Skip to main content
Log in

Telomeres in evolution and evolution of telomeres

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

This paper examines telomeres from an evolutionary perspective. In the monocot plant order Asparagales two evolutionary switch-points in telomere sequence are known. The first occurred when the Arabidopsis-type telomere was replaced by a telomere based on a repeat motif more typical of vertebrates. The replacement is associated with telomerase activity, but the telomerase has low fidelity and this may have implications for the binding of telomeric proteins. At the second evolutionary switch-point, the telomere and its mode of synthesis are replaced by an unknown mechanism. Elsewhere in plants (Sessia, Vestia, Cestrum) and in arthropods, the telomere “typical” of the group is lost. Probably many other groups with “unusual” telomeres will be found. We question whether telomerase is indeed the original end-maintenance system and point to other candidate processes involving t-loops, t-circles, rolling circle replication and recombination. Possible evolutionary outcomes arising from the loss of telomerase activity in alternative lengthening of telomere (ALT) systems are discussed. We propose that elongation of minisatellite repeats using recombination/replication processes initially substitutes for the loss of telomerase function. Then in more established ALT groups, subtelomeric satellite repeats may replace the telomeric minisatellite repeat whilst maintaining the recombination/replication mechanisms for telomere elongation. Thereafter a retrotransposition-based end-maintenance system may become established. The influence of changing sequence motifs on the properties of the telomere cap is discussed. The DNA and protein components of telomeres should be regarded – as with any other chromosome elements – as evolving and co-evolving over time and responding to changes in the genome and to environmental stresses. We describe how telomere dysfunction, resulting in end-to-end chromosome fusions, can have a profound effect on chromosome evolution and perhaps even speciation.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Adams SP, Hartman TP, Lim KY et al. (2001) Loss and recovery of Arabidopsis-type telomere repeat sequences 5′-(TTTAGGG)(n)-3′ in the evolution of a major radiation of flowering plants. Proc R Soc Lond B Biol Sci 268: 1541–1546.

    Article  Google Scholar 

  • Adams SP, Leitch IJ, Bennett MD, Leitch AR (2000) Aloe L. – a second plant family without (TTTAGGG)n telomeres. Chromosoma 109: 201–205.

    Article  PubMed  Google Scholar 

  • Barnes SR, James AM, Jamieson G (1985) The organisation, nucleotide sequence, and chromosomal distribution of satellite DNA from Allium cepa. Chromosoma 92: 185–192.

    Google Scholar 

  • Barton NH, Hewitt GM (1981) A chromosomal cline in the grasshopper Podisma pedestris. Evolution 35: 1008–1018.

    Google Scholar 

  • Bedoyan JK, Lejnine S, Makarov VL, Langmore JP (1996) Condensation of rat telomere-specific nucleosomal arrays containing unusually short DNA repeats and histone H1. J Biol Chem 271: 18485–18493.

    Article  PubMed  Google Scholar 

  • Blackburn EH, Gall JG (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120: 33–53.

    Article  PubMed  Google Scholar 

  • Boulton SJ, Jackson SP (1996) Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res 24: 4639–4648.

    Article  PubMed  Google Scholar 

  • Broun P, Ganal MW, Tanksley SD (1992) Telomeric arrays display high levels of heritable polymorphism among closely related plant varieties. Proc Natl Acad Sci USA 89: 1354–1357.

    PubMed  Google Scholar 

  • Bryan TM, Marusic L, Bacchetti S, Namba M, Reddel RR (1997) The telomere lengthening mechanism in telomerase-negative immortal human cells does not involve the telomerase RNA subunit. Hum Mol Genet 6: 921–926.

    Article  PubMed  Google Scholar 

  • Butlin RK (1993) Barriers to gene flow. Nature 366: 27.

    Article  Google Scholar 

  • Chen Q, Ijpma A, Greider CW (2001) Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol Cell Biol 21: 1819–1827.

    Article  PubMed  Google Scholar 

  • Dudasova Z, Dudas A, Chovanec M (2004) Non-homologous end-joining factors of Saccharomyces cerevisiae. FEMS Microbiol Rev 28: 581–601.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Fajkus J, Novotná M, Ptáček J (2002) Analysis of chromosome termini in potato varieties. Rostl Výroba 48: 477–479.

    Google Scholar 

  • Fajkus J, Sykorova E, Leitch AR (2005) Techniques in plant telomere biology. Biotechniques 38: 233–243.

    PubMed  Google Scholar 

  • Fay MF, Rudall PJ, Sullivan S et al. (2000) Phylogentic studies of Asparagales based on four plastid regions. In: Wilson KL, Morrison DA eds., Monocots: Systematics and Evolution. Melbourne: CSIRO, pp. 360–371.

    Google Scholar 

  • Featherstone C, Jackson SP (1998) DNA repair: the Nijmegen breakage syndrome protein. Curr Biol 8: R622–625.

    Article  PubMed  Google Scholar 

  • Fitzgerald MS, Riha K, Gao F, Ren S, McKnight TD, Shippen DE (1999) Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci USA 96: 14813–14818.

    Google Scholar 

  • Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJ, Zabel P, de Jong JH (1996) High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J 9: 421–430.

    Article  PubMed  Google Scholar 

  • Frydrychova R, Marec F (2002) Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115: 179–187.

    PubMed  Google Scholar 

  • Frydrychova R, Grossmann P, Trubac P, Vitkova M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47: 163–178.

    Article  PubMed  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3: 87–94.

    PubMed  Google Scholar 

  • Garcia-Cao M, O’Sullivan R, Peters AH, Jenuwein T, Blasco MA (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36: 94–99.

    PubMed  Google Scholar 

  • Gazdova B, Siroky J, Fajkus J et al. (1995) Characterization of a new family of tobacco highly repetitive DNA, GRS, specific for the Nicotiana tomentosiformis genomic component. Chromosome Res 3: 245–254.

    Article  PubMed  Google Scholar 

  • Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405–413.

    Article  PubMed  Google Scholar 

  • Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51: 887–898.

    Article  PubMed  Google Scholar 

  • Hartmann N, Scherthan H (2004) Characterization of ancestral chromosome fusion points in the Indian muntjac deer. Chromosoma 112: 213–220.

    Article  PubMed  Google Scholar 

  • Hauffe HC, Panithanarak T, Dallas JF, Pialek J, Gunduz I, Searle JB (2004) The tobacco mouse and its relatives: a “tail” of coat colors, chromosomes, hybridization and speciation. Cytogenet Genome Res 105: 395–405.

    Article  PubMed  Google Scholar 

  • Hewitt GM, Nichols RA, Barton NH (1987) Homogamy in a hybrid zone in the alpine grasshopper Podisma pedestris. Heredity 59: 457–466.

    Google Scholar 

  • Ioshikhes I, Bolshoy A, Trifonov EN (1992) Preferred positions of AA and TT dinucleotides in aligned nucleosomal DNA sequences. J Biomol Struct Dyn 9: 1111–1117.

    PubMed  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  Google Scholar 

  • King M (1993) Species Evolution. The role of chromosome change, Cambridge: Cambridge University Press.

    Google Scholar 

  • Kovařík A, Fajkus J, Koukalová BE, Bezděk M (1996) Species-specific evolution of telomeric and rDNA repeats in the tobacco composite genome. Theor Appl Genet 92: 1108–1111.

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Kuchar M, Fajkus J (2004) Interactions of putative telomere-binding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Lett 578: 311–315.

    Article  PubMed  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.

    PubMed  Google Scholar 

  • Lei M, Podell ER, Cech TR (2004) Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat Struct Mol Biol 11: 1223–1229.

    Article  PubMed  Google Scholar 

  • Lejnine S, Makarov VL, Langmore JP (1995) Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc Natl Acad Sci USA 92: 2393–2397.

    PubMed  Google Scholar 

  • Levin DA (2002) The Role of Chromosomal Change in Plant Evolution. New York: Oxford University Press.

    Google Scholar 

  • Liu D, Safari A, O’Connor MS et al. (2004) PTOP interacts with POT1 and regulates its localization to telomeres. Nat Cell Biol 6: 673–680.

    Article  PubMed  Google Scholar 

  • Lopez CC, Rodriguez E, Diez JL, Edstrom J, Morcillo G (1999) Histochemical localization of reverse transcriptase in polytene chromosomes of chironomids. Chromosoma 108: 302–307.

    Article  PubMed  Google Scholar 

  • Louis EJ (2002) Are Drosophila telomeres an exception or the rule? Genome Biol 3: Review S0007.

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

    Article  PubMed  Google Scholar 

  • McClintock B (1938) The fusion of broken chromosome ends of sister half-chromatids following chromatid breakage at meiotic anaphases. Missouri Agric Exp Station Res Bull 290: 1–48.

    Google Scholar 

  • McClintock B (1941) The stability of broken ends of chromosomes in Zea mays. Genetics 26: 234–282.

    Google Scholar 

  • Muller HJ (1938) The remaking of chromosomes. Collecting Net. 13: 181–195, 198.

    Google Scholar 

  • Nosek J, Rycovska A, Makhov AM, Griffith JD, Tomaska L (2005) Amplification of telomeric arrays via rolling-circle mechanism. J Biol Chem 280: 10840–10845.

    PubMed  Google Scholar 

  • K Oguchi H Liu K Tamura H Takahashi (1999) ArticleTitleMolecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana FEBS Lett 457 465–469 Occurrence Handle10.1016/S0014-5793(99)01083-2 Occurrence Handle10471830

    Article  PubMed  Google Scholar 

  • Pearce SR, Pich U, Harrison G, Flavell AJ et al. (1996) The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the terminal heterochromatin. Chromosome Res 4: 357–364.

    PubMed  Google Scholar 

  • Pich U, Schubert I (1998) Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosome Res 6: 315–321.

    Article  PubMed  Google Scholar 

  • Pich U, Fritsch R, Schubert I (1996a) Closely related Allium species (Alliaceae) share a very similar satellite sequence. Plant Syst Evol 202: 255–264.

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Porter G, Westmoreland J, Priebe S, Resnick MA (1996) Homologous and homeologous intermolecular gene conversion are not differentially affected by mutations in the DNA damage or the mismatch repair genes RAD1, RAD50, RAD51, RAD52, RAD54, PMS1 and MSH2. Genetics 143: 755–767.

    PubMed  Google Scholar 

  • Puizina J, Weiss-Schneeweiss H, Pedrosa-Harand A et al. (2003) Karyotype analysis in Hyacinthella dalmatica (Hyacinthaceae) reveals vertebrate-type telomere repeats at the chromosome ends. Genome 46: 1070–1076.

    Article  PubMed  Google Scholar 

  • Puizina J, Siroky J, Mokros P, Schweizer D, Riha K (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16: 1968–1978.

    Article  PubMed  Google Scholar 

  • K Ríha DE Shippen (2003) ArticleTitleKu is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis Proc Natl Acad Sci USA 100 611–615 Occurrence Handle10.1073/pnas.0236128100 Occurrence Handle12511598

    Article  PubMed  Google Scholar 

  • Ríha K, McKnight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291: 1797–1800.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rosen M, Edstrom J (2000) DNA structures common for chironomid telomeres terminating with complex repeats. Insect Mol Biol 9: 341–347.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rotkova G, Sklenickova M, Dvorackova M, Sykorova E, Leitch AR, Fajkus J (2004) An evolutionary change in telomere sequence motif within the plant section Asparagales had significance for telomere nucleoprotein complexes. Cytogenet Genome Res 107: 132–138.

    PubMed  Google Scholar 

  • Sadaie M, Naito T, Ishikawa F (2003) Stable inheritance of telomere chromatin structure and function in the absence of telomeric repeats. Genes Dev 17: 2271–2282.

    Article  PubMed  Google Scholar 

  • Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7: 449–460.

    Article  PubMed  Google Scholar 

  • Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267: 3025–3031.

    PubMed  Google Scholar 

  • Schrumpfova P, Kuchar M, Mikova G, Skrisovska L, Kubicarova T, Fajkus J (2004) Characterization of two Arabidopsis thaliana myb-like proteins showing affinity to telomeric DNA sequence. Genome 47: 316–324.

    PubMed  Google Scholar 

  • Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92: 143–148.

    Article  Google Scholar 

  • Siroky J, Zluvova J, Riha K, Shippen DE, Vyskot B (2003) Rearrangements of ribosomal DNA clusters in late generation telomerase-deficient Arabidopsis. Chromosoma 112: 116–123.

    Article  PubMed  Google Scholar 

  • Sykorova E, Fajkus J, Ito M, Fukui K (2001) Transition between two forms of heterochromatin at plant subtelomeres. Chromosome Res 9: 309–323.

    Article  PubMed  Google Scholar 

  • Sykorova E, Lim KY, Fajkus J, Leitch AR (2003a) The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)n telomeres. Chromosoma 112: 164–172.

    Article  PubMed  Google Scholar 

  • Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003b) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34: 283–291.

    Article  PubMed  Google Scholar 

  • Sykorova E, Lim KY, Kunicka Z et al. (2003c) Telomere variability in the monocotyledonous plant order Asparagales. Proc R Soc Lond B Biol Sci 270: 1893–1904.

    Article  Google Scholar 

  • Teng SC, Zakian VA (1999) Telomere–telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19: 8083–8093.

    PubMed  Google Scholar 

  • Tomaska L, Nosek J, Makhov AM, Pastorakova A, Griffith JD (2000) Extragenomic double-stranded DNA circles in yeast with linear mitochondrial genomes: potential involvement in telomere maintenance. Nucleic Acids Res 28: 4479–4487.

    Article  PubMed  Google Scholar 

  • Tomaska L, McEachern MJ, Nosek J (2004) Alternatives to telomerase: keeping linear chromosomes via telomeric circles. FEBS Lett 567: 142–146.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • van Steensel B, Smogorzewska A, de Lange T (1998) TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401–413.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Vitkova M, Kral J, Traut W, Zrzavy J, Marec F (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13: 145–156.

    Article  PubMed  Google Scholar 

  • Weiss H, Scherthan H (2002) Aloe spp. – plants with vertebrate-like telomeric sequences. Chromosome Res 10: 155–164.

    Article  PubMed  Google Scholar 

  • Weiss-Schneeweiss H, Riha K, Jang CG, Puizina J, Scherthan H, Schweizer D (2004) Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesises vertebrate-type telomere sequences. Plant J 37: 484–493.

    Article  PubMed  Google Scholar 

  • West CE, Waterworth WM, Sunderland PA, Bray CM (2004) Arabidopsis DNA double-strand break repair pathways. Biochem Soc Trans 32: 964–966.

    Article  PubMed  Google Scholar 

  • White MJD (1973) Animal Cytology and Evolution. London: Cambridge University Press.

    Google Scholar 

  • Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642–652.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jiří Fajkus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fajkus, J., Sýkorová, E. & Leitch, A.R. Telomeres in evolution and evolution of telomeres. Chromosome Res 13, 469–479 (2005). https://doi.org/10.1007/s10577-005-0997-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-005-0997-2

Key words

Navigation