Skip to main content
SpringerLink
Log in

Repetitive sequence-derived markers tag centromeres and telomeres and provide insights into chromosome evolution in Brassica napus

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Centromeres and telomeres are obvious markers on chromosomes but their location on genetic maps is difficult to determine, which hampers many basic and applied research programmes. In this study, we used the characteristic distribution of five Brassica repeated sequences to generate physically anchored molecular markers tentatively tagging Brassica centromeres (84 markers) and telomeres (31 markers). These markers were mapped to the existing oilseed rape genetic map. Clusters of centromere-related loci were observed on 14 linkage groups; in addition to previous reports, we could thus provide information about the most likely position of centromeres on 17 of the 19 B. napus linkage groups. The location of centromeres on linkage groups usually matches their position on chromosomes and coincides with sites of evolutionary breakage between chromosomes. Most telomere sequence-derived markers mapped interstitially or in the proximity of centromeres; this result echoes previous reports on many eukaryote genomes and may reflect different forms of chromosome evolution. Seven telomere sequence-derived markers were located at the outermost positions of seven linkage groups and therefore probably tagged telomeres.

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

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

    Article  Google Scholar 

  • Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54: 895–909.

    Google Scholar 

  • Alix K, Ryder CD, Moore J, King GJ, Heslop-Harrison JS (2005) The genomic organization of retrotransposons in Brassica oleracea. Plant Mol Biol 59: 839–851.

    Article  PubMed  CAS  Google Scholar 

  • Ashikawa I, Kurata N, Nagamura Y, Minobe Y (1994) Cloning and mapping of telomere-associated sequencesfrom rice. DNA Res 1: 67–76.

    Article  PubMed  CAS  Google Scholar 

  • Azzalin CM, Nergadze SG, Giulotto E (2001) Human intrachromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110: 75–82.

    Article  PubMed  CAS  Google Scholar 

  • Brandes A, Heslop-Harrison JS, Kamm A, Kubis S, Doudrick RL, Schmidt T (1997) Comparative analysis of the chromosomal and genomic organization of Ty1-copia-like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol Biol 33: 11–21.

    Article  PubMed  CAS  Google Scholar 

  • Casa AM, Brouwer C, Nagel A et al. (2000) Inaugural article: the MITE family heartbreaker (Hbr): molecular markers in maize. Proc Natl Acad Sci U S A 97: 10083–10089.

    Article  PubMed  CAS  Google Scholar 

  • Causse MA, Fulton TM, Cho YG et al. (1994) Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138: 1251–1274.

    PubMed  CAS  Google Scholar 

  • Cheung WY, Money TA, Abbo S, Devos KM, Gale MD, Moore G (1994) A family of related sequences associated with (TTTAGGG)n repeats are located in the interstitial regions of wheat chromosomes. Mol Gen Genet 245: 349–354.

    Article  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 U S A 95: 247–252.

    Article  PubMed  CAS  Google Scholar 

  • Delourme R, Falentin C, Huteau V et al. (2006) Genetic control of oil content in oilseed rape (Brassica napus L.). Theor Appl Genet 113: 1331–1345.

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13–15.

    Google Scholar 

  • Eichler EE, Sankoff D (2003) Structural dynamics of eukaryotic chromosome evolution. Science 301:793–797.

    Article  PubMed  CAS  Google Scholar 

  • Ellis TH, Poyser SJ, Knox MR, Vershinin AV, Ambrose MJ (1998) Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. Mol Gen Genet 260: 9–19.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fan Y, Linardopoulou E, Friedman C, Williams E, Trask BJ (2002) Genomic structure and evolution of the ancestral chromosome fusion site 2q13–2q14.1 and paralogous regions on other human chromosomes. Genome Res 12: 1651–1662.

    Article  PubMed  CAS  Google Scholar 

  • Ferreira ME, Williams PH, Osborn TC (1994) RFLP mapping of Brassica napus using doubled haploid lines. Theor Appl Genet 89: 615–621.

    Article  CAS  Google Scholar 

  • Foisset N, Delourme R, Barret P, Hubert N, Landry BS, Renard M (1996) Molecular mapping analysis in Brassica napus using isozyme, RAPD and RFLP markers on a doubled-haploid progeny. Theor Appl Genet 93: 1017–1025.

    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 

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

    Article  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 

  • Howell EC, Barker GC, Jones GH et al. (2002) Integration of the cytogenetic and genetic linkage maps of Brassica oleracea. Genetics 161: 1225–1234.

    PubMed  CAS  Google Scholar 

  • Hu J (2006) Defining the sunflower (Helianthus annuus L.) linkage group ends with the Arabidopsis-type telomere sequence repeat-derived markers. Chromosome Res 14: 535–548.

    Article  PubMed  CAS  Google Scholar 

  • Ijdo JW, Baldini A, Ward DC, Reeders ST, Wells RA (1991) Origin of human chromosome 2: an ancestral telomere-telomere fusion. Proc Natl Acad Sci U S A 88: 9051–9055.

    Article  PubMed  CAS  Google Scholar 

  • Inoue M, Gao Z, Hirata M, Fujimori M, Cai H (2004) Construction of a high-density linkage map of italian ryegrass (Lolium multiflorum Lam.) using restriction fragment length polymorphism, amplified fragment length polymorphism, and telomeric repeat associated sequence markers. Genome 47: 57–65.

    Article  PubMed  CAS  Google Scholar 

  • Kalendar R, Grob T, Regina M, Suoniemi A, Schulman A (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98: 704–711.

    Article  CAS  Google Scholar 

  • Kawabe A, Hansson B, Hagenblad J, Forrest A, Charlesworth D (2006) Centromere locations and associated chromosome rearrangements in Arabidopsis lyrata and A. thaliana. Genetics 173: 1613–1619.

    Article  PubMed  CAS  Google Scholar 

  • Kilian A, Kleinhofs A (1992) Cloning and mapping of telomere-associated sequences from Hordeum vulgare L. Mol Gen Genet 235: 153–156.

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M (1983) The use of telotrisomics for centromere mapping in Arabidopsis thaliana (L.) Heynh. Genetica 62: 33–40.

    Article  Google Scholar 

  • Kunzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154: 397–412.

    PubMed  CAS  Google Scholar 

  • Landry BS, Hubert N, Etoh T, Harada J, Lincoln SE (1991) A genetic map for Brassica napus based on restriction fragment length polymorphisms detected with expressed DNA sequences. Genome 34: 543–552.

    CAS  Google Scholar 

  • Lee C, Sasi R, Lin CC (1993) Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs. Cytogenet Cell Genet 63: 156–159.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lim KB, Yang TJ, Hwang YJ et al. (2007) Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. Plant J 49: 173–183.

    Article  PubMed  CAS  Google Scholar 

  • Lin BY, Chang SJ, Lin HM (2001) RFLP mapping of the centromere of chromosomes 1, 6 and 9 by B-A translocations in maize. Bot Bull Acad Sinica 42: 273–279.

    CAS  Google Scholar 

  • Linardopoulou EV, Williams EM, Fan Y et al. (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94–100.

    Article  PubMed  CAS  Google Scholar 

  • Lincoln S, Daly M, Lander E (1992) Constructing Genetic Linkage Maps with Mapmaker/Exp 3.0: A Tutorial and Reference Manual. Whitehead Institute Technical Report, 3rd edn.

  • Liti G, Louis EJ (2005) Yeast evolution and comparative genomics. Annu Rev Microbiol 59: 135–154.

    Article  PubMed  CAS  Google Scholar 

  • Lombard V, Delourme R (2001) A consensus linkage map for rapeseed (Brassica napus L.): construction and integration of three individual maps from DH populations. Theor Appl Genet 103: 491–507.

    Article  CAS  Google Scholar 

  • Luce AC, Sharma A, Mollere OS et al. (2006) Precise centromere mapping using a combination of repeat junction markers and chromatin immunoprecipitation-polymerase chain reaction. Genetics 174: 1057–1061.

    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 U S A 103: 5224–5229.

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23: 134–139.

    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 

  • Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG) n among vertebrates. Proc Natl Acad Sci U S A 86: 7049–7053.

    Article  PubMed  CAS  Google Scholar 

  • Murphy WJ, Larkin DM, Everts-van der Wind A et al. (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309: 613–617.

    Article  PubMed  CAS  Google Scholar 

  • Nanda I, Schrama D, Feichtinger W, Haaf T, Schartl M, Schmid M (2002) Distribution of telomeric (TTAGGG) n sequences in avian chromosomes. Chromosoma 111: 215–227.

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Shields CR, Cohen DB, Orton TJ (1983) Chloroplast DNA evolution and the origin of amphidiploid Brassica. Theor Appl Genet 65: 181–189.

    Article  CAS  Google Scholar 

  • Park TH, Kim JB, Hutten RC, van Eck HJ, Jacobsen E, Visser RG (2007) Genetic positioning of centromeres using half-tetrad analysis in a 4×–2× cross population of potato. Genetics 176: 85–94.

    Article  PubMed  CAS  Google Scholar 

  • Parkin IAP, Lydiate D (1997) Conserved patterns of chromosome pairing and recombination in Brassica napus crosses. Genome 40: 496–504.

    Article  PubMed  CAS  Google Scholar 

  • Parkin IAP, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38: 1122–1131.

    PubMed  CAS  Google Scholar 

  • Parkin IA, Gulden SM, Sharpe AG et al. (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171: 765–781.

    Article  PubMed  CAS  Google Scholar 

  • Parkin IA, Sharpe AG, Lydiate DJ (2003) Patterns of genome duplication within the Brassica napus genome. Genome 46: 291–303.

  • Perry J, Slater HR, Choo KHA (2004) Centric fission—simple and complex mechanisms. Chromosome Res 12: 627–640.

    Article  PubMed  CAS  Google Scholar 

  • Piquemal J, Cinquin E, Couton F et al. (2005) Construction of an oilseed rape (Brassica napus L.) genetic map with SSR markers. Theor Appl Genet 111: 1514–1523.

    Article  PubMed  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 

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

    Article  PubMed  CAS  Google Scholar 

  • Richards EJ, Goodman HM, Ausubel FM (1991) The centromere region of Arabidopsis thaliana chromosome 1 contains telomere-similar sequences. Nucleic Acids Res 19: 3351–3357.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sandhu D, Champoux JA, Bondareva SN, Gill KS (2001) Identification and physical localization of useful genes and markers to a major gene-rich region on wheat group 1S chromosomes. Genetics 157: 1735–1747.

    PubMed  CAS  Google Scholar 

  • Schertan H (1995) Chromosome evolution in muntjac revealed by centromere, telomere and whole chromosome paint probes. Kew Chromosome Conf. IV: 264–280.

  • 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 

  • Schneerman MC, Lee WS, Doyle G, Weber DF (1998) RFLP mapping of the centromere of chromosome 4 in maize using isochromosomes for 4S. Theor Appl Genet 96: 361–368.

    Article  CAS  Google Scholar 

  • Shen L, Zhu L (1998) Direct PCR-based genetic mapping of rice telomeric repeat associated sequences. Genome 41: 193–198.

    Article  CAS  Google Scholar 

  • Song K, Osborn TC (1992) Polyphyletic origins of Brassica napus: new evidence based on organelle and nuclear RFLP analyses. Genome 35: 992–1001.

    Google Scholar 

  • Sun Z, Wang Z, Tu J et al. (2007) An ultradense genetic recombination map for Brassica napus, consisting of 13551 SRAP markers. Theor Appl Genet 114: 1305–1317.

    Article  PubMed  CAS  Google Scholar 

  • Sýkorová E, Lim KY, Kunická Z et al. (2003) Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270: 1893–1904.

    Article  PubMed  CAS  Google Scholar 

  • Tek AL, Jiang J (2004) The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 113: 77–83.

    Article  PubMed  CAS  Google Scholar 

  • Tremousaygue D, Manevski A, Bardet C, Lescure N, Lescure B (1999) Plant interstitial telomere motifs participate in the control of gene expression in root meristems. Plant J 20: 553–561.

    Article  PubMed  CAS  Google Scholar 

  • UN (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japan J Bot 7: 389–452.

    Google Scholar 

  • Uchida W, Matsunaga S, Sugiyama R, Kawano S (2002) Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77: 63–67.

    Article  PubMed  CAS  Google Scholar 

  • Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homologous recombination in four mapping populations of Brassica napus L. Genetics 169: 967–979.

    Article  PubMed  CAS  Google Scholar 

  • Uzunova M, Ecke W, Weissleder K, Robbelen G (1995) Mapping the genome of rapeseed (Brassica napus L.) I. Construction of an RFLP linkage map and localization of QTLs for seed glucosinolate content. Theor Appl Genet 90: 194–204.

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407–4414.

    Article  PubMed  CAS  Google Scholar 

  • Waugh R, McLean K, Flavell AJ et al. (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253: 687–694.

    Article  PubMed  CAS  Google Scholar 

  • Wu HK, Chung MC, Wu TY, Ning CN, Wu R (1991) Localization of specific repetitive DNA sequences in individual rice chromosomes. Chromosoma 100: 330–338.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Obrien PCM, Wienberg J, Fergusson-Smith FA (1997) A reappraisal of the tandem fusion theory of karyotype evolution in the Indian muntjac using chromosome painting. Chromosome Res 5: 109–117.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. INRA, Agrocampus Rennes, Université Rennes 1, UMR 118 Amélioration des Plantes et Biotechnologies Végétales, Le Rheu Cedex, France

    Nicolas Pouilly & Régine Delourme

  2. Laboratoire des Interactions Plantes Micro-organismes, UMR CNRS-INRA 2594/441, Castanet Tolosan Cedex, France

    Nicolas Pouilly

  3. UMR de Génétique Végétale INRA / Université Paris-Sud / CNRS / AgroParisTech, Gif sur Yvette, France

    Karine Alix

  4. INRA, Institut Jean Pierre Bourgin, Station de Génétique et Amélioration des Plantes, Versailles, Route de Saint Cyr, F-78026, Versailles, France

    Eric Jenczewski

Authors
  1. Nicolas Pouilly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Régine Delourme
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karine Alix
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric Jenczewski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric Jenczewski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pouilly, N., Delourme, R., Alix, K. et al. Repetitive sequence-derived markers tag centromeres and telomeres and provide insights into chromosome evolution in Brassica napus . Chromosome Res 16, 683–700 (2008). https://doi.org/10.1007/s10577-008-1219-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-008-1219-5

Key words

Search

Navigation