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LINEs and gypsy-like retrotransposons in Hordeum species

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Abstract

LINE and gypsy-like retroelements were studied in the genome of Hordeum vulgare, and compared with the representatives of the major sections of the genus Hordeum. We isolated reverse transcriptase (RT) genes from four gypsy-like and three LINE families using PCR primers specific for the corresponding conserved domains. A full-length barley LINE of 6295 bp, named BLIN, was isolated from a BAC genomic library. BLIN looks alien in the barley genome because its G+C content is 62% compared to an average of 45%. The BLIN nucleotide sequence showed it was structurally intact with the features typical of non-LTR retrotransposons, including 16 bp target site duplications, two short cysteine motifs, and two degenerate open reading frames (ORFs). The high degeneracy was also found in RT domain of both gypsy-like and, particularly, LINE families. The copy numbers of the gypsy-like families were relatively low compared to well-characterized copia-like element BARE-1. Each gypsy-like family gave unique RFLP patterns when hybridized to genomic DNA from each of the four basic Hordeum genomes. H. vulgare (I genome) had accumulated more copies than the wild Hordeum species (H, X, Y genomes), with the other I genome species, H. bulbosum, being intermediate. Analysis of the BAC library and in situ hybridization with LINE RT domains showed the low copy number of the LINE families, but there was little correlation between hybridization patterns and the division of the genus into four basic genomes. The distribution and content of gypsy retrotransposons in the BAC library indicated that a few copies are nested, although most are present as single, distinct, copies. Our results suggest that the major groups of retroelements make individual contributions to the shape of the plant genome; the factors involved in their amplification and distribution are independent, also varying among species.

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References

  • Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. 1987. Current Protocols in Molecular Biology. Greene/Wiley Interscience, New York.

    Google Scholar 

  • Belyayev, A., Raskina, O. and Nevo, E. 2001. Chromosomal distribution of reverse transcriptase-containing retroelements in two Triticeae species. Chrom. Res. 9: 129-136.

    Google Scholar 

  • Bennett, M.D. and Smith, J.B. 1976. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. Lond. B. 274: 227-274.

    Google Scholar 

  • Birnboim, H.C. and Doly, J. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl. Acids Res. 7: 1513-1523.

    Google Scholar 

  • Boer, P.H. and Gray, M.W. 1988. Genes encoding a subunit of respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (RTL) are linked to ribosomal RNA gene pieces in Chlamydomonas reinhardii mitochondrial DNA. EMBO J. 9: 3353-3362.

    Google Scholar 

  • Brandes, A., Heslop-Harrison, J.S., Kamm, A., Kubis, S., Doudrick, R.L. and Schmidt, T. 1997. Comparative analysis of the chromosomal and genomic organization of Ty1-copia-like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol. Biol. 33: 11-21.

    Google Scholar 

  • Capello, J., Cohen, S.M. and Lodish, H.F. 1984. Dictyostelium transposable element DIRS-1 preferentially inserts into DIRS-1 sequences. Mol. Cell Biol. 4: 2207-2213.

    Google Scholar 

  • Church, G.M. and Gilbert W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.

    Google Scholar 

  • Doolittle, R.F., Feng, D.-F., Johnson, M.S. and McClure M.A. 1989. Origins and evolutionary relationships of retroviruses. Q. Rev. Biol. 64: 1-30.

    Google Scholar 

  • Eickbush, T.H. 1992. Transposing without ends: the non-LTR retrotransposable elements. New Biol. 4: 430-440.

    Google Scholar 

  • Eickbush, T.H. 1994. Origin and evolutionary relationships of retroelements. In: S.S. Morse (Ed.) The Evolutionary Biology of Viruses, Raven Press, New York, pp. 121-157.

    Google Scholar 

  • Fawcett, D.H., Lister, C.K., Kellett, E. and Finnegan, D.J., 1986. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47: 1007-1015.

    Google Scholar 

  • Feinberg, A.P. and Vogelstein, B. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6-13.

    Google Scholar 

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

    Google Scholar 

  • Friesen, N., Brandes A. and Heslop-Harrison, J.S. 2001. Diversity, origin and distribution of retrotransposons (gypsy and copia) in conifers. Mol. Biol. Evol., Molecular Biology & Evolution 18: 1176-1188.

    Google Scholar 

  • Gabriel, A., Yen, T.J., Schwartz, D.C., Smith, C.L., Boeke, J.D., Sollner-Webb, B. and Cleveland, D.W. 1990. A rapidly rearranging retrotransposons within the miniexon gene locus of Crithidia fasciculata. Mol. Cell Biol. 10: 615-624.

    Google Scholar 

  • Goubely, C., Arnaud, P., Tatout, C., Heslop-Harrison, J.S. and Deragon, J.-M. 1999. S1 SINE retroelements are methylated at symmetrical and non-symmetrical positions in Brassica napus: identification of a preferred target site for asymmetrical methylation. Plant Mol. Biol. 39: 243-255.

    Google Scholar 

  • Hirochika, H., Fukuchi, A. and Kikuchi, F. 1992. Retrotransposon families in rice plants. Mol. Gen. Genet. 233: 209-216.

    Google Scholar 

  • Hisatomi, Y., Hanada, K. and Iida, S. 1997. The retrotransposon Rtip1 is integrated into a novel type of minisatellite, MiniSip1, in the genome of the common morning glory and carries another new type of minisatellite, MiniSip2. Theor. Appl. Genet. 95: 1049-1056.

    Google Scholar 

  • Hull, R. and Covey, S.N. 1996. Retroelements: propagation and adaptation. Virus Genes 11: 105-118.

    Google Scholar 

  • Inouye, M. and Inouye, S. 1991. Retroelements in bacteria. Trends Biochem. Sci. 16: 18-21.

    Google Scholar 

  • Jakubczak, J.L., Xiong, Y. and Eickbush, T.H. 1990. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J. Mol. Biol. 212: 37-52.

    Google Scholar 

  • Kleinhofs, A. and Graner, A. 2000. An integrated map of the barley genome. In: R.L. Phillips and I. Vasil (Eds.), DNA Based Markers in Plants, Kluwer Academic Publishers, Dordrecht, Netherlands, in press.

    Google Scholar 

  • Kleinhofs, A., Killan, A., Saghai Maroof, M.A., Biyashev, R.M., Hayes, P.M., Chen, F.Q., Lapitan, N., Fenwick, A., Blake, T.K., Kanazin, V., Ananiev, E., Dahleen, L., Kudrna, D., Bollinger, J., Knapp, S.J., Liu, B., Sorrells, M., Heun, M., Franckowiak, J.D., Hoffman, D., Skadsen, R. and Steffenson, B.J. 1993. A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor. Appl. Genet. 86: 705-712.

    Google Scholar 

  • Kossack, D.S. and Kinlaw, C.S. 1999. IFG, a gypsy-like retrotransposon in Pinus (Pinaceae), has an extensive history in pines. Plant Mol. Biol. 39: 417-426.

    Google Scholar 

  • Kubis, S.E., Heslop-Harrison, J.S., Desel, C. and Schmidt, T. 1998. The genomic organization of non-LTR retrotransposons (LINEs) from three Beta species and five other angiosperms. Plant Mol. Biol. 36: 821-831.

    Google Scholar 

  • Kumar, A. and Bennetzen, J.L. 1999. Plant retrotransposons. Annu. Rev. Genet. 33: 479-532.

    Google Scholar 

  • Kumekawa, N., Ohtsubo, H., Horiuchi, T. and Ohtsubo, E. 1999. Identification and characterization of novel retrotransposons of the gypsy type in rice. Mol. Gen. Genet. 260: 593-602.

    Google Scholar 

  • Leeton, P.R.J. and Smyth, D.R. 1993. An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol. Gen. Genet. 237: 97-104.

    Google Scholar 

  • Luan, D.D., Korman, M.H., Jakubczak, J.L. and Eickbush, T.H. 1993. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595-605.

    Google Scholar 

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

    Google Scholar 

  • Matsuoka, Y. and Tsunewaki, K. 1996. Wheat retrotransposon families identified by reverse transcriptase domain analysis. Mol. Biol. Evol. 13: 1384-1392.

    Google Scholar 

  • McClure, M.A. 1991. Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol. Biol. Evol. 8: 835-857.

    Google Scholar 

  • Melzer, I.M. and Kleinhofs, A. 1987. Molecular genetics of barley. In: S. Yasuda and T. Konishi (Eds.) Barley Genetics V, Okayama, Japan, pp. 481-491.

  • Michel, F. and Lang, B.F. 1985. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature 316: 641-643.

    Google Scholar 

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

    Google Scholar 

  • Mount, S.M. and Rubin, G.M. 1985. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol. Cell Biol. 5: 1630-1638.

    Google Scholar 

  • Panstruga, R., Buschges, R., Piffanelli, P. and Schulze-Lefert, P. 1998. A contiguous 60 kb genomic stretch from barley reveals molecular evidence for gene islands in a monocot genome. Nucl. Acids Res. 26: 1056-1062.

    Google Scholar 

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

    Google Scholar 

  • Peleman, J., Cttyn, B., Van Camp, W., Van Montagu, M. and Inzé, D. 1991. Transient occurrence of extrachromosomal DNA of an Arabidopsis thaliana transposon-like element, Tat1. Proc. Natl. Acad. Sci. USA 88: 3618-3622.

    Google Scholar 

  • Pelissier, T., Tutois, S., Deragon, J., Tourmente, S., Genestier, S. and Picard, G. 1995. Athila, a new retroelement from Arabidopsis thaliana. Plant Mol. Biol. 29: 441-452.

    Google Scholar 

  • Presting, G.G., Malysheva, L., Fuchs, J. and Schubert, I. 1998. A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J. 16: 721-728.

    Google Scholar 

  • Purugganan, M.D. and Wessler, S.R. 1994. Molecular evolution of magellan, a maize Ty3/gypsy-like retrotransposon. Proc. Natl. Acad. Sci. USA 91: 11674-11678.

    Google Scholar 

  • Ramsay, L., Macaulay, M., Cardle, L., Morgante, M., Ivanissevich, S., Maestri, E., Powell, W. and Waugh, R. 1999. Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J. 17: 415-425.

    Google Scholar 

  • SanMiguel, P. and Bennetzen, J.L. 1998. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann. Bot. 82: 37-44.

    Google Scholar 

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

    Google Scholar 

  • Schmidt, T., Kubis, S. and Heslop-Harrison, J.S. 1995. Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs and Ty-copia-like elements as major components of the genome. Chrom. Res. 3: 335-345.

    Google Scholar 

  • Schwarz-Sommer, Z., Leclercq, L., Gobel, E. and Saedler, H. 1987. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of non-viral retrotransposons. EMBO J. 6: 3873-3880.

    Google Scholar 

  • Shcherban', A.B. and Vershinin, A.V. 1997. BARE-ID, a representative of a family of BARE-like elements of the barley genome. Genetica 100: 231-240.

    Google Scholar 

  • Schwarzacher, T. and Heslop-Harrison, J.S. 2000. Practical in situ Hybridization. BIOS, Oxford.

    Google Scholar 

  • Song, S., Gerasimova, T., Kurkulos, M., Boeke, J. and Corces, V. 1994. An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is a infectious retrovirus. Genes Dev. 8: 2046-2057.

    Google Scholar 

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

    Google Scholar 

  • Svitashev, S., Bryngelsson, T., Vershinin, A.V., Pedersen, C., Sall, T. and von Bothmer, R. 1994. Phylogenetic analysis of the genus Hordeum using repetitive DNA sequences. Theor. Appl. Genet. 89: 801-810.

    Google Scholar 

  • Temin, H. M. 1989. Retrons in bacteria. Nature 339: 254-255.

    Google Scholar 

  • Vanyushin, B.F., Kadyrova, D.Kh., Karimov, Kh.Kh. and Belozersky, A.H. 1971. Minor bases in DNA of higher plants. Biokhimiya (Russian) 36: 1251-1258.

    Google Scholar 

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

    Google Scholar 

  • von Bothmer, R., Flink, J. and Landstrom, T. 1986. Meiosis in interspecific Hordeum hybrids. I. Diploid combinations. Can. J. Genet. Cytol. 28: 525-535.

    Google Scholar 

  • von Bothmer, R., Flink, J. and Landstrom, T. 1987. Meiosis in interspecific Hordeum hybrids. II. Triploid hybrids. Evol. Trends Plants 1: 41-50.

    Google Scholar 

  • Voytas, D.F. 1996. Retroelements in genome organization. Science 274: 737-738.

    Google Scholar 

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

    Google Scholar 

  • Wang, S., Zhang, Q., Mauughan, P.J. and Saghai Maroof, M.A. 1997. Copia-like retrotransposons in rice: sequence heterogeneity species distribution and chromosomal locations. Plant Mol. Biol. 33: 1051-1058.

    Google Scholar 

  • Wright, D.A. and Voytas, D.F. 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.

    Google Scholar 

  • Wright, D.A., Ke, N., Smalle, J., Hauge, B.M., Goodman, H.M. and Voytas, D.F. 1996. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics 142: 569-578.

    Google Scholar 

  • Xiong, Y. and Eickbush, T.H. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9: 3353-3362.

    Google Scholar 

  • Yu, Y., Tomkins, J.P., Waugh, R., Frisch, D.A., Kudrna, D., Kleinhofs, A., Brueggeman, R.S., Muehlbauer, G.J. and Wing, R.A. 2000. A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor. Appl. Genet. 101: 1093-1099.

    Google Scholar 

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Vershinin, A.V., Druka, A., Alkhimova, A.G. et al. LINEs and gypsy-like retrotransposons in Hordeum species. Plant Mol Biol 49, 1–14 (2002). https://doi.org/10.1023/A:1014469830680

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