Telomerase RNAs in Land Plants

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2019 Aug 9

PMID 31392988

Citations 40

Authors

Petr Fajkus

Vratislav Peska

Michal Zavodnik

Miloslava Fojtova

Jana Fulneckova

Simon Dobias

Agata Kilar

Martina Dvorackova

Dagmar Zachova

Ivona Necasova

Jason Sims

Eva Sykorova

Jiri Fajkus

Affiliations

Soon will be listed here.

Abstract

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.

Citing Articles

A degenerate telomerase RNA directs telomeric DNA synthesis in lepidopteran insects.

Chou Y, Logeswaran D, Chow C, L Dunn P, Podlevsky J, Liu T Proc Natl Acad Sci U S A. 2025; 122(9):e2424443122.

PMID: 40020192 PMC: 11892584. DOI: 10.1073/pnas.2424443122.

Telomeres: an organized string linking plants and mammals.

Di Pietro E, Burla R, La Torre M, Gonzalez-Garcia M, Dello Ioio R, Saggio I Biol Direct. 2024; 19(1):119.

PMID: 39568075 PMC: 11577926. DOI: 10.1186/s13062-024-00558-y.

Atlas of telomeric repeat diversity in Arabidopsis thaliana.

Tao Y, Xian W, Bao Z, Rabanal F, Movilli A, Lanz C Genome Biol. 2024; 25(1):244.

PMID: 39285474 PMC: 11406999. DOI: 10.1186/s13059-024-03388-3.

Molecular and Evolutionary Analysis of RNA-Protein Interactions in Telomerase Regulation.

Davis J, Chakrabarti K Noncoding RNA. 2024; 10(3).

PMID: 38921833 PMC: 11206666. DOI: 10.3390/ncrna10030036.

Arabidopsis AN3 and OLIGOCELLULA genes link telomere maintenance mechanisms with cell division and expansion control.

Agabekian I, Abdulkina L, Lushnenko A, Young P, Valeeva L, Boskovic O Plant Mol Biol. 2024; 114(3):65.

PMID: 38816532 PMC: 11372841. DOI: 10.1007/s11103-024-01457-6.

References

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. 1999; 260(5):470-4. DOI: 10.1007/s004380050918. View

Cifuentes-Rojas C, Kannan K, Tseng L, Shippen D . Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc Natl Acad Sci U S A. 2010; 108(1):73-78. PMC: 3017190. DOI: 10.1073/pnas.1013021107. View

Adams S, Hartman T, Lim K, Chase M, Bennett M, Leitch I . 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. 2001; 268(1476):1541-6. PMC: 1088775. DOI: 10.1098/rspb.2001.1726. View

Schorova S, Fajkus J, Drabkova L, Honys D, Prochazkova Schrumpfova 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(2):195-212. DOI: 10.1111/tpj.14306. View

Sykorova E, Lim K, Fajkus J, Leitch A . The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)n telomeres. Chromosoma. 2003; 112(4):164-72. DOI: 10.1007/s00412-003-0256-2. View

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(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

Riha K, McKnight T, Griffing L, Shippen D . Living with genome instability: plant responses to telomere dysfunction. Science. 2001; 291(5509):1797-800. DOI: 10.1126/science.1057110. View

Cohn M, McEachern M, Blackburn E . Telomeric sequence diversity within the genus Saccharomyces. Curr Genet. 1998; 33(2):83-91. DOI: 10.1007/s002940050312. View

Samach A, Melamed-Bessudo C, Avivi-Ragolski N, Pietrokovski S, Levy A . Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes. Plant Cell. 2011; 23(12):4266-79. PMC: 3269865. DOI: 10.1105/tpc.111.091744. View

10.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

11.

Musgrove C, Jansson L, Stone M . New perspectives on telomerase RNA structure and function. Wiley Interdiscip Rev RNA. 2017; 9(2). PMC: 5815921. DOI: 10.1002/wrna.1456. View

12.

Richter J, Watson J, Stasnik P, Borowska M, Neuhold J, Berger M . Multiplex mutagenesis of four clustered CrRLK1L with CRISPR/Cas9 exposes their growth regulatory roles in response to metal ions. Sci Rep. 2018; 8(1):12182. PMC: 6093868. DOI: 10.1038/s41598-018-30711-3. View

13.

Oguchi K, Liu H, Tamura K, Takahashi H . Molecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana. FEBS Lett. 1999; 457(3):465-9. DOI: 10.1016/s0014-5793(99)01083-2. View

14.

Podlevsky J, Li Y, Chen J . The functional requirement of two structural domains within telomerase RNA emerged early in eukaryotes. Nucleic Acids Res. 2016; 44(20):9891-9901. PMC: 5175330. DOI: 10.1093/nar/gkw605. View

15.

Greider C, Blackburn E . Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985; 43(2 Pt 1):405-13. DOI: 10.1016/0092-8674(85)90170-9. View

16.

Adams S, Leitch I, Bennett M, Leitch A . Aloe L.--a second plant family without (TTTAGGG)n telomeres. Chromosoma. 2000; 109(3):201-5. DOI: 10.1007/s004120050429. View

17.

Matasci N, Hung L, Yan Z, Carpenter E, Wickett N, Mirarab S . Data access for the 1,000 Plants (1KP) project. Gigascience. 2015; 3:17. PMC: 4306014. DOI: 10.1186/2047-217X-3-17. View

18.

Ruckova E, Friml J, Prochazkova Schrumpfova P, Fajkus J . Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol Biol. 2008; 66(6):637-46. DOI: 10.1007/s11103-008-9295-7. View

19.

Weiss H, Scherthan H . Aloe spp.--plants with vertebrate-like telomeric sequences. Chromosome Res. 2002; 10(2):155-64. DOI: 10.1023/a:1014905319557. View

20.

Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P . Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301(5633):653-7. DOI: 10.1126/science.1086391. View