Skip to main content
SpringerLink
Log in

Patterns of DNA Variation Among Three Centromere Satellite Families in Arabidopsis halleri and A. lyrata

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

We describe patterns of DNA variation among the three centromeric satellite families in Arabidopsis halleri and lyrata. The newly studied subspecies (A. halleri ssp. halleri and A. lyrata ssp. lyrata and petraea), like the previously studied A. halleri ssp. gemmifera and A. lyrata ssp. kawasakiana, have three different centromeric satellite families, the older pAa family (also present in A. arenosa) and two families, pAge1 and pAge2, that probably evolved more recently. Sequence variability is high in all three satellite families, and the pAa sequences do not cluster by their species of origin. Diversity in the pAge2 family is complex, and different from variation among copies of the other two families, showing clear evidence for exchange events among family members, especially in A. halleri ssp. halleri. In A. lyrata ssp. lyrata there is some evidence for recent rapid spread of pAge2 variants, suggesting selection favoring these sequences.

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. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Ananiev EV, Phillips RL, Rines HW (1998) Chromosome-specific molecular organization of maize (Zea Mays L.) centromeric regions. Proc Natl Acad Sci USA 95:13073–13078

    Article  PubMed  CAS  Google Scholar 

  • Cabot EL, Doshi P, Wu ML, Wu CI (1993) Population genetics of tandem repeats in centromeric heterochromatin: unequal crossing over and chromosomal divergence at the Responder locus of Drosophila melanogaster. Genetics 135:477–487

    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 

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

    Google Scholar 

  • Choo KHA (1998) Why is the centromere so cold? Genome Res 8:81–82

    PubMed  CAS  Google Scholar 

  • Copenhaver GP, Browne WE, Preuss D (1998). Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc Natl Acad Sci USA 95:247–252

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dooner HK (2004) Extensive interallelic polymorphisms drive meiotic recombination into a crossover pathway. Plant Cell 14:1173–1183

    Article  CAS  Google Scholar 

  • Dooner HK, Martinez-Férez IM (1997) Recombination occurs uniformly in the bronze gene, a recombination hotspot in the maize genome. Plant Cell 9:1633–1646

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D (2004) The rapidly evolving field of plant centromeres. Curr Opin Plant Biol 7:108–114

    Article  PubMed  CAS  Google Scholar 

  • Hall AE, Kettler GC, Preuss D (2006) Dynamic evolution at pericentromeres. Genome Res 16:355–364

    Article  PubMed  CAS  Google Scholar 

  • Hall SE, Luo S, Hall AE, Preuss D (2005) Differential rates of local and global homogenization in centromere satellites from Arabidopsis relatives. Genetics 170:1913–1927

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hosouchi T, Kumekawa N, Tsuruoka H, Kotani H (2002) Physical map-based sized of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. DNA Res 9:117–121

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    PubMed  CAS  Google Scholar 

  • Innan H (2004) Theories for analyzing polymorphism data in duplicated genes. Gen Genet Sys 79:65–75

    Article  CAS  Google Scholar 

  • Jensen MA, Charlesworth B, Kreitman M (2002) Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. Genetics 160:493–507

    PubMed  CAS  Google Scholar 

  • Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ (2005) Evolution of genome size in Brassicaceae. Ann Bot 95:229–235

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Kawabe A, Nasuda S (2005) Structure and genomic organization of centromeric repeat in Arabidopsis species. Mol Genet Genomics 272:593–602

    Article  PubMed  CAS  Google Scholar 

  • Kawabe A, Nasuda S (2006) Polymorphic chromosomal specificity of centromere satellite families in Arabidopsis halleri ssp. gemmifera. Genetica 126:335–342

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Jacobsen I, Nei M (2000) MEGA2: Molecular Evolutionary Genetics Analysis, version 2.0. Pennsylvania and Arizona State universities, University Park and Tempe

    Google Scholar 

  • Lo AW, Magliano DJ, Sibson P, Kalitsis P, Craig JM, Choo KHA (2001) A novel chromatin immunoprecipitation and array (CIA) analysis identifies a 460-kb CENP-A-binding neocentromere DNA. Genome Res 11:448–457

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Mestrovic N, Plohl M, Mravinac B, Ugarkovic D (1998) Evolution of satellite DNAs from the genus Palorus—experimental evidence for the “library” hypothesis. Mol Biol Evol 15:1062–1068

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Morgante M, Jurman I, Shi L, Zhu T, Keim P, Rafalski JA (1997) The STR120 satellite DNA of soybean: organization, evolution and chromosomal specificity. Chromosome Res 5:363–373

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  PubMed  CAS  Google Scholar 

  • Nagylaki T, Petes TD (1982) Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100:315–337

    PubMed  CAS  Google Scholar 

  • Nijman JJ, Lenstra JA (2001) Mutation and recombination in cattle satellite DNA: a feedback model for the evolution of satellite DNA repeat. J Mol Evol 52:361–371

    PubMed  CAS  Google Scholar 

  • Ohta T (1983) Time until fixation of a mutant belonging to a multigene family. Genet Res 41:47–55

    Article  Google Scholar 

  • Ohta T, Dover GA (1983) Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci USA 80:4079–4083

    Article  PubMed  CAS  Google Scholar 

  • Ohta T, Dover GA (1984) The cohesive population genetics of molecular drive. Genetics 108:501–521

    PubMed  CAS  Google Scholar 

  • Ramos-Onsins SE, Stranger BE, Mitchell-Olds T, Aguade M (2004) Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373–388

    Article  PubMed  CAS  Google Scholar 

  • Robles F, De La Herran R, Ludwig A, Rejon CR, Rejon MR, Garrido-Ramos MA (2004) Evolution of ancient satellite DNA in sturgeon genomes. Gene 338:133–142

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Saffery R, Sumer H, Hassan S, Wong LH, Craig JM, Todokoro K, Anderson M, Srafford A, Choo KHA (2003) Transcription within a functional human centromere. Mol Cell 12:509–516

    Article  PubMed  CAS  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University, St. Louis; available at: http://www.math.wustl.edu/∼sawyer

  • Schindelhauer D, Schwarz T (2002) Evidence for a fast intrachromosomal conversion mechanism from mapping of nucleotide variants within a homogeneous α-satellite DNA array. Genome Res 12:1815–1826

    Article  PubMed  CAS  Google Scholar 

  • Stephan W (1989) Tandem-repetitive noncoding DNA: forms and forces. Mol Biol Evol 6:198–212

    PubMed  CAS  Google Scholar 

  • Vershinin AV, Alkhimova EG, Heslop-Harrison JS (1996) Molecular diversification of tandemly organized DNA sequences and heterochromatic chromosome regions in some Triticeae species. Chromosome Res 4:517–525

    Article  PubMed  CAS  Google Scholar 

  • Wright SI, Lauga B, Charlesworth D (2003) Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol 12:1247–1263

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank S. Preuss for technical assistance and the Institute of Evolutionary Biology, Edinburgh University, sequencing service for sequencing.

Author information

Authors and Affiliations

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

    Akira Kawabe & Deborah Charlesworth

Authors
  1. Akira Kawabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deborah Charlesworth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akira Kawabe.

Additional information

[Reviewing Editor: Dr. Brian Morton]

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawabe, A., Charlesworth, D. Patterns of DNA Variation Among Three Centromere Satellite Families in Arabidopsis halleri and A. lyrata . J Mol Evol 64, 237–247 (2007). https://doi.org/10.1007/s00239-006-0097-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-006-0097-8

Keywords

Search

Navigation