Telomerase RNAs in land plants

. 2019 Oct 10 ; 47 (18) : 9842-9856.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31392988

To elucidate the molecular nature of evolutionary changes of telomeres in the plant order Asparagales, we aimed to characterize telomerase RNA subunits (TRs) in these plants. The unusually long telomere repeat unit in Allium plants (12 nt) allowed us to identify TRs in transcriptomic data of representative species of the Allium genus. Orthologous TRs were then identified in Asparagales plants harbouring telomere DNA composed of TTAGGG (human type) or TTTAGGG (Arabidopsis-type) repeats. Further, we identified TRs across the land plant phylogeny, including common model plants, crop plants, and plants with unusual telomeres. Several lines of functional testing demonstrate the templating telomerase function of the identified TRs and disprove a functionality of the only previously reported plant telomerase RNA in Arabidopsis thaliana. Importantly, our results change the existing paradigm in plant telomere biology which has been based on the existence of a relatively conserved telomerase reverse transcriptase subunit (TERT) associating with highly divergent TRs even between closely related plant taxa. The finding of a monophyletic origin of genuine TRs across land plants opens the possibility to identify TRs directly in transcriptomic or genomic data and/or predict telomere sequences synthesized according to the respective TR template region.

Zobrazit více v PubMed

Greider C.W., Blackburn E.H.. Identification of a specific telomere terminal transferase-activity in tetrahymena extracts. Cell. 1985; 43:405–413. PubMed

Greider C.W., Blackburn E.H.. A telomeric sequence in the Rna of tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989; 337:331–337. PubMed

Nguyen T.H.D., Tam J., Wu R.A., Greber B.J., Toso D., Nogales E., Collins K.. Cryo-EM structure of substrate-bound human telomerase holoenzyme. Nature. 2018; 557:190–195. PubMed PMC

Jiang J.S., Wang Y.Q., Susac L., Chan H., Basu R., Zhou Z.H., Feigon J.. Structure of telomerase with telomeric DNA. Cell. 2018; 173:1179–1190. PubMed PMC

Egan E.D., Collins K.. Biogenesis of telomerase ribonucleoproteins. RNA. 2012; 18:1747–1759. PubMed PMC

Chan H., Wang Y.Q., Feigon J.. Progress in human and tetrahymena telomerase structure determination. Annu. Rev. Biophys. 2017; 46:199–225. PubMed PMC

Musgrove C., Jansson L.I., Stone M.D.. New perspectives on telomerase RNA structure and function. Wiley Interdiscipl. Rev.-RNA. 2018; 9:e1456. PubMed PMC

Meyne J., Ratliff R.L., Moyzis R.K.. Conservation of the human telomere sequence (Ttaggg)N among vertebrates. Proc. Natl. Acad. Sci. U.S.A. 1989; 86:7049–7053. PubMed PMC

Cohn M., McEachern M.J., Blackburn E.H.. Telomeric sequence diversity within the genus Saccharomyces. Curr. Genet. 1998; 33:83–91. PubMed

Gunisova S., Elboher E., Nosek J., Gorkovoy V., Brown Y., Lucier J.F., Laterreur N., Wellinger R.J., Tzfati Y., Tomaska L.. Identification and comparative analysis of telomerase RNAs from Candida species reveal conservation of functional elements. RNA. 2009; 15:546–559. PubMed PMC

Fulneckova J., Hasikova T., Fajkus J., Lukesova A., Elias M., Sykorova E.. Dynamic evolution of telomeric sequences in the green algal order chlamydomonadales. Genome Biol. Evol. 2012; 4:248–264. PubMed PMC

Fulneckova J., Sevcikova T., Fajkus J., Lukesova A., Lukes M., Vlcek C., Lang B.F., Kim E., Elias M., Sykorova E.. A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol. Evol. 2013; 5:468–483. PubMed PMC

Fajkus J., Sykorova E., Leitch A.R.. Telomeres in evolution and evolution of telomeres. Chromosome Res. 2005; 13:469–479. PubMed

Richards E.J., Ausubel F.M.. Isolation of a higher eukaryotic telomere from arabidopsis thaliana. Cell. 1988; 53:127–136. PubMed

Fuchs J., Brandes A., Schubert I.. Telomere sequence localization and karyotype evolution in higher-plants. Plant Syst. Evol. 1995; 196:227–241.

Pich U., Fuchs J., Schubert I.. How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences. Chromosome Res. 1996; 4:207–213. PubMed

Adams S.P., Hartman T.P.V., Lim K.Y., Chase M.W., Bennett M.D., Leitch I.J., Leitch A.R.. Loss and recovery of Arabidopsis-type telomere repeat sequences 5’-(TTTAGGG)(n)-3’ in the evolution of a major radiation of flowering plants. Proc. Natl. Acad. Sci. U.S.A. 2001; 268:1541–1546. PubMed PMC

Adams S.P., Leitch I.J., Bennett M.D., Leitch A.R.. Aloe L. - a second plant family without (TTTAGGG)(n) telomeres. Chromosoma. 2000; 109:201–205. PubMed

Weiss H., Scherthan H.. Aloe spp.–plants with vertebrate-like telomeric sequences. Chromosome Res. 2002; 10:155–164. PubMed

Sykorova E., Lim K.Y., Kunicka Z., Chase M.W., Bennett M.D., Fajkus J., Leitch A.R.. Telomere variability in the monocotyledonous plant order Asparagales. Proc. Roy.Soc. B-Biol. Sci. 2003; 270:1893–1904. PubMed PMC

Sykorova E., Lim K.Y., Fajkus J., Leitch A.R.. The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)(n) telomeres. Chromosoma. 2003; 112:164–172. PubMed

Sykorova E., Lim K.Y., Chase M.W., Knapp S., Leitch I.J., Leitch A.R., Fajkus J.. The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J. 2003; 34:283–291. PubMed

Tran T.D., Cao H.X., Jovtchev G., Neumann P., Novak P., Fojtova M., Vu G.T.H., Macas J., Fajkus J., Schubert I. et al. .. Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J. 2015; 84:1087–1099. PubMed

Sykorova E., Fajkus J., Meznikova M., Lim K.Y., Neplechova K., Blattner F.R., Chase M.W., Leitch A.R.. Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am. J. Bot. 2006; 93:814–823. PubMed

Fajkus P., Peska V., Sitova Z., Fulneckova J., Dvorackova M., Gogela R., Sykorova E., Hapala J., Fajkus J.. Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG)(n) is synthesized by telomerase. Plant J. 2016; 85:337–347. PubMed

Chakrabarti K., Pearson M., Grate L., Sterne-Weiler T., Deans J., Donohue J.P., Ares M.. Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA. 2007; 13:1923–1939. PubMed PMC

Podlevsky J.D., Chen J.J.L.. Evolutionary perspectives of telomerase RNA structure and function. Rna Biol. 2016; 13:720–732. PubMed PMC

Cifuentes-Rojas C., Kannan K., Tseng L., Shippen D.E.. Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl. Acad. Sci. U.S.A. 2011; 108:73–78. PubMed PMC

Sykorova E., Leitch A.R., Fajkus J.. Asparagales telomerases which synthesize the human type of telomeres. Plant Mol. Biol. 2006; 60:633–646. PubMed

Wu J., Okada T., Fukushima T., Tsudzuki T., Sugiura M., Yukawa Y.. A novel hypoxic stress-responsive long non-coding RNA transcribed by RNA polymerase III in Arabidopsis. RNA Biol. 2012; 9:302–313. PubMed

Brunaud V., Balzergue S., Dubreucq B., Aubourg S., Samson F., Chauvin S., Bechtold N., Cruaud C., DeRose R., Pelletier G. et al. .. T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep. 2002; 3:1152–1157. PubMed PMC

Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H.M., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R. et al. .. Genome-wide Insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301:653–657. PubMed

Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q. et al. .. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011; 29:644–652. PubMed PMC

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J.. Basic local alignment search tool. J. Mol. Biol. 1990; 215:403–410. PubMed

Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J.. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25:3389–3402. PubMed PMC

Zhang Z., Schwartz S., Wagner L., Miller W.. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 2000; 7:203–214. PubMed

Wickett N.J., Mirarab S., Nguyen N., Warnow T., Carpenter E., Matasci N., Ayyampalayam S., Barker M.S., Burleigh J.G., Gitzendanner M.A. et al. .. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl. Acad. Sci. U.S.A. 2014; 111:E4859–E4868. PubMed PMC

Xie Y.L., Wu G.X., Tang J.B., Luo R.B., Patterson J., Liu S.L., Huang W.H., He G.Z., Gu S.C., Li S.K. et al. .. SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads. Bioinformatics. 2014; 30:1660–1666. PubMed

Matasci N., Hung L.H., Yan Z.X., Carpenter E.J., Wickett N.J., Mirarab S., Nguyen N., Warnow T., Ayyampalayam S., Barker M. et al. .. Data access for the 1,000 Plants (1KP) project. Gigascience. 2014; 3:17. PubMed PMC

Johnson M.T.J., Carpenter E.J., Tian Z.J., Bruskiewich R., Burris J.N., Carrigan C.T., Chase M.W., Clarke N.D., Covshoff S., dePamphilis C.W. et al. .. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One. 2012; 7:e50226. PubMed PMC

Katoh K., Misawa K., Kuma K., Miyata T.. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30:3059–3066. PubMed PMC

Fitzgerald M.S., McKnight T.D., Shippen D.E.. Characterization and developmental patterns of telomerase expression in plants. Proc. Natl. Acad. Sci. U.S.A. 1996; 93:14422–14427. PubMed PMC

Fajkus J., Fulneckova J., Hulanova M., Berkova K., Riha K., Matyasek R.. Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol. Gen. Genet. 1998; 260:470–474. PubMed

Pfaffl M.W. Bustin SA. A-Z of Quantitative PCR. 2004; La Jolla: International University Line; 87–112.

Sykorova E., Fulneckova J., Mokros P., Fajkus J., Fojtova M., Peska V.. Three TERT genes in Nicotiana tabacum. Chromosome Res. 2012; 20:381–394. PubMed

Oguchi K., Liu H.T., Tamura K., Takahashi H.. Molecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana. FEBS Lett. 1999; 457:465–469. PubMed

Shimada T.L., Shimada T., Hara-Nishimura I.. A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 2010; 61:519–528. PubMed

Richter J., Watson J.M., Stasnik P., Borowska M., Neuhold J., Berger M., Stolt-Bergner P., Schoft V., Hauser M.T.. Multiplex mutagenesis of four clustered CrRLK1L with CRISPR/Cas9 exposes their growth regulatory roles in response to metal ions. Sci. Rep.-UK. 2018; 8:12182. PubMed PMC

Ruckova E., Friml J., Schrumpfova P.P., Fajkus J.. Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol. Biol. 2008; 66:637–646. PubMed

Lyčka M., Hapala J., Fajkus P., Fojtová M., Fajkus J., Peška V.. Foret F, Křenková J, Drobníková I, Klepárník K, Přikryl J. CECE 2018 - 15th International Interdisciplinary Meeting on Bioanalysis. 2018; Brno: Institute of Analytical Chemistry of the CAS, v. v. i; 82–86.

Regad F., Lebas M., Lescure B.. Interstitial telomeric repeats within the arabidopsis-thaliana genome. J. Mol. Biol. 1994; 239:163–169. PubMed

Tremousaygue D., Manevski A., Bardet C., Lescure N., Lescure B.. Plant interstitial telomere motifs participate in the control of gene expression in root meristems. Plant J. 1999; 20:553–561. PubMed

Peska V., Fajkus P., Fojtova M., Dvorackova M., Hapala J., Dvoracek V., Polanska P., Leitch A.R., Sykorova E., Fajkus J.. Characterisation of an unusual telomere motif (TTTTTTAGGG)(n) in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J. 2015; 82:644–654. PubMed

Schrumpfova P.P., Fojtova M., Fajkus J.. Telomeres in plants and humans: not so different, not so similar. Cells. 2019; 8:E58. PubMed PMC

Schorova S., Fajkus J., Zaveska Drabkova L., Honys D., Schrumpfova P.P.. The plant Pontin and Reptin homologues, RuvBL1 and RuvBL2a, colocalize with TERT and TRB proteins in vivo, and participate in telomerase biogenesis. Plant J. 2019; 98:195–212. PubMed

Fajkus J., Kovarik A., Kralovics R.. Telomerase activity in plant cells. FEBS Lett. 1996; 391:307–309. PubMed

Beilstein M.A., Brinegar A.E., Shippen D.E.. Evolution of the Arabidopsis telomerase RNA. Front. Genet. 2012; 3:188. PubMed PMC

Ogrocka A., Sykorova E., Fajkus J., Fojtova M.. Developmental silencing of the AtTERT gene is associated with increased H3K27me3 loading and maintenance of its euchromatic environment. J. Exp. Bot. 2012; 63:4233–4241. PubMed PMC

Riha K., McKnight T.D., Griffing L.R., Shippen D.E.. Living with genome instability: Plant responses to telomere dysfunction. Science. 2001; 291:1797–1800. PubMed

Fojtova M., Peska V., Dobsakova Z., Mozgova I., Fajkus J., Sykorova E.. Molecular analysis of T-DNA insertion mutants identified putative regulatory elements in the AtTERT gene. J. Exp. Bot. 2011; 62:5531–5545. PubMed PMC

Crhak T., Zachova D., Fojtova M., Sykorova E.. The region upstream of the telomerase reverse transcriptase gene is essential for in planta telomerase complementation. Plant Sci. 2019; 281:41–51. PubMed

Derelle R., Torruella G., Klimes V., Brinkmann H., Kim E., Vlcek C., Lang B.F., Elias M.. Bacterial proteins pinpoint a single eukaryotic root. Proc. Natl. Acad. Sci. U.S.A. 2015; 112:E693–E699. PubMed PMC

He D., Fiz-Palacios O., Fu C.J., Fehling J., Tsai C.C., Baldauf S.L.. An alternative root for the eukaryote tree of life. Curr. Biol. 2014; 24:465–470. PubMed

Podlevsky J.D., Li Y., Chen J.J.L.. The functional requirement of two structural domains within telomerase RNA emerged early in eukaryotes. Nucleic Acids Res. 2016; 44:9891–9901. PubMed PMC

Orum H., Nielsen H., Engberg J.. Structural organization of the genes encoding the small nuclear Rnas U1 to U6 of tetrahymena-thermophila is very similar to that of plant small Nuclear-Rna genes. J. Mol. Biol. 1992; 227:114–121. PubMed

Koonin E.V. The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate. Biol. Direct. 2006; 1:22. PubMed PMC

Samach A., Melamed-Bessudo C., Avivi-Ragolski N., Pietrokovski S., Levy A.A.. Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-Like genes. Plant Cell. 2011; 23:4266–4279. PubMed PMC

Xu H.T., Nelson A.D.L., Shippen D.E.. A transposable element within the Non-canonical telomerase RNA of arabidopsis thaliana modulates telomerase in response to DNA damage. PLos Genet. 2015; 11:e1005281. PubMed PMC

Wu J., Liu C.X., Liu Z.G., Li S., Li D.D., Liu S.Y., Huang X.Q., Liu S.K., Yukawa Y.. Pol III-dependent cabbage BoNR8 long ncRNA affects seed germination and growth in Arabidopsis. Plant Cell Physiol. 2019; 60:421–435. PubMed

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Characterisation of the Arabidopsis thaliana telomerase TERT-TR complex

. 2024 May 14 ; 114 (3) : 56. [epub] 20240514

Optimizing ChIRP-MS for Comprehensive Profiling of RNA-Protein Interactions in Arabidopsis thaliana: A Telomerase RNA Case Study

. 2024 Mar 15 ; 13 (6) : . [epub] 20240315

TeloBase: a community-curated database of telomere sequences across the tree of life

. 2024 Jan 05 ; 52 (D1) : D311-D321.

Identification of the Sequence and the Length of Telomere DNA

Telomerase RNA in Hymenoptera (Insecta) switched to plant/ciliate-like biogenesis

. 2023 Jan 11 ; 51 (1) : 420-433.

GERONIMO: A tool for systematic retrieval of structural RNAs in a broad evolutionary context

. 2022 Dec 28 ; 12 () : . [epub] 20231017

Telomeres and Their Neighbors

. 2022 Sep 16 ; 13 (9) : . [epub] 20220916

Telomerase Interaction Partners-Insight from Plants

. 2021 Dec 29 ; 23 (1) : . [epub] 20211229

Editorial: Telomere Flexibility and Versatility: A Role of Telomeres in Adaptive Potential

. 2021 ; 12 () : 771938. [epub] 20211004

Evolution of plant telomerase RNAs: farther to the past, deeper to the roots

. 2021 Jul 21 ; 49 (13) : 7680-7694.

Extraordinary diversity of telomeres, telomerase RNAs and their template regions in Saccharomycetaceae

. 2021 Jun 17 ; 11 (1) : 12784. [epub] 20210617

G-Quadruplex Structures Colocalize with Transcription Factories and Nuclear Speckles Surrounded by Acetylated and Dimethylated Histones H3

. 2021 Feb 17 ; 22 (4) : . [epub] 20210217

Origin and Fates of TERT Gene Copies in Polyploid Plants

. 2021 Feb 11 ; 22 (4) : . [epub] 20210211

Composition and Function of Telomerase-A Polymerase Associated with the Origin of Eukaryotes

. 2020 Oct 08 ; 10 (10) : . [epub] 20201008

Origin, Diversity, and Evolution of Telomere Sequences in Plants

. 2020 ; 11 () : 117. [epub] 20200221

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...