Skip to main content
SpringerLink
Log in

Divergence of satellite DNA and interspersion of dispersed repeats in the genome of the wild beet Beta procumbens

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Several repetitive sequences of the genome of Beta procumbens Chr. Sm., a wild beet species of the section Procumbentes of the genus Beta have been isolated. According to their genomic organization, the repeats were assigned to satellite DNA and families of dispersed DNA sequences.

The tandem repeats are 229–246 bp long and belong to an AluI restriction satellite designated pAp11. Monomers of this satellite DNA form subfamilies which can be distinguished by the divergence or methylation of an internal restriction site. The satellite is amplified in the section Procumbentes, but is also found in species of the section Beta including cultivated beet (Beta vulgaris). The existence of the pAp11 satellite in distantly related species suggests that the AluI sequence family is an ancient component of Beta genomes and the ancestor of the diverged satellite subfamily pEV4 in B. vulgaris. Comparative fluorescent in-situ hybridization revealed remarkable differences in the chromosomal position between B. procumbens and B. vulgaris, indicating that the pAp11 and pEV4 satellites were most likely involved in the expansion or rearrangement of the intercalary B. vulgaris heterochromatin.

Furthermore, we describe the molecular structure, and genomic and chromosomal organization of two repetitive DNA families which were designated pAp4 and pAp22 and are 1354 and 582 bp long, respectively. The families consist of sequence elements which are widely dispersed along B. procumbens chromosomes with local clustering and exclusion from distal euchromatic regions. FISH on meiotic chromosomes showed that both dispersed repeats are colocalized in some chromosomal regions. The interspersion of repeats of the pAp4 and pAp22 family was studied by PCR and enabled the determination of repeat flanking sequences. Sequence analysis revealed that pAp22 is either derived from or part of a long terminal repeat (LTR) of an Athila-like retrotransposon. Southern analysis and FISH with pAp4 and pAp22 showed that both dispersed repeats are species-specific and can be used as DNA probes to discriminate parental genomes in interspecific hybrids. This was tested in the sugar beet hybrid PRO1 which contains a small B. procumbens chromosome fragment.

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

  • Aledo R, Raz R, Monfort A, Vicient CM, Puigdomenech P, Martinez-Izquierdo JA (1995) Chromosome localization and characterization of a family of long interspersed repetitive DNA elements from the genus Zea. Theor Appl Genet 90:1094-1100.

    Google Scholar 

  • Anamthawat-Jónsson K, Bödvarsdòttir SK (1998) Meiosis of wheat ×lymegrass hybrids. Chromosome Res 6: 339-343.

    Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species.PlantMol BiolRep 9: 208-218.

    Google Scholar 

  • Barciszewska M, Barciszewski J (1988) Yellow lupin cytoplasmic tRNAGlu is not a cofactor in chlorophyll biosynthesis. Mol Biol Rep 13: 11-14.

    Google Scholar 

  • Barthes L, Ricroch A (2001) Interspecific chromosomal rearrangements in monosomic addition lines of Allium. Genome 44:929-935.

    Google Scholar 

  • Bennetzen JL, Schrick K, Springer PS, Brown WE, SanMiguel P( 1994) Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37: 565-576.

    Google Scholar 

  • Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution.Plant Mol Biol 42:251-269.

    Google Scholar 

  • Brandes A, Tompson H, Dean C, Heslop-Harrison JS (1997) Multiple repetitive DNA sequences in the paracentromeric regions of Arabidopsis thaliana L. Chromosome Res 5:238-246.

    Google Scholar 

  • Chavanne F, Zhang DX, Liaud MF, Cerff R (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.

    Google Scholar 

  • Copenhaver GP, Nickel K, Kuromori T et al. (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468-2474.

    Google Scholar 

  • Dong F, Miller JT, Jackson SA, Wang GL, Ronald PC, Jiang J (1998) Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci USA 95: 8135-8140.

    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.

    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.

    Google Scholar 

  • Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95: 1971-1974.

    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.

    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.

    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.

    Google Scholar 

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

    Google Scholar 

  • Hemleben V, Schmidt T, Torres-Ruiz RA, Zentgraf U (2000) Molecular cell biology: Role of repetitive DNA in nuclear architecture and chromosome structure. Progr Botany 61: 91-117.

    Google Scholar 

  • Heslop-Harrison JS (1996) Comparative analysis of plant genome architecture. Symp Soc Exp Biol 50: 17-23.

    Google Scholar 

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

    Google Scholar 

  • Heslop-Harrison JS, Brandes A, Taketa S et al. (1997) The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100: 197-204.

    Google Scholar 

  • Heslop-Harrison JS, Murata M, Ogura Y, Schwarzacher T, Motoyoshi F (1999) Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11:31-42.

    Google Scholar 

  • Horakova M, Fajkus J (2000) TAS49 —a dispersed repetitive sequence isolated from subtelomeric regions of Nicotiana tomentosiformis chromosomes. Genome 43: 273-284.

    Google Scholar 

  • Hudakova S, Michalek W, Presting GG et al. (2001) Sequence organization of barley centromeres. Nucleic Acids Res 29: 5029-5035.

    Google Scholar 

  • Hueros G, Loarce Y, Ferrer E (1993) A structural and evolutionary analysis of a dispersed repetitive sequence. Plant Mol Biol 22:635-643.

    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.

    Google Scholar 

  • Jansen R (1999) Molekulare und zytologische Analyse von repetitiven DNA-Sequenzen der Sektion Corollinae der Gattung Beta. PhD Thesis. Christian-Albrechts University, Kiel.

    Google Scholar 

  • Jin YK, Bennetzen JL (1994) Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6:1177-1186.

    Google Scholar 

  • Jung C, Wricke G (1987) Selection of diploid nematoderesistant sugar beets from addition lines. Plant Breeding 98: 205-214.

    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.

    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.

    Google Scholar 

  • Kapila R, Negi MS, This P, Delseny M, Srivastava PS, Lakshmikumaran M (1996) A new family of dispersed repeats from Brassica nigra: characterization and localization. Theor Appl Genet 93: 1123-1129.

    Google Scholar 

  • Katsiotis A, Schmidt T, Heslop-Harrison JS (1995) Sequences of Ty1-copia-like retrotransposon elements in genus Avena. Chromosome Res 3: 52-53.

    Google Scholar 

  • Kiefer-Meyer MC, Reddy AS, Delseny M (1995) Characterization of a dispersed repetitive DNA sequence associated with the CCDD genome of wild rice. Genome 38: 681-688.

    Google Scholar 

  • Kiefer-Meyer MC, Reddy AS, Delseny M (1996) Complex arrangement of dispersed repeated DNA sequences in Oryza officinalis. Genome 39: 183-190.

    Google Scholar 

  • Kovarik A, Koukalova B, Lim KY et al. (2000) Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chromosome Res 8: 527-541.

    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.

    Google Scholar 

  • Kubis S, Heslop-Harrison JS, S chmidt T (1998) RepetitiveDNA elements as a major component of plant genomes. Ann Bot 82: 45-55.

    Google Scholar 

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

    Google Scholar 

  • Kumekawa N, Ohmido N, Fukui K, Ohtsubo E, Ohtsubo H (2001) A new gypsy-type retrotransposon, RIRE7: preferential insertion into the tandem repeat sequence TrsD in pericentromeric heterochromatin regions of rice chromosomes. Mol Genet Genomics 265: 480-488.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • McNeil D, Lagudah ES, Hohmann U, Appels R (1994) Amplification of DNA sequences in wheat and its relatives: the Dgas44 and R350 families of repetitive sequences. Genome 37: 320-327.

    Google Scholar 

  • Nagaki K, Tsujimoto H, Sasakuma T (1998) A novel repetitive sequence of sugar cane, SCEN family, locating on centromeric regions. Chromosome Res 6: 295-302.

    Google Scholar 

  • Nelson M, Raschke E, McClelland M (1993) Effect of site-specific methylation on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res 21:3139-3154.

    Google Scholar 

  • Neumann P, Nouzova M, Macas J (2001) Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Genome 44: 716-728.

    Google Scholar 

  • Nouzova M, Neumann P, Navratilova A, Galbraith DW, Macas J (2001) Microarray-based survey of repetitive genomic sequences in Vicia spp. Plant Mol Biol 45: 229-244.

    Google Scholar 

  • Ohmido N, Kijima K, Akiyama Y, de Jong JH, Fukui K (2000) Quantification of total genomic DNA and selected repetitive sequences reveals concurrent changes in different DNA families in indica and japonica rice. Mol Gen Genet 263: 388-394.

    Google Scholar 

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

    Google Scholar 

  • Peterson DG, Tomkins JP, Fritsch DA, Wing RA, Paterson AH (2000) Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. J Agricult Genomics 5. Edited by B. Beavis and G. May. Available from http://www.ncgr.org/jag/

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

    Google Scholar 

  • Salentijn EMJ, Sandal NN, Klein-Lankhorst R et al. (1994) Long-range organization of a satellite DNA family flanking the beet cyst nematode resistance locus (Hs1) on chromosome 1 of B. patellaris and B. procumbens. Theor Appl Genet 89:459-466.

    Google Scholar 

  • SanMiguel P, Tikhonov A, Jin YK et al. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765-768.

    Google Scholar 

  • Schmidt T, Junghans H, Metzlaff M (1990) Construction of Beta procumbens-specific DNA probes and their application for the screening of B. vulgaris ×B. procumbens (2n = 19) addition lines. Theor Appl Genet 79: 177-181.

    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.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Schmidt T, Kubis S, Heslop-Harrison J S (1995) Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs and Ty1-copia-like elements as major components of the genome. Chromosome Res 3: 335-345.

    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.

    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.

    Google Scholar 

  • Schmidt T, Kubis S, Katsiotis A, Jung C, Heslop-Harrison J S (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.

    Google Scholar 

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

    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.

    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.

    Google Scholar 

  • Vicient CM, Kalendar R, Schulman AH (2001) Envelope-class retrovirus-like elements are widespread, transcribed and spliced, and insertionally polymorphic in plants. Genome Res 11: 2041-2049.

    Google Scholar 

  • Willard HF, Waye JS (1987) Hierarchical order in chromosome-specific human alpha satellite DNA. Trends Genet 3: 192-198.

    Google Scholar 

  • Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12: 122-131.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Molecular Cytogenetics Group, Institute of Crop Science and Plant Breeding, Christian-Albrechts-University of Kiel, Olshausenstr. 40, D-24118, Kiel, Germany

    Daryna Dechyeva & Thomas Schmidt

  2. CellTec GmbH Biotechnologie, Frohmestrasse 110, 22459, Hamburg, Germany

    Frank Gindullis

Authors
  1. Daryna Dechyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frank Gindullis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. 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., Gindullis, F. & Schmidt, T. Divergence of satellite DNA and interspersion of dispersed repeats in the genome of the wild beet Beta procumbens . Chromosome Res 11, 3–21 (2003). https://doi.org/10.1023/A:1022005514470

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022005514470

Search

Navigation