Santamaria, A. Pelisson, N. Prud'homme & A. Bucheton, 1994. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 91: 1285–1289.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J.M., S. Vanguri, J.D. Boeke, A. Gabriel & D.F. Voytas, 1998. Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8: 464–478.

    PubMed  CAS  Google Scholar 

  • Kumar, A. & J. Bennetzen, 1999. Plant Retrotransposons. Annu. Rev. Genet. 33: 479–532.

    Article  PubMed  CAS  Google Scholar 

  • Laten, H., A. Majumdar & E.A. Gaucher, 1998. SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc. Natl. Acad. Sci. USA 95: 6897–6902.

    Article  PubMed  CAS  Google Scholar 

  • Lauermann, V., M. Hermankova & J.D. Boeke, 1997. Increased length of long terminal repeats inhibits Ty1 transposition and leads to the formation of tandem multimers. Genetics 145: 911–922.

    PubMed  CAS  Google Scholar 

  • Lucas, H., F. Feuerbach, K. Kunert, M.-A. Grandbastien & M. Caboche, 1995. RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J. 14: 2364–2373.

    PubMed  CAS  Google Scholar 

  • Lucas, H., G. Moore, G. Murphy & R.B. Flavell, 1992. Inverted repeats in the long-terminal repeats of the wheat retrotransposon Wis2–1A. Mol. Biol. Evol. 9: 716–728.

    PubMed  CAS  Google Scholar 

  • Manninen, O., R. Kalendar, J. Robinson & A.H. Schulman. Application of BARE-1 retrotransposon markers to map a major resistance gene for net blotch in barley. Submitted.

  • Manninen, I. & A.H. Schulman, 1993. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol. Biol. 22: 829–846.

    Article  PubMed  CAS  Google Scholar 

  • Marillonnet, S. & S.R. Wessler, 1998. Extreme structural heterogeneity among the members of a maize retrotransposon family. Genetics 150: 1245–1256.

    PubMed  CAS  Google Scholar 

  • Matsuoka, Y. & K. Tsunewaki, 1999. Evolutionary dynamics of Ty1-copia group retrotransposons in grass shown by reverse transcriptase domain analysis. Mol. Biol. Evol. 16: 208–217.

    PubMed  CAS  Google Scholar 

  • Noma, K., R. Nakajima, H. Ohtsubo & E. Ohtsubo, 1997. RIRE1, a retrotransposon from wild rice Oryza australiensis. Genes Genet. Syst. 72: 131–140.

    Article  PubMed  CAS  Google Scholar 

  • Pearce, S.R., G. Harrison, J.S. Heslop-Harrison, A.J. Flavell & A. Kumar, 1997. Characterization and genomic organisation of Ty1-copia group retrotransposons in rye (Secale cereale). Genome 40: 617–625.

    PubMed  CAS  Google Scholar 

  • Pearce, S.R., G. Harrison, D. Li, J.S. Heslop-Harrison, A. Kumar & A.J. Flavell, 1996. The Ty1-copia group retrotransposons in Vicia species: copy number, sequence heterogeneity and chromosomal localisation. Mol. Gen. Genet. 250: 305–315.

    PubMed  CAS  Google Scholar 

  • Pearce, SR, C. Stuart-Rogers, M.R. Knox, A. Kumar, T.H.N. Ellis & A.J. Flavell, 1999. Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J. 19: 711–717.

    Article  PubMed  CAS  Google Scholar 

  • Pelisson, A., L. Teysset, F. Chalvet, A. Kim, N. Prud'homme, C. Terzian & A. Bucheton, 1997. About the origin of retroviruses and the co-evolution of the gypsy retrovirus with the Drosophila flamenco host gene. Genetica 100: 29–37.

    Article  PubMed  CAS  Google Scholar 

  • Pimpinelli, S., M. Berloco, L. Fanti, P. Demitri, E. Bonaccorsi et al., 1995. Transposable elements are stable components of Drosophila melanogaster heterochromatin. Proc. Natl. Acad. Sci. USA 92: 3804–3808.

    Article  PubMed  CAS  Google Scholar 

  • Pouteau, S., E. Huttner, M.A. Grandbastien & M. Caboche, 1991. Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 10: 1911–1918.

    PubMed  CAS  Google Scholar 

  • Reamon-Buttner, S.M., T. Schmidt & C. Jung, 1999. AFLPs represent highly repetitive sequences in Asparagus officinalis L. Chrom. Res. 7: 297–304.

    Article  PubMed  CAS  Google Scholar 

  • Reddy, S.J., J.V. Degregori, H. von Melchinger & E. Ruley, 1991. Retrovirus promoter trap vector to induce lacZ gene fusion in mammalian cells. J. Virol. 65: 1507–1515.

    PubMed  CAS  Google Scholar 

  • Royo, J., N. Nass, D.P. Matton, S. Okamoto, A.E. Clarke & E. Newbigin, 1996. A retrotransposon-like sequence linked to the S-locus of Nicotiana alata is expressed in styles in response to touch. Mol. Gen. Genet. 250: 180–188.

    PubMed  CAS  Google Scholar 

  • SanMiguel, P., A. Tikhonov, Y.K. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer, K.J. Edwards, M. Lee, Z. Avramova & J.L. Bennetzen, 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, T., 1999. LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol. Biol. 40: 903–910.

    Article  PubMed  CAS  Google Scholar 

  • Scortecci, K.C., R. Raina, N.V. Fedoroff & M.A. van Sluys, 1999. Negative effect of the 5′-untranslated leader sequence on Ac transposon promoter expression. Plant Mol. Biol. 40: 935–944.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd, N.S., Z. Schwarz-Sommer, J. Blumberg vel Spalve, M. Gupta, U. Wienand & H. Saedler, 1984. Similarity of the Cin1 repetitive family of Zea mays to eukaryotic transposable elements. Nature 307: 185–187.

    Article  PubMed  CAS  Google Scholar 

  • Shimamura, M., H. Yasue, K. Ohshima, H. Abe, H. Kato, T. Kishiro, M. Goto, I. Munechika & N. Okada, 1997. Molecular evidence from retrotransposons that whales form a clade within even-toed ungulates. Nature 388: 666–670.

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi, A., K. Anamthawat-Jonsson, T. Arna & A.H. Schulman, 1996. Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome. Plant Mol. Biol. 30: 1321–1329.

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi, A., A. Narvanto & A.H. Schulman, 1996. The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol. Biol. 31: 295–306.

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi, A., D. Schmidt & A.H. Schulman, 1997. BARE-1 insertion site preferences and evolutionary conservation of RNA and cDNA processing sites. Genetica 100(1–3): 219–230.

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi, A., J. Tanskanen, O. Pentikäinen, M.S. Johnson & A.H. Schulman, 1998. The core domain of retrotransposon integrase in Hordeum: predicted structure and evolution. Mol. Biol. Evol. 15: 1135–1144.

    PubMed  CAS  Google Scholar 

  • Suoniemi, A., J. Tanskanen & A.H. Schulman, 1998. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 13: 699–705.

    Article  PubMed  CAS  Google Scholar 

  • Temin, H.W., 1981. Structure, variation and synthesis of retrovirus long terminal repeat. Cell 27: 1–3.

    Article  PubMed  CAS  Google Scholar 

  • VanderWiel, P.L., D.F. Voytas & J.F. Wendel, 1993. Copia-like retrotransposable element evolution in diploid and polyploid cotton (Gossypium L.). J. Mol. Evol. 36: 429–447.

    Article  PubMed  CAS  Google Scholar 

  • van Gent, D.C., A.M.M. Oude Groeneger & R.H.A. Plasterk, 1992. Mutational analysis of the integrase protein of human immunodeficiency virus type 2. Proc. Natl. Acad. Sci. USA 89: 9598–9602.

    Article  PubMed  CAS  Google Scholar 

  • Varmus, H. & P. Brown, 1989. Retroviruses, pp. 53–108 in Mobile DNA, edited by D.E. Berg and M.M. Howe. Am. Soc. Microbiol. Washington, DC.

    Google Scholar 

  • Vicient, C.M., A. Suoniemi, K. Anamthawat-Jonsson, J. Tanskanen, A. Beharav, E. Nevo & A.H. Schulman, 1999. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11: 1769–1784.

    Article  PubMed  CAS  Google Scholar 

  • Voytas, D.F., M.P. Cummings, A. Koniczny, F.M. Ausubel & S.R. Rodermel, 1992. Copia-like retrotransposons are ubiquitous among plants. Proc. Natl. Acad. Sci. USA 89: 7124–7128.

    Article  PubMed  CAS  Google Scholar 

  • Wang, R.R. & J.Z. Wein, 1995. Variations of two repetitive DNA sequences in several Triticeae genomes revealed by polymerase chain reaction and sequencing. Genome 38: 1221–1229.

    PubMed  CAS  Google Scholar 

  • Waugh, R., K. McLean, A.J. Flavell, S.R. Pearce, A. Kumar, B.B. Thomas & W. Powell, 1997. Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol. Gen. Genet. 253: 687–694.

    Article  PubMed  CAS  Google Scholar 

  • Wright, D.A. & D.F. Voytas, 1998. Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149: 703–715.

    PubMed  CAS  Google Scholar 

  • Xiong, Y. & T.H. Eickbush, 1992. Origin and evolution of retroelements based upon their novel reverse transcriptase sequences. EMBO J. 9: 3353–3362.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biotechnology, University of Helsinki, Plant Genomics Laboratory, Viikki Biocenter, P.O. Box 56, FIN-00014, Helsinki, Finland (Phone: +

    Carlos M. Vicient, Ruslan Kalendar & Alan H. Schulman

  2. Faculty of Sciences, University of Iceland, Grensásvegi 12, Reykjavík, 108, Iceland

    Kesara Anamthawat-Jónsson

  3. Valio Ltd., P.O. Box 30, FIN-00039, Valio, Finland

    Annu Suoniemi

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  1. Carlos M. Vicient
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  2. Ruslan Kalendar
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  5. Alan H. Schulman
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Correspondence to Alan H. Schulman.

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Vicient, C.M., Kalendar, R., Anamthawat-Jónsson, K. et al. Structure, functionality, and evolution of the BARE-1 retrotransposon of barley. Genetica 107, 53–63 (1999). https://doi.org/10.1023/A:1003929913398

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