Skip to main content
SpringerLink
Log in

Structure and genomic organization of centromeric repeats in Arabidopsis species

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Centromeric repetitive sequences were isolated from Arabidopsis halleri ssp. gemmifera and A. lyrata ssp. kawasakiana. Two novel repeat families isolated from A. gemmifera were designated pAge1 and pAge2. These repeats are 180 bp in length and are organized in a head-to-tail manner. They are similar to the pAL1 repeats of A. thaliana and the pAa units of A. arenosa. Both A. gemmifera and A. kawasakiana possess the pAa, pAge1 and pAge2 repeat families. Sequence comparisons of different centromeric repeats revealed that these families share a highly conserved region of approximately 50 bp. Within each of the four repeat families, two or three regions showed low levels of sequence variation. The average difference in nucleotide sequence was approximately 10% within families and 30% between families, which resulted in clear distinctions between families upon phylogenetic analysis. FISH analysis revealed that the localization patterns for the pAa, pAge1 and pAge2 families were chromosome specific in A. gemmifera and A. kawasakiana. In one pair of chromosomes in A. gemmifera, and three pairs of chromosomes in A. kawasakiana, two repeat families were present. The presence of three families of centromeric repeats in A. gemmifera and A. kawasakiana indicates that the first step toward homogenization of centromeric repeats occurred at the chromosome level.

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

Fig. 1
Fig. 2A–D
Fig. 3
Fig. 4
Fig. 5A–L

Similar content being viewed by others

References

  • Aragon-Alcaide L, Miller T, Schwarzacher T, Reader S, Moore G (1996) A cereal centromeric sequence. Chromosoma 105:261–268

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cheng ZJ, Murata M (2003) A centromeric tandem repeat family originating from a part of a Ty3/gypsy -retroelement in wheat and its relatives. Genetics 164:665–672

    CAS  PubMed  Google Scholar 

  • Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, Gu M, Blattner FR, Jang J (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704

    Article  CAS  PubMed  Google Scholar 

  • Choo KHA (1997) The Centromere. Oxford University Press, New York

  • Choo KH, Vissel B, Nagy A, Earle E, Kalitsis P (1991) A survey of the genomic distribution of alpha satellite DNA on all human chromosomes, and derivation of a new consensus sequence. Nucleic Acids Res 19:1179–1182

    CAS  PubMed  Google Scholar 

  • Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, McCombie WR, Martienssen RA, Marra M, Preuss D (1999) Genetic definition and sequence analysis of Arabidopsis centromere. Science 286:2468–2474

    CAS  PubMed  Google Scholar 

  • Csink AK, Henikoff S (1998) Something from nothing: the evolution and utility of satellite repeats. Trends Genet 14:200–204

    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

    Article  CAS  PubMed  Google Scholar 

  • Fransz P, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA, Ward DC (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J 136:867–876

    Article  Google Scholar 

  • Haaf T, Willard HF (1997) Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma 106:226–232

    Article  CAS  PubMed  Google Scholar 

  • Hall SE, Kettler G, Preuss D (2003) Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res 13:195–205

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Haupt W, Fischer TC, Winderl S, Fransz P, Torres-Ruiz RA (2001) The CENTROMERE1 (CEN1) region of Arabidopsis thaliana: architecture and functional impact of chromatin. Plant J 27:285–296

    CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison JS, Brandes A, Schwarzacher T (2003) Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res 11:241–253

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Nasuda S, Dong F, Scherrer CW, Woo SS, Wing RA, Gill BS, Ward DC (1996) A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci USA 136:14210–14213

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kawabe A, Miyashita NT (1999) DNA variation in the basic chitinase locus ( ChiB) region of the wild plant Arabidopsis thaliana. Genetics 153:1445–1453

    CAS  PubMed  Google Scholar 

  • Kawabe A, Innan H, Terauchi R, Miyashita NT (1997) Nucleotide polymorphism in the acidic chitinase locus ( ChiA) region of the wild plant Arabidopsis thaliana. Mol Biol Evol 14:1303–1315

    Google Scholar 

  • Kawabe A, Yamane K, Miyashita NT (2000) DNA polymorphism at the cytosolic phosphoglucose isomerase ( PgiC) locus of the wild plant Arabidopsis thaliana. Genetics 156:1339–1347

    CAS  PubMed  Google Scholar 

  • Kishii M, Nagaki K, Tsujimoto H (2001) A tandem repetitive sequence located in the centromeric region of common wheat ( Triticum aestivum) chromosomes. Chromosome Res 9:417–428

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Bishop J, Mitchell-Olds T (1999) Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol 1:529–539

    Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis , and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Google Scholar 

  • Kumar S, Tamura K, Jacobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17:1244–1245

    Article  CAS  PubMed  Google Scholar 

  • Kumekawa N, Hosouchi T, Tsuruoka H, Kotani H (2000) The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 5. DNA Res 7:315–321

    CAS  PubMed  Google Scholar 

  • Kumekawa N, Hosouchi T, Tsuruoka H, Kotani H (2001) The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 4. DNA Res 8:285–290

    CAS  PubMed  Google Scholar 

  • Laurent AM, Marcais B, Muleris M, Roizes G (1994) A rapid and simple method to isolate and characterize highly polymorphic markers from the centromeric regions of the human chromosomes. Nucleic Acids Res 22:194–199

    CAS  PubMed  Google Scholar 

  • Malik HS, Henikoff S (2001) Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157:1293–1298

    CAS  PubMed  Google Scholar 

  • Maluszynska J, Heslop-Harrison JS (1991) Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1:159–166

    Article  Google Scholar 

  • Martinez-Zapater J, Estelle MA, Somerville CR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204:417–423

    CAS  Google Scholar 

  • Miyashita NT, Innan H, Terauchi R (1996) Intra- and inter specific variation in the alcohol dehydrogenase locus region of wild plants Arabis gemmifera and Arabidopsis thaliana. Mol Biol Evol 13:433–436

    CAS  PubMed  Google Scholar 

  • Miyashita NT, Kawabe A, Innan H, Terauchi R (1998) Intra- and interspecific DNA variation and codon bias of alcohol dehydrogenase ( Adh) locus in Arabis and Arabidopsis species. Mol Biol Evol 15:1420–1429

    Google Scholar 

  • Murata M, Ogura Y, Motoyoshi F (1994) Centromeric repetitive sequence in Arabidopsis thaliana. Jpn J Genet 69:361–370

    CAS  PubMed  Google Scholar 

  • Murphy TD, Karpen GH (1998) Centromeres take flight: alpha satellite and the quest for the human centromere. Cell 93:317–320

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J (2003) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163:1221–1225

    CAS  PubMed  Google Scholar 

  • Pidoux AL, Allshire RC (2000) Centromeres: getting a grip of chromosomes. Curr Opin Cell Biol 12:308–319

    Article  CAS  PubMed  Google Scholar 

  • Presting GG, Malysheva L, Fuchs J, Schubert I (1998) A TY3/GYPSY retrotransposon-like sequence localizes to the centromeric region of cereal chromosomes. Plant J 16:721–728

    Article  CAS  PubMed  Google Scholar 

  • Richards EJ, Dawe RK (1998) Plant centromere: structure and control. Curr Opin Plant Biol 1:130–135

    Article  CAS  PubMed  Google Scholar 

  • Round EK, Flowers SK, Richards EJ (1997) Arabidopsis thaliana centromere regions: genetic map position and repetitive DNA structure. Genome Res 7:1045–1053

    CAS  PubMed  Google Scholar 

  • Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schubert I, Shi F, Fuchs J, Endo TR (1998) An efficient screening for terminal deletions and translocations of barley chromosomes added to common wheat. Plant J 14:489–495

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sullivan BA, Blower MD, Karpen GH (2001) Determining centromere identity: cyclical stories and forking paths. Nature Rev Genet 2:584–596

    Article  CAS  Google Scholar 

  • Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066

    Article  CAS  PubMed  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  PubMed  Google Scholar 

  • Warburton PE, Waye PE, Willard HF (1993) Nonrandom localization of recombination events in human alpha satellite repeat unit variants: implications for higher-order structural characteristics within centromeric heterochromatin. Mol Cell Biol 13:6520–6529

    CAS  PubMed  Google Scholar 

  • Warburton PE, Haaf T, Gosden J, Lawson D, Willard HF (1996) Characterization of a chromosome-specific chimpanzee alpha satellite subset: evolutionary relationship to subsets on human chromosomes. Genomics 33:220–228

    Article  CAS  PubMed  Google Scholar 

  • Yoda K, Kitagawa K, Masumoto H, Muro Y, Okazaki T (1992) A human centromere protein, CENP-B, has a DNA-binding domain containing four potential α helices at the NH2 terminus, which is separable from dimerizing activity. J Cell Biol 119:1413–1427

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank N. Goto for providing seeds. We also thank M. Murata for technical advice, suggestions and comments, and T. R. Endo for use of his facilities and for technical suggestions. We are grateful to D. Charlesworth for proofreading and suggestions. A.K. was supported by a research fellowship for young scientists awarded by the Japan Society for the Promotion of Science. This article is Contribution No. 579 from the Laboratory of Plant Genetics, Graduate School of Agriculture, Kyoto University

Author information

Authors and Affiliations

  1. Laboratory of Plant Genetics, Graduate School of Agriculture, Kyoto University, 606-8502, Kyoto, Japan

    A. Kawabe & S. Nasuda

  2. CREST, Japan Science and Technology Corporation, 101-0062, Tokyo, Japan

    A. Kawabe & S. Nasuda

  3. Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, King’s Buildings, West Mains Road, Edinburgh, EH9 3JT, UK

    A. Kawabe

Authors
  1. A. Kawabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Nasuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by W. R. McCombie

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawabe, A., Nasuda, S. Structure and genomic organization of centromeric repeats in Arabidopsis species. Mol Genet Genomics 272, 593–602 (2005). https://doi.org/10.1007/s00438-004-1081-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-004-1081-x

Keywords

Search

Navigation