Skip to main content
Log in

Transition between two forms of heterochromatin at plant subtelomeres

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The manner of packing of the terminal DNA loci into nucleosomes and higher order structures may strongly influence their functional interactions. Besides the structural flexibility of telomeric DNA sequences, conserved features of their chromatin including short nucleosome phasing (157 bp) and nucleosome sliding have been described previously. To gain a complementary knowledge of subtelomeres, we have analysed the chromatin structure of two subtelomeric tandem repeats from the plant Silene latifolia: X43.1 and 15Ssp. X43.1 shows two distinct nucleosome periodicities – 157 and 188 bp. Preferred positions of its two nucleosomes have been mapped at both low and high resolution and the experimental results correspond to computer-predicted positions. 15Ssp is a newly-discovered sequence showing a telomere-associated position by PCR and a subtelomeric location by pulsed-field gel electrophoresis and fluorescence in situ hybridisation. Its 159 bp sequence unit shows a tandem arrangement and the presence of micrococcal nuclease-hypersensitive sites when either naked DNA or chromatin is digested. Use of a chemical nuclease results in a regular nucleosome ladder of 157 bp periodicity. Moreover, 15Ssp mononucleosomes show instability and absence of specific positioning, features typical for telomeric chromatin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anselmi C, Bocchinfuso G, De Santis P, Savino M, Scipioni A (1999) Dual role of DNA intrinsic curvature and £exibility in determining nucleosome stability. J Mol Biol 286: 1293–1301.

    Article  PubMed  CAS  Google Scholar 

  • Ausio J, Dong F, van Holde KE (1989) Use of selectively trypsinized nucleosome core particles to analyze the role of the histone tails in the stabilization of the nucleosome. J Mol Biol 206: 451–463.

    Article  PubMed  CAS  Google Scholar 

  • Benezra R, Cantor CR, Axel R (1986) Nucleosomes are phased along the mouse beta-major globin gene in erythroid and nonerythroid cells. Cell 44: 697–704.

    Article  PubMed  CAS  Google Scholar 

  • Bužek J, Koutníková H, Houben A, Říha K, Janous ek B, Široký J, Grant S, Vyskot B (1997) Isolation and characterization of X chromosome-derived DNA sequences from a dioecious plant Melandrium album. Cromosome Res 5: 57–65.

    Article  Google Scholar 

  • Cartwright IL, Hertzberg RP, Dervan PB, Elgin SC (1983) Cleavage of chromatin with methidiumpropyl-EDTA. iron(II). Proc Natl Acad Sci USA 80: 3213–3217.

    Article  PubMed  CAS  Google Scholar 

  • Cohen P, Blackburn EH (1998) Two types of telomeric chromatin in Tetrahymena thermophila. J Mol Biol 280: 327–344.

    Article  PubMed  CAS  Google Scholar 

  • Dingwall C, Lomonossoff GP, Laskey RA (1981) High sequence specificity of micrococcal nuclease. Nucleic Acids Res 9: 2659–2673.

    PubMed  CAS  Google Scholar 

  • Eisenberg H, Felsenfeld G (1981) Hydrodynamic studies of the interaction between nucleosome core particles and core histones. J Mol Biol 150: 537–555

    Article  PubMed  CAS  Google Scholar 

  • Espina¨ s ML, Carballo M (1993) Pulsed-field electrophoresis analysis of higher-order chromatin structures of Zea mays. Highly methylated DNA in the 50 kb chromatin structure. Plant Molecular Biology 21: 847–857.

    Article  CAS  Google Scholar 

  • Fajkus J, Trifonov EN (2001) Columnar packing of telomeric nucleosomes. Biochem Biophys Res Commun 280: 961–963.

    Article  PubMed  CAS  Google Scholar 

  • Fajkus J, Vyskot B, Bezde k M (1992) Changes in chromatin structure due to hypomethylation induced with 5–azacytidine or DL-ethionine. FEBS Letters 314: 13–16.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fajkus J, Kralovics R, Kovarik A, Fajkusova L (1995b) The telomeric sequence is directly attached to the HRS60 sub-telomeric tandem repeat in tobacco chromosomes. FEBS Lett 364: 33–35.

    Article  PubMed  CAS  Google Scholar 

  • Feldman M, Liu B, Segal G, Abbo S, Levy AA, Vega JM(1997) Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of hom-oeologous chromosomes. Genetics 147: 1381–1387.

    PubMed  CAS  Google Scholar 

  • Fukui K, Iijima K (1991) Somatic chromosome map of rice by imaging methods. Theor Appl Genet 81: 589–596.

    Article  Google Scholar 

  • Garrido-Ramos MA, de la Herran R, Ruiz Rejon M, Ruiz Rejon C (1999) A subtelomeric satellite DNA family isolated from the genome of the dioecious plant Silene latifolia. Genome 42: 442–446.

    Article  PubMed  CAS  Google Scholar 

  • Guidet F, Langridge P (1992) Megabase DNA preparation from plant tissue. Methods in Enzymology 216: 3–12.

    Article  PubMed  CAS  Google Scholar 

  • Henderson E (1995) Telomere DNA structure. In: Blackburn EH, Greider CW, eds. Telomeres. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, pp. 11–34

    Google Scholar 

  • Hennig W (1999) Heterochromatin. Chromosoma 108: 1–9.

    Article  PubMed  CAS  Google Scholar 

  • Ioshikhes I, Bolshoy A, Derenshteyn K, Borodovsky M, Trifonov EN (1996) Nucleosome DNA sequence pattern revealed by multiple alignment of experimentally mapped sequences. J Mol Biol 262: 129–139.

    Article  PubMed  CAS  Google Scholar 

  • Kralovics R, Fajkus J, Kovarik A, Bezdek M (1995) DNA cur-vature of the tobacco GRS repetitive sequence family and its relation to nucleosome positioning. J Biomol Struct Dyn 12: 1103–1119.

    PubMed  CAS  Google Scholar 

  • Levitsky VG, Ponomarenko MP, Ponomarenko JV, Frolov AS, Kolchanov NA (1999) Nucleosomal DNA property database. Bioinformatics 15: 582–592.

    Article  PubMed  CAS  Google Scholar 

  • Li G, Chandler SP, Wolffe AP, Hall TC (1998) Architectural specificity in chromatin structure at the TATA box in vivo: nucleosome displacement upon beta-phaseolin gene acti-vation. Proc Natl Acad Sci USA 95: 4772–4777.

    Article  PubMed  CAS  Google Scholar 

  • Louis EJ (1995) The chromosome ends of Saccharomyces cerevisiae. Yeast 11: 1553–1573.

    Article  PubMed  CAS  Google Scholar 

  • Lu Q, Wallrath LL, Elgin SC (1994) Nucleosome positioning and gene regulation. J Cell Biochem 55: 83–92.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga S, Kawano S, Michimoto T, Higashiyama T, Nakao S, Sakai A, Kuroiwa T (1999) Semi-automatic laser beam microdissection of the Y chromosome and analysis of Y chromosome DNA in a dioecious plant, Silene latifolia. Plant Cell Physiol 40: 60–68.

    PubMed  CAS  Google Scholar 

  • Mengeritsky G, Trifonov EN (1983) Nucleotide sequence-directed mapping of the nucleosomes. Nucleic Acids Res 11: 3833–3851.

    PubMed  CAS  Google Scholar 

  • Ohmido N, Fukui K (1997) Visual verification of close dispo-sition between a rice A genome-specific DNA sequence (TrsA) and the telomere sequence. Plant Mol Biol 38: 963–968.

    Article  Google Scholar 

  • Palladino F, Gasser SM (1994) Telomere maintenance and gene represion: a common end? Current Opinion in Cell Biology 6: 373–379.

    Article  PubMed  CAS  Google Scholar 

  • Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4: 207–213.

    Article  PubMed  CAS  Google Scholar 

  • Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10: 1691–1698.

    Article  PubMed  CAS  Google Scholar 

  • Rossetti L, Cacchione S, Fua M, Savino M (1998) Nucleosome assembly on telomeric sequences. Biochemistry 37: 6727–6737.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning a laboratory manual (second edition). Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1998) Genomes, genes, and junk: the large-scale organization of plant chromosomes. Trends in Plant Science 3: 195–199.

    Article  Google Scholar 

  • Shpigelman ES, Trifonov EN, Bolshoy A (1993) CURVA-TURE: software for the analysis of curved DNA. CABIOS 9: 435–440.

    PubMed  CAS  Google Scholar 

  • Simpson RT (1991) Nucleosome positioning: occurrence, mechanisms, and functional consequences. Prog Nucleic Acid Res Mol Biol 40: 143–184.

    Article  PubMed  CAS  Google Scholar 

  • Sí iroky¨ J, Hodurkova¨ J, Negrutiu I, Vyskot B (1999) Functional and structural chromosome analyses in autotetraploid Silene latifolia. Annals of Botany 84: 633–638.

    Article  CAS  Google Scholar 

  • Thoma F (1992) Nucleosome positioning. Biochim Biophys Acta 1130: 1–19.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Trifonov EN (1989) The multiple codes of nucleotide sequences. Bulletin of Mathematical Biology 51: 417–432.

    Article  PubMed  CAS  Google Scholar 

  • Vagera J, Paulikova D, Dolezel J (1994) The development of male and female regenerants by in vitro andogenesis in dioecious plant Melandrium album. Annals of Botany 73: 455–459.

    Article  Google Scholar 

  • Vershinin AV, Heslop-Harrison JS (1998) Comparative analy-sis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol Biol 36: 149–161.

    Article  PubMed  CAS  Google Scholar 

  • Voordouw G, Eisenberg H (1978) Binding of additional his-tones to chromatin core particles. Nature 273: 446–448

    Article  PubMed  CAS  Google Scholar 

  • Vyskot B, Siroky J, Hladilova R, Belyaev ND, Turner BM (1999) Euchromatic domains in plant chromosomes as revealed by H4 histone acetylation and early DNA replication. Genome 42: 343–350.

    Article  PubMed  CAS  Google Scholar 

  • Wellinger RJ, Sen D (1997) The DNA structures at the ends of eukaryotic chromosomes. Eur J Cancer 33: 735–749.

    Article  PubMed  CAS  Google Scholar 

  • Widlund HR, Cao H, Simonsson S, Magnusson E, Simonsson T, Nielsen PE, Kahn JD, Crothers DM, Kubista M (1997) Identification and characterization of genomic nucleosome-positioning sequences. J Mol Biol 267: 807–817.

    Article  PubMed  CAS  Google Scholar 

  • Wu CI, Lyttle TW, Wu ML, Lin GF (1988) Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell 54: 179–189.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sýkorová, E., Fajkus, J., Ito, M. et al. Transition between two forms of heterochromatin at plant subtelomeres. Chromosome Res 9, 309–323 (2001). https://doi.org/10.1023/A:1016698713959

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016698713959

Navigation