Cellular and Molecular Life Sciences

, Volume 71, Issue 5, pp 847–865 | Cite as

If the cap fits, wear it: an overview of telomeric structures over evolution

  • Nick Fulcher
  • Elisa Derboven
  • Sona Valuchova
  • Karel RihaEmail author


Genome organization into linear chromosomes likely represents an important evolutionary innovation that has permitted the development of the sexual life cycle; this process has consequently advanced nuclear expansion and increased complexity of eukaryotic genomes. Chromosome linearity, however, poses a major challenge to the internal cellular machinery. The need to efficiently recognize and repair DNA double-strand breaks that occur as a consequence of DNA damage presents a constant threat to native chromosome ends known as telomeres. In this review, we present a comparative survey of various solutions to the end protection problem, maintaining an emphasis on DNA structure. This begins with telomeric structures derived from a subset of prokaryotes, mitochondria, and viruses, and will progress into the typical telomere structure exhibited by higher organisms containing TTAGG-like tandem sequences. We next examine non-canonical telomeres from Drosophila melanogaster, which comprise arrays of retrotransposons. Finally, we discuss telomeric structures in evolution and possible switches between canonical and non-canonical solutions to chromosome end protection.


Telomeres Telomerase Chromosomes Genome evolution DNA repair Retrotransposons 



Our research on telomeres is supported by the Austrian Science Fund (FWF, Y418-B03) and Austrian Academy of Sciences.


  1. 1.
    Egel R (2012) Primal eukaryogenesis: on the communal nature of precellular states, ancestral to modern life. Life 2:170–212Google Scholar
  2. 2.
    Lode T (2012) For quite a few chromosomes more: the origin of eukaryotes. J Mol Biol 423(2):135–142. doi: 10.1016/jjmb201207005S0022-2836(12)00557-8 PubMedGoogle Scholar
  3. 3.
    Ishikawa F, Naito T (1999) Why do we have linear chromosomes? A matter of Adam and Eve. Mutat Res 434(2):99–107PubMedGoogle Scholar
  4. 4.
    Deng Z, Wang Z, Lieberman PM (2012) Telomeres and viruses: common themes of genome maintenance. Front Oncol 2:201. doi: 10.3389/fonc.2012.00201 PubMedCentralPubMedGoogle Scholar
  5. 5.
    Valach M, Farkas Z, Fricova D, Kovac J, Brejova B, Vinar T, Pfeiffer I, Kucsera J, Tomaska L, Lang BF, Nosek J (2011) Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res 39(10):4202–4219. doi: 10.1093/nar/gkq1345gkq1345 PubMedCentralPubMedGoogle Scholar
  6. 6.
    Volff JN, Altenbuchner J (2000) A new beginning with new ends: linearisation of circular chromosomes during bacterial evolution. FEMS Microbiol Lett 186(2):143–150. doi: S0378-1097(00)00118-X PubMedGoogle Scholar
  7. 7.
    McEachern MJ (2008) Telomeres: guardians of genomic integrity or double agents of evolution? In: Nosek J, Tomaska L (eds) Origin and evolution of telomeres. Land Bioscience, Austin, pp 100–113Google Scholar
  8. 8.
    Tomaska L, Nosek J (2009) Telomere heterogeneity: taking advantage of stochastic events. FEBS Lett 583(7):1067–1071. doi: 10.1016/j.febslet.2009.02.032S0014-5793(09)00147-1 PubMedCentralPubMedGoogle Scholar
  9. 9.
    Olovnikov AM (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 201(6):1496–1499PubMedGoogle Scholar
  10. 10.
    Watson JD (1972) Origin of concatemeric T7 DNA. Nat New Biol 239(94):197–201PubMedGoogle Scholar
  11. 11.
    Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408(6811):433–439. doi: 10.1038/35044005 PubMedGoogle Scholar
  12. 12.
    Lenhart JS, Schroeder JW, Walsh BW, Simmons LA (2012) DNA repair and genome maintenance in Bacillus subtilis. Microbiol Mol Biol Rev 76(3):530–564. doi: 10.1128/MMBR.05020-1176/3/530 PubMedCentralPubMedGoogle Scholar
  13. 13.
    Kwon T, Huq E, Herrin DL (2010) Microhomology-mediated and nonhomologous repair of a double-strand break in the chloroplast genome of Arabidopsis. Proc Natl Acad Sci USA 107(31):13954–13959. doi: 10.1073/pnas.10043261071004326107 PubMedGoogle Scholar
  14. 14.
    Suyama Y, Miura K (1968) Size and structural variations of mitochondrial DNA. Proc Natl Acad Sci USA 60(1):235–242PubMedGoogle Scholar
  15. 15.
    Barbour AG, Garon CF (1987) Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237(4813):409–411PubMedGoogle Scholar
  16. 16.
    Casjens S, Huang WM (2008) Prokaryotic telomeres: replication mechanisms and evolution. In: Nosek J, Tomaska L (eds) Origin and evolution of telomeres. Landes Bioscience, Austin, pp 154–162Google Scholar
  17. 17.
    McLeod MP, Warren RL, Hsiao WW, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103(42):15582–15587. doi: 10.1073/pnas.0607048103 PubMedGoogle Scholar
  18. 18.
    Redenbach M, Scheel J, Schmidt U (2000) Chromosome topology and genome size of selected actinomycetes species. Antonie Van Leeuwenhoek 78(3–4):227–235PubMedGoogle Scholar
  19. 19.
    Bendich AJ (1993) Reaching for the ring: the study of mitochondrial genome structure. Curr Genet 24(4):279–290PubMedGoogle Scholar
  20. 20.
    Nosek J, Tomaska L (2002) Mitochondrial telomeres: alternative solutions to the end-replication problem. In: Krupp G, Parwaresch R (eds) Telomeres, telomerases and cancer. Kluwer Academic/Plenum Publishers, New York, pp 396–417Google Scholar
  21. 21.
    Raimond R, Marcade I, Bouchon D, Rigaud T, Bossy JP, Souty-Grosset C (1999) Organization of the large mitochondrial genome in the isopod Armadillidium vulgare. Genetics 151(1):203–210PubMedGoogle Scholar
  22. 22.
    Morgan JA, Macbeth M, Broderick D, Whatmore P, Street R, Welch DJ, Ovenden JR (2013) Hybridisation, paternal leakage and mitochondrial DNA linearization in three anomalous fish (Scombridae). Mitochondrion. doi: 10.1016/j.mito.2013.06.002 PubMedGoogle Scholar
  23. 23.
    Smith DR, Kayal E, Yanagihara AA, Collins AG, Pirro S, Keeling PJ (2012) First complete mitochondrial genome sequence from a box jellyfish reveals a highly fragmented linear architecture and insights into telomere evolution. Genome Biol Evol 4(1):52–58. doi: 10.1093/gbe/evr127evr127 PubMedCentralPubMedGoogle Scholar
  24. 24.
    Voigt O, Erpenbeck D, Worheide G (2008) A fragmented metazoan organellar genome: the two mitochondrial chromosomes of Hydra magnipapillata. BMC Genomics 9:350. doi: 10.1186/1471-2164-9-350 PubMedCentralPubMedGoogle Scholar
  25. 25.
    Martin FN (1995) Linear mitochondrial genome organization in vivo in the genus Pythium. Curr Genet 28(3):225–234PubMedGoogle Scholar
  26. 26.
    Nosek J, Tomaska L, Fukuhara H, Suyama Y, Kovac L (1998) Linear mitochondrial genomes: 30 years down the line. Trends Genet 14(5):184–188PubMedGoogle Scholar
  27. 27.
    Baroudy BM, Venkatesan S, Moss B (1982) Incompletely base-paired flip-flop terminal loops link the two DNA strands of the vaccinia virus genome into one uninterrupted polynucleotide chain. Cell 28(2):315–324. doi: 0092-8674(82)90349-X PubMedGoogle Scholar
  28. 28.
    Baroudy BM, Venkatesan S, Moss B (1983) Structure and replication of vaccinia virus telomeres. Cold Spring Harb Symp Quant Biol 47(Pt 2):723–729PubMedGoogle Scholar
  29. 29.
    Beaud G (1995) Vaccinia virus DNA replication: a short review. Biochimie 77(10):774–779. doi: 0300-9084(96)88195-8 PubMedGoogle Scholar
  30. 30.
    Rybchin VN, Svarchevsky AN (1999) The plasmid prophage N15: a linear DNA with covalently closed ends. Mol Microbiol 33(5):895–903. doi: mmi1533 PubMedGoogle Scholar
  31. 31.
    Casjens SR, Gilcrease EB, Huang WM, Bunny KL, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW (2004) The pKO2 linear plasmid prophage of Klebsiella oxytoca. J Bacteriol 186(6):1818–1832PubMedCentralPubMedGoogle Scholar
  32. 32.
    Casjens S (1999) Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr Opin Microbiol 2(5):529–534. doi: S1369-5274(99)00012-0 PubMedGoogle Scholar
  33. 33.
    Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Goldman BS, Cao Y, Askenazi M, Halling C, Mullin L, Houmiel K, Gordon J, Vaudin M, Iartchouk O, Epp A, Liu F, Wollam C, Allinger M, Doughty D, Scott C, Lappas C, Markelz B, Flanagan C, Crowell C, Gurson J, Lomo C, Sear C, Strub G, Cielo C, Slater S (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294(5550):2323–2328. doi: 10.1126/science.1066803 PubMedGoogle Scholar
  34. 34.
    Chaconas G, Kobryn K (2010) Structure, function, and evolution of linear replicons in Borrelia. Annu Rev Microbiol 64:185–202. doi: 10.1146/annurev.micro.112408.134037 PubMedGoogle Scholar
  35. 35.
    Kobryn K, Briffotaux J, Karpov V (2009) Holliday junction formation by the Borrelia burgdorferi telomere resolvase, ResT: implications for the origin of genome linearity. Mol Microbiol 71(5):1117–1130. doi: 10.1111/j.1365-2958.2008.06584 PubMedGoogle Scholar
  36. 36.
    Huang WM, DaGloria J, Fox H, Ruan Q, Tillou J, Shi K, Aihara H, Aron J, Casjens S (2012) Linear chromosome-generating system of Agrobacterium tumefaciens C58: protelomerase generates and protects hairpin ends. J Biol Chem 287(30):25551–25563. doi: 10.1074/jbc.M112.369488 PubMedGoogle Scholar
  37. 37.
    Dinouel N, Drissi R, Miyakawa I, Sor F, Rousset S, Fukuhara H (1993) Linear mitochondrial DNAs of yeasts: closed-loop structure of the termini and possible linear-circular conversion mechanisms. Mol Cell Biol 13(4):2315–2323PubMedCentralPubMedGoogle Scholar
  38. 38.
    de Jong RN, van der Vliet PC (1999) Mechanism of DNA replication in eukaryotic cells: cellular host factors stimulating adenovirus DNA replication. Gene 236(1):1–12. doi: S0378-1119(99)00249-8 PubMedGoogle Scholar
  39. 39.
    Rekosh DM, Russell WC, Bellet AJ, Robinson AJ (1977) Identification of a protein linked to the ends of adenovirus DNA. Cell 11(2):283–295. doi: 0092-8674(77)90045-9 PubMedGoogle Scholar
  40. 40.
    Meijer WJ, Serna-Rico A, Salas M (2001) Characterization of the bacteriophage phi29-encoded protein p16.7: a membrane protein involved in phage DNA replication. Mol Microbiol 39(3):731–746. doi: mmi2260 PubMedGoogle Scholar
  41. 41.
    Grahn AM, Bamford JK, O’Neill MC, Bamford DH (1994) Functional organization of the bacteriophage PRD1 genome. J Bacteriol 176(10):3062–3068PubMedCentralPubMedGoogle Scholar
  42. 42.
    Chen CW, Huang CH, Lee HH, Tsai HH, Kirby R (2002) Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet 18(10):522–529. doi: S0168-9525(02)02752-X PubMedGoogle Scholar
  43. 43.
    Lin YR, Hahn MY, Roe JH, Huang TW, Tsai HH, Lin YF, Su TS, Chan YJ, Chen CW (2009) Streptomyces telomeres contain a promoter. J Bacteriol 191(3):773–781. doi: 10.1128/JB.01299-08JB.01299-08 PubMedCentralPubMedGoogle Scholar
  44. 44.
    Chen CW, Yu TW, Lin YS, Kieser HM, Hopwood DA (1993) The conjugative plasmid SLP2 of Streptomyces lividans is a 50 kb linear molecule. Mol Microbiol 7(6):925–932PubMedGoogle Scholar
  45. 45.
    Hirochika H, Sakaguchi K (1982) Analysis of linear plasmids isolated from Streptomyces: association of protein with the ends of the plasmid DNA. Plasmid 7(1):59–65. doi: 0147-619X(82)90027-0 PubMedGoogle Scholar
  46. 46.
    Kirby R, Chen CW (2011) Genome architecture. In: Dyson P (ed) Streptomyces: molecular biology and biotechnology. Caister Academic Press, Norfolk, pp 5–26Google Scholar
  47. 47.
    Fricova D, Valach M, Farkas Z, Pfeiffer I, Kucsera J, Tomaska L, Nosek J (2010) The mitochondrial genome of the pathogenic yeast Candida subhashii: GC-rich linear DNA with a protein covalently attached to the 5′ termini. Microbiology 156(Pt 7):2153–2163. doi: 10.1099/mic.0.038646-0mic.0.038646-0 PubMedGoogle Scholar
  48. 48.
    Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24(3):241–247PubMedGoogle Scholar
  49. 49.
    Nosek J, Dinouel N, Kovac L, Fukuhara H (1995) Linear mitochondrial DNAs from yeasts: telomeres with large tandem repetitions. Mol Gen Genet 247(1):61–72PubMedGoogle Scholar
  50. 50.
    Tomaska L, Nosek J, Fukuhara H (1997) Identification of a putative mitochondrial telomere-binding protein of the yeast Candida parapsilosis. J Biol Chem 272(5):3049–3056PubMedGoogle Scholar
  51. 51.
    Nosek J, Tomaska L, Pagacova B, Fukuhara H (1999) Mitochondrial telomere-binding protein from Candida parapsilosis suggests an evolutionary adaptation of a nonspecific single-stranded DNA-binding protein. J Biol Chem 274(13):8850–8857PubMedGoogle Scholar
  52. 52.
    Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T (1999) Mammalian telomeres end in a large duplex loop. Cell 97(4):503–514. doi: S0092-8674(00)80760-6 PubMedGoogle Scholar
  53. 53.
    Tomaska L, Makhov AM, Griffith JD, Nosek J (2002) T-loops in yeast mitochondria. Mitochondrion 1(5):455–459. doi: S1567-7249(02)00009-0 PubMedGoogle Scholar
  54. 54.
    de Lange T (2002) Protection of mammalian telomeres. Oncogene 21(4):532–540. doi: 10.1038/sj.onc.1205080 PubMedGoogle Scholar
  55. 55.
    Nosek J, Tomaska L (2008) Mitochondrial telomeres: an evolutionary paradigm for the emergence of telomeric structures and their replication strategies. In: Nosek J, Tomaska L (eds) Origin and evolution of telomeres. Landes Bioscience, Austin, pp 163–171Google Scholar
  56. 56.
    Burger G, Forget L, Zhu Y, Gray MW, Lang BF (2003) Unique mitochondrial genome architecture in unicellular relatives of animals. Proc Natl Acad Sci USA 100(3):892–897. doi: 10.1073/pnas.03361151000336115100 PubMedGoogle Scholar
  57. 57.
    Shukla GC, Nene V (1998) Telomeric features of Theileria parva mitochondrial DNA derived from cycle sequence data of total genomic DNA. Mol Biochem Parasitol 95(1):159–163. doi: S0166-6851(98)00098-X PubMedGoogle Scholar
  58. 58.
    Takano H, Kawano S, Kuroiwa T (1994) Genetic organization of a linear mitochondrial plasmid (mF) that promotes mitochondrial fusion in Physarum polycephalum. Curr Genet 26(5–6):506–511PubMedGoogle Scholar
  59. 59.
    Walther TC, Kennell JC (1999) Linear mitochondrial plasmids of F. oxysporum are novel, telomere-like retroelements. Mol Cell 4(2):229–238. doi: S1097-2765(00)80370-6 PubMedGoogle Scholar
  60. 60.
    Given D, Yee D, Griem K, Kieff E (1979) DNA of Epstein–Barr virus. V. Direct repeats of the ends of Epstein–Barr virus DNA. J Virol 30(3):852–862PubMedCentralPubMedGoogle Scholar
  61. 61.
    Zimmermann J, Hammerschmidt W (1995) Structure and role of the terminal repeats of Epstein–Barr virus in processing and packaging of virion DNA. J Virol 69(5):3147–3155PubMedCentralPubMedGoogle Scholar
  62. 62.
    Kintner CR, Sugden B (1979) The structure of the termini of the DNA of Epstein–Barr virus. Cell 17(3):661–671. doi: 0092-8674(79)90273-3 PubMedGoogle Scholar
  63. 63.
    Matsuo T, Heller M, Petti L, O’Shiro E, Kieff E (1984) Persistence of the entire Epstein–Barr virus genome integrated into human lymphocyte DNA. Science 226(4680):1322–1325PubMedGoogle Scholar
  64. 64.
    Gompels UA, Macaulay HA (1995) Characterization of human telomeric repeat sequences from human herpesvirus 6 and relationship to replication. J Gen Virol 76(Pt 2):451–458PubMedGoogle Scholar
  65. 65.
    Martin ME, Thomson BJ, Honess RW, Craxton MA, Gompels UA, Liu MY, Littler E, Arrand JR, Teo I, Jones MD (1991) The genome of human herpesvirus 6: maps of unit-length and concatemeric genomes for nine restriction endonucleases. J Gen Virol 72(Pt 1):157–168PubMedGoogle Scholar
  66. 66.
    Thomson BJ, Dewhurst S, Gray D (1994) Structure and heterogeneity of the a sequences of human herpesvirus 6 strain variants U1102 and Z29 and identification of human telomeric repeat sequences at the genomic termini. J Virol 68(5):3007–3014PubMedCentralPubMedGoogle Scholar
  67. 67.
    Bulboaca GH, Deng H, Dewhurst S, Calos MP (1998) Telomeric sequences from human herpesvirus 6 do not mediate nuclear retention of episomal DNA in human cells. Arch Virol 143(3):563–570PubMedGoogle Scholar
  68. 68.
    Arbuckle JH, Medveczky MM, Luka J, Hadley SH, Luegmayr A, Ablashi D, Lund TC, Tolar J, De Meirleir K, Montoya JG, Komaroff AL, Ambros PF, Medveczky PG (2010) The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. Proc Natl Acad Sci USA 107(12):5563–5568. doi: 10.1073/pnas.09135861070913586107 PubMedGoogle Scholar
  69. 69.
    Arbuckle JH, Medveczky PG (2011) The molecular biology of human herpesvirus-6 latency and telomere integration. Microbes Infect 13(8–9):731–741. doi: 10.1016/j.micinf.2011.03.006S1286-4579(11)00089-X PubMedCentralPubMedGoogle Scholar
  70. 70.
    Kaufer BB, Jarosinski KW, Osterrieder N (2011) Herpesvirus telomeric repeats facilitate genomic integration into host telomeres and mobilization of viral DNA during reactivation. J Exp Med 208(3):605–615. doi: 10.1084/jem.20101402jem.20101402 PubMedCentralPubMedGoogle Scholar
  71. 71.
    Blackburn EH, Gall JG (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120(1):33–53. doi: 0022-2836(78)90294-2 PubMedGoogle Scholar
  72. 72.
    Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu JR (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85(18):6622–6626PubMedGoogle Scholar
  73. 73.
    Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci USA 86(18):7049–7053PubMedGoogle Scholar
  74. 74.
    Gornung E, Gabrielli I, Sola L (1998) Localization of the (TTAGGG)n telomeric sequence in zebrafish chromosomes. Genome 41(1):136–138. doi: 10.1139/g97-098 Google Scholar
  75. 75.
    Cangiano G, La Volpe A (1993) Repetitive DNA sequences located in the terminal portion of the Caenorhabditis elegans chromosomes. Nucleic Acids Res 21(5):1133–1139PubMedCentralPubMedGoogle Scholar
  76. 76.
    McEachern MJ, Blackburn EH (1994) A conserved sequence motif within the exceptionally diverse telomeric sequences of budding yeasts. Proc Natl Acad Sci USA 91(8):3453–3457PubMedGoogle Scholar
  77. 77.
    Murray AW, Schultes NP, Szostak JW (1986) Chromosome length controls mitotic chromosome segregation in yeast. Cell 45(4):529–536. doi: 0092-8674(86)90284-9 PubMedGoogle Scholar
  78. 78.
    Shampay J, Szostak JW, Blackburn EH (1984) DNA sequences of telomeres maintained in yeast. Nature 310(5973):154–157PubMedGoogle Scholar
  79. 79.
    Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53(1):127–136. doi: 0092-8674(88)90494-1 PubMedGoogle Scholar
  80. 80.
    Petracek ME, Lefebvre PA, Silflow CD, Berman J (1990) Chlamydomonas telomere sequences are A+T-rich but contain three consecutive G–C base pairs. Proc Natl Acad Sci USA 87(21):8222–8226PubMedGoogle Scholar
  81. 81.
    Gatbonton T, Imbesi M, Nelson M, Akey JM, Ruderfer DM, Kruglyak L, Simon JA, Bedalov A (2006) Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet 2(3):e35. doi: 10.1371/journal.pgen.0020035 PubMedCentralPubMedGoogle Scholar
  82. 82.
    de Lange T (2010) How shelterin solves the telomere end-protection problem. Cold Spring Harb Symp Quant Biol 75:167–177. doi: 10.1101/sqb.2010.75.017 PubMedGoogle Scholar
  83. 83.
    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(5):633–638PubMedGoogle Scholar
  84. 84.
    Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43(2 Pt 1):405–413. doi: 0092-8674(85)90170-9 PubMedGoogle Scholar
  85. 85.
    Osterhage JL, Friedman KL (2009) Chromosome end maintenance by telomerase. J Biol Chem 284(24):16061–16065. doi: 10.1074/jbc.R900011200R900011200 PubMedGoogle Scholar
  86. 86.
    Nandakumar J, Cech TR (2013) Finding the end: recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol 14(2):69–82. doi: 10.1038/nrm3505nrm3505 PubMedCentralPubMedGoogle Scholar
  87. 87.
    Watson JM, Riha K (2010) Comparative biology of telomeres: where plants stand. FEBS Lett 584(17):3752–3759. doi: 10.1016/j.febslet.2010.06.017S0014-5793(10)00507-7 PubMedCentralPubMedGoogle Scholar
  88. 88.
    Cesare AJ, Quinney N, Willcox S, Subramanian D, Griffith JD (2003) Telomere looping in P. sativum (common garden pea). Plant J 36(2):271–279. doi: 1882 PubMedGoogle Scholar
  89. 89.
    Nikitina T, Woodcock CL (2004) Closed chromatin loops at the ends of chromosomes. J Cell Biol 166(2):161–165. doi: 10.1083/jcb.200403118jcb.200403118 PubMedGoogle Scholar
  90. 90.
    Vannier JB, Pavicic-Kaltenbrunner V, Petalcorin MI, Ding H, Boulton SJ (2012) RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149(4):795–806. doi: 10.1016/j.cell.2012.03.030S0092-8674(12)00418-7 PubMedGoogle Scholar
  91. 91.
    Chai W, Sfeir AJ, Hoshiyama H, Shay JW, Wright WE (2006) The involvement of the Mre11/Rad50/Nbs1 complex in the generation of G-overhangs at human telomeres. EMBO Rep 7(2):225–230. doi: 740060010.1038/sj.embor.7400600 PubMedCentralPubMedGoogle Scholar
  92. 92.
    Verdun RE, Crabbe L, Haggblom C, Karlseder J (2005) Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol Cell 20(4):551–561. doi: 10.1016/j.molcel.2005.09.024 PubMedGoogle Scholar
  93. 93.
    Zhu XD, Kuster B, Mann M, Petrini JH, de Lange T (2000) Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet 25(3):347–352. doi: 10.1038/77139 PubMedGoogle Scholar
  94. 94.
    Czornak K, Chughtai S, Chrzanowska KH (2008) Mystery of DNA repair: the role of the MRN complex and ATM kinase in DNA damage repair. J Appl Genet 49(4):383–396. doi: 10.1007/BF03195638473 PubMedGoogle Scholar
  95. 95.
    Larrivee M, LeBel C, Wellinger RJ (2004) The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev 18(12):1391–1396. doi: 10.1101/gad.119940418/12/1391 PubMedGoogle Scholar
  96. 96.
    Broccoli D, Smogorzewska A, Chong L, de Lange T (1997) Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet 17(2):231–235. doi: 10.1038/ng1097-231 PubMedGoogle Scholar
  97. 97.
    Bilaud T, Brun C, Ancelin K, Koering CE, Laroche T, Gilson E (1997) Telomeric localization of TRF2, a novel human telobox protein. Nat Genet 17(2):236–239. doi: 10.1038/ng1097-236 PubMedGoogle Scholar
  98. 98.
    Chong L, van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J, Tempst P, de Lange T (1995) A human telomeric protein. Science 270(5242):1663–1667PubMedGoogle Scholar
  99. 99.
    Loayza D, De Lange T (2003) POT1 as a terminal transducer of TRF1 telomere length control. Nature 423(6943):1013–1018. doi: 10.1038/nature01688 PubMedGoogle Scholar
  100. 100.
    Ye JZ, Donigian JR, van Overbeek M, Loayza D, Luo Y, Krutchinsky AN, Chait BT, de Lange T (2004) TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J Biol Chem 279(45):47264–47271. doi: 10.1074/jbc.M409047200 PubMedGoogle Scholar
  101. 101.
    Houghtaling BR, Cuttonaro L, Chang W, Smith S (2004) A dynamic molecular link between the telomere length regulator TRF1 and the chromosome end protector TRF2. Curr Biol 14(18):1621–1631. doi: 10.1016/j.cub.2004.08.052 PubMedGoogle Scholar
  102. 102.
    Liu D, Safari A, O’Connor MS, Chan DW, Laegeler A, Qin J, Songyang Z (2004) PTOP interacts with POT1 and regulates its localization to telomeres. Nat Cell Biol 6(7):673–680. doi: 10.1038/ncb1142ncb1142 PubMedGoogle Scholar
  103. 103.
    Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101(5):471–483. doi: S0092-8674(00)80858-2 PubMedGoogle Scholar
  104. 104.
    Stansel RM, de Lange T, Griffith JD (2001) T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang. EMBO J 20(19):5532–5540. doi: 10.1093/emboj/20.19.5532 PubMedGoogle Scholar
  105. 105.
    Wang RC, Smogorzewska A, de Lange T (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119(3):355–368. doi: 10.1016/j.cell.2004.10.011 PubMedGoogle Scholar
  106. 106.
    Fouche N, Cesare AJ, Willcox S, Ozgur S, Compton SA, Griffith JD (2006) The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J Biol Chem 281(49):37486–37495. doi: 10.1074/jbc.M608778200 PubMedGoogle Scholar
  107. 107.
    Bianchi A, Smith S, Chong L, Elias P, de Lange T (1997) TRF1 is a dimer and bends telomeric DNA. EMBO J 16(7):1785–1794. doi: 10.1093/emboj/16.7.1785 PubMedGoogle Scholar
  108. 108.
    Verdun RE, Karlseder J (2006) The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127(4):709–720. doi: 10.1016/j.cell.2006.09.034 PubMedGoogle Scholar
  109. 109.
    Lewis KA, Wuttke DS (2012) Telomerase and telomere-associated proteins: structural insights into mechanism and evolution. Structure 20(1):28–39. doi: 10.1016/j.str.2011.10.017 PubMedGoogle Scholar
  110. 110.
    Gottschling DE, Zakian VA (1986) Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell 47(2):195–205. doi: 0092-8674(86)90442-3 PubMedGoogle Scholar
  111. 111.
    Horvath MP, Schweiker VL, Bevilacqua JM, Ruggles JA, Schultz SC (1998) Crystal structure of the Oxytricha nova telomere end binding protein complexed with single-strand DNA. Cell 95(7):963–974PubMedGoogle Scholar
  112. 112.
    Baumann P, Cech TR (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292(5519):1171–1175. doi: 10.1126/science.1060036 PubMedGoogle Scholar
  113. 113.
    Churikov D, Price CM (2008) Pot1 and cell cycle progression cooperate in telomere length regulation. Nat Struct Mol Biol 15(1):79–84PubMedCentralPubMedGoogle Scholar
  114. 114.
    Hockemeyer D, Sfeir AJ, Shay JW, Wright WE, de Lange T (2005) POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J 24(14):2667–2678PubMedGoogle Scholar
  115. 115.
    Wu L, Multani AS, He H, Cosme-Blanco W, Deng Y, Deng JM, Bachilo O, Pathak S, Tahara H, Bailey SM, Behringer RR, Chang S (2006) Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell 126(1):49–62PubMedGoogle Scholar
  116. 116.
    Baumann P, Price C (2010) Pot1 and telomere maintenance. FEBS Lett 584(17):3779–3784. doi: 10.1016/j.febslet.2010.05.024 PubMedCentralPubMedGoogle Scholar
  117. 117.
    Gao H, Cervantes RB, Mandell EK, Otero JH, Lundblad V (2007) RPA-like proteins mediate yeast telomere function. Nat Struct Mol Biol 14(3):208–214PubMedGoogle Scholar
  118. 118.
    Giraud-Panis MJ, Teixeira MT, Geli V, Gilson E (2010) CST meets shelterin to keep telomeres in check. Mol Cell 39(5):665–676. doi: 10.1016/j.molcel.2010.08.024 PubMedGoogle Scholar
  119. 119.
    Maringele L, Lydall D (2002) EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Delta mutants. Genes Dev 16(15):1919–1933PubMedGoogle Scholar
  120. 120.
    Nugent CI, Hughes TR, Lue NF, Lundblad V (1996) Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274(5285):249–252PubMedGoogle Scholar
  121. 121.
    Miyake Y, Nakamura M, Nabetani A, Shimamura S, Tamura M, Yonehara S, Saito M, Ishikawa F (2009) RPA-like mammalian Ctc1-Stn1-Ten1 complex binds to single-stranded DNA and protects telomeres independently of the Pot1 pathway. Mol Cell 36(2):193–206PubMedGoogle Scholar
  122. 122.
    Song X, Leehy K, Warrington RT, Lamb JC, Surovtseva YV, Shippen DE (2008) STN1 protects chromosome ends in Arabidopsis thaliana. Proc Natl Acad Sci USA 105(50):19815–19820PubMedGoogle Scholar
  123. 123.
    Surovtseva YV, Churikov D, Boltz KA, Song X, Lamb JC, Warrington R, Leehy K, Heacock M, Price CM, Shippen DE (2009) Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol Cell 36(2):207–218PubMedCentralPubMedGoogle Scholar
  124. 124.
    Gu P, Min JN, Wang Y, Huang C, Peng T, Chai W, Chang S (2012) CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. EMBO J 31(10):2309–2321. doi: 10.1038/emboj.2012.96 PubMedGoogle Scholar
  125. 125.
    Huang C, Dai X, Chai W (2012) Human Stn1 protects telomere integrity by promoting efficient lagging-strand synthesis at telomeres and mediating C-strand fill-in. Cell Res 22(12):1681–1695. doi: 10.1038/cr.2012.132 PubMedGoogle Scholar
  126. 126.
    Wang F, Stewart JA, Kasbek C, Zhao Y, Wright WE, Price CM (2012) Human CST has independent functions during telomere duplex replication and C-strand fill-in. Cell Rep 2(5):1096–1103. doi: 10.1016/j.celrep.2012.10.007 PubMedCentralPubMedGoogle Scholar
  127. 127.
    Raices M, Verdun RE, Compton SA, Haggblom CI, Griffith JD, Dillin A, Karlseder J (2008) C. elegans telomeres contain G-strand and C-strand overhangs that are bound by distinct proteins. Cell 132(5):745–757. doi: 10.1016/j.cell.2007.12.039 PubMedGoogle Scholar
  128. 128.
    Lackner DH, Raices M, Maruyama H, Haggblom C, Karlseder J (2012) Organismal propagation in the absence of a functional telomerase pathway in Caenorhabditis elegans. EMBO J 31(8):2024–2033. doi: 10.1038/emboj.2012.61 PubMedGoogle Scholar
  129. 129.
    Oganesian L, Karlseder J (2011) Mammalian 5′ C-rich telomeric overhangs are a mark of recombination-dependent telomere maintenance. Mol Cell 42(2):224–236. doi: 10.1016/j.molcel.2011.03.015 PubMedCentralPubMedGoogle Scholar
  130. 130.
    Oganesian L, Karlseder J (2013) 5′ C-rich telomeric overhangs are an outcome of rapid telomere truncation events. DNA Repair (Amst) 12(3):238–245. doi: 10.1016/j.dnarep.2012.12.008 Google Scholar
  131. 131.
    McElligott R, Wellinger RJ (1997) The terminal DNA structure of mammalian chromosomes. EMBO J 16(12):3705–3714. doi: 10.1093/emboj/16.12.3705 PubMedGoogle Scholar
  132. 132.
    Makarov VL, Hirose Y, Langmore JP (1997) Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88(5):657–666. doi: S0092-8674(00)81908-X PubMedGoogle Scholar
  133. 133.
    Lenain C, Bauwens S, Amiard S, Brunori M, Giraud-Panis MJ, Gilson E (2006) The Apollo 5′ exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr Biol 16(13):1303–1310. doi: 10.1016/j.cub.2006.05.021 PubMedGoogle Scholar
  134. 134.
    Wu P, van Overbeek M, Rooney S, de Lange T (2010) Apollo contributes to G overhang maintenance and protects leading-end telomeres. Mol Cell 39(4):606–617. doi: 10.1016/j.molcel.2010.06.031 PubMedCentralPubMedGoogle Scholar
  135. 135.
    Wu P, Takai H, de Lange T (2012) Telomeric 3′ overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell 150(1):39–52. doi: 10.1016/j.cell.2012.05.026 PubMedCentralPubMedGoogle Scholar
  136. 136.
    Riha K, McKnight TD, Fajkus J, Vyskot B, Shippen DE (2000) Analysis of the G-overhang structures on plant telomeres: evidence for two distinct telomere architectures. Plant J 23(5):633–641. doi: tpj831 PubMedGoogle Scholar
  137. 137.
    Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K (2012) Chromosome end protection by blunt-ended telomeres. Genes Dev 26(15):1703–1713. doi: 10.1101/gad.194944.112 PubMedGoogle Scholar
  138. 138.
    Muller HJ (1938) The remaking of chromosomes. Collecting Net 8:182–198Google Scholar
  139. 139.
    Abad JP, De Pablos B, Osoegawa K, De Jong PJ, Martin-Gallardo A, Villasante A (2004) TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol Biol Evol 21(9):1620–1624. doi: 10.1093/molbev/msh180 PubMedGoogle Scholar
  140. 140.
    Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75(6):1083–1093. doi: 0092-8674(93)90318-K PubMedGoogle Scholar
  141. 141.
    Rubin GM (1978) Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 42(Pt 2):1041–1046PubMedGoogle Scholar
  142. 142.
    Young BS, Pession A, Traverse KL, French C, Pardue ML (1983) Telomere regions in Drosophila share complex DNA sequences with pericentric heterochromatin. Cell 34(1):85–94. doi: 0092-8674(83)90138-1 PubMedGoogle Scholar
  143. 143.
    Rashkova S, Athanasiadis A, Pardue ML (2003) Intracellular targeting of gag proteins of the Drosophila telomeric retrotransposons. J Virol 77(11):6376–6384PubMedCentralPubMedGoogle Scholar
  144. 144.
    Rashkova S, Karam SE, Kellum R, Pardue ML (2002) Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends. J Cell Biol 159(3):397–402. doi: 10.1083/jcb.200205039jcb.200205039 PubMedGoogle Scholar
  145. 145.
    Rashkova S, Karam SE, Pardue ML (2002) Element-specific localization of Drosophila retrotransposon gag proteins occurs in both nucleus and cytoplasm. Proc Natl Acad Sci USA 99(6):3621–3626. doi: 10.1073/pnas.032071999 PubMedGoogle Scholar
  146. 146.
    Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267(10):3025–3031. doi: ejb1323 PubMedGoogle Scholar
  147. 147.
    Biessmann H, Mason JM, Ferry K, d’Hulst M, Valgeirsdottir K, Traverse KL, Pardue ML (1990) Addition of telomere-associated HeT DNA sequences “heals” broken chromosome ends in Drosophila. Cell 61(4):663–673. doi: 0092-8674(90)90478-W PubMedGoogle Scholar
  148. 148.
    Sheen FM, Levis RW (1994) Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc Natl Acad Sci USA 91(26):12510–12514PubMedGoogle Scholar
  149. 149.
    Nakamura TM, Cech TR (1998) Reversing time: origin of telomerase. Cell 92(5):587–590. doi: S0092-8674(00)80950-2 PubMedGoogle Scholar
  150. 150.
    Danilevskaya ON, Arkhipova IR, Traverse KL, Pardue ML (1997) Promoting in tandem: the promoter for telomere transposon HeT-A and implications for the evolution of retroviral LTRs. Cell 88(5):647–655. doi: S0092-8674(00)81907-8 PubMedGoogle Scholar
  151. 151.
    Danilevskaya ON, Traverse KL, Hogan NC, DeBaryshe PG, Pardue ML (1999) The two Drosophila telomeric transposable elements have very different patterns of transcription. Mol Cell Biol 19(1):873–881PubMedCentralPubMedGoogle Scholar
  152. 152.
    Capkova Frydrychova R, Biessmann H, Mason JM (2008) Regulation of telomere length in Drosophila. Cytogenet Genome Res 122(3–4):356–364. doi: 10.1159/000167823 PubMedGoogle Scholar
  153. 153.
    Pardue ML, Danilevskaya ON, Lowenhaupt K, Slot F, Traverse KL (1996) Drosophila telomeres: new views on chromosome evolution. Trends Genet 12(2):48–52. doi: 0168-9525(96)81399-0 PubMedGoogle Scholar
  154. 154.
    Levis RW (1989) Viable deletions of a telomere from a Drosophila chromosome. Cell 58(4):791–801. doi: 0092-8674(89)90112-8 PubMedGoogle Scholar
  155. 155.
    Mason JM, Strobel E, Green MM (1984) μ-2: mutator gene in Drosophila that potentiates the induction of terminal deficiencies. Proc Natl Acad Sci USA 81(19):6090–6094PubMedGoogle Scholar
  156. 156.
    Biessmann H, Carter SB, Mason JM (1990) Chromosome ends in Drosophila without telomeric DNA sequences. Proc Natl Acad Sci USA 87(5):1758–1761PubMedGoogle Scholar
  157. 157.
    Biessmann H, Mason JM (1988) Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J 7(4):1081–1086PubMedGoogle Scholar
  158. 158.
    Kern AD, Begun DJ (2008) Recurrent deletion and gene presence/absence polymorphism: telomere dynamics dominate evolution at the tip of 3L in Drosophila melanogaster and D. simulans. Genetics 179(2):1021–1027. doi: 10.1534/genetics.107.078345 PubMedGoogle Scholar
  159. 159.
    Raffa GD, Ciapponi L, Cenci G, Gatti M (2011) Terminin: a protein complex that mediates epigenetic maintenance of Drosophila telomeres. Nucleus 2(5):383–391. doi: 10.4161/nucl.2.5.17873 PubMedGoogle Scholar
  160. 160.
    Cenci G, Siriaco G, Raffa GD, Kellum R, Gatti M (2003) The Drosophila HOAP protein is required for telomere capping. Nat Cell Biol 5(1):82–84. doi: 10.1038/ncb902ncb902 PubMedGoogle Scholar
  161. 161.
    Fanti L, Giovinazzo G, Berloco M, Pimpinelli S (1998) The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 2(5):527–538. doi: S1097-2765(00)80152-5 PubMedGoogle Scholar
  162. 162.
    Gao G, Walser JC, Beaucher ML, Morciano P, Wesolowska N, Chen J, Rong YS (2010) HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. EMBO J 29(4):819–829. doi: 10.1038/emboj.2009.394 PubMedGoogle Scholar
  163. 163.
    Raffa GD, Raimondo D, Sorino C, Cugusi S, Cenci G, Cacchione S, Gatti M, Ciapponi L (2010) Verrocchio, a Drosophila OB fold-containing protein, is a component of the terminin telomere-capping complex. Genes Dev 24(15):1596–1601. doi: 10.1101/gad.57481024/15/1596 PubMedGoogle Scholar
  164. 164.
    Raffa GD, Siriaco G, Cugusi S, Ciapponi L, Cenci G, Wojcik E, Gatti M (2009) The Drosophila Modigliani (moi) gene encodes a HOAP-interacting protein required for telomere protection. Proc Natl Acad Sci USA 106(7):2271–2276. doi: 10.1073/pnas.08127021060 PubMedGoogle Scholar
  165. 165.
    Shareef MM, King C, Damaj M, Badagu R, Huang DW, Kellum R (2001) Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol Biol Cell 12(6):1671–1685PubMedCentralPubMedGoogle Scholar
  166. 166.
    Komonyi O, Schauer T, Papai G, Deak P, Boros IM (2009) A product of the bicistronic Drosophila melanogaster gene CG31241, which also encodes a trimethylguanosine synthase, plays a role in telomere protection. J Cell Sci 122(Pt 6):769–774. doi: 10.1242/jcs.035097jcs.035097 PubMedGoogle Scholar
  167. 167.
    Titen SW, Golic KG (2010) Healing of euchromatic chromosome breaks by efficient de novo telomere addition in Drosophila melanogaster. Genetics 184(1):309–312. doi: 10.1534/genetics.109.109934 PubMedGoogle Scholar
  168. 168.
    Cenci G, Rawson RB, Belloni G, Castrillon DH, Tudor M, Petrucci R, Goldberg ML, Wasserman SA, Gatti M (1997) UbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior. Genes Dev 11(7):863–875PubMedGoogle Scholar
  169. 169.
    Raffa GD, Cenci G, Siriaco G, Goldberg ML, Gatti M (2005) The putative Drosophila transcription factor woc is required to prevent telomeric fusions. Mol Cell 20(6):821–831. doi: 10.1016/j.molcel.2005.12.003 PubMedGoogle Scholar
  170. 170.
    Bi X, Srikanta D, Fanti L, Pimpinelli S, Badugu R, Kellum R, Rong YS (2005) Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc Natl Acad Sci USA 102(42):15167–15172. doi: 10.1073/pnas.0504981102 PubMedGoogle Scholar
  171. 171.
    Bi X, Wei SC, Rong YS (2004) Telomere protection without a telomerase; the role of ATM and Mre11 in Drosophila telomere maintenance. Curr Biol 14(15):1348–1353. doi: 10.1016/j.cub.2004.06.063 PubMedGoogle Scholar
  172. 172.
    Ciapponi L, Cenci G, Ducau J, Flores C, Johnson-Schlitz D, Gorski MM, Engels WR, Gatti M (2004) The Drosophila Mre11/Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Curr Biol 14(15):1360–1366. doi: 10.1016/j.cub.2004.07.019 PubMedGoogle Scholar
  173. 173.
    Ciapponi L, Cenci G, Gatti M (2006) The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173(3):1447–1454. doi: 10.1534/genetics.106.058081 PubMedGoogle Scholar
  174. 174.
    Oikemus SR, McGinnis N, Queiroz-Machado J, Tukachinsky H, Takada S, Sunkel CE, Brodsky MH (2004) Drosophila atm/telomere fusion is required for telomeric localization of HP1 and telomere position effect. Genes Dev 18(15):1850–1861. doi: 10.1101/gad.12025041202504 PubMedGoogle Scholar
  175. 175.
    Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fujiwara H (1993) Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol Cell Biol 13(3):1424–1432PubMedCentralPubMedGoogle Scholar
  176. 176.
    Okazaki S, Ishikawa H, Fujiwara H (1995) Structural analysis of TRAS1, a novel family of telomeric repeat-associated retrotransposons in the silkworm Bombyx mori. Mol Cell Biol 15(8):4545–4552PubMedCentralPubMedGoogle Scholar
  177. 177.
    Takahashi H, Okazaki S, Fujiwara H (1997) A new family of site-specific retrotransposons, SART1, is inserted into telomeric repeats of the silkworm Bombyx mori. Nucleic Acids Res 25(8):1578–1584. doi: gka277 PubMedCentralPubMedGoogle Scholar
  178. 178.
    Anzai T, Takahashi H, Fujiwara H (2001) Sequence-specific recognition and cleavage of telomeric repeat (TTAGG)(n) by endonuclease of non-long terminal repeat retrotransposon TRAS1. Mol Cell Biol 21(1):100–108. doi: 10.1128/MCB.21.1.100-108.2001 PubMedCentralPubMedGoogle Scholar
  179. 179.
    Osanai M, Kojima KK, Futahashi R, Yaguchi S, Fujiwara H (2006) Identification and characterization of the telomerase reverse transcriptase of Bombyx mori (silkworm) and Tribolium castaneum (flour beetle). Gene 376(2):281–289. doi: S0378-1119(06)00281-210.1016/j.gene.2006.04.022 PubMedGoogle Scholar
  180. 180.
    Fujiwara H, Osanai M, Matsumoto T, Kojima KK (2005) Telomere-specific non-LTR retrotransposons and telomere maintenance in the silkworm Bombyx mori. Chromosome Res 13(5):455–467. doi: 10.1007/s10577-005-0990-9 PubMedGoogle Scholar
  181. 181.
    Cohn M, Edstrom JE (1992) Telomere-associated repeats in Chironomus form discrete subfamilies generated by gene conversion. J Mol Evol 35(2):114–122PubMedGoogle Scholar
  182. 182.
    Biessmann H, Donath J, Walter MF (1996) Molecular characterization of the Anopheles gambiae 2L telomeric region via an integrated transgene. Insect Mol Biol 5(1):11–20PubMedGoogle Scholar
  183. 183.
    Roth CW, Kobeski F, Walter MF, Biessmann H (1997) Chromosome end elongation by recombination in the mosquito Anopheles gambiae. Mol Cell Biol 17(9):5176–5183PubMedCentralPubMedGoogle Scholar
  184. 184.
    Walter MF, Bozorgnia L, Maheshwari A, Biessmann H (2001) The rate of terminal nucleotide loss from a telomere of the mosquito Anopheles gambiae. Insect Mol Biol 10(1):105–110. doi: imb245 PubMedGoogle Scholar
  185. 185.
    Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4(3):207–213PubMedGoogle Scholar
  186. 186.
    Fulneckova J, Hasikova T, Fajkus J, Lukesova A, Elias M, Sykorova E (2012) Dynamic evolution of telomeric sequences in the green algal order Chlamydomonadales. Genome Biol Evol 4(3):248–264. doi: 10.1093/gbe/evs007evs007 PubMedCentralPubMedGoogle Scholar
  187. 187.
    Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003) The absence of Arabidopsis-type telomeres in cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34(3):283–291. doi: 1731 PubMedGoogle Scholar
  188. 188.
    Peska V, Sykorova E, Fajkus J (2008) Two faces of Solanaceae telomeres: a comparison between Nicotiana and Cestrum telomeres and telomere-binding proteins. Cytogenet Genome Res 122(3–4):380–387. doi: 10.1159/000167826000167826 PubMedGoogle Scholar
  189. 189.
    Fukuhara H, Sor F, Drissi R, Dinouel N, Miyakawa I, Rousset S, Viola AM (1993) Linear mitochondrial DNAs of yeasts: frequency of occurrence and general features. Mol Cell Biol 13(4):2309–2314PubMedCentralPubMedGoogle Scholar
  190. 190.
    Kosa P, Valach M, Tomaska L, Wolfe KH, Nosek J (2006) Complete DNA sequences of the mitochondrial genomes of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis: insight into the evolution of linear DNA genomes from mitochondrial telomere mutants. Nucleic Acids Res 34(8):2472–2481. doi: 34/8/247210.1093/nar/gkl327 PubMedCentralPubMedGoogle Scholar
  191. 191.
    Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida NF Jr, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Bovee D Sr, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li MJ, McClelland E, Palmieri A, Raymond C, Rouse G, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao ZY, Dolan M, Chumley F, Tingey SV, Tomb JF, Gordon MP, Olson MV, Nester EW (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294(5550):2317–2323. doi: 10.1126/science.1066804 PubMedGoogle Scholar
  192. 192.
    Nosek J, Tomaska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44(2):73–84. doi: 10.1007/s00294-003-0426-z PubMedGoogle Scholar
  193. 193.
    Schardl CL, Lonsdale DM, Pring DR, Rose KR (1984) Linearization of maize mitochondrial chromosomes by recombination with linear episomes. Nature 310:292–296. doi: 10.1038/310292a0 Google Scholar
  194. 194.
    Swart EC, Nowacki M, Shum J, Stiles H, Higgins BP, Doak TG, Schotanus K, Magrini VJ, Minx P, Mardis ER, Landweber LF (2012) The Oxytricha trifallax mitochondrial genome. Genome Biol Evol 4(2):136–154. doi: 10.1093/gbe/evr136evr136 PubMedCentralPubMedGoogle Scholar
  195. 195.
    Takano H, Kawano S, Kuroiwa T (1992) Constitutive homologous recombination between mitochondrial DNA and a linear mitochondrial plasmid in Physarum polycephalum. Curr Genet 22(3):221–227PubMedGoogle Scholar
  196. 196.
    Kempken F (1995) Horizontal transfer of a mitochondrial plasmid. Mol Gen Genet 248(1):89–94PubMedGoogle Scholar
  197. 197.
    Handa H (2008) Linear plasmids in plant mitochondria: peaceful coexistences or malicious invasions? Mitochondrion 8(1):15–25PubMedGoogle Scholar
  198. 198.
    Delaroque N, Boland W, Muller DG, Knippers R (2003) Comparisons of two large phaeoviral genomes and evolutionary implications. J Mol Evol 57(6):613–622. doi: 10.1007/s00239-003-2501-y PubMedGoogle Scholar
  199. 199.
    Delaroque N, Muller DG, Bothe G, Pohl T, Knippers R, Boland W (2001) The complete DNA sequence of the Ectocarpus siliculosus Virus EsV-1 genome. Virology 287(1):112–132. doi: 10.1006/viro.2001.1028 PubMedGoogle Scholar
  200. 200.
    Wilson WH, Schroeder DC, Allen MJ, Holden MT, Parkhill J, Barrell BG, Churcher C, Hamlin N, Mungall K, Norbertczak H, Quail MA, Price C, Rabbinowitsch E, Walker D, Craigon M, Roy D, Ghazal P (2005) Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309(5737):1090–1092. doi: 10.1126/science.1113109 PubMedGoogle Scholar
  201. 201.
    Kirby R (2011) Chromosome diversity and similarity within the Actinomycetales. FEMS Microbiol Lett 319(1):1–10. doi: 10.1111/j.1574-6968.2011.02242.x PubMedGoogle Scholar
  202. 202.
    Chen CW (2007) Streptomyces linear plasmids: replication and telomeres. In: Meinhardt F, Klassen R (eds) Microbial linear plasmids. Springer, Berlin Heidelberg New York, pp 33–61Google Scholar
  203. 203.
    de Lange T (2004) T-loops and the origin of telomeres. Nat Rev Mol Cell Biol 5(4):323–329. doi: 10.1038/nrm1359nrm1359 PubMedGoogle Scholar
  204. 204.
    Nosek J, Kosa P, Tomaska L (2006) On the origin of telomeres: a glimpse at the pre-telomerase world. BioEssays 28(2):182–190. doi: 10.1002/bies.20355 PubMedGoogle Scholar
  205. 205.
    Malik HS, Burke WD, Eickbush TH (2000) Putative telomerase catalytic subunits from Giardia lamblia and Caenorhabditis elegans. Gene 251(2):101–108. doi: S0378-1119(00)00207-9 PubMedGoogle Scholar
  206. 206.
    Fajkus J, Sykorova E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13(5):469–479. doi: 10.1007/s10577-005-0997-2 PubMedGoogle Scholar
  207. 207.
    Jain D, Hebden AK, Nakamura TM, Miller KM, Cooper JP (2010) HAATI survivors replace canonical telomeres with blocks of generic heterochromatin. Nature 467(7312):223–227. doi: 10.1038/nature09374 PubMedGoogle Scholar
  208. 208.
    Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73(2):347–360. doi: 0092-8674(93)90234-H PubMedGoogle Scholar
  209. 209.
    Teng SC, Chang J, McCowan B, Zakian VA (2000) Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent Rif-inhibited recombinational process. Mol Cell 6(4):947–952. doi: S1097-2765(05)00094-8 PubMedGoogle Scholar
  210. 210.
    Teng SC, Zakian VA (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19(12):8083–8093PubMedCentralPubMedGoogle Scholar
  211. 211.
    Yamada M, Hayatsu N, Matsuura A, Ishikawa F (1998) Y’-Help1, a DNA helicase encoded by the yeast subtelomeric Y’ element, is induced in survivors defective for telomerase. J Biol Chem 273(50):33360–33366PubMedGoogle Scholar
  212. 212.
    Maxwell PH, Coombes C, Kenny AE, Lawler JF, Boeke JD, Curcio MJ (2004) Ty1 mobilizes subtelomeric Y’ elements in telomerase-negative Saccharomyces cerevisiae survivors. Mol Cell Biol 24(22):9887–9898. doi: 24/22/988710.1128/MCB.24.22.9887-9898.2004 PubMedCentralPubMedGoogle Scholar
  213. 213.
    Scholes DT, Kenny AE, Gamache ER, Mou Z, Curcio MJ (2003) Activation of a LTR-retrotransposon by telomere erosion. Proc Natl Acad Sci USA 100(26):15736–15741. doi: 10.1073/pnas.2136609100 PubMedGoogle Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Nick Fulcher
    • 1
  • Elisa Derboven
    • 1
  • Sona Valuchova
    • 1
  • Karel Riha
    • 1
    • 2
    Email author
  1. 1.Gregor Mendel InstituteAustrian Academy of SciencesViennaAustria
  2. 2.Central European Institute of TechnologyBrnoCzech Republic

Personalised recommendations