Chromosoma

, Volume 125, Issue 3, pp 437–451

Transitions between the Arabidopsis-type and the human-type telomere sequence in green algae (clade Caudivolvoxa, Chlamydomonadales)

  • Jana Fulnečková
  • Tereza Ševčíková
  • Alena Lukešová
  • Eva Sýkorová
Research Article

Abstract

Telomeres are nucleoprotein structures that distinguish native chromosomal ends from double-stranded breaks. They are maintained by telomerase that adds short G-rich telomeric repeats at chromosomal ends in most eukaryotes and determines the TnAmGo sequence of canonical telomeres. We employed an experimental approach that was based on detection of repeats added by telomerase to identify the telomere sequence type forming the very ends of chromosomes. Our previous studies that focused on the algal order Chlamydomonadales revealed several changes in telomere motifs that were consistent with the phylogeny and supported the concept of the Arabidopsis-type sequence being the ancestral telomeric motif for green algae. In addition to previously described independent transitions to the Chlamydomonas-type sequence, we report that the ancestral telomeric motif was replaced by the human-type sequence in the majority of algal species grouped within a higher order clade, Caudivolvoxa. The Arabidopsis-type sequence was apparently retained in the Polytominia clade. Regarding the telomere sequence, the Chlorogonia clade within Caudivolvoxa bifurcates into two groups, one with the human-type sequence and the other group with the Arabidopsis-type sequence that is solely formed by the Chlorogonium species. This suggests that reversion to the Arabidopsis-type telomeric motif occurred in the common ancestral Chlorogonium species. The human-type sequence is also synthesized by telomerases of algal strains from Arenicolinia, Dunaliellinia and Stephanosphaerinia, except a distinct subclade within Stephanosphaerinia, where telomerase activity was not detected and a change to an unidentified telomeric motif might arise. We discuss plausible reasons why changes in telomeric motifs were tolerated during evolution of green algae.

Keywords

Green algae Telomere evolution Telomerase activity TRAP 18S rDNA phylogeny 

Supplementary material

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Fig. S1

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High Resolution (TIF 2298 kb)
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ESM 1(PDF 497 kb)

References

  1. Ai W, Bertram PG, Tsang CK, Chan TF, Zheng XF (2002) Regulation of subtelomeric silencing during stress response. Mol Cell 10:1295–1305CrossRefPubMedGoogle Scholar
  2. Alexander MK, Zakian VA (2003) Rap1p telomere association is not required for mitotic stability of a C(3)TA(2) telomere in yeast. EMBO J 22:1688–1696. doi:10.1093/emboj/cdg154 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88. doi:10.1016/j.cub.2008.11.067 CrossRefPubMedGoogle Scholar
  4. Blackburn EH, Gall JG (1978) Tandemly repeated sequence at termini of extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120:33–53CrossRefPubMedGoogle Scholar
  5. Blanc G et al (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13:R39. doi:10.1186/gb-2012-13-5-r39 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  7. Chong L, van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J, Tempst P, de Lange T (1995) A human telomeric protein. Science 270:1663–1667CrossRefPubMedGoogle Scholar
  8. Collard BCY, Das A, Virk PS, Mackill DJ (2007) Evaluation of “quick” and “dirty” DNA extraction methods for marker-assisted selection in rice (Oryza sativa L.). Plant Breed 126:47–50CrossRefGoogle Scholar
  9. de Lange T (2004) T-loops and the origin of telomeres. Nat Rev Mol Cell Biol 5:323–329. doi:10.1038/nrm1359 CrossRefPubMedGoogle Scholar
  10. Derelle E et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103:11647–11652. doi:10.1073/pnas.0604795103 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H (2004) The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci U S A 101:15386–15391. doi:10.1073/pnas.0403984101 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Eickbush TH (1997) Telomerase and retrotransposons: which came first? Science 277:911–912CrossRefPubMedGoogle Scholar
  13. Fabre E, Muller H, Therizols P, Lafontaine I, Dujon B, Fairhead C (2005) Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol Biol Evol 22:856–873. doi:10.1093/molbev/msi070 CrossRefPubMedGoogle Scholar
  14. Fajkus J, Fulneckova J, Hulanova M, Berkova K, Riha K, Matyasek R (1998) Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol Gen Genet 260:470–474CrossRefPubMedGoogle Scholar
  15. Fajkus J, Sykorova E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosom Res 13:469–479. doi:10.1007/s10577-005-0997-2 CrossRefGoogle Scholar
  16. Fitzgerald MS, McKnight TD, Shippen DE (1996) Characterization and developmental patterns of telomerase expression in plants. Proc Natl Acad Sci U S A 93:14422–14427CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fojtova M, Peska V, Dobsakova Z, Mozgova I, Fajkus J, Sykorova E (2011) Molecular analysis of T-DNA insertion mutants identified putative regulatory elements in the AtTERT gene. J Exp Bot 62:5531–5545. doi:10.1093/jxb/err235 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Frydrychova R, Grossmann P, Trubac P, Vitkova M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178. doi:10.1139/g03-100 CrossRefPubMedGoogle Scholar
  19. Fuchs J, Schubert I (1996) Arabidopsis-type telomere sequences on chromosome termini of Selaginella martensii Spring (Pteridophyta). Biol Zentralbl 115:260–265Google Scholar
  20. Fuchs J, Brandes A, Schubert I (1995) Telomere sequence localization and karyotype evolution in higher plants. Pl Syst Evol 196:227–241CrossRefGoogle Scholar
  21. 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 4:248–264. doi:10.1093/gbe/evs007 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fulneckova J et al (2013) A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5:468–483. doi:10.1093/gbe/evt019 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413CrossRefPubMedGoogle Scholar
  24. Higashiyama T, Maki S, Yamada T (1995) Molecular organization of Chlorella vulgaris chromosome I: presence of telomeric repeats that are conserved in higher plants. Mol Gen Genet 246:29–36CrossRefPubMedGoogle Scholar
  25. Horn D, Barry JD (2005) The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosom Res 13:525–533. doi:10.1007/s10577-005-0991-8 CrossRefGoogle Scholar
  26. Hunt C et al (2001) Subtelomeric sequence from the right arm of Schizosaccharomyces pombe chromosome I contains seven permease genes. Yeast 18:355–361CrossRefPubMedGoogle Scholar
  27. Katana A, Kwiatowski J, Spalik K, Zakrys B, Szalacha E, Szymanska H (2001) Phylogenetic position of Koliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. J Phycol 37:443–451CrossRefGoogle Scholar
  28. Klobutcher LA, Swanton MT, Donini P, Prescott DM (1981) All gene-sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3′ terminus. Proc Natl Acad Sci U S A 78:3015–3019CrossRefPubMedPubMedCentralGoogle Scholar
  29. Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11:209. doi:10.1186/gb-2010-11-5-209 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Leblancq SM, Kase RS, Vanderploeg LHT (1991) Analysis of a Giardia lamblia ribosomal-RNA encoding telomere with [TAGGG]n as the telomere repeat. Nucleic Acids Res 19:5790–5790. doi:10.1093/nar/19.20.5790 CrossRefGoogle Scholar
  31. Maita N, Anzai T, Aoyagi H, Mizuno H, Fujiwara H (2004) Crystal structure of the endonuclease domain encoded by the telomere-specific long interspersed nuclear element, TRAS1. J Biol Chem 279:41067–41076. doi:10.1074/jbc.M406556200 CrossRefPubMedGoogle Scholar
  32. McFadden GI, van Dooren GG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14:R514–R516. doi:10.1016/j.cub.2004.06.041 CrossRefPubMedGoogle Scholar
  33. Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci U S A 86:7049–7053CrossRefPubMedPubMedCentralGoogle Scholar
  34. Miller MA, Pfeiffer W, Schwartz T Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, 14 Nov. 2010. pp 1–8Google Scholar
  35. Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48:281–291. doi:10.1016/j.ympev.2008.03.016 CrossRefPubMedGoogle Scholar
  36. Nakada T, Nozaki H, Tomita M (2010) Another origin of coloniality in volvocaleans: the phylogenetic position of Pyrobotrys arnoldi (Spondylomoraceae, Volvocales). J Eukaryot Microbiol 57:379–382. doi:10.1111/j.1550-7408.2010.00488.x CrossRefPubMedGoogle Scholar
  37. Nemcova Y, Elias M, Skaloud P, Hodac L, Neustupa J (2011) Jenufa Gen. Nov.: a new genus of coccoid green algae (Chlorophyceae, Incertae Sedis) previously recorded by environmental sequencing. J Phycol 47:928–938. doi:10.1111/j.1529-8817.2011.01009.x CrossRefPubMedGoogle Scholar
  38. Neustupa J, Elias M, Skaloud P, Nemcova Y, Sejnohova L (2011) Xylochloris irregularis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel subaerial coccoid green alga. Phycologia 50:57–66. doi:10.2216/08-64.1 CrossRefGoogle Scholar
  39. Nozaki H et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28. doi:10.1186/1741-7007-5-28 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 13:1424–1432CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 122:380–387. doi:10.1159/000167826 CrossRefPubMedGoogle Scholar
  42. Peska V et al (2015) Characterisation of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J 82:644–654. doi:10.1111/tpj.12839 CrossRefPubMedGoogle Scholar
  43. 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 U S A 87:8222–8226CrossRefPubMedPubMedCentralGoogle Scholar
  44. Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53:127–136CrossRefPubMedGoogle Scholar
  45. Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029
  46. Rotkova G, Sklenickova M, Dvorackova M, Sykorova E, Leitch AR, Fajkus J (2004) An evolutionary change in telomere sequence motif within the plant section Asparagales had significance for telomere nucleoprotein complexes. Cytogenet Genome Res 107:132–138. doi:10.1159/000079584 CrossRefPubMedGoogle Scholar
  47. Rotkova G, Sykorova E, Fajkus J (2007) Characterization of nucleoprotein complexes in plants with human-type telomere motifs. Plant Physiol Biochem 45:716–721. doi:10.1016/j.plaphy.2007.07.009 CrossRefPubMedGoogle Scholar
  48. Schechtman MG (1990) Characterization of telomere DNA from Neurospora crassa. Gene 88:159–165CrossRefPubMedGoogle Scholar
  49. Schrumpfova P, Kuchar M, Mikova G, Skrisovska L, Kubicarova T, Fajkus J (2004) Characterization of two Arabidopsis thaliana myb-like proteins showing affinity to telomeric DNA sequence. Genome 47:316–324. doi:10.1139/g03-136 CrossRefPubMedGoogle Scholar
  50. Shampay J, Szostak JW, Blackburn EH (1984) DNA sequences of telomeres maintained in yeast. Nature 310:154–157CrossRefPubMedGoogle Scholar
  51. Skolakova P, Foldynova-Trantirkova S, Bednarova K, Fiala R, Vorlickova M, Trantirek L (2015) Unique C. elegans telomeric overhang structures reveal the evolutionarily conserved properties of telomeric DNA. Nucleic Acids Res 43:4733–4745. doi:10.1093/nar/gkv296 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sohanpal BK, Morzaria SP, Gobright EI, Bishop RP (1995) Characterisation of the telomeres at opposite ends of a 3 Mb Theileria parva chromosome. Nucleic Acids Res 23:1942–1947CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771. doi:10.1080/10635150802429642 CrossRefPubMedGoogle Scholar
  54. Strahl-Bolsinger S, Hecht A, Luo K, Grunstein M (1997) SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 11:83–93CrossRefPubMedGoogle Scholar
  55. Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003a) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34:283–291CrossRefPubMedGoogle Scholar
  56. Sykorova E, Lim KY, Kunicka Z, Chase MW, Bennett MD, Fajkus J, Leitch AR (2003b) Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270:1893–1904. doi:10.1098/rspb.2003.2446 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sykorova E et al (2006) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am J Bot 93:814–823CrossRefPubMedGoogle Scholar
  58. Tran PL, Mergny JL, Alberti P (2011) Stability of telomeric G-quadruplexes. Nucleic Acids Res 39:3282–3294. doi:10.1093/nar/gkq1292 CrossRefPubMedGoogle Scholar
  59. Wright JH, Gottschling DE, Zakian VA (1992) Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev 6:197–210CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jana Fulnečková
    • 1
    • 2
  • Tereza Ševčíková
    • 3
  • Alena Lukešová
    • 4
  • Eva Sýkorová
    • 1
    • 2
  1. 1.Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.Faculty of Science, and CEITEC – Central European Institute of TechnologyMasaryk UniversityBrnoCzech Republic
  3. 3.Department of Biology and Ecology, Life Science Research Centre & Institute of Environmental Technologies, Faculty of ScienceUniversity of OstravaOstravaCzech Republic
  4. 4.Institute of Soil BiologyBiology Centre Academy of Sciences of the Czech Republic, v.vi.České BudějoviceCzech Republic

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