Skip to main content
SpringerLink
Log in

Molecular organization of terminal repetitive DNA in Beta species

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

We have isolated families of subtelomeric satellite DNA sequences from species of four sections of the genus Beta and from spinach, a related Chenopodiaceae. Twenty-five clones were sequenced and representative repeats of each family were characterized by Southern blotting and FISH. The families of ApaI restriction satellite repeats were designated pAv34, pAc34, the families of RsaI repeats pRp34, pRn34 and pRs34. The repeating units are 344–362 bp long and 45.7–98.8% homologous with a clear species-specific divergence. Each satellite monomer consists of two subrepeats SR1 and SR2 of 165–184 bp, respectively. The repeats of each subrepeat group are highly identical across species, but share only a homology of 40.8–54.8% with members of the other subrepeat group. Two evolutionary steps could be supposed in the phylogeny of the subtelomeric satellite family: the diversification of an ancestor satellite into groups representing SR1 and SR2 in the progenitor of Beta and Spinacea species, followed by the dimerization and diversification of the resulting 360 bp repeats into section-specific satellite DNA families during species radiation. The chromosomal localization of telomeric, subtelomeric and rDNA tandem repeats was investigated by multi-colour FISH. High-resolution analysis by fibre FISH revealed a unique physical organization of B. vulgaris chromosome ends with telomeric DNA and subtelomeric satellites extending over a maximum of 63 kb and 125 kb, respectively.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams SP, Hartman TP, Lim KY et al. (2001) Loss and recovery of Arabidopsis-type telomere repeat sequences 5′-(TTTAGGG)(n)-3′ in the evolution of a major radiation of flowering plants. Proc R Soc Lond B Biol Sci 268: 1541–1546.

    Article  CAS  Google Scholar 

  • Alkhimova OG, Heslop-Harrison JS, Shchapova AI, Vershinin AV (1999) Rye chromosome variability in wheat–rye addition and substitution lines. Chromosome Res 7: 205–212.

    Article  PubMed  CAS  Google Scholar 

  • Alkhimova OG, Mazurok NA, Potapova TA, Zakian SM, Heslop-Harrison JS, Vershinin AV (2004) Diverse patterns of the tandem repeats organization in rye chromosomes. Chromosoma 113: 42–52.

    Article  PubMed  CAS  Google Scholar 

  • Ansari HA, Ellison NW, Griffiths AG, Williams WM (2004) A lineage-specific centromeric satellite sequence in the genus Trifolium. Chromosome Res 12: 357–367.

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9: 208–218.

    CAS  Google Scholar 

  • Barker RF, Harberd NP, Jarvis MG, Flavell RB (1988) Structure and evolution of the intergenic region in a ribosomal DNA repeat unit of wheat. J Mol Biol 201: 1–17.

    Article  PubMed  CAS  Google Scholar 

  • Bosemark NO, Bormotov VE (1971) Chromosome morphology in a homozygous line of sugar beet. Hereditas 69: 205–212.

    Google Scholar 

  • Broun P, Ganal MW, Tanksley SD (1992) Telomeric arrays display high levels of heritable polymorphism among closely related plant varieties. Proc Natl Acad Sci USA 89: 1354–1357.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215–220.

    Article  PubMed  CAS  Google Scholar 

  • Dechyeva D, Gindullis F, Schmidt T (2003) Divergence of satellite DNA and interspersion of dispersed repeats in the genome of the wild beet Beta procumbens. Chromosome Res 11: 3–21.

    Article  PubMed  CAS  Google Scholar 

  • De Jong H, De Bock TSM (1978) Use of haploids of Beta vulgaris L. for the study of orcein- and Giemsa-stained chromosomes. Euphytica 27: 41–47.

    Google Scholar 

  • De Jong JH, Blom GH (1981) The pachytene chromosomes of Beta procumbens Chr. Sm. In De Jong JH (ed) Investigation into Chromosome Morphology of Sugar Beet and Related Wild Species. PhD thesis, University of Amsterdam, The Netherlands, pp. 33–39.

  • De Jong JH, Fransz P, Zabel P (1999) High resolution FISH in plants-techniques and applications. Trends Plant Sci 4: 258–263.

    Article  Google Scholar 

  • Desel C (2002) Chromosomale Lokalisierung von repetitiven und unikalen DNA-Sequenzen durch Fluoreszenz-in situ-Hybridisierung in der Genomanalyse bei Beta-Arten. PhD thesis, Christian-Albrechts University, Kiel.

  • Desel C, Jung C, Cai D, Kleine M, Schmidt T (2001) High resolution mapping of YACs and single-copy gene Hs1 pro-1 on Beta vulgaris chromosomes by multi-colour fluorescence in situ hybridization. Plant Mol Biol 45: 113–122.

    Article  PubMed  CAS  Google Scholar 

  • Dong F, Jiang J (1998) Non-Rabl patterns of centromere and telomere distribution in the interphase nuclei of plant cells. Chromosome Res 6: 551–558.

    Article  CAS  Google Scholar 

  • Fajkus J, Kovarik A, Kralovics R, Bezdek M (1995) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247: 633–638.

    Article  PubMed  CAS  Google Scholar 

  • Fajkus J, Sykorova E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13: 469–479.

    Article  CAS  Google Scholar 

  • Fischer H (1989) Origin of the ‘Weisse Schlesische Rübe’ (white Silesian beet) and resynthesis of sugar beet. Euphytica 41: 75–80.

    Article  Google Scholar 

  • Fischer TC, Groner S, Zentgraf U, Hemleben V (1994) Evidence for nucleosomal phasing and a novel protein specifically binding to cucumber satellite DNA. Z Naturforsch 49: 79–86.

    CAS  Google Scholar 

  • Flavell RB, Moore G (1996). Plant genome constituents and their organisation. In Foster GD, Twell D, eds., Plant Gene Isolation: Principles and Practice. Chichester: Wiley, pp. 1–25.

    Google Scholar 

  • Flavell RB, Bennett MD, Smith JB, Smith DB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12: 257–269.

    Article  PubMed  CAS  Google Scholar 

  • Florijn RJ, Bonden LA, Vrolijk H et al. (1995) High-resolution DNA fiber-FISH for genomic DNA mapping and colour bar-coding of large genes. Hum Mol Genet 4: 831–836.

    Article  PubMed  CAS  Google Scholar 

  • Fransz PF, Alonso-Blanco C, Liharska T, Peeters AJM, Zabel P, De Jong JH (1996) High resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridisation to extended DNA fibres. Plant J 9: 421–430.

    Article  PubMed  CAS  Google Scholar 

  • Fuchs J, Brandes A, Schubert I (1995) Telomere sequence localization and karyotype evolution in higher plants. Plant Syst Evol 196: 227–241.

    Article  CAS  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3: 87–94.

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Broun P, Tanksley SD (1992) Genetic mapping of tandemly repeated telomeric DNA sequences in tomato (Lycopersicon esculentum). Genomics 14: 444–448.

    Article  PubMed  CAS  Google Scholar 

  • Gao D, Schmidt T, Jung C (2000) Molecular characterization and chromosomal distribution of species-specific repetitive DNA sequences from Beta corolliflora, a wild relative of sugar beet. Genome 43: 1073–1080.

    Article  PubMed  CAS  Google Scholar 

  • Gao D, Guo D, Jung C (2001) Monosomic addition lines of Beta corolliflora Zoss in sugar beet: cytological and molecular-marker analysis. Theor Appl Genet 103: 240–247.

    Article  CAS  Google Scholar 

  • Gindullis F, Desel C, Galasso I, Schmidt T (2001) The large-scale organization of the centromeric DNA in Beta species. Genome Res 11: 253–265.

    Article  PubMed  CAS  Google Scholar 

  • Grebenstein B, Grebenstein O, Sauer W, Hemleben V (1996) Distribution and complex organization of satellite DNA sequences in Aveneae species. Genome 39: 1045–1050.

    PubMed  CAS  Google Scholar 

  • Harrison GE, Heslop-Harrison JS (1995) Centromeric repetitive DNA sequences in the genus Brassica. Theor Appl Genet 90: 157–165.

    Article  CAS  Google Scholar 

  • Hemleben V, Leweke B, Roth A, Stadler J (1982) Organization of highly repetitive satellite DNA of two Cucurbitaceae species (Cucumis melo and Cucumis sativus). Nucleic Acids Res 10: 631–644.

    Article  PubMed  CAS  Google Scholar 

  • Heslop-Harrison JS (2000) Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell 12: 617–635.

    Article  PubMed  CAS  Google Scholar 

  • Heslop-Harrison JS, Leitch AR, Schwarzacher T (1993) The physical organization of plant interphase nuclei. In Heslop-Harrison JS, Flavell RB, eds., The Chromosomes. Oxford: BIOS Scientific Publishers, pp. 221–232.

    Google Scholar 

  • Hizume M, Shibata F, Matsusaki Y, Garajova Z (2002) Chromosome identification and comparative karyotypic analyses of four Pinus species. Theor Appl Genet 105: 491–497.

    Article  PubMed  Google Scholar 

  • Ingham LD, Hanna WW, Baier JW, Hannah LC (1993) Origin of the main class of repetitive DNA within selected Pennisetum species. Mol Gen Genet 238: 350–356.

    Article  PubMed  CAS  Google Scholar 

  • Kamm A, Schmidt T, Heslop-Harrison JS (1994) Molecular and physical organization of highly repetitive, undermethylated DNA from Pennisetum glaucum. Mol Gen Genet 244: 420–425.

    Article  PubMed  CAS  Google Scholar 

  • Kamm A, Galasso I, Schmidt T, Heslop-Harrison JS (1995) Analysis of a repetitive DNA family from Arabidopsis arenosa and relationships between Arabidopsis species. Plant Mol Biol 27: 853–862.

    Article  PubMed  CAS  Google Scholar 

  • Kazama Y, Sugiyama R, Matsunaga S et al. (2003) Organization of the KpnI family of chromosomal distal-end satellite DNAs in Silene latifolia. J Plant Res 116: 317–326.

    Article  PubMed  CAS  Google Scholar 

  • Kubis S, Heslop-Harrison JS, Schmidt T (1997) A family of differentially amplified repetitive DNA sequences in the genus Beta reveals genetic variation in Beta vulgaris subspecies and cultivars. J Mol Evol 44: 310–320.

    Article  PubMed  CAS  Google Scholar 

  • Kubis S, Heslop-Harrison JS, Schmidt T (1998) Repetitive DNA elements as a major components of plant genomes. Ann Bot 82: 45–55.

    Article  CAS  Google Scholar 

  • Lagercrantz U, Lydiate DJ (1996) Comparative genome mapping in Brassica. Genetics 144: 1903–1910.

    PubMed  CAS  Google Scholar 

  • Lim KB, de Jong H, Yang TJ et al. (2005a) Characterization of rDNAs and tandem repeats in the heterochromatin of Brassica rapa. Mol Cells 19: 436–444.

    PubMed  CAS  Google Scholar 

  • Lim KY, Matyasek R, Kovarik A, Fulnecek J, Leitch AR (2005b) Molecular cytogenetics and tandem repeat sequence evolution in the allopolyploid Nicotiana rustica compared with diploid progenitors N. paniculata and N. undulata. Cytogenet Genome Res 109: 298–309.

    Article  PubMed  CAS  Google Scholar 

  • Lin XY, Kaul S, Rounsley S et al. (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402: 761–768.

    Article  PubMed  CAS  Google Scholar 

  • Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA 103: 5224–5229.

    Article  PubMed  CAS  Google Scholar 

  • Macas J, Meszaros T, Nouzova M (2002) PlantSat: a specialized database for plant satellite repeats. Bioinformatics 18: 28–35.

    Article  PubMed  CAS  Google Scholar 

  • Mao L, Devos KM, Zhu L, Gale MD (1997) Cloning and genetic mapping of wheat telomere-associated sequences. Mol Gen Genet 254: 584–591.

    Article  PubMed  CAS  Google Scholar 

  • McKnight TD, Shippen DE (2004) Plant telomere biology. Plant Cell 16: 794–803.

    Article  PubMed  CAS  Google Scholar 

  • Moore G, Devos KM, Wang Z, Gale MD (1995) Cereal genome evolution. Grasses, line up and form a circle. Curr Biol 5: 737–739.

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S et al. (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36: 138–145.

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Neumannn P, Zhang D et al. (2005) Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol Biol Evol 22: 845–855.

    Article  PubMed  CAS  Google Scholar 

  • Ohmido N, Kijima K, Ashikawa I, de Jong JH, Fukui K (2001) Visualization of the terminal structure of rice chromosomes 6 and 12 with multicolor FISH to chromosomes and extended DNA fibers. Plant Mol Biol 47: 413–421.

    Article  PubMed  CAS  Google Scholar 

  • Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4: 207–213.

    Article  CAS  Google Scholar 

  • Presting GG, Frary A, Pillen K, Tanksley SD (1996) Telomere–homologous sequences occur near the centromeres of many tomato chromosomes. Mol Gen Genet 251: 526–531.

    Article  PubMed  CAS  Google Scholar 

  • Prince JP, Pochard E, Tanksley SD (1993) Construction of a molecular linkage map of pepper and a comparison of synteny with tomato. Genome 36: 404–417.

    CAS  PubMed  Google Scholar 

  • Raap AK, Florijn RJ, Blonden LAJ et al. (1996) Fiber FISH as a DNA mapping tool. Meth 9: 67–73.

    Article  CAS  Google Scholar 

  • Rabl C (1885) Über Zelltheilung. Morphol Jahrb 10: 214–330.

    Google Scholar 

  • Reeves A, Tear J (2000) MicroMeasure for Windows, version 3.3. Free program distributed by the authors over the Internet from http://www.colostate.edu/Depts/Biology/ MicroMeasure.

  • Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 127–136.

    Article  PubMed  CAS  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms: mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci 81: 8014–8018.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Doudrick RL, Heslop-Harrison JS, Schmidt T (2000) The contribution of short repeats of low sequence complexity to large conifer genomes. Theor Appl Genet 101: 7–14.

    Article  CAS  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1993) Variability and evolution of highly repeated DNA sequences in the genus Beta. Genome 36: 1074–1079.

    PubMed  CAS  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1996) High resolution mapping of repetitive DNA by in situ hybridization: molecular and chromosomal features of prominent dispersed and discretely localized DNA families from the wild beet species Beta procumbens. Plant Mol Biol 30: 1099–1119.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3: 195–199.

    Article  Google Scholar 

  • Schmidt T, Kudla J (1996) The molecular structure, chromosomal organization, and interspecies distribution of a family of tandemly repeated DNA sequences of Antirrhinum majus L. Genome 39: 243–248.

    PubMed  CAS  Google Scholar 

  • Schmidt T, Metzlaff M (1991) Cloning and characterization of a Beta vulgaris satellite DNA family. Gene 101: 247–250.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, Jung C, Metzlaff M (1991) Distribution and evolution of two satellite DNAs in the genus Beta. Theor Appl Genet 82: 793–799.

    Article  CAS  Google Scholar 

  • Schmidt T, Kubis S, Katsiotis A, Jung C, Heslop-Harrison JS (1998) Molecular and chromosomal organization of two repetitive DNA sequences with intercalary locations in sugar beet and other Beta species. Theor Appl Genet 97: 696–704.

    Article  CAS  Google Scholar 

  • Schmidt T, Schwarzacher T, Heslop-Harrison JS (1994) Physical mapping of rRNA genes by fluorescent in situ hybridization and structural analysis of 5S rRNA genes and intergenic spacer sequences in sugar beet (Beta vulgaris). Theor Appl Genet 88: 629–636.

    Article  CAS  Google Scholar 

  • Schwarzacher T, Heslop-Harrison JS (1991) In situ hybridization to plant telomeres using synthetic oligomers. Genome 34: 317–323.

    Google Scholar 

  • Schwarzacher T, Heslop-Harrison JS (2000) Preparation of chromosome spreads. In Practical In Situ Hybridization. Oxford: BIOS Scientific Publishers, p. 60.

  • Shi L, Zhu T, Morgante M, Rafalski JA, Keim P (1996) Soybean chromosome painting: a strategy for somatic cytogenetics. J Hered 87: 308–313.

    PubMed  CAS  Google Scholar 

  • Simoens CR, Gielen J, Van Montagu M, Inze D (1988) Characterization of highly repetitive sequences of Arabidopsis thaliana. Nucleic Acids Res 16: 6753–6766.

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2004) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Program distributed by the author. Sinauer, Sunderland, MA.

  • Sykorova E, Cartagena J, Horakova M, Fukui K, Fajkus J (2003a) Characterization of telomere-subtelomere junctions in Silene latifolia. Mol Genet Genomics 269: 13–20.

    PubMed  CAS  Google Scholar 

  • Sykorova E, Fajkus J, Meznikova M et al. (2006a) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am J Bot 93: 814–823.

    CAS  Google Scholar 

  • Sykorova E, Leitch AR, Fajkus J (2006b) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60: 633–646.

    Article  PubMed  CAS  Google Scholar 

  • Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003b) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34: 283–291.

    Article  PubMed  CAS  Google Scholar 

  • Sykorova E, Lim KY, Kunicka Z et al. (2003c). Telomere variability in the monocotyledonous plant order Asparagales. Proc R Soc Lond B Biol Sci 270: 1893–1904.

    Article  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP et al. (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141–1160.

    PubMed  CAS  Google Scholar 

  • Tek AL, Junqui S, Macas J, Jiang J (2005) Sobo, a recently amplified satellite repeat and its implications on origin of tandemly repeated sequences. Genetics 170: 1231–1238.

    Article  PubMed  CAS  Google Scholar 

  • Vershinin AV, Heslop-Harrison JS (1998) Comparative analysis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol Biol 36: 1459–1461.

    Article  Google Scholar 

  • Vershinin AV, Schwarzacher T, Heslop-Harrison JS (1995) The large-scale genomic organization of repetitive DNA families at the telomeres of rye chromosomes. Plant Cell 7: 1823–1833.

    Article  PubMed  CAS  Google Scholar 

  • Vischi M, Jurman I, Bianchi G, Morgante M (2003) Karyotype of Norway spruce by multicolor FISH. Theor Appl Genet 107: 591–597.

    Article  PubMed  CAS  Google Scholar 

  • Weiss H, Scherthan H (2002) Aloe spp. – plants with vertebrate-like telomeric sequences. Chromosome Res 10: 155–164.

    Article  CAS  Google Scholar 

  • Wu J, Yamagata H, Hayashi-Tsugane M et al. (2004) Composition and structure of the centromeric region of rice chromosome 8. Plant Cell 16: 967–976.

    Article  PubMed  CAS  Google Scholar 

  • Wu KS, Tanksley SD (1993) Genetic and physical mapping of telomeres and macrosatellites of rice. Plant Mol Biol 22: 861–872.

    Article  PubMed  CAS  Google Scholar 

  • Zhong XB, Fransz PF, Wennekes-Eden J et al. (1998) FISH studies reveal the molecular and chromosomal organization of individual telomere domains in tomato. Plant J 13: 507–517.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Botany, Dresden University of Technology, Zellescher Weg 20b, 01062, Dresden, Germany

    Daryna Dechyeva & Thomas Schmidt

Authors
  1. Daryna Dechyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Schmidt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dechyeva, D., Schmidt, T. Molecular organization of terminal repetitive DNA in Beta species. Chromosome Res 14, 881–897 (2006). https://doi.org/10.1007/s10577-006-1096-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1096-8

Key words

Search

Navigation