Abstract
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.
Similar content being viewed by others
References
Egel R (2012) Primal eukaryogenesis: on the communal nature of precellular states, ancestral to modern life. Life 2:170–212
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
Ishikawa F, Naito T (1999) Why do we have linear chromosomes? A matter of Adam and Eve. Mutat Res 434(2):99–107
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
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
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:https://doi.org/10.1111/j.1574-6968.2000.tb09095.x
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 100–113
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
Olovnikov AM (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 201(6):1496–1499
Watson JD (1972) Origin of concatemeric T7 DNA. Nat New Biol 239(94):197–201
Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408(6811):433–439. doi:10.1038/35044005
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
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
Suyama Y, Miura K (1968) Size and structural variations of mitochondrial DNA. Proc Natl Acad Sci USA 60(1):235–242
Barbour AG, Garon CF (1987) Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237(4813):409–411
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 154–162
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
Redenbach M, Scheel J, Schmidt U (2000) Chromosome topology and genome size of selected actinomycetes species. Antonie Van Leeuwenhoek 78(3–4):227–235
Bendich AJ (1993) Reaching for the ring: the study of mitochondrial genome structure. Curr Genet 24(4):279–290
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 396–417
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):203–210
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
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
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
Martin FN (1995) Linear mitochondrial genome organization in vivo in the genus Pythium. Curr Genet 28(3):225–234
Nosek J, Tomaska L, Fukuhara H, Suyama Y, Kovac L (1998) Linear mitochondrial genomes: 30 years down the line. Trends Genet 14(5):184–188
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:https://doi.org/10.1016/0092-8674(82)90349-x
Baroudy BM, Venkatesan S, Moss B (1983) Structure and replication of vaccinia virus telomeres. Cold Spring Harb Symp Quant Biol 47(Pt 2):723–729
Beaud G (1995) Vaccinia virus DNA replication: a short review. Biochimie 77(10):774–779. doi:https://doi.org/10.1016/0300-9084(96)88195-8
Rybchin VN, Svarchevsky AN (1999) The plasmid prophage N15: a linear DNA with covalently closed ends. Mol Microbiol 33(5):895–903. doi:https://doi.org/10.1046/j.1365-2958.1999.01533.x
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):1818–1832
Casjens S (1999) Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr Opin Microbiol 2(5):529–534. doi:https://doi.org/10.1016/s1369-5274(99)00012-0
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
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
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
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
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):2315–2323
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:https://doi.org/10.1016/s0378-1119(99)00249-8
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:https://doi.org/10.1016/0092-8674(77)90045-9
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:https://doi.org/10.1046/j.1365-2958.2001.02260.x
Grahn AM, Bamford JK, O’Neill MC, Bamford DH (1994) Functional organization of the bacteriophage PRD1 genome. J Bacteriol 176(10):3062–3068
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:https://doi.org/10.1016/s0168-9525(02)02752-x
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
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):925–932
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:https://doi.org/10.1016/0147-619x(82)90027-0
Kirby R, Chen CW (2011) Genome architecture. In: Dyson P (ed) Streptomyces: molecular biology and biotechnology. Caister Academic Press, Norfolk, pp 5–26
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
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):241–247
Nosek J, Dinouel N, Kovac L, Fukuhara H (1995) Linear mitochondrial DNAs from yeasts: telomeres with large tandem repetitions. Mol Gen Genet 247(1):61–72
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):3049–3056
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):8850–8857
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:https://doi.org/10.1016/s0092-8674(00)80760-6
Tomaska L, Makhov AM, Griffith JD, Nosek J (2002) T-loops in yeast mitochondria. Mitochondrion 1(5):455–459. doi:https://doi.org/10.1016/s1567-7249(02)00009-0
de Lange T (2002) Protection of mammalian telomeres. Oncogene 21(4):532–540. doi:10.1038/sj.onc.1205080
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 163–171
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
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:https://doi.org/10.1016/s0166-6851(98)00098-x
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):506–511
Walther TC, Kennell JC (1999) Linear mitochondrial plasmids of F. oxysporum are novel, telomere-like retroelements. Mol Cell 4(2):229–238. doi:https://doi.org/10.1016/s1097-2765(00)80370-6
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):852–862
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):3147–3155
Kintner CR, Sugden B (1979) The structure of the termini of the DNA of Epstein–Barr virus. Cell 17(3):661–671. doi:https://doi.org/10.1016/0092-8674(79)90273-3
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):1322–1325
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):451–458
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):157–168
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):3007–3014
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):563–570
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
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
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
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:https://doi.org/10.1016/0022-2836(78)90294-2
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):6622–6626
Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci USA 86(18):7049–7053
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
Cangiano G, La Volpe A (1993) Repetitive DNA sequences located in the terminal portion of the Caenorhabditis elegans chromosomes. Nucleic Acids Res 21(5):1133–1139
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):3453–3457
Murray AW, Schultes NP, Szostak JW (1986) Chromosome length controls mitotic chromosome segregation in yeast. Cell 45(4):529–536. doi:https://doi.org/10.1016/0092-8674(86)90284-9
Shampay J, Szostak JW, Blackburn EH (1984) DNA sequences of telomeres maintained in yeast. Nature 310(5973):154–157
Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53(1):127–136. doi:https://doi.org/10.1016/0092-8674(88)90494-1
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):8222–8226
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
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
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):633–638
Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43(2 Pt 1):405–413. doi:https://doi.org/10.1016/0092-8674(85)90170-9
Osterhage JL, Friedman KL (2009) Chromosome end maintenance by telomerase. J Biol Chem 284(24):16061–16065. doi:10.1074/jbc.R900011200R900011200
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
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
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:https://doi.org/10.1046/j.1365-313X.2003.01882.x
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
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
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:https://doi.org/10.1038/sj.embor.7400600
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
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
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
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
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
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
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):1663–1667
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
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
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
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
Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101(5):471–483. doi:https://doi.org/10.1016/s0092-8674(00)80858-2
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
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
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
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
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
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
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:https://doi.org/10.1016/0092-8674(86)90442-3
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):963–974
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
Churikov D, Price CM (2008) Pot1 and cell cycle progression cooperate in telomere length regulation. Nat Struct Mol Biol 15(1):79–84
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):2667–2678
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):49–62
Baumann P, Price C (2010) Pot1 and telomere maintenance. FEBS Lett 584(17):3779–3784. doi:10.1016/j.febslet.2010.05.024
Gao H, Cervantes RB, Mandell EK, Otero JH, Lundblad V (2007) RPA-like proteins mediate yeast telomere function. Nat Struct Mol Biol 14(3):208–214
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
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):1919–1933
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):249–252
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):193–206
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):19815–19820
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):207–218
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
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
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
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
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
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
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
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
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:https://doi.org/10.1016/s0092-8674(00)81908-x
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
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
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
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:https://doi.org/10.1046/j.1365-313x.2000.00831.x
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
Muller HJ (1938) The remaking of chromosomes. Collecting Net 8:182–198
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
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:https://doi.org/10.1016/0092-8674(93)90318-k
Rubin GM (1978) Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 42(Pt 2):1041–1046
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:https://doi.org/10.1016/0092-8674(83)90138-1
Rashkova S, Athanasiadis A, Pardue ML (2003) Intracellular targeting of gag proteins of the Drosophila telomeric retrotransposons. J Virol 77(11):6376–6384
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
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
Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267(10):3025–3031. doi:https://doi.org/10.1046/j.1432-1033.2000.01323.x
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:https://doi.org/10.1016/0092-8674(90)90478-w
Sheen FM, Levis RW (1994) Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc Natl Acad Sci USA 91(26):12510–12514
Nakamura TM, Cech TR (1998) Reversing time: origin of telomerase. Cell 92(5):587–590. doi:https://doi.org/10.1016/s0092-8674(00)81123-x
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:https://doi.org/10.1016/s0092-8674(00)81907-8
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):873–881
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
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:https://doi.org/10.1016/0168-9525(96)81399-0
Levis RW (1989) Viable deletions of a telomere from a Drosophila chromosome. Cell 58(4):791–801. doi:https://doi.org/10.1016/0092-8674(89)90112-8
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):6090–6094
Biessmann H, Carter SB, Mason JM (1990) Chromosome ends in Drosophila without telomeric DNA sequences. Proc Natl Acad Sci USA 87(5):1758–1761
Biessmann H, Mason JM (1988) Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J 7(4):1081–1086
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
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
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
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:https://doi.org/10.1016/s1097-2765(00)80152-5
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
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
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
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):1671–1685
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
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
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):863–875
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
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
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
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
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
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
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):1424–1432
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):4545–4552
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:https://doi.org/10.1093/nar/25.8.1578
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
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:https://doi.org/10.1016/j.gene.2006.04.022
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
Cohn M, Edstrom JE (1992) Telomere-associated repeats in Chironomus form discrete subfamilies generated by gene conversion. J Mol Evol 35(2):114–122
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):11–20
Roth CW, Kobeski F, Walter MF, Biessmann H (1997) Chromosome end elongation by recombination in the mosquito Anopheles gambiae. Mol Cell Biol 17(9):5176–5183
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:https://doi.org/10.1046/j.1365-2583.2001.00245.x
Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4(3):207–213
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
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:https://doi.org/10.1046/j.1365-313X.2003.01731.x
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
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):2309–2314
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:https://doi.org/10.1093/nar/gkl327
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
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
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
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
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):221–227
Kempken F (1995) Horizontal transfer of a mitochondrial plasmid. Mol Gen Genet 248(1):89–94
Handa H (2008) Linear plasmids in plant mitochondria: peaceful coexistences or malicious invasions? Mitochondrion 8(1):15–25
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
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
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
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
Chen CW (2007) Streptomyces linear plasmids: replication and telomeres. In: Meinhardt F, Klassen R (eds) Microbial linear plasmids. Springer, Berlin Heidelberg New York, pp 33–61
de Lange T (2004) T-loops and the origin of telomeres. Nat Rev Mol Cell Biol 5(4):323–329. doi:10.1038/nrm1359nrm1359
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
Malik HS, Burke WD, Eickbush TH (2000) Putative telomerase catalytic subunits from Giardia lamblia and Caenorhabditis elegans. Gene 251(2):101–108. doi:https://doi.org/10.1016/s0378-1119(00)00207-9
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
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
Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73(2):347–360. doi:https://doi.org/10.1016/0092-8674(93)90234-h
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:https://doi.org/10.1016/s1097-2765(05)00094-8
Teng SC, Zakian VA (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19(12):8083–8093
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):33360–33366
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:https://doi.org/10.1128/MCB.24.22.9887-9898.2004
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
Acknowledgments
Our research on telomeres is supported by the Austrian Science Fund (FWF, Y418-B03) and Austrian Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fulcher, N., Derboven, E., Valuchova, S. et al. If the cap fits, wear it: an overview of telomeric structures over evolution. Cell. Mol. Life Sci. 71, 847–865 (2014). https://doi.org/10.1007/s00018-013-1469-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-013-1469-z