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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species.Plant Mol Biol Rep 9: 208–218.
Bennett MD, Smith JB (1976) Nuclear DNA amounts of angiosperms.Proc R Soc Lond B 274: 227–274.
Bennett MD, Smith JB (1991) Nuclear DNA amounts of angiosperms.Proc R Soc Lond B 334 309–345.
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.
Bureau TE, White SE, Wessler SR (1994) Transduction of a cellular gene by a plant retroelement.Cell 77: 479–480.
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.
Chen TL, Manuelides L (1989) SINEs and LINEs cluster in distinct DNA fragments of Giemsa band size.Chromosoma 98 309–316.
Deininger PL, Batzer MA Hutchinson II CA, Edgell MH (1992) Master genes in mammalian repetitive DNA amplification.Trends Genet 8: 307–311.
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.
Flavell AJ (1992)Ty1-copia group retrotransposons and the evolution of retroelements in the eukaryotes.Genetica 86: 203–214.
Flavell RB, Bennett MD, Smith JB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants.Biochem Genet 12: 257–269.
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.
Flavell AJ, Smith DB, Kumar A (1992b) Extreme heterogeneity ofTy1-copia group retrotransposons in plants.Mol Gen Genet 231: 233–242.
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.
Grandbastien MA (1992) Retroelements in higher plants.Trends Genet 8: 103–108.
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.
Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture.EMBO J 12: 2521–2528.
Hirochika H, Fukuchi A, Kikuchi F (1992) Retrotransposon families in rice.Mol Gen Genet 233: 209–216.
Hirochika H, Hirochika R (1993)Ty1-copia group retrotransposons as ubiquitous components of plant genomes.Jpn J Genet 68: 35–46.
Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S (1982) Rapid evolution of RNA genomes.Science 215: 1577–1585.
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.
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.
Johns MA, Mottinger J, Freeling M (1985) A low copy number,copia-like transposon in maize.EMBO J 4: 1093–1102.
Johns MA, Babcock MS, Fuerstenberg SMet al. (1989) An unusually compact retrotransposon in maize.Plant Mol Biol 12: 633–642.
Kidwell MG (1992) Horizontal transfer.Curr Opinion Gen Dev 2: 868–873.
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.
Konieczny A, Voytas DF, Cummings MP, Ausubel FM (1991) A superfamily ofArabidopsis thaliana retrotransposons.Genetics 127: 801–809.
Korenberg JR, Rykowski MC (1988) Human genome organization: Alu, Lines, and the molecular structure of metaphase chromosome bands.Cell 53: 391–400.
Kumar S, Tamura K, Nei M (1993)MEGA: Molecular Evolutionary Genetics Analysis, version 1.0. University Park, PA: Pennsylvania State University.
Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplified in the genome ofLilium speciosum.Mol Gen Genet 237: 97–104.
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: 595–605
Manninen I, Schulman AH (1993)BARE-1, acopia-like retroelement in barley (Hordeum vulgare L.)Plant Mol Biol 22: 829–846.
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.
Meyerowitz EM (1994) Plant developmental biology: green genes for the 21st century.BioEssays 16: 621–625.
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.
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.
Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991a) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts.EMBO J 10: 1911–1918.
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.
Pryciak PM, Varmus HE (1992) Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection.Cell 69: 769–780.
Sambrook J, Fritsch EF, Maniatis T (1989)Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Schmidt T, Heslop-Harrison JS (1993) Variability and evolution of highly repeated DNA sequences in the genusBeta.Genome 36: 1074–1079.
Schmidt T, Jung C, Metzlaff M (1991) Distribution and evolution of two satellite DNAs in the genusBeta.Theor Appl Genet 82: 793–799.
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.
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.
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.
Singer M (1982) Highly repeated sequences inmammalian genomes.Int Rev Cytol 76: 67–112.
Taruscio D, Manuelidis L (1991) Integration site preferences of endogenous retroviruses.Chromosoma 101: 141–156.
Voytas DF, Ausubel FM (1988) Acopia-like transposable element family inArabidopsis thaliana.Nature 336: 242–244.
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.
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.
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.
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J9: 3353–3362.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schmidt, T., Kubis, S. & Heslop-Harrison, J.S. Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs andTy1-copia-like elements as major components of the genome. Chromosome Res 3, 335–345 (1995). https://doi.org/10.1007/BF00710014
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00710014