Telomerase RNA evolution: a journey from plant telomeres to broader eukaryotic diversity
Language English Country Great Britain, England Media electronic
Document type Journal Article, Review, Research Support, Non-U.S. Gov't
PubMed
39889303
PubMed Central
PMC12133305
DOI
10.1042/bcj20240501
PII: 235630
Knihovny.cz E-resources
- Keywords
- TR evolution, TR identification, non-coding RNA, telomerase RNA, telomere,
- MeSH
- Phylogeny MeSH
- Evolution, Molecular * MeSH
- RNA, Plant * genetics MeSH
- RNA * genetics metabolism MeSH
- Plants * genetics MeSH
- Telomerase * genetics metabolism MeSH
- Telomere * genetics metabolism MeSH
- Viridiplantae * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- RNA, Plant * MeSH
- RNA * MeSH
- Telomerase * MeSH
- telomerase RNA MeSH Browser
Telomeres, essential for maintaining genomic stability, are typically preserved through the action of telomerase, a ribonucleoprotein complex that synthesizes telomeric DNA. One of its two core components, telomerase RNA (TR), serves as the template for this synthesis, and its evolution across different species is both complex and diverse. This review discusses recent advancements in understanding TR evolution, with a focus on plants (Viridiplantae). Utilizing novel bioinformatic tools and accumulating genomic and transcriptomic data, combined with corresponding experimental validation, researchers have begun to unravel the intricate pathways of TR evolution and telomere maintenance mechanisms. Contrary to previous beliefs, a monophyletic origin of TR has been demonstrated first in land plants and subsequently across the broader phylogenetic megagroup Diaphoretickes. Conversely, the discovery of plant-type TRs in insects challenges assumptions about the monophyletic origin of TRs in animals, suggesting evolutionary innovations coinciding with arthropod divergence. The review also highlights key challenges in TR identification and provides examples of how these have been addressed. Overall, this work underscores the importance of expanding beyond model organisms to comprehend the full complexity of telomerase evolution, with potential applications in agriculture and biotechnology.
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Olovnikov, A.M . (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl. Akad. Nauk SSSR 201, 394–397 PubMed
Olovnikov, A.M . (1973) A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41, 181–190 10.1016/0022-5193(73)90198-7 PubMed DOI
Greider, C.W. and Blackburn, E.H . (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43, 405–413 10.1016/0092-8674(85)90170-9 PubMed DOI
Greider, C.W. and Blackburn, E.H . (1987) The telomere terminal transferase of tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51, 887–898 10.1016/0092-8674(87)90576-9 PubMed DOI
Fajkus, J. , Kovarík, A. and Královics, R . (1996) Telomerase activity in plant cells. FEBS Lett. 391, 307–309 10.1016/0014-5793(96)00757-0 PubMed DOI
Jiang, J.S. , Miracco, E.J. , Hong, K. , Eckert, B. , Chan, H. , Cash, D.D. et al. (2013) The architecture of Tetrahymena telomerase holoenzyme. Nature New Biol. 496, 187–192 10.1038/nature12062 PubMed DOI PMC
He, Y. , Wang, Y. , Liu, B. , Helmling, C. , Sušac, L. , Cheng, R. et al. (2021) Structures of telomerase at several steps of telomere repeat synthesis. Nature New Biol. 593, 454–459 10.1038/s41586-021-03529-9 PubMed DOI PMC
Liu, B.C. , He, Y. , Wang, Y.Q. , Song, H. , Zhou, Z.H. and Feigon, J . (2022) Structure of active human telomerase with telomere shelterin protein TPP1. Nature New Biol. 604, 578–583 10.1038/s41586-022-04582-8 PubMed DOI PMC
Wang, Y. , Gallagher-Jones, M. , Sušac, L. , Song, H. and Feigon, J . (2021) A structurally conserved human and Tetrahymena telomerase catalytic core. Biophys. J. 117, 31078–31087 10.1016/j.bpj.2020.11.1037 PubMed DOI PMC
Richards, E.J. and Ausubel, F.M . (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53, 127–136 10.1016/0092-8674(88)90494-1 PubMed DOI
Fitzgerald, M.S. , McKnight, T.D. and Shippen, D.E . (1996) Characterization and developmental patterns of telomerase expression in plants. Proc. Natl. Acad. Sci. U.S.A. 93, 14422–14427 10.1073/pnas.93.25.14422 PubMed DOI PMC
Fajkus, J. , Fulnecková, J. , Hulánová, M. , Berková, K. , Ríha, K. and Matyásek, R . (1998) Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol. Gen. Genet. 260, 470–474 10.1007/s004380050918 PubMed DOI
Riha, K. , Fajkus, J. , Siroky, J. and Vyskot, B . (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10, 1691–1698 10.1105/tpc.10.10.1691 PubMed DOI PMC
Pich, U. , Fuchs, J. and Schubert, I . (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res. 4, 207–213 10.1007/BF02254961 PubMed DOI
Sykorova, E. , Lim, K.Y. , Chase, M.W. , Knapp, S. , Leitch, I.J. , Leitch, A.R. et al. (2003) The absence of Arabidopsis-type telomeres in cestrum and closely related genera vestia and sessea (Solanaceae): first evidence from eudicots. Plant J. 34, 283–291 10.1046/j.1365-313x.2003.01731.x PubMed DOI
Sýkorová, E. , Lim, K.Y. , Kunická, Z. , Chase, M.W. , Bennett, M.D. , Fajkus, J. et al. (2003) Telomere variability in the monocotyledonous plant order Asparagales. Proc. Biol. Sci. 270, 1893–1904 10.1098/rspb.2003.2446 PubMed DOI PMC
Tran, T.D. , Cao, H.X. , Jovtchev, G. , Neumann, P. , Novák, P. , Fojtová, M. et al. (2015) Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J. 84, 1087–1099 10.1111/tpj.13058 PubMed DOI
Peška, V. , Fajkus, P. , Fojtová, M. , Dvořáčková, M. , Hapala, J. , Dvořáček, 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 10.1111/tpj.12839 PubMed DOI
Fajkus, P. , Peška, V. , Sitová, Z. , Fulnečková, J. , Dvořáčková, M. , Gogela, R. et al. (2016) Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG)n is synthesized by telomerase. Plant J. 85, 337–347 10.1111/tpj.13115 PubMed DOI
Greider, C.W. and Blackburn, E.H . (1996) Telomeres, telomerase and cancer. Sci. Am. 274, 92–97 10.1038/scientificamerican0296-92 PubMed DOI
Gladyshev, E.A. , Meselson, M. and Arkhipova, I.R . (2007) A deep-branching clade of retrovirus-like retrotransposons in bdelloid rotifers. Gene 390, 136–145 10.1016/j.gene.2006.09.025 PubMed DOI PMC
Fajkus, P. , Adámik, M. , Nelson, A.D.L. , Kilar, A.M. , Franek, M. , Bubeník, M. et al. (2023) Telomerase RNA in Hymenoptera (Insecta) switched to plant/ciliate-like biogenesis. Nucleic Acids Res. 51, 420–433 10.1093/nar/gkac1202 PubMed DOI PMC
Podlevsky, J.D. and Chen, J.J.L . (2016) Evolutionary perspectives of telomerase RNA structure and function. RNA Biol. 13, 720–732 10.1080/15476286.2016.1205768 PubMed DOI PMC
Greider, C.W. and Blackburn, E.H . (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature New Biol. 337, 331–337 10.1038/337331a0 PubMed DOI
Shippen-Lentz, D. and Blackburn, E.H . (1990) Functional evidence for an RNA template in telomerase. Science 247, 546–552 10.1126/science.1689074 PubMed DOI
Lingner, J. , Hendrick, L.L. and Cech, T.R . (1994) Telomerase RNAs of different ciliates have a common secondary structure and a permuted template. Genes Dev. 8, 1984–1998 10.1101/gad.8.16.1984 PubMed DOI
Singer, M.S. and Gottschling, D.E . (1994) TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science 266, 404–409 10.1126/science.7545955 PubMed DOI
Villeponteau, B . (1996) The RNA components of human and mouse telomerases. Semin. Cell Dev. Biol. 7, 15–21 10.1006/scdb.1996.0004 DOI
Feng, J. , Funk, W.D. , Wang, S.S. , Weinrich, S.L. , Avilion, A.A. , Chiu, C.P. et al. (1995) The RNA component of human telomerase. Science 269, 1236–1241 10.1126/science.7544491 PubMed DOI
Blasco, M.A. , Funk, W. , Villeponteau, B. and Greider, C.W . (1995) Functional characterization and developmental regulation of mouse telomerase RNA. Science 269, 1267–1270 10.1126/science.7544492 PubMed DOI
Cifuentes-Rojas, C. , Kannan, K. , Tseng, L. and Shippen, D.E . (2011) Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl. Acad. Sci. U.S.A. 108, 73–78 10.1073/pnas.1013021107 PubMed DOI PMC
Cifuentes-Rojas, C. , Nelson, A.D.L. , Boltz, K.A. , Kannan, K. , She, X. and Shippen, D.E . (2012) An alternative telomerase RNA in Arabidopsis modulates enzyme activity in response to DNA damage. Genes Dev. 26, 2512–2523 10.1101/gad.202960.112 PubMed DOI PMC
Nelson, A.D.L. and Shippen, D.E . (2015) Evolution of TERT-interacting lncRNAs: expanding the regulatory landscape of telomerase. Front. Genet. 6, 277 10.3389/fgene.2015.00277 PubMed DOI PMC
Sykorová, E. , Fajkus, J. , Mezníková, M. , Lim, K.Y. , Neplechová, K. , Blattner, F.R. et al. (2006) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am. J. Bot. 93, 814–823 10.3732/ajb.93.6.814 PubMed DOI
Fajkus, P. , Peška, V. , Závodník, M. , Fojtová, M. , Fulnečková, J. , Dobias, Š. et al. (2019) Telomerase RNAs in land plants. Nucleic Acids Res. 47, 9842–9856 10.1093/nar/gkz695 PubMed DOI PMC
Song, J. , Logeswaran, D. , Castillo-González, C. , Li, Y. , Bose, S. , Aklilu, B.B. et al. (2019) The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans. Proc. Natl. Acad. Sci. U.S.A. 116, 24542–24550 10.1073/pnas.1915312116 PubMed DOI PMC
Wu, J. , Okada, T. , Fukushima, T. , Tsudzuki, T. , Sugiura, M. and Yukawa, Y . (2012) A novel hypoxic stress-responsive long non-coding RNA transcribed by RNA polymerase III in Arabidopsis. RNA Biol. 9, 302–313 10.4161/rna.19101 PubMed DOI
Dew-Budd, K. , Cheung, J. , Palos, K. , Forsythe, E.S. and Beilstein, M.A . (2020) Evolutionary and biochemical analyses reveal conservation of the Brassicaceae telomerase ribonucleoprotein complex. PLoS ONE 15, e0222687 10.1371/journal.pone.0222687 PubMed DOI PMC
Waibel, F. and Filipowicz, W . (1990) RNA-polymerase specificity of transcription of Arabidopsis U snRNA genes determined by promoter element spacing. Nature New Biol. 346, 199–202 10.1038/346199a0 PubMed DOI
Waibel, F. and Filipowicz, W . (1990) U6 snRNA genes of Arabidopsis are transcribed by RNA polymerase III but contain the same two upstream promoter elements as RNA polymerase II-transcribed U-snRNA genes. Nucleic Acids Res. 18, 3451–3458 10.1093/nar/18.12.3451 PubMed DOI PMC
Waibel, F. and Filipowicz, W . (1990) The spacing between two promoter elements determines RNA polymerase specificity during transcription of U small nuclear RNA genes of Arabidopsis. Mol. Biol. Rep. 14, 149, 149 10.1007/BF00360453 PubMed DOI
Yu, Q. , Gates, P.B. , Rogers, S. , Mikicic, I. , Elewa, A. , Salomon, F , et al. (2022) Telomerase-independent maintenance of telomere length in a vertebrate. Molecular Biology. 10.1101/2022.03.25.485759 DOI
Vítková, M. , Král, J. , Traut, W. , Zrzavý, J. and Marec, F . (2005) The evolutionary origin of insect telomeric repeats, (TTAGG). Chromosome Res. 13, 145–156 10.1007/s10577-005-7721-0 PubMed DOI
Mota, A.P.Z. , Koutsovoulos, G.D. , Perfus-Barbeoch, L. , Despot-Slade, E. , Labadie, K. , Aury, J.-M. et al. (2024) Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats. Nat. Commun. 15, 773 10.1038/s41467-024-44914-y PubMed DOI PMC
Tawari, B. , Ali, I.K.M. , Scott, C. , Quail, M.A. , Berriman, M. , Hall, N. et al. (2008) Patterns of evolution in the unique tRNA gene arrays of the genus Entamoeba. Mol. Biol. Evol. 25, 187–198 10.1093/molbev/msm238 PubMed DOI PMC
Seah, B.K.B. , Singh, A. , Vetter, D.E. , Emmerich, C. , Peters, M. , Soltys, V , et al. (2024) Nuclear dualism without extensive DNA elimination in the ciliate. Proceedings of the National Academy of Sciences 121, e2400503121 10.1073/pnas.2400503121 PubMed DOI PMC
Fulnecková, J. , Sevcíková, T. , Fajkus, J. , Lukesová, A. , Lukes, M. , Vlcek, C. et al. (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. and Sýkorová, E . (2016) 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
Bailey, T.L. and Elkan, C . (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28–36 PubMed
Raden, M. , Ali, S.M. , Alkhnbashi, O.S. , Busch, A. , Costa, F. , Davis, J.A. et al. (2018) Freiburg RNA tools: a central online resource for RNA-focused research and teaching. Nucleic Acids Res. 46, W25–W29 10.1093/nar/gky329 PubMed DOI PMC
Nawrocki, E.P. and Eddy, S.R . (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 10.1093/bioinformatics/btt509 PubMed DOI PMC
Fajkus, P. , Kilar, A. , Nelson, A.D.L. , Holá, M. , Peška, V. , Goffová, I. et al. (2021) Evolution of plant telomerase RNAs: farther to the past, deeper to the roots. Nucleic Acids Res. 49, 7680–7694 10.1093/nar/gkab545 PubMed DOI PMC
Bozděchová, L. , Havlová, K. , Fajkus, P. and Fajkus, J . (2024) Analysis of telomerase RNA structure in physcomitrium patens indicates functionally relevant transitions between open and closed conformations. J. Mol. Biol. 436, 168417 10.1016/j.jmb.2023.168417 PubMed DOI
Yang, M. , Zhu, P. , Cheema, J. , Bloomer, R. , Mikulski, P. , Liu, Q. et al. (2022) In vivo single-molecule analysis reveals COOLAIR RNA structural diversity. Nature New Biol. 609, 394–399 10.1038/s41586-022-05135-9 PubMed DOI PMC
Štefanovie, B. , Jenner, L.P. , Bozděchová, L. , Fajkus, P. , Sýkorová, E. , Fajkus, J. et al. (2024) Characterisation of the Arabidopsis thaliana telomerase TERT-TR complex. Plant Mol. Biol. 114, 56 10.1007/s11103-024-01461-w PubMed DOI PMC
Závodník, M. , Fajkus, P. , Franek, M. , Kopecký, D. , Garcia, S. , Dodsworth, S. et al. (2023) Telomerase RNA gene paralogs in plants - the usual pathway to unusual telomeres. New Phytol. 239, 2353–2366 10.1111/nph.19110 PubMed DOI
Ohno, S . (1970) Evolution by Gene Duplication, Springer-Verlag New York, Inc;
Louis, E.J . (2007) Evolutionary genetics: making the most of redundancy. Nature New Biol. 449, 673–674 10.1038/449673a PubMed DOI
Louis, E.J. and Vershinin, A.V . (2005) Chromosome ends: different sequences may provide conserved functions. Bioessays 27, 685–697 10.1002/bies.20259 PubMed DOI
Fajkus, J. , Sýkorová, E. and Leitch, A.R . (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res. 13, 469–479 10.1007/s10577-005-0997-2 PubMed DOI
Sepsiova, R. , Necasova, I. , Willcox, S. , Prochazkova, K. , Gorilak, P. , Nosek, J. et al. (2016) Evolution of telomeres in Schizosaccharomyces pombe and its possible relationship to the diversification of telomere binding proteins. PLoS ONE 11, e0154225 10.1371/journal.pone.0154225 PubMed DOI PMC
Červenák, F. , Sepšiová, R. , Nosek, J. and Tomáška, Ľ . (2021) Step-by-step evolution of telomeres: lessons from yeasts. Genome Biol. Evol. 13, evaa268 10.1093/gbe/evaa268 PubMed DOI PMC
Lyčka, M. , Bubeník, M. , Závodník, M. , Peska, V. , Fajkus, P. , Demko, M. et al. (2024) TeloBase: a community-curated database of telomere sequences across the tree of life. Nucleic Acids Res. 52, D311–D321 10.1093/nar/gkad672 PubMed DOI PMC
Kilar, A.M. , Fajkus, P. and Fajkus, J . (2022) Geronimo: a tool for systematic retrieval of structural RNAs in A broad evolutionary context. Gigascience 12, giad080 10.1093/gigascience/giad080 PubMed DOI PMC