Skip to main content
Log in

Chromosome healing by addition of telomeric repeats in wheat occurs during the first mitotic divisions of the sporophyte and is a gradual process

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Alien gametocidal chromosomes cause extensive chromosome breakage prior to S-phase in the first mitotic division of gametophytes lacking the alien chromosome. The broken chromosomes may be healed either by addition of telomeric repeats in the gametophyte or undergo fusions to form dicentric or translocation chromosomes. We show that dicentric chromosomes undergo breakage–fusion–bridge (BFB) cycles in the first few mitotic divisions of the sporophyte, are partially healed before the germ line differentiation regimen, and are healed completely in the ensuing gametophytic stage. The gametocidal factor on chromosome 4Mg of Aegilops geniculata was used to induce dicentrics involving the satellite chromosomes1B and 6B of wheat, Triticum aestivum. The dicentrics 1BS·1BL-2AL·2AS and 6BS·6BL-4BL·4BS initiated BFB cycles that ceased 2 to 4 weeks after seed germination. At the end of the BFB cycles, we observed deficient 1B and 6B chromosomes with breakpoints in proximal regions of the 1BL and 6BL arms. The process of chromosome healing was analyzed in root tip meristems, at meiotic metaphase I, and in the derived progenies by fluorescence in-situ hybridization analysis using a telomeric probe pAtT4. The results show that chromosome healing in wheat occurs during very early mitotic divisions in the sporophyte by de-novo addition of telomeric repeats and is a gradual process. Broken chromosome ends have to pass through several cell divisions in the sporophyte to acquire the full telomeric repeat length.

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

  • Blackburn EH (1991) Structure and function of telomeres. Nature 350: 56–573.

    Google Scholar 

  • Endo TR (1988) Induction of chromosomal changes by a chromosome from Aegilops cylindrica L. J Hered 79: 36–370.

    Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87: 29–307.

    Google Scholar 

  • Finch RA, Miller TE, Bennett MD (1984) ``Cuckoo'' Aegilops addition chromosome in wheat ensures its transmission by causing chromosome breaks in meiospores lacking it. Chromosoma 90: 8–88.

    Google Scholar 

  • Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7: 186–1885.

    Google Scholar 

  • Gill BS, Friebe B (1998) Plant cytogenetics at the dawn of the 21st century. Curr Opin Plant Biol 1: 10–115.

    Google Scholar 

  • Gill BS, Kimber G (1974) Giemsa C-banding and the evolution of wheat. Proc Natl Acad Sci. USA 71: 408–4090.

    Google Scholar 

  • Gill BS, Friebe B, Endo TR (1991) Karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34: 83–839.

    Google Scholar 

  • Gill KS, Gill BS, Endo TR (1993) A chromosome region-speci¢c mapping strategy reveals gene-rich telomeric ends in wheat. Chromosoma 102: 37–381.

    Google Scholar 

  • Harrington LA, Greidler CW (1991) Telomerase primer sensivity and chromosome healing. Nature 353: 45–454.

    Google Scholar 

  • Heller K, Kilian A, Piatyzek MA, Kleinhofs A (1996) Telomerase activity in plant extracts. Mol Gen Genet 252: 34–345.

    Google Scholar 

  • Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci USA 92: 955–9559.

    Google Scholar 

  • King IP, Laurie DA (1993) Chromosome damage in early embryo and endosperm development in crosses involving the preferentially transmitted 4Sl chromosome of Aegilops longissima. Heredity 70: 5–59.

    Google Scholar 

  • Kipling D (1995) The Telomere. Oxford, New York, Tokyo: Oxford University Press, pp 208.

    Google Scholar 

  • Kynast RG, Friebe B, Gill BS (2000) Fate of multicentric and ring chromosomes induced by a new gametocidal factor located on chromosome 4Mg of Aegilops geniculata. Chromosome Res 8: 13–139.

    Google Scholar 

  • Lamb J, Harris PC, Wilkie AOM, Wood WG, Dauwerse JUG, Higgs DR (1993) De novo truncation of chromosome 16p and healing with (TTAGGG)n in the a-thalassemia/mental retardation syndrome (ATR-16). Am J Hum Genet 52: 66–676.

    Google Scholar 

  • Lingner J, Cooper GP, Cech TR (1995) Telomerase and DNA replication: No longer a lagging strand problem? Science 269: 153–1534.

    Google Scholar 

  • Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR (1997) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 56–567.

    Google Scholar 

  • Meltzer PS, Guan X-Y, Trent JM (1993) Telomere capture stabilizes chromosome breakage. Nature Genet 4: 25–255.

    Google Scholar 

  • McClintock B (1938) The production of homozygous de¢cient tissues with mutant characteristics by means of the aberrant mitotic behavior of ring-shaped chromosomes. Genetics 23: 31–376.

    Google Scholar 

  • McClintock B (1941) The stability of broken ends of chromo-somes in Zea mays. Genetics 26: 23–282.

    Google Scholar 

  • McClintock B (1942) The fusion of broken ends of chromo-somes following nuclear fusion. Proc Natl Acad Sci USA 28: 45–463.

    Google Scholar 

  • McClintock B (1984) The signi¢cance of responses of the genome to challenge. Science 226: 79–801.

    Google Scholar 

  • Muller HJ (1940) Analysis of the process of structural changes in chromosomes of Drosophila. J Genet 40:1-66.

    Google Scholar 

  • Nasuda S, Friebe B, Gill BS (1998) Gametocidal genes induce chromosome breakage in the interphase prior to the ¢rst mitotic cell division of the male gametophyte in wheat. Genetics 149: 111–1124.

    Google Scholar 

  • Qi LL, Wang SL, Chen PD, Liu DJ, Friebe B, Gill BS (1997) Molecular cytogenetic analysis of Leymus racemosus chromosomes added to wheat. Theor Appl Genet 95: 108–1091.

    Google Scholar 

  • Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 12–136.

    Google Scholar 

  • Tsujimoto H (1993a) Synthesis of telomere repetitive sequences at the broken ends in common wheat chromosomes. WIS 76: 6–62.

    Google Scholar 

  • Tsujimoto H (1993b) Molecular cytogenetic evidence for grad-ual telomere synthesis at the broken ends in wheat. J Plant Res 106: 23–244.

    Google Scholar 

  • Tsujimoto H, Yamada T, Sasakuma T (1997) Molecular struc-ture of a wheat chromosome end healed after gametocidal gene-induced breakage. Proc Natl Acad Sci USA 94: 314–3144.

    Google Scholar 

  • Tsujimoto H, Usami N, Hasegawa K, Yamada T, Nagaki K, Sasakuma T (1999) De novo synthesis of telomere sequences at the healed breakpoints of wheat deletion chromosomes. Mol Gen Genet 262: 85–856.

    Google Scholar 

  • Wang SS, Zakian VA (1990) Telomere telomere recombination provides an express pathway for telomere acquisition. Nature 345: 45–458.

    Google Scholar 

  • Wang S, Lapitan NLV, RÎder M, Tsuchia T (1993) Characterization of telomeres in Hordeum vulgare chromosomes by in situ hybridization. II. Healed broken chromosomes in telotrisomic 4L and acrotrisomic 4L4S lines. Genome 35: 97–980.

    Google Scholar 

  • Wellinger RY, Sen D (1997) The DNA structures at the ends of eukaryotic chromosomes. Eur J Cancer 33, 73–749.

    Google Scholar 

  • Weng Y, Tuleen NA, Hart GE (2000) Extended physical maps and a consensus physical map of the homoeologous group-6 chromosomes of wheat (Triticum aestivum L. em Thell.). Theor Appl Genet 100: 51–527.

    Google Scholar 

  • Werner JE, Kota RS, Gill BS, Endo TR (1992) Distribution of telomeric repeats and their role in the healing of broken chromosomes in wheat. Genome 35: 84–848.

    Google Scholar 

  • Wilkie A, Lamb J, Harris P, Finney R, Higgs D (1990) A truncated human chromosome 16 associated with L. thalassemia is stabilized by addition of telomeric repeat (TTTAGGG)n. Nature 346: 86–871.

    Google Scholar 

  • Zakian VA (1989) Structure and function of telomeres. AnnRev Genet 23: 57–604.

    Google Scholar 

  • Zakian VA (1995) Telomeres: beginning to understand the end. Science 270: 160–1607.

    Google Scholar 

  • Zheng Y-Z, Roseman RR, Carlson WR (1999) Time course study of the chromosome-type breakage fusion bridge cycle in maize. Genetics 153: 143–1444.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Friebe, B., Kynast, R.G., Zhang, P. et al. Chromosome healing by addition of telomeric repeats in wheat occurs during the first mitotic divisions of the sporophyte and is a gradual process. Chromosome Res 9, 137–146 (2001). https://doi.org/10.1023/A:1009283003903

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009283003903

Navigation