Advertisement

Chromosome Research

, Volume 16, Issue 5, pp 683–700 | Cite as

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

  • Nicolas Pouilly
  • Régine Delourme
  • Karine Alix
  • Eric Jenczewski
Article

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.

Key words

Brassica napus genetic mapping Retrotransposons satellite DNA S-SAP 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.CrossRefGoogle Scholar
  2. Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54: 895–909.Google Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. Ashikawa I, Kurata N, Nagamura Y, Minobe Y (1994) Cloning and mapping of telomere-associated sequencesfrom rice. DNA Res 1: 67–76.PubMedCrossRefGoogle Scholar
  5. Azzalin CM, Nergadze SG, Giulotto E (2001) Human intrachromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110: 75–82.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13–15.Google Scholar
  13. Eichler EE, Sankoff D (2003) Structural dynamics of eukaryotic chromosome evolution. Science 301:793–797.PubMedCrossRefGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. Fajkus J, Sykorová E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13: 469–479.PubMedCrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. Ferreira ME, Williams PH, Osborn TC (1994) RFLP mapping of Brassica napus using doubled haploid lines. Theor Appl Genet 89: 615–621.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3: 87–94.PubMedCrossRefGoogle Scholar
  20. Ganal MW, Broun P, Tanksley SD (1992) Genetic mapping of tandemly repeated telomeric DNA sequences in tomato (Lycopersicon esculentum). Genomics 14: 444–448.PubMedCrossRefGoogle Scholar
  21. Hall AE, Kettler GC, Preuss D (2006) Dynamic evolution at pericentromeres. Genome Res 16: 355–364.PubMedCrossRefGoogle Scholar
  22. Harrison GE, Heslop-Harrison JS (1995) Centromeric repetitive DNA sequences in the genus Brassica. Theor Appl Genet 90: 157–165.CrossRefGoogle Scholar
  23. Howell EC, Barker GC, Jones GH et al. (2002) Integration of the cytogenetic and genetic linkage maps of Brassica oleracea. Genetics 161: 1225–1234.PubMedGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. Kilian A, Kleinhofs A (1992) Cloning and mapping of telomere-associated sequences from Hordeum vulgare L. Mol Gen Genet 235: 153–156.PubMedCrossRefGoogle Scholar
  30. Koornneef M (1983) The use of telotrisomics for centromere mapping in Arabidopsis thaliana (L.) Heynh. Genetica 62: 33–40.CrossRefGoogle Scholar
  31. 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.PubMedGoogle Scholar
  32. 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.Google Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.Google Scholar
  37. Linardopoulou EV, Williams EM, Fan Y et al. (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94–100.PubMedCrossRefGoogle Scholar
  38. 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.Google Scholar
  39. Liti G, Louis EJ (2005) Yeast evolution and comparative genomics. Annu Rev Microbiol 59: 135–154.PubMedCrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23: 134–139.PubMedCrossRefGoogle Scholar
  44. Mao L, Devos KM, Zhu L, Gale MD (1997) Cloning and genetic mapping of wheat telomere-associated sequences. Mol Gen Genet 254: 584–591.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. Palmer JD, Shields CR, Cohen DB, Orton TJ (1983) Chloroplast DNA evolution and the origin of amphidiploid Brassica. Theor Appl Genet 65: 181–189.CrossRefGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. Parkin IAP, Lydiate D (1997) Conserved patterns of chromosome pairing and recombination in Brassica napus crosses. Genome 40: 496–504.PubMedCrossRefGoogle Scholar
  51. 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.PubMedGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. Parkin IA, Sharpe AG, Lydiate DJ (2003) Patterns of genome duplication within the Brassica napus genome. Genome 46: 291–303.Google Scholar
  54. Perry J, Slater HR, Choo KHA (2004) Centric fission—simple and complex mechanisms. Chromosome Res 12: 627–640.PubMedCrossRefGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. 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.PubMedCrossRefGoogle Scholar
  57. Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 127–136.PubMedCrossRefGoogle Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. Round EK, Flowers SK, Richards EJ (1997) Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res 7: 1045–1053.PubMedGoogle Scholar
  60. 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.PubMedGoogle Scholar
  61. Schertan H (1995) Chromosome evolution in muntjac revealed by centromere, telomere and whole chromosome paint probes. Kew Chromosome Conf. IV: 264–280.Google Scholar
  62. Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large scale organization of plant chromosomes. Trends Plant Sci 3: 195–199.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. Shen L, Zhu L (1998) Direct PCR-based genetic mapping of rice telomeric repeat associated sequences. Genome 41: 193–198.CrossRefGoogle Scholar
  65. 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
  66. 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.PubMedCrossRefGoogle Scholar
  67. Sýkorová E, Lim KY, Kunická Z et al. (2003) Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270: 1893–1904.PubMedCrossRefGoogle Scholar
  68. Tek AL, Jiang J (2004) The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 113: 77–83.PubMedCrossRefGoogle Scholar
  69. 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.PubMedCrossRefGoogle Scholar
  70. 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
  71. Uchida W, Matsunaga S, Sugiyama R, Kawano S (2002) Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77: 63–67.PubMedCrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. Vos P, Hogers R, Bleeker M et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407–4414.PubMedCrossRefGoogle Scholar
  75. 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.PubMedCrossRefGoogle Scholar
  76. 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.PubMedCrossRefGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Nicolas Pouilly
    • 1
    • 2
  • Régine Delourme
    • 1
  • Karine Alix
    • 3
  • Eric Jenczewski
    • 4
  1. 1.INRA, Agrocampus Rennes, Université Rennes 1UMR 118 Amélioration des Plantes et Biotechnologies VégétalesLe Rheu CedexFrance
  2. 2.Laboratoire des Interactions Plantes Micro-organismesUMR CNRS-INRA 2594/441Castanet Tolosan CedexFrance
  3. 3.UMR de Génétique Végétale INRA / Université Paris-Sud / CNRS / AgroParisTechGif sur YvetteFrance
  4. 4.INRA, Institut Jean Pierre BourginStation de Génétique et Amélioration des PlantesVersaillesFrance

Personalised recommendations