Molecular characterization of Chlamydomonas reinhardtii telomeres and telomerase mutants
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31160377
PubMed Central
PMC6549138
DOI
10.26508/lsa.201900315
PII: 2/3/e201900315
Knihovny.cz E-zdroje
- MeSH
- Chlamydomonas reinhardtii genetika MeSH
- genetická variace MeSH
- homeostáza telomer MeSH
- polymorfismus délky restrikčních fragmentů MeSH
- repetitivní sekvence nukleových kyselin MeSH
- sekvence aminokyselin MeSH
- sekvence nukleotidů MeSH
- telomerasa chemie genetika metabolismus MeSH
- telomery genetika MeSH
- zkracování telomer MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- telomerasa MeSH
Telomeres are repeated sequences found at the end of the linear chromosomes of most eukaryotes and are required for chromosome integrity. Expression of the reverse-transcriptase telomerase allows for extension of telomeric repeats to counteract natural telomere shortening. Although Chlamydomonas reinhardtii, a photosynthetic unicellular green alga, is widely used as a model organism in photosynthesis and flagella research, and for biotechnological applications, the biology of its telomeres has not been investigated in depth. Here, we show that the C. reinhardtii (TTTTAGGG)n telomeric repeats are mostly nondegenerate and that the telomeres form a protective structure, with a subset ending with a 3' overhang and another subset presenting a blunt end. Although telomere size and length distributions are stable under various standard growth conditions, they vary substantially between 12 genetically close reference strains. Finally, we identify CrTERT, the gene encoding the catalytic subunit of telomerase and show that telomeres shorten progressively in mutants of this gene. Telomerase mutants eventually enter replicative senescence, demonstrating that telomerase is required for long-term maintenance of telomeres in C. reinhardtii.
Zobrazit více v PubMed
Akimcheva S, Zellinger B, Riha K (2008) Genome stability in Arabidopsis cells exhibiting alternative lengthening of telomeres. Cytogenet Genome Res 122: 388–395. 10.1159/000167827 PubMed DOI
Aksenova AY, Han G, Shishkin AA, Volkov KV, Mirkin SM (2015) Expansion of interstitial telomeric sequences in yeast. Cell Rep 13: 1545–1551. 10.1016/j.celrep.2015.10.023 PubMed DOI PMC
Arneric M, Lingner J (2007) Tel1 kinase and subtelomere-bound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast. EMBO Rep 8: 1080–1085. 10.1038/sj.embor.7401082 PubMed DOI PMC
Arora R, Azzalin CM (2015) Telomere elongation chooses TERRA ALTernatives. RNA Biol 12: 938–941. 10.1080/15476286.2015.1065374 PubMed DOI PMC
Askree SH, Yehuda T, Smolikov S, Gurevich R, Hawk J, Coker C, Krauskopf A, Kupiec M, McEachern MJ (2004) A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci USA 101: 8658–8663. 10.1073/pnas.0401263101 PubMed DOI PMC
Azzalin CM, Nergadze SG, Giulotto E (2001) Human intrachromosomal telomeric-like repeats: Sequence organization and mechanisms of origin. Chromosoma 110: 75–82. 10.1007/s004120100135 PubMed DOI
Borevitz JO, Liang D, Plouffe D, Chang HS, Zhu T, Weigel D, Berry CC, Winzeler E, Chory J (2003) Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res 13: 513–523. 10.1101/gr.541303 PubMed DOI PMC
Burr B, Burr FA, Matz EC, Romero-Severson J (1992) Pinning down loose ends: Mapping telomeres and factors affecting their length. Plant cell 4: 953–960. 10.2307/3869462 PubMed DOI PMC
Cesare AJ, Reddel RR (2010) Alternative lengthening of telomeres: Models, mechanisms and implications. Nat Rev Genet 11: 319–330. 10.1038/nrg2763 PubMed DOI
Cetin B, Cleveland DW (2010) How to survive aneuploidy. Cell 143: 27–29. 10.1016/j.cell.2010.09.030 PubMed DOI PMC
Chang HY, Lawless C, Addinall SG, Oexle S, Taschuk M, Wipat A, Wilkinson DJ, Lydall D (2011) Genome-wide analysis to identify pathways affecting telomere-initiated senescence in budding yeast. G3 (Bethesda) 1: 197–208. 10.1534/g3.111.000216 PubMed DOI PMC
Clark DJ. (2010) Nucleosome positioning, nucleosome spacing and the nucleosome code. J Biomol Struct Dyn 27: 781–793. 10.1080/073911010010524945 PubMed DOI PMC
Cross FR, Umen JG (2015) The Chlamydomonas cell cycle. Plant J 82: 370–392. 10.1111/tpj.12795 PubMed DOI PMC
Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101: 17312–17315. 10.1073/pnas.0407162101 PubMed DOI PMC
Fajkus J, Sykorova E, Leitch AR (2005) Techniques in plant telomere biology. BioTechniques 38: 233–243. 10.2144/05382rv01 PubMed DOI
Findinier J, Delevoye C, Cohen MM (2019) The dynamin-like protein Fzl promotes thylakoid fusion and resistance to light stress in Chlamydomonas reinhardtii. PLoS Genet 15: e1008047 10.1371/journal.pgen.1008047 PubMed DOI PMC
Forstemann K, Hoss M, Lingner J (2000) Telomerase-dependent repeat divergence at the 3’ ends of yeast telomeres. Nucleic Acids Res 28: 2690–2694. 10.1093/nar/28.14.2690 PubMed DOI PMC
Fulcher N, Derboven E, Valuchova S, Riha K (2014) If the cap fits, wear it: An overview of telomeric structures over evolution. Cell Mol Life Sci 71: 847–865. 10.1007/s00018-013-1469-z PubMed DOI PMC
Fulcher N, Teubenbacher A, Kerdaffrec E, Farlow A, Nordborg M, Riha K (2015) Genetic architecture of natural variation of telomere length in Arabidopsis thaliana. Genetics 199: 625–635. 10.1534/genetics.114.172163 PubMed DOI PMC
Fulnečková J, Hasíková T, Fajkus J, Lukešová A, Eliáš M, Sýkorová E (2012) Dynamic evolution of telomeric sequences in the green algal order Chlamydomonadales. Genome Biol Evol 4: 248–264. 10.1093/gbe/evs007 PubMed DOI PMC
Fulnecková J, Sevcíková T, Fajkus J, Lukesová A, Lukes M, Vlcek C, Lang BF, Kim E, Elias M, Sykorová E (2013) A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5: 468–483. 10.1093/gbe/evt019 PubMed DOI PMC
Fulnečková J, Ševčíková T, Lukešová A, Sýkorová E (2015) Transitions between the Arabidopsis-type and the human-type telomere sequence in green algae (clade Caudivolvoxa, Chlamydomonadales). Chromosoma 125: 437–451. 10.1007/s00412-015-0557-2 PubMed DOI
Gallaher SD, Fitz-Gibbon ST, Glaesener AG, Pellegrini M, Merchant SS (2015) Chlamydomonas genome resource for laboratory strains reveals a mosaic of sequence variation, identifies true strain histories, and enables strain-specific studies. Plant Cell 27: 2335–2352. 10.1105/tpc.15.00508 PubMed DOI PMC
Gaspin C, Rami JF, Lescure B (2010) Distribution of short interstitial telomere motifs in two plant genomes: Putative origin and function. BMC Plant Biol 10: 283 10.1186/1471-2229-10-283 PubMed DOI PMC
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: e35 10.1371/journal.pgen.0020104 PubMed DOI PMC
Giraud-Panis MJ, Teixeira MT, Geli V, Gilson E (2010) CST meets shelterin to keep telomeres in check. Mol Cell 39: 665–676. 10.1016/j.molcel.2010.08.024 PubMed DOI
Gohring J, Fulcher N, Jacak J, Riha K (2014) TeloTool: A new tool for telomere length measurement from terminal restriction fragment analysis with improved probe intensity correction. Nucleic Acids Res 42: e21 10.1093/nar/gkt1315 PubMed DOI PMC
Greenwood J, Patel H, Cech TR, Cooper JP (2018) Fission yeast telosomes: Non-canonical histone-containing chromatin structures dependent on shelterin and RNA. Nucleic Acids Res 46: 8865–8875. 10.1093/nar/gky605 PubMed DOI PMC
Gross CH, Ranum LP, Lefebvre PA (1988) Extensive restriction fragment length polymorphisms in a new isolate of Chlamydomonas reinhardtii. Curr Genet 13: 503–508. 10.1007/bf02427756 PubMed DOI
Hails T, Huttner O, Day A (1995) Isolation of a Chlamydomonas reinhardtii telomere by functional complementation in yeast. Curr Genet 28: 437–440. 10.1007/bf00310812 PubMed DOI
Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458–460. 10.1038/345458a0 PubMed DOI
Harris EH. (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52: 363–406. 10.1146/annurev.arplant.52.1.363 PubMed DOI
Harris EH. (2009) The Chlamydomonas Sourcebook (Second Edition). Canada: Elsevier Academic Press.
Heacock M, Spangler E, Riha K, Puizina J, Shippen DE (2004) Molecular analysis of telomere fusions in Arabidopsis: Multiple pathways for chromosome end-joining. EMBO J 23: 2304–2313. 10.1038/sj.emboj.7600236 PubMed DOI PMC
Johnston SD, Lew JE, Berman J (1999) Gbp1p: A protein with RNA recognition motifs, binds single-stranded telomeric DNA and changes its binding specificity upon dimerization. Mol Cell Biol 19: 923–933. 10.1128/mcb.19.1.923 PubMed DOI PMC
Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K (2012) Chromosome end protection by blunt-ended telomeres. Genes Dev 26: 1703–1713. 10.1101/gad.194944.112 PubMed DOI PMC
Lewis KA, Wuttke DS (2012) Telomerase and telomere-associated proteins: Structural insights into mechanism and evolution. Structure 20: 28–39. 10.1016/j.str.2011.10.017 PubMed DOI PMC
Li X, Zhang R, Patena W, Gang SS, Blum SR, Ivanova N, Yue R, Robertson JM, Lefebvre P, Fitz-Gibbon ST, et al. (2016) An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell 28: 367–387. 10.1105/tpc.15.00465 PubMed DOI PMC
Lingner J, Cech TR, Hughes TR, Lundblad V (1997a) Three Ever Shorter Telomere (EST) genes are dispensable for in vitro yeast telomerase activity. Proc Natl Acad Sci USA 94: 11190–11195. 10.1073/pnas.94.21.11190 PubMed DOI PMC
Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR (1997b) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561–567. 10.1126/science.276.5312.561 PubMed DOI
Liti G, Haricharan S, Cubillos FA, Tierney AL, Sharp S, Bertuch AA, Parts L, Bailes E, Louis EJ (2009) Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet 5: e1000659 10.1371/journal.pgen.1000659 PubMed DOI PMC
Lodha M, Schroda M (2005) Analysis of chromatin structure in the control regions of the chlamydomonas HSP70A and RBCS2 genes. Plant Mol Biol 59: 501–513. 10.1007/s11103-005-0450-0 PubMed DOI
Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73: 347–360. 10.1016/0092-8674(93)90234-h PubMed DOI
Lundblad V, Szostak JW (1989) A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57: 633–643. 10.1016/0092-8674(89)90132-3 PubMed DOI
Marzec P, Armenise C, Perot G, Roumelioti FM, Basyuk E, Gagos S, Chibon F, Dejardin J (2015) Nuclear-receptor-mediated telomere insertion leads to genome instability in ALT cancers. Cell 160: 913–927. 10.1016/j.cell.2015.01.044 PubMed DOI
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250. 10.1126/science.1143609 PubMed DOI PMC
Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, Ward OG, Wiley JE, Wurster-Hill DH, Yates TL, Moyzis RK (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99: 3–10. 10.1007/bf01737283 PubMed DOI
Millet C, Ausiannikava D, Le Bihan T, Granneman S, Makovets S (2015) Cell populations can use aneuploidy to survive telomerase insufficiency. Nat Commun 6: 8664 10.1038/ncomms9664 PubMed DOI PMC
Millet C, Makovets S (2016) Aneuploidy as a mechanism of adaptation to telomerase insufficiency. Curr Genet 62: 557–564. 10.1007/s00294-015-0559-x PubMed DOI PMC
Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, Harley CB, Cech TR (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277: 955–959. 10.1126/science.277.5328.955 PubMed DOI
Oguchi K, Liu H, Tamura K, Takahashi H (1999) Molecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana. FEBS Lett 457: 465–469. 10.1016/s0014-5793(99)01083-2 PubMed DOI
Palm W, de Lange T (2008) How shelterin protects mammalian telomeres. Annu Rev Genet 42: 301–334. 10.1146/annurev.genet.41.110306.130350 PubMed DOI
Petracek ME, Berman J (1992) Chlamydomonas reinhardtii telomere repeats form unstable structures involving guanine-guanine base pairs. Nucleic Acids Res 20: 89–95. 10.1093/nar/20.1.89 PubMed DOI PMC
Petracek ME, Konkel LMC, Kable ML, Berman J (1994) A Chlamydomonas protein that binds single-stranded G-strand telomere DNA. EMBO J 13: 3648–3658. 10.1002/j.1460-2075.1994.tb06672.x PubMed DOI PMC
Petracek ME, Lefebvre PA, Silflow CD, Berman J (1990) Chlamydomonas telomere sequences are A+T-rich but contain three consecutive G-C basepairs. Proc Natl Acad Sci USA 87: 8222–8226. 10.1073/pnas.87.21.8222 PubMed DOI PMC
Pfeiffer V, Lingner J (2013) Replication of telomeres and the regulation of telomerase. Cold Spring Harbor Perspect Biol 5: a010405 10.1101/cshperspect.a010405 PubMed DOI PMC
Platt JM, Ryvkin P, Wanat JJ, Donahue G, Ricketts MD, Barrett SP, Waters HJ, Song S, Chavez A, Abdallah KO, et al. (2013) Rap1 relocalization contributes to the chromatin-mediated gene expression profile and pace of cell senescence. Genes Dev 27: 1406–1420. 10.1101/gad.218776.113 PubMed DOI PMC
Raices M, Maruyama H, Dillin A, Karlseder J (2005) Uncoupling of longevity and telomere length in C. elegans. PLoS Genet 1: e30 10.1371/journal.pgen.0010081 PubMed DOI PMC
Rochaix JD. (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29: 209–230. 10.1146/annurev.ge.29.120195.001233 PubMed DOI
Romano GH, Harari Y, Yehuda T, Podhorzer A, Rubinstein L, Shamir R, Gottlieb A, Silberberg Y, Pe’er D, Ruppin E, et al. (2013) Environmental stresses disrupt telomere length homeostasis. PLoS Genet 9: e1003721 10.1371/journal.pgen.1003721 PubMed DOI PMC
Sasso S, Stibor H, Mittag M, Grossman AR (2018) From molecular manipulation of domesticated Chlamydomonas reinhardtii to survival in nature. Elife 7: e39233. PubMed PMC
Scaife MA, Nguyen GT, Rico J, Lambert D, Helliwell KE, Smith AG (2015) Establishing Chlamydomonas reinhardtii as an industrial biotechnology host. Plant J 82: 532–546. 10.1111/tpj.12781 PubMed DOI PMC
Scranton MA, Ostrand JT, Fields FJ, Mayfield SP (2015) Chlamydomonas as a model for biofuels and bio-products production. Plant J 82: 523–531. 10.1111/tpj.12780 PubMed DOI PMC
Shakirov EV, Shippen DE (2004) Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell 16: 1959–1967. 10.1105/tpc.104.023093 PubMed DOI PMC
Shay JW, Reddel RR, Wright WE (2012) Cancer. Cancer and telomeres: An ALTernative to telomerase. Science 336: 1388–1390. 10.1126/science.1222394 PubMed DOI
Uchida W, Matsunaga S, Sugiyama R, Kawano S (2002) Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77: 63–67. 10.1266/ggs.77.63 PubMed DOI
Ungar L, Yosef N, Sela Y, Sharan R, Ruppin E, Kupiec M (2009) A genome-wide screen for essential yeast genes that affect telomere length maintenance. Nucleic Acids Res 37: 3840–3849. 10.1093/nar/gkp259 PubMed DOI PMC
von Zglinicki T. (2000) Role of oxidative stress in telomere length regulation and replicative senescence. Ann New York Acad Sci 908: 99–110. 10.1111/j.1749-6632.2000.tb06639.x PubMed DOI
Vysotskaia VS, Curtis DE, Voinov AV, Kathir P, Silflow CD, Lefebvre PA (2001) Development and characterization of genome-wide single nucleotide polymorphism markers in the green alga Chlamydomonas reinhardtii. Plant Physiol 127: 386–389. 10.1104/pp.010485 PubMed DOI PMC
Walmsley RM, Petes TD (1985) Genetic control of chromosome length in yeast. Proc Natl Acad Sci USA 82: 506–510. 10.1073/pnas.82.2.506 PubMed DOI PMC
Watson JM, Platzer A, Kazda A, Akimcheva S, Valuchova S, Nizhynska V, Nordborg M, Riha K (2016) Germline replications and somatic mutation accumulation are independent of vegetative life span in Arabidopsis. Proc Natl Acad Sci USA 113: 12226–12231. 10.1073/pnas.1609686113 PubMed DOI PMC
Wellinger RJ, Zakian VA (2012) Everything you ever wanted to know about Saccharomyces cerevisiae telomeres: Beginning to end. Genetics 191: 1073–1105. 10.1534/genetics.111.137851 PubMed DOI PMC
Wright JH, Gottschling DE, Zakian VA (1992) Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev 6: 197–210. 10.1101/gad.6.2.197 PubMed DOI
Wu RA, Upton HE, Vogan JM, Collins K (2017) Telomerase mechanism of telomere synthesis. Annu Rev Biochem 86: 439–460. 10.1146/annurev-biochem-061516-045019 PubMed DOI PMC
Zakian VA. (1995) Telomeres: Beginning to understand the end. Science 270: 1601–1607. 10.1126/science.270.5242.1601 PubMed DOI
Zellinger B, Akimcheva S, Puizina J, Schirato M, Riha K (2007) Ku suppresses formation of telomeric circles and alternative telomere lengthening in Arabidopsis. Mol Cell 27: 163–169. 10.1016/j.molcel.2007.05.025 PubMed DOI
Zhu L, Hathcock KS, Hande P, Lansdorp PM, Seldin MF, Hodes RJ (1998) Telomere length regulation in mice is linked to a novel chromosome locus. Proc Natl Acad Sci USA 95: 8648–8653. 10.1073/pnas.95.15.8648 PubMed DOI PMC