Telomeres are basic structures of eukaryote genomes. They distinguish natural chromosome ends from double-stranded breaks in DNA and protect chromosome ends from degradation or end-to-end fusion with other chromosomes. Telomere sequences are usually tandemly arranged minisatellites, typically following the formula (TxAyGz)n. Although they are well conserved across large groups of organisms, recent findings in plants imply that their diversity has been underestimated. Changes in telomeres are of enormous evolutionary importance as they can affect whole-genome stability. Even a small change in the telomere motif of each repeat unit represents an important interference in the system of sequence-specific telomere binding proteins. Here, we provide an overview of telomere sequences, considering the latest phylogenomic evolutionary framework of plants in the broad sense (Archaeplastida), in which new telomeric sequences have recently been found in diverse and economically important families such as Solanaceae and Amaryllidaceae. In the family Lentibulariaceae and in many groups of green algae, deviations from the typical plant telomeric sequence have also been detected recently. Ancestry and possible homoplasy in telomeric motifs, as well as extant gaps in knowledge are discussed. With the increasing availability of genomic approaches, it is likely that more telomeric diversity will be uncovered in the future. We also discuss basic methods used for telomere identification and we explain the implications of the recent discovery of plant telomerase RNA on further research about the role of telomerase in eukaryogenesis or on the molecular causes and consequences of telomere variability.

Department of Cell Biology and Radiobiology The Czech Academy of Sciences Institute of Biophysics Brno Czechia

Institut Botànic de Barcelona Barcelona Spain

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Adams S. P., Hartman T. P., Lim K. Y., Chase M. W., Bennett M. D., Leitch I. J., et al. (2001). Loss and recovery of Arabidopsis-type telomere repeat sequences 5'-(TTTAGGG)(n)-3' in the evolution of a major radiation of flowering plants. Proc. Biol. Sci. 268 (1476), 1541–1546. 10.1098/rspb.2001.1726 PubMed DOI PMC

Beilstein M. A., Brinegar A. E., Shippen D. E. (2012). Evolution of the Arabidopsis telomerase RNA. Front. Genet. 3, 188. 10.3389/fgene.2012.00188 PubMed DOI PMC

Benson G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27 (2), 573–580. 10.1093/nar/27.2.573 PubMed DOI PMC

Biessmann H., Mason J. M. (2003). Telomerase-independent mechanisms of telomere elongation. Cell Mol. Life Sci. 60 (11), 2325–2333. 10.1007/s00018-003-3247-9 PubMed DOI PMC

Blackburn E. H., Gall J. G. (1978). A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol. 120 (1), 33–53. 10.1016/0022-2836(78)90294-2 PubMed DOI

Blasco M. A., Funk W., Villeponteau B., Greider C. W. (1995). Functional characterization and developmental regulation of mouse telomerase RNA. Science 269 (5228), 1267–1270. 10.1126/science.7544492 PubMed DOI

Bremer B., Bremer K., Chase M. W., Fay M. F., Reveal J. L., Soltis D. E., et al. (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161 (2), 105–121. 10.1111/j.1095-8339.2009.00996.x DOI

Byng J. W., Chase M. W., Christenhusz M. J. M., Fay M. F., Judd W. S., Mabberley D. J., et al. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181 (1), 1–20. 10.1111/boj.12385 DOI

Cervenak F., Jurikova K., Devillers H., Kaffe B., Khatib A., Bonnell E., et al. (2019). Identification of telomerase RNAs in species of the Yarrowia clade provides insights into the co-evolution of telomerase, telomeric repeats and telomere-binding proteins. Sci. Rep. 9 (1), 13365. 10.1038/s41598-019-49628-6 PubMed DOI PMC

Cifuentes-Rojas C., Kannan K., Tseng L., Shippen D. E. (2011). Two RNA subunits and POT1a are components Arabidopsis telomerase. Proc. Natl. Acad. Sci. U. S. A. 108 (1), 73–78. 10.1073/pnas.1013021107 PubMed DOI PMC

Cox A. V., Bennett S. T., Parokonny A. S., Kenton A., Callimassia M. A., Bennett M. D. (1993). Comparison of plant telomere locations using a Pcr-generated synthetic probe. Ann. Bot. 72 (3), 239–247. 10.1006/anbo.1993.1104 DOI

Danilevskaya O. N., Lowenhaupt K., Pardue M. L. (1998). Conserved subfamilies of the Drosophila HeT-A telomere-specific retrotransposon. Genetics 148 (1), 233–242. https://www.genetics.org/content/148/1/233.short PubMed PMC

Derelle E., Ferraz C., Rombauts S., Rouze P., Worden A. Z., Robbens S., et al. (2006). Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. U. States America 103 (31), 11647–11652. 10.1073/pnas.0604795103 PubMed DOI PMC

Dew-Budd K., Cheung J., Palos K., Forsythe E. S., Beilstein M. A. (2019). Evolutionary and biochemical analyses reveal conservation of the Brassicaceae telomerase ribonucleoprotein complex. BioRxiv 760785. 10.1101/760785 PubMed DOI PMC

Emery H. S., Weiner A. M. (1981). An irregular satellite sequence is found at the termini of the linear extrachromosomal rDNA in Dictyostelium discoideum. Cell 26 (3 Pt 1), 411–419. 10.1016/0092-8674(81)90210-5 PubMed DOI

Fajkus J., Sýkorová E., Leitch A. R. (2005). Telomeres in evolution and evolution of telomeres. Chromosome Res. 13 (5), 469–479. 10.1007/s10577-005-0997-2 PubMed DOI

Fajkus P., Peska V., Sitova Z., Fulneckova J., Dvorackova M., Gogela R., et al. (2016). Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG)n is synthesized by telomerase. Plant J. 85 (3), 337–347. 10.1111/tpj.13115 PubMed DOI

Fajkus P., Peska V., Zavodnik M., Fojtova M., Fulneckova J., Dobias S., et al. (2019). Telomerase RNAs in land plants. Nucleic Acids Res. 47 (18), 9842–9856. 10.1093/nar/gkz695 PubMed DOI PMC

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 (5228), 1236–1241. 10.1126/science.7544491 PubMed DOI

Ferdows M. S., Barbour A. G. (1989). Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc. Natl. Acad. Sci. U. S. A. 86 (15), 5969–5973. 10.1073/pnas.86.15.5969 PubMed DOI PMC

Fojtova M., Sykorova E., Najdekrova L., Polanska P., Zachova D., Vagnerova R., et al. (2015). Telomere dynamics in the lower plant Physcomitrella patens. Plant Mol. Biol. 87 (6), 591–601. 10.1007/s11103-015-0299-9 PubMed DOI

Forstemann K., Zaug A. J., Cech T. R., Lingner J. (2003). Yeast telomerase is specialized for C/A-rich RNA templates. Nucleic Acids Res. 31 (6), 1646–1655. 10.1093/nar/gkg261 PubMed DOI PMC

Frydrychova R., Grossmann P., Trubac P., Vitkova M., Marec F. (2004). Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47 (1), 163–178. 10.1139/g03-100 PubMed DOI

Fuchs J., Brandes A., Schubert I. (1995). Telomere sequence localization and karyotype evolution in higher-plants. Plant Syst. Evol. 196 (3-4), 227–241. 10.1007/Bf00982962 DOI

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. 10.1093/gbe/evs007 PubMed DOI PMC

Fulneckova J., Sevcikova T., Fajkus J., Lukesova 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 (3), 468–483. 10.1093/gbe/evt019 PubMed DOI PMC

Fulneckova J., Sevcikova T., Lukesova A., Sykorova E. (2016). Transitions between the Arabidopsis-type and the human-type telomere sequence in green algae (clade Caudivolvoxa, Chlamydomonadales). Chromosoma 125 (3), 437–451. 10.1007/s00412-015-0557-2 PubMed DOI

Garcia S., Garnatje T., Kovarik A. (2012). Plant rDNA database: ribosomal DNA loci information goes online. Chromosoma 121 (4), 389–394. 10.1007/s00412-012-0368-7 PubMed DOI

Gladyshev E. A., Arkhipova I. R. (2007). Telomere-associated endonuclease-deficient Penelope-like retroelements in diverse eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 104 (22), 9352–9357. 10.1073/pnas.0702741104 PubMed DOI PMC

Greider C. W., Blackburn E. H. (1985). Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43 (2 Pt 1), 405–413. 10.1016/0092-8674(85)90170-9 PubMed DOI

Greider C. W., Blackburn E. H. (1989). A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337 (6205), 331–337. 10.1038/337331a0 PubMed DOI

Higashiyama T., Noutoshi Y., Akiba M., Yamada T. (1995). Telomere and LINE-like elements at the termini of the Chlorella chromosome I. Nucleic Acids Symp. Ser. (34), 71–72. https://europepmc.org/article/med/8841557 PubMed

Hofr C., Sultesova P., Zimmermann M., Mozgova I., Prochazkova Schrumpfova P., Wimmerova M., et al. (2009). Single-Myb-histone proteins from Arabidopsis thaliana: a quantitative study of telomere-binding specificity and kinetics. Biochem. J. 419 (1), 221–228. 10.1042/BJ20082195 PubMed DOI

Hu Y., Shi G., Zhang L. C., Li F., Jiang Y. L., Jiang S., et al. (2016). Switch telomerase to ALT mechanism by inducing telomeric DNA damages and dysfunction of ATRX and DAXX. Sci. Rep. 6. 10.1038/Srep32280 PubMed DOI PMC

Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L., et al. (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266 (5193), 2011–2015. 10.1126/science.7605428 PubMed DOI

Koo D. H., Molin W. T., Saski C. A., Jiang J., Putta K., Jugulam M., et al. (2018). Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc. Natl. Acad. Sci. U. S. A. 115 (13), 3332–3337. 10.1073/pnas.1719354115 PubMed DOI PMC

Koonin E. V. (2006). The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol. Direct. 1, 22. 10.1186/1745-6150-1-22 PubMed DOI PMC

Majerska J., Schrumpfova P. P., Dokladal L., Schorova S., Stejskal K., Oboril M., et al. (2017). Tandem affinity purification of AtTERT reveals putative interaction partners of plant telomerase in vivo . Protoplasma 254 (4), 1547–1562. 10.1007/s00709-016-1042-3 PubMed DOI

Mason J. M., Randall T. A., Capkova Frydrychova R. (2016). Telomerase lost? Chromosoma 125 (1), 65–73. 10.1007/s00412-015-0528-7 PubMed DOI PMC

Meyne J., Ratliff R. L., Moyzis R. K. (1989). Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc. Natl. Acad. Sci. U. S. A. 86 (18), 7049–7053. 10.1073/pnas.86.18.7049 PubMed DOI PMC

Mravinac B., Mestrovic N., Cavrak V. V., Plohl M. (2011). TCAGG, an alternative telomeric sequence in insects. Chromosoma 120 (4), 367–376. 10.1007/s00412-011-0317-x PubMed DOI

Muller F., Wicky C., Spicher A., Tobler H. (1991). New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin diminution in Ascaris lumbricoides. Cell 67 (4), 815–822. 10.1016/0092-8674(91)90076-b PubMed DOI

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. 10.1007/bf00425822 PubMed DOI

Nosek J., Kosa P., Tomaska L. (2006). On the origin of telomeres: a glimpse at the pre-telomerase world. Bioessays 28 (2), 182–190. 10.1002/bies.20355 PubMed DOI

Novak P., Neumann P., Macas J. (2010). Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinf. 11, 378. 10.1186/1471-2105-11-378 PubMed DOI PMC

Nozaki H., Takano H., Misumi O., Terasawa K., Matsuzaki M., Maruyama S., et al. (2007). A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol. 5, 28. 10.1186/1741-7007-5-28 PubMed DOI PMC

Olovnikov A. M. (1973). Theory of marginotomy - incomplete copying of template margin in enzymic-synthesis of polynucleotides and biological significance of phenomenon. J. Theor. Biol. 41 (1), 181–190. 10.1016/0022-5193(73)90198-7 PubMed DOI

One Thousand Plant Transcriptomes Initiative (2019). One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574 (7780), 679–685. 10.1038/s41586-019-1693-2 PubMed DOI PMC

Pardue M. L., Danilevskaya O. N., Traverse K. L., Lowenhaupt K. (1997). Evolutionary links between telomeres and transposable elements. Genetica 100 (1–3), 73–84. 10.1007/978-94-011-4898-6_7 PubMed DOI

Peska V., Sykorova E., Fajkus J. (2008). Two faces of solanaceae telomeres: a comparison between Nicotiana and Cestrum telomeres and telomere-binding proteins. Cytogenetic. Genome Res. 122 (3-4), 380–387. 10.1159/000167826 PubMed DOI

Peska V., Fajkus P., Fojtova M., Dvorackova M., Hapala J., Dvoracek 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 (4), 644–654. 10.1111/tpj.12839 PubMed DOI

Peska V., Sitova Z., Fajkus P., Fajkus J. (2017). BAL31-NGS approach for identification of telomeres de novo in large genomes. Methods 114, 16–27. 10.1016/j.ymeth.2016.08.017 PubMed DOI

Peska V., Mandakova T., Ihradska V., Fajkus J. (2019). Comparative dissection of three giant genomes: allium cepa, allium sativum, and allium ursinum. Int. J. Mol. Sci. 20 (3). 10.3390/ijms20030733 PubMed DOI PMC

Petracek M. E., Lefebvre P. A., Silflow C. D., 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 (21), 8222–8226. 10.1073/pnas.87.21.8222 PubMed DOI PMC

Pfeiffer V., Lingner J. (2012). TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genet. 8 (6). 10.1371/journal.pgen.1002747 PubMed DOI PMC

Pich U., Schubert I. (1998). Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosome Res. 6 (4), 315–321. 10.1023/a:1009227009121 PubMed DOI

Podlevsky J. D., Chen J. J. (2016). Evolutionary perspectives of telomerase RNA structure and function. RNA Biol. 13 (8), 720–732. 10.1080/15476286.2016.1205768 PubMed DOI PMC

Polotnianka R. M., Li J., Lustig A. J. (1998). The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8 (14), 831–834. 10.1016/S0960-9822(98)70325-2 PubMed DOI

Puizina J., Weiss-Schneeweiss H., Pedrosa-Harand A., Kamenjarin J., Trinajstic I., Riha K., Schweizer D. (2003). Karyotype analysis in Hyacinthella dalmatica (Hyacinthaceae) reveals vertebrate-type telomere repeats at the chromosome ends. Genome 46 (6), 1070–6. 10.1139/g03-078 PubMed DOI

Qi X. D., Li Y., Honda S., Hoffmann S., Marz M., Mosig A., et al. (2013). The common ancestral core of vertebrate and fungal telomerase RNAs. Nucleic Acids Res. 41 (1), 450–462. 10.1093/nar/gks980 PubMed DOI PMC

Richards E. J., Ausubel F. M. (1988). Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53 (1), 127–136. 10.1016/0092-8674(88)90494-1 PubMed DOI

Rubin G. M. (1978). Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harb. Symp. Quant. Biol. 42 Pt 2, 1041–1046. 10.1101/sqb.1978.042.01.104 PubMed DOI

Ruckova E., Friml J., Schrumpfova P. P., Fajkus J. (2008). Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol. Biol. 66 (6), 637–646. 10.1007/s11103-008-9295-7 PubMed DOI

Sekhri K. (2014). Telomeres and telomerase: understanding basic structure and potential new therapeutic strategies targeting it in the treatment of cancer. Postgrad. Med. J. 60 (3), 303. 10.4103/0022-3859.138797 PubMed DOI

Seyfried T. N., Huysentruyt L. C. (2013). On the origin of cancer metastasis. Crit. Rev. Oncog. 18 (1-2), 43–73. 10.1615/critrevoncog.v18.i1-2.40 PubMed DOI PMC

Shibata F., Hizume M. (2011). Survey of arabidopsis- and human-type telomere repeats in plants using fluorescence in situ Hybridisation. Cytologia 76 (3), 353–360. 10.1508/cytologia.76.353 DOI

Somanathan I., Baysdorfer C. (2018). A bioinformatics approach to identify telomere sequences. Biotechniques 65 (1), 20–25. 10.2144/btn-2018-0057 PubMed DOI

Spiegel J., Adhikari S., Balasubramanian S. (2020). The structure and function of DNA G-quadruplexes. Trends Chem. 2 (2), 123–136. 10.1016/j.trechm.2019.07.002 PubMed DOI PMC

Sykorova E., Lim K. Y., Fajkus J., Leitch A. R. (2003. a). The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)n telomeres. Chromosoma 112 (4), 164–172. 10.1007/s00412-003-0256-2 PubMed DOI

Sykorova E., Lim K. Y., Chase M. W., Knapp S., Leitch I. J., Leitch A. R., et al. (2003. b). 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. 10.1046/j.1365-313x.2003.01731.x PubMed DOI

Sykorova E., Lim K. Y., Kunicka Z., Chase M. W., Bennett M. D., Fajkus J., et al. (2003. c). Telomere variability in the monocotyledonous plant order Asparagales. Proc. Biol. Sci. 270 (1527), 1893–1904. 10.1098/rspb.2003.2446 PubMed DOI PMC

Tran P. L., De Cian A., Gros J., Moriyama R., Mergny J. L. (2013). Tetramolecular quadruplex stability and assembly. Top. Curr. Chem. 330, 243–273. 10.1007/128_2012_334 PubMed DOI

Tran T. D., Cao H. X., Jovtchev G., Neumann P., Novak P., Fojtova M., et al. (2015). Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J. 84 (6), 1087–1099. 10.1111/tpj.13058 PubMed DOI

Traut W., Szczepanowski M., Vitkova M., Opitz C., Marec F., Zrzavy J. (2007). The telomere repeat motif of basal Metazoa. Chromosome Res. 15 (3), 371–382. 10.1007/s10577-007-1132-3 PubMed DOI

Uzlikova M., Fulneckova J., Weisz F., Sykorova E., Nohynkova E., Tumova P. (2017). Characterization of telomeres and telomerase from the single-celled eukaryote Giardia intestinalis. Mol. Biochem. Parasitol. 211, 31–38. 10.1016/j.molbiopara.2016.09.003 PubMed DOI

vanSteensel B., deLange T. (1997). Control of telomere length by the human telomeric protein TRF1. Nature 385 (6618), 740–743. 10.1038/385740a0 PubMed DOI

Vilenchik M. M., Knudson A. G. (2003). Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. U. S. A. 100 (22), 12871–12876. 10.1073/pnas.2135498100 PubMed DOI PMC

Villasante A., Abad J. P., Mendez-Lago M. (2007). Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome. Proc. Natl. Acad. Sci. U. S. A. 104 (25), 10542–10547. 10.1073/pnas.0703808104 PubMed DOI PMC

Visacka K., Hofr C., Willcox S., Necasova I., Pavlouskova J., Sepsiova R., et al. (2012). Synergism of the two Myb domains of Tay1 protein results in high affinity binding to telomeres. J. Biol. Chem. 287 (38), 32206–32215. 10.1074/jbc.M112.385591 PubMed DOI PMC

Vitales D., D'Ambrosio U., Galvez F., Kovarik A., Garcia S. (2017). Third release of the plant rDNA database with updated content and information on telomere composition and sequenced plant genomes. Plant Syst. Evol. 303 (8), 1115–1121. 10.1007/s00606-017-1440-9 DOI

Vitkova M., Kral J., Traut W., Zrzavy J., Marec F. (2005). The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res. 13 (2), 145–156. 10.1007/s10577-005-7721-0 PubMed DOI

Volff J. N., Altenbuchner J. (2000). A new beginning with new ends: linearisation of circular chromosomes during bacterial evolution. FEMS Microbiol. Lett. 186 (2), 143–150. 10.1111/j.1574-6968.2000.tb09095.x PubMed DOI

Wang Y., Susac L., Feigon J. (2019). Structural biology of telomerase. Cold Spring Harb. Perspect. Biol. 11, a032383. 10.1101/cshperspect.a032383 PubMed DOI PMC

Watson J. M., Shippen D. E. (2007). Telomere rapid deletion regulates telomere length in Arabidopsis thaliana. Mol. Cell. Biol. 27 (5), 1706–1715. 10.1128/Mcb.02059-06 PubMed DOI PMC

Watson J. D. (1972). Origin of Concatemeric T7 DNA. Nature-New Biol. 239 (94), 197–201. 10.1038/newbio239197a0 PubMed DOI

Weiss H., Scherthan H. (2002). Aloe spp.–plants with vertebrate-like telomeric sequences. Chromosome Res. 10 (2), 155–164. 10.1023/a:1014905319557 PubMed DOI

Wellinger R. J., Ethier K., Labrecque P., Zakian V. A. (1996). Evidence for a new step in telomere maintenance. Cell 85 (3), 423–433. 10.1016/S0092-8674(00)81120-4 PubMed DOI

Wu J., Okada T., Fukushima T., Tsudzuki T., Sugiura M., Yukawa Y. (2012). A novel hypoxic stress-responsive long non-coding RNA transcribed by RNA polymerase III in Arabidopsis. RNA Biol. 9 (3), 302–313. 10.4161/rna.19101 PubMed DOI

Zhang J. M., Yadav T., Ouyang J., Lan L., Zou L. (2019). Alternative lengthening of telomeres through two distinct break-induced replication pathways. Cell Rep. 26 (4), 955–95+. 10.1016/j.celrep.2018.12.102 PubMed DOI PMC

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