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Chromosome Research

, Volume 3, Issue 6, pp 335–345 | Cite as

Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs andTy1-copia-like elements as major components of the genome

Article

Abstract

DNA sequences of the reverse transcriptase gene of long terminal repeat (LTR) and non-LTR (non-viral) retrotransposons have been isolated and cloned from the genome of sugar beet (Beta vulgaris). Both retrotransposon types are highly amplified in sugar beet and may account for 2–5% of the genome. The BNR1 family, representing the first non-viral retrotransposon reported from a dicotyledonous species, shows homology to the mammalian L1 family of long interspersed repeated sequences (LINEs) and to retrotransposable elements from maize and lily. Sequences of the Tbv family are homologous to theTy1-copia class of LTR retrotransposons. The BNR1 and Tbv retrotransposon families are characterized by sequence heterogeneity and are probably defective. The deduced peptide sequences were used to investigate the relation to other retroelements from plants, insects and mammals. Fluorescencein situ hybridization was used to investigate the physical distribution and revealed that both retrotransposon families are present on all sugar beet chromosomes and largely excluded from chromosomal regions harbouring the 18S–5.8S–25S rRNA genes. The BNR1 family is organized in discrete clusters, while the Tbv family ofTy1-copia-like retrotransposons shows a more uniform distribution along chromosome arms and is absent from some chromosomal regions. These contrasting distributions emphasize the differences in evolutionary amplification and dispersion mechanisms between the two types of retrotransposons. Thein situ results of both elements reflect significant features of a higher order structure of the genome, as it is known for both short interspersed repeated sequences (SINEs) and LINEs in human.

Key words

Beta vulgaris in situ hybridization LINE LTR retrotransposons non-LTR (non-viral) retrotransposons Ty1-copia 

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References

  1. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species.Plant Mol Biol Rep 9: 208–218.Google Scholar
  2. Bennett MD, Smith JB (1976) Nuclear DNA amounts of angiosperms.Proc R Soc Lond B 274: 227–274.Google Scholar
  3. Bennett MD, Smith JB (1991) Nuclear DNA amounts of angiosperms.Proc R Soc Lond B 334 309–345.Google Scholar
  4. Boyle AL, Feltquite DM, Dracopoli NC, Housman DE, Ward DC (1992) Rapid physical mapping of cloned DNA on banded mouse chromosomes by fluorescencein situ hybridization.Genomics 12: 106–115.Google Scholar
  5. Bureau TE, White SE, Wessler SR (1994) Transduction of a cellular gene by a plant retroelement.Cell 77: 479–480.Google Scholar
  6. Burke WD, Calalang CC, Eickbush TH (1987) The site-specific ribosomal insertion element type II ofBombyx moori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.Mol Cell Biol 7: 2221–2230.Google Scholar
  7. Chen TL, Manuelides L (1989) SINEs and LINEs cluster in distinct DNA fragments of Giemsa band size.Chromosoma 98 309–316.Google Scholar
  8. Deininger PL, Batzer MA Hutchinson II CA, Edgell MH (1992) Master genes in mammalian repetitive DNA amplification.Trends Genet 8: 307–311.Google Scholar
  9. Dorn R, Krauss V, Reuter G, Saumweber H (1993) The enhancer of position-effect variegation ofDrosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators.Proc Natl Acad Sci USA 90: 11376–11380.Google Scholar
  10. Flavell AJ (1992)Ty1-copia group retrotransposons and the evolution of retroelements in the eukaryotes.Genetica 86: 203–214.Google Scholar
  11. Flavell RB, Bennett MD, Smith JB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants.Biochem Genet 12: 257–269.Google Scholar
  12. Flavell AJ, Dunbar E, Anderson R,et al. (1992a)Ty1-copia group retrotransposons are ubiquitous and heterogenous in higher plants.Nucleic Acids Res 20: 3639–3644.Google Scholar
  13. Flavell AJ, Smith DB, Kumar A (1992b) Extreme heterogeneity ofTy1-copia group retrotransposons in plants.Mol Gen Genet 231: 233–242.Google Scholar
  14. Gojobori T, Yokoyama S (1985) Rates of evolution of the retroviral oncogene of Moloney murine sarcoma virus and of its cellular homologues.Proc Natl Acad Sci USA 82: 4198–4201.Google Scholar
  15. Grandbastien MA (1992) Retroelements in higher plants.Trends Genet 8: 103–108.Google Scholar
  16. Grandbastien MA, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337: 376–380.Google Scholar
  17. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture.EMBO J 12: 2521–2528.Google Scholar
  18. Hirochika H, Fukuchi A, Kikuchi F (1992) Retrotransposon families in rice.Mol Gen Genet 233: 209–216.Google Scholar
  19. Hirochika H, Hirochika R (1993)Ty1-copia group retrotransposons as ubiquitous components of plant genomes.Jpn J Genet 68: 35–46.Google Scholar
  20. Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes.Science 215: 1577–1585.Google Scholar
  21. Hutchinson CA, Hardies SC, Loeb DD, Shehee WR, Edgell MH (1989) LINEs and related retroposons: long interspersed repeated sequences in the eukaryotic genome. In: Berg DH, Howe MM, eds.Mobile DNA. Washington, DC: American Society of Microbiology, pp 593–617.Google Scholar
  22. Jakubczak JL, Burke WD, Eickbush TH (1991) Retrotransposable elementsR1 andR2 interrupt the rRNA genes of most insects.Proc Natl Acad Sci USA 88: 3295–3299.Google Scholar
  23. Johns MA, Mottinger J, Freeling M (1985) A low copy number,copia-like transposon in maize.EMBO J 4: 1093–1102.Google Scholar
  24. Johns MA, Babcock MS, Fuerstenberg SMet al. (1989) An unusually compact retrotransposon in maize.Plant Mol Biol 12: 633–642.Google Scholar
  25. Kidwell MG (1992) Horizontal transfer.Curr Opinion Gen Dev 2: 868–873.Google Scholar
  26. Kimmel BE, ole-Moiyoi OK, Young JR (1987)Ingi, a 5.2-kb dispersed sequence element fromTrypanosoma brucei that carries half of a smaller mobile element at either end and has homology to mammalian LINEs.Mol Cell Biol 7: 1465–1475.Google Scholar
  27. Konieczny A, Voytas DF, Cummings MP, Ausubel FM (1991) A superfamily ofArabidopsis thaliana retrotransposons.Genetics 127: 801–809.Google Scholar
  28. Korenberg JR, Rykowski MC (1988) Human genome organization: Alu, Lines, and the molecular structure of metaphase chromosome bands.Cell 53: 391–400.Google Scholar
  29. Kumar S, Tamura K, Nei M (1993)MEGA: Molecular Evolutionary Genetics Analysis, version 1.0. University Park, PA: Pennsylvania State University.Google Scholar
  30. Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplified in the genome ofLilium speciosum.Mol Gen Genet 237: 97–104.Google Scholar
  31. Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition.Cell 72: 595–605Google Scholar
  32. Manninen I, Schulman AH (1993)BARE-1, acopia-like retroelement in barley (Hordeum vulgare L.)Plant Mol Biol 22: 829–846.Google Scholar
  33. Meyer C, Pouteau S, Rouze P, Caboche M (1994) Isolation and molecular characterization of dTnp1, a mobile and defective transposable element ofNicotiana plumbaginifolia. Mol Gen Genet: 194–200.Google Scholar
  34. Meyerowitz EM (1994) Plant developmental biology: green genes for the 21st century.BioEssays 16: 621–625.Google Scholar
  35. Moore G, Cheung W, Schwarzacher T, 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
  36. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous gene in trans.Plant Cell 2: 279–289.Google Scholar
  37. Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991a) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts.EMBO J 10: 1911–1918.Google Scholar
  38. Pouteau S, Spielman A, Meyer C, Grandbastien MA, Caboche M (1991b) Effects of Tnt1 tobacco retrotransposon insertion on target gene transcription.Mol Gen Gent 228: 233–239.Google Scholar
  39. Pryciak PM, Varmus HE (1992) Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection.Cell 69: 769–780.Google Scholar
  40. Sambrook J, Fritsch EF, Maniatis T (1989)Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
  41. Schmidt T, Heslop-Harrison JS (1993) Variability and evolution of highly repeated DNA sequences in the genusBeta.Genome 36: 1074–1079.Google Scholar
  42. Schmidt T, Jung C, Metzlaff M (1991) Distribution and evolution of two satellite DNAs in the genusBeta.Theor Appl Genet 82: 793–799.Google Scholar
  43. Schmidt T, Boblenz K, Metzlaff M, Kaemmer D, Weising K, Kahl G (1993) DNA fingerprinting in sugar beet (Beta vulgaris) — identification of double-haploid breeding lines.Theor Appl Genet 85: 653–657.Google Scholar
  44. Schmidt T, Schwarzacher T, Heslop-Harrison JS (1994) Physical mapping of rRNA genes by fluorescentin situ hybridization and structural analysis of 5S rRNA genes and intergenic spacer sequences in sugar beet (Beta vulgaris).Theor Appl Genet 88: 629–636.Google Scholar
  45. Schwarz-Sommer Z, Leclercq L, Göbel E, Saedler H (1987) Cin4, an insert altering the structure of theA1 gene inZea mays, exhibits properties of non-viral retrotransposons.EMBO J 6: 3873–3880.Google Scholar
  46. Singer M (1982) Highly repeated sequences inmammalian genomes.Int Rev Cytol 76: 67–112.Google Scholar
  47. Taruscio D, Manuelidis L (1991) Integration site preferences of endogenous retroviruses.Chromosoma 101: 141–156.Google Scholar
  48. Voytas DF, Ausubel FM (1988) Acopia-like transposable element family inArabidopsis thaliana.Nature 336: 242–244.Google Scholar
  49. Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992)copia-like retrotransposons are ubiquitous among plants.Proc Natl Acad Sci USA 89: 7124–7128.Google Scholar
  50. Wichmann HA, Van Den Bussche RA, Hamilton MJ, Baker RJ (1992) Transposable elements and the evolution of genome organization in mammals.Genetica 86: 287–293.Google Scholar
  51. Xiong Y, Eickbush TH (1988) The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons.Mol Cell Biol 8: 114–123.Google Scholar
  52. Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J9: 3353–3362.Google Scholar

Copyright information

© Rapid Communications of Oxford Ltd. 1995

Authors and Affiliations

  1. 1.the Karyobiology Group, Department of Cell BiologyJohn Innes CentreNorwichUK

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