Skip to main content
SpringerLink
Log in

Comparative analysis of the nucleosomal structure of rye, wheat and their relatives

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Analysis of the structure of chromatin in cereal species using micrococcal nuclease (MNase) cleavage showed nucleosomal organization and a ladder with typical nucleosomal spacing of 175–185 bp. Probing with a set of DNA probes localized in the authentic telomeres, subtelomeric regions and bulk chromatin revealed that these chromosomal regions have nucleosomal organization but differ in size of nucleosomes and rate of cleavage between both species and regions. Chromatin from Secale and Dasypyrum cleaved more quickly than that from wheat and barley, perhaps because of their higher content of repetitive sequences with hairpin structures accessible to MNase cleavage. In all species, the telomeric chromatin showed more rapid cleavage kinetics and a shorter nucleosome length (160 bp spacing) than bulk chromatin. Rye telomeric repeat arrays were shortest, ranging from 8 kb to 50 kb while those of wheat ranged from 15 kb up to 175 kb. A gradient of sensitivity to MNase was detected along rye chromosomes. The rye-specific subtelomeric sequences pSc200 and pSc250 have nucleosomes of two lengths, those of the telomeric and of bulk nucleosomes, indicating that the telomeric structure may extended into the chromosomes. More proximal sequences common to rye and wheat, the short tandem-repeat pSc119.2 and rDNA sequence pTa71, showed longer nucleosomal sizes characteristic of bulk chromatin in both species. A strictly defined spacing arrangement (phasing) of nucleosomes was demonstrated along arrays of tandem repeats with different monomer lengths (118, 350 and 550 bp) by combining MNase and restriction enzyme digestion.

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

  1. Bavykin SG, Usachenko SI, Zalensky AO, Mirzaberov AD: Structure of nucleosomes and organization of internucleosomal DNA in chromatin. J Mol Biol 212: 495–511 (1990).

    PubMed  Google Scholar 

  2. Belostotsky DA, Ananiev EV: Characterization of relic DNA from barley genome. Theor Appl Genet 80: 374–380 (1990).

    Google Scholar 

  3. Bendich AJ, McCarthy BJ: DNA comparisons among barley, oats, rye and wheat. Genetics 65: 545–566 (1970).

    Google Scholar 

  4. Bennett MD, Gustafson JP, Smith JB: Variation in nuclearDNA in the genus Secale. Chromosoma 61: 149–176 (1977).

    Google Scholar 

  5. Bennett MD, Smith JB: NuclearDNAamounts in angiosperms. Phil Trans R Soc Lond 274: 227–274 (1976).

    Google Scholar 

  6. Brinkley BR: Centromeres, kinetochores: integrated domains on eukaryotic chromosomes. Curr Opin Cell Biol 2: 446–452 (1990).

    Google Scholar 

  7. Budarf ML, Blackburn EH: Chromatin structure of the telomeric region and 30-nontranscribed spacer of Tetrahymena ribosomal RNA genes. J Biol Chem 261: 363–369 (1986).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  9. Cheah KSE, Osborne DJ: Analysis of nucleosomal deoxyribonucleic acid in a higher plant. Biochem J 163: 141–144 (1977).

    PubMed  Google Scholar 

  10. Cheung WY, Gale MD: The isolation of high molecular weight DNAfrom wheat, barley and rye for analysis by pulse-field gel electrophoresis. Plant Mol Biol 14: 881–888 (1990).

    PubMed  Google Scholar 

  11. Cheung WY, Money TA, Abbo S, Devos KM, Gale MD, Moore G: 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, (1994).

    PubMed  Google Scholar 

  12. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S: Telomere shortening associated with chromosome instability is arrested in immortal cellswhich express telomerase activity. EMBO J. 11: 1921–1929 (1992).

    PubMed  Google Scholar 

  13. Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P, Scherthan H, Ried T, Cremer C, Lichter P: Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harbor Symp Quant Biol 58: 777–791 (1993).

    PubMed  Google Scholar 

  14. Devos KM, Millan T, Gale M: Comparative RFLP maps of homoeologous group 2 chromosomes of wheat, rye and barley. Theor Appl Genet 85: 784–792 (1993).

    Google Scholar 

  15. Dingwall C, Lomonossoff GP, Laskey RA: High sequence specificity ofmicrococcal nuclease. Nucl Acids Res 9: 2659–2673 (1981).

    PubMed  Google Scholar 

  16. Dover GA: Molecular drive: a cohesive mode of species evolution. Nature 299: 111–117 (1982).

    PubMed  Google Scholar 

  17. Drew HR: Structural specificities of five commonly used DNA nucleases. J Mol Biol 176: 535–557 (1984).

    PubMed  Google Scholar 

  18. Endo TR, Gill BS: Somatic karyotype, heterochromatin distribution, and nature of chromosome differentiation in common wheat, Triticum aestivum L. em Thell. Chromosoma 89: 361–369 (1984).

    Google Scholar 

  19. Fajkus J, Kovarik A, Kralovics R, Bezdek M: Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247: 633–638 (1995).

    PubMed  Google Scholar 

  20. Fischer TC, Groner S, Zentgraf U, Hemleben V: Evidence for nucleosomal phasing and a novel protein specifically binding to cucumber satellite DNA. Z Naturforsch 49c: 79–86 (1994).

    Google Scholar 

  21. Flavell RB: Repetitive DNA and chromosome evolution in plants. Phil Trans R Soc London 312: 227–242 (1986).

    Google Scholar 

  22. Fuchs J, Brandes A, Schubert I: Telomere sequence localization and karyotype evolution in higher plants. Plant Syst Evol 196: 227–241 (1995).

    Google Scholar 

  23. Gazdova B, Siroky J, Brzobohaty B, Kenton A, Parokonny A, Heslop-Harrison JS, Palme K, Bezdek M: Characterization of a new family of tobacco highly repetitive DNA, GRS, specific for the Nicotiana tomentosiformis genomic component. Chromosome Res 3: 245–254 (1995).

    PubMed  Google Scholar 

  24. Gerlach W, Bedbrook L: Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucl Acids Res 7: 1869–1885 (1979).

    PubMed  Google Scholar 

  25. Greider CW, Autexier C, Avilion AA, Collins K, Harrington LA, Mantell LL, Prouse KR, Smith SK, Allsopp RC, Counter CM, Vaziri H, Bacchetti S, Harley CB: Telomeres and telomerase: biochemistry and regulation in senescence and immortalization. In: Heslop-Harrison JS, Flavell RB (eds) The Chromosome, pp. 115–126. BIOS, Oxford (1993).

    Google Scholar 

  26. Gross DS, Garrard WT: Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 57: 159–197 (1988).

    PubMed  Google Scholar 

  27. Gustafson JP, Lukaszewski AJ, Bennett MD: Somatic deletion and redistribution of telomeric heterochromatin in the genus Secale and in Triticale. Chromosoma 88: 293–298 (1983).

    Google Scholar 

  28. Heslop-Harrison JS, Leitch AR, Schwarzacher T: The physical organization of interphase nuclei. In: Heslop-Harrison JS, Flavell RB (eds) The Chromosome, pp. 221–232. BIOS, Oxford (1993).

    Google Scholar 

  29. Jofuku KD, Goldberg RB: Analysis of plant gene structure. In: Shaw CH (ed) PlantMolecular Biology: APractical Approach, pp. 37–66. IRL Press, Oxford (1988).

    Google Scholar 

  30. Kilian A, Stiff C, Kleinhofs A: Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci USA 92: 9555–9559 (1995).

    PubMed  Google Scholar 

  31. Leitch IJ, Heslop-Harrison JS: Physical mapping of the 18S-5._8S-25S rRNA genes in barley by in situ hybridization. Genome 35: 1013–1018 (1992).

    Google Scholar 

  32. Linde-Laursen I, Frederiksen S: Comparison of the Giemsa Cbanded karyotypes of Dasypyrum villosum (2X) and D. breviaristatum (4X) from Greece. Hereditas 114: 237–244 (1991).

    Google Scholar 

  33. Linde-Laursen I, von Bothmer R, Jacobsen N: Relationships in the genus Hordeum: Giemsa C-banded karyotypes. Hereditas 116: 111–116 (1992).

    Google Scholar 

  34. Makarov VL, Lejnine S, Bedoyan J, Langmore JP: Nucleosomal organization of telomere-specific chromatin in rat. Cell 73: 775–787 (1993).

    PubMed  Google Scholar 

  35. Manuelidis L, Chen TL: A unified model of eukaryotic chromosomes. Cytometry 11: 8–25 (1990).

    PubMed  Google Scholar 

  36. McIntyre CL, Pereira S, Moran LB, Appels R: New Secale cereale (rye) DNA derivatives for the detection of rye chromosome segments in wheat. Genome 33: 317–323 (1990).

    Google Scholar 

  37. Meersseman G, Pennings S, Bradbury EM: Mobile nucleosomes – a general behavior. EMBO J 11: 2951–2959 (1992).

    PubMed  Google Scholar 

  38. Mukai Y, Endo TR, Gill BS: Physical mapping of the 18S–26S rRNA multigene family in common wheat: Identification of a new locus. Chromosoma 100: 71–78 (1991).

    Google Scholar 

  39. Mukai Y, Nakahara Y, Yamamoto M: Simultaneous discrimination of the three genomes in hexaploid wheat by multicolor fluorescence in situ hybridization using total genomic and highly repeated DNA probes. Genome 36: 489–494 (1993).

    Google Scholar 

  40. Muller A, Philipps G, Gigot C: Properties of condensed chromatin in barley nuclei. Planta 149: 69–77 (1980).

    Google Scholar 

  41. Palmer DK, O'Day K, Le Trong K, Charbonneau K, Margous L: Purification of the centromeric protein CENP-A and demonstration that it is a centromere specific histone. Proc Natl Acad Sci USA 88: 3734–3738 (1991).

    PubMed  Google Scholar 

  42. Philipps G, Gigot C: DNA associated with nucleosomes in plants. Nucl Acids Res 4: 3617–3626 (1977).

    PubMed  Google Scholar 

  43. Pluta A, Cooke FCA, Earnshaw WC: Structure of the human centromere at metaphase. Trends Biol Sci 15: 181–185 (1990).

    Google Scholar 

  44. Polizzi C, Clarke L: The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J Cell Biol 112: 191–201 (1991).

    PubMed  Google Scholar 

  45. Radic MZ, Lundgren K, Hamkalo BA: Curvature of mouse satellite DNA and condensation of heterochromatin. Cell 50: 1101–1108 (1987).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  47. Richards EJ, Vongs A, Walsh M, Yang J, Chao S: Substructure of telomere repeat arrays. In: Heslop-Harrison JS, Flavell RB (eds) The Chromosome, pp. 103–114. BIOS, Oxford (1993).

    Google Scholar 

  48. Roder MS, Lapitan NLV, Sorrells ME, Tanksley SD: Genetic and physicalmapping of barley telomeres. MolGen Genet 238: 294–303 (1993).

    Google Scholar 

  49. Schildkraut CL, Marmur J, Doty P: Determination of the base composition of deoxyribonucleic acid from its buoyant density in CsCl. J Mol Biol 4: 430–433 (1962).

    PubMed  Google Scholar 

  50. Schwarzacher T, Heslop-Harrison JS: In situ hybridization to plant telomeres using synthetic oligomers. Genome 34: 317–323 (1990).

    Google Scholar 

  51. Simpson RT: Nucleosome positioning: occurrence, mechanism, and functional consequences. Prog Nucl Acids Res Mol Biol 40: 143–184 (1991).

    Google Scholar 

  52. Smith JG, Hill RS, Baldwin JP: Plant chromatin structure and post-translation modifications. CRC Crit Rev Plant Sci 14: 299–328 (1995).

    Google Scholar 

  53. Tommerup H, Dousmanis A, de Lange T: Unusual chromatin in human telomeres. Mol Cel Biol 14: 5777–5785 (1994).

    Google Scholar 

  54. Trifonov EN: Curved DNA. CRC Crit Rev Biochem 19: 89–106 (1985).

    PubMed  Google Scholar 

  55. van Holde KE: Chromatin. Springer-Verlag, New York (1989).

    Google Scholar 

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

    PubMed  Google Scholar 

  57. Vershinin AV, Schwarzacher T, Heslop-Harrison JS: The largescale genomic organization of repetitive DNA families at the telomeres of rye chromosomes. PlantCell 7 1823–1833 (1995).

    Google Scholar 

  58. Wallrath LL, Elgin SCR: Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Devel 9: 1263–1277 (1995).

    PubMed  Google Scholar 

  59. Wright JH, Gottschling DE, Zakian VA: Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Devel 6: 197–210 (1992).

    PubMed  Google Scholar 

  60. Wolffe AP: Chromatin: Structure and Function. Academic Press, San Diego (1995).

    Google Scholar 

  61. Wolffe AP, Pruss D: Deviant nucleosomes: the functional specialization of chromatin. Trends Genet 12: 58–62 (1996).

    PubMed  Google Scholar 

  62. Zakian V: Telomeres: beginning to undestand the end. Science 270: 1601–1607 (1995).

    PubMed  Google Scholar 

  63. Zhang X-Y, Fittler F, Horz W: Eight different highly specific nucleosome phases on α-satellite DNA in the African green monkey. Nucl Acids Res 11: 4287–4305 (1983).

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Alexander V. Vershinin

    Present address: Institute of Cytology and Genetics, Novosibirsk, Russia

Authors and Affiliations

  1. Department of Cell Biology, John Innes Centre, Colney, Karyobiology Group, Lane, Norwich, NR4 7UH, UK

    Alexander V. Vershinin & John S. Heslop-Harrison

Authors
  1. Alexander V. Vershinin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John S. Heslop-Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vershinin, A.V., Heslop-Harrison, J.S. Comparative analysis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol Biol 36, 149–161 (1998). https://doi.org/10.1023/A:1005912822671

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005912822671

Search

Navigation