Skip to main content
SpringerLink
Log in

Telomere Structure, Function, and Maintenance in Plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Telomeres in eukaryotes comprise specific repetitive DNA sequences and binding proteins. Since their absence results in chromosomal end fusions and gene deletions, they are considered critical for genomic stability. In plants, as in yeasts and mammals, telomeres are essential for normal development and differentiation. Despite recent discoveries concerning plant telomeres, many questions remain about the mechanism of telomere homeostasis in plants. In this review, we summarize the roles of telomeres and telomerasebinding proteins in plant biology and explain how the length of a plant telomere is regulated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amiard S, Depeiges A, Allain E, White CI, Gallego ME (2011) Arabidopsis ATM and ATR kinases prevent propagation of genome damage caused by telomere dysfunction. Plant Cell 23: 4254–4265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arat NO, Griffith JD (2012) Human Rap1 interacts directly with telomeric DNA and regulates TRF2 localization at the telomere. J Biol Chem 287:41583–41594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baumann P, Cech TR (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171–1175

    Article  PubMed  CAS  Google Scholar 

  • Blasco MA, Lee H-W, Hande MP, Samper E, Lansdorp PM, De Pinho RA, Geider CW (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25–34

    Article  PubMed  CAS  Google Scholar 

  • Broccoli D, Smogorzewska A, Chong L, De Lange T (1997) Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet 17:231–235

    Article  PubMed  CAS  Google Scholar 

  • Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR (1995) Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 14:4240–4248

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cerone MA, Autexier C, Londono-Vallejo JA, Bacchetti S (2005) A human cell line that maintains telomeres in the absence of telomerase and of key markers of ALT. Oncogene 24:7893–78901

    Article  PubMed  CAS  Google Scholar 

  • Cesare AJ, Quinney N, Willcox S, Subramanian D, Griffith JD (2003) Telomere looping in P. sativum (common garden pea). Plant J 36:271–279

    Article  PubMed  CAS  Google Scholar 

  • Court R, Chapman L, Fairall L, Rhodes D (2005) How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep 6:39–45

    Article  PubMed  CAS  Google Scholar 

  • de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100–2110

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald MS, Riha K, Gao F, Ren S, McKnight TD, Shippen DE (1999) Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci USA 96:14813–14818

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3:87–94

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garvik B, Carson M, Hartwell L (1995) Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol Cell Biol 15:6128–6138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grandin N, Damon C, Charbonneau M (2001) Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J 20:1173–1183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grandin N, Reed SI, Charbonneau M (1997) Stn1, a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev 11:512–527

    Article  PubMed  CAS  Google Scholar 

  • Greider CW (1996) Telomere length regulation. Annu Rev Biochem 65:337–365

    Article  PubMed  CAS  Google Scholar 

  • Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413

    Article  PubMed  CAS  Google Scholar 

  • Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51:887–898

    Article  PubMed  CAS  Google Scholar 

  • Greider CW, Blackburn EH (1989) Atelomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337

    Article  PubMed  CAS  Google Scholar 

  • Griffith JD, Comeau L, Rosenfeld S, Stansel RM, Bianchi A, Moss H, De Lange T (1999) Mammalian telomeres end in a large duplex loop. Cell 97:503–514

    Article  PubMed  CAS  Google Scholar 

  • Harrington L (2005) Making the most of a little: dosage effects in eukaryotic telomere length maintenance. Chromosome Res 13: 493–504

    Article  PubMed  CAS  Google Scholar 

  • Henson JD, Neumann AA, Yeager TR, Reddel RR (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene. 21: 598–610

    Article  PubMed  CAS  Google Scholar 

  • Hong JP, Byun MY, Koo DH, An K, Bang JW, Chung IK, An G, Kim WT (2007) Suppression of RICE TELOMERE BINDING PROTEIN 1 results in severe and gradual developmental defects accompanied by genome instability in rice. Plant cell 6:1770–1781

    Article  CAS  Google Scholar 

  • Hwang MG, Chung IK, Kang BG, Cho MH (2001) Sequence-specific binding property of Arabidopsis thaliana telomeric DNA binding protein 1 (AtTBP1). FEBS Lett 503:35–40

    Article  PubMed  CAS  Google Scholar 

  • Hwang MG, Kim K, Lee WK, Cho MH (2005) AtTBP2 and AtTRP2 in Arabidopsis encode proteins that bind plant telomeric DNA and induce DNA bending in vitro. Mol Gen Genom 273:66–75

    Article  CAS  Google Scholar 

  • Jahn A, Rane G, Paszkowski-Rogacz M, Sayols S, Bluhm A, Han CT, Draškovic I, Londoño-Vallejo JA, Kumar AP, Buchholz F, Butter F, Kappei D (2017) ZBTB48 is both a vertebrate telomerebinding protein and a transcriptional activator. EMBO Rep 2017 18:929–946

    CAS  Google Scholar 

  • Kilian A, Kleinhofs A (1992) Cloning and mapping of telomereassociated sequences from Hordeumvulgare L. Mol Gen Genet 235:153–156

    Article  PubMed  CAS  Google Scholar 

  • Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–2015

    Article  PubMed  CAS  Google Scholar 

  • Kwon C, Chung IK (2004) Interaction of an Arabidopsis RNAbinding protein with plant single-stranded telomeric DNA modulates telomerase activity. J Biol Chem 279:12812–12818

    Article  PubMed  CAS  Google Scholar 

  • Lee H-W, Blasco MA, Gottlieb GJ, Horner JW, Greider CW, De Pinho RA (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392:569–574

    Article  PubMed  CAS  Google Scholar 

  • Lee YW, Kim WT (2010) Tobacco GTBP1, a homolog of human heterogeneous nuclear ribonucleoprotein, protects telomeres from aberrant homologous recombination. Plant Cell 22:2781–2795

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee YW, Kim WT (2013) Telomerase-dependent 3’G-strand overhang maintenance facilitates GTBP1-mediated telomere protection from misplaced homologous recombination. Plant Cell 25: 1329–1342

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee WK, Cho MH (2016) Telomere-binding protein regulates the chromosome ends through the interaction with histone deacetylases in Arabidopsis thaliana. Nucl Acids Res 44:4610–4624

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leehy KA, Lee JR, Song X, Renfrew KB, Shippen, DE (2013) MERISTEM DISORGANIZATION1 encodes TEN1, an essential telomere protein that modulates telomerase processivity in Arabidopsis. Plant Cell 25:1343–1354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li JS, Miralles Fusté J, Simavorian T, Bartocci C, Tsai J, Karlseder J, Lazzerini Denchi E (2017) TZAP: A telomere-associated protein involved in telomere length control. Science 355:638–641

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lingner J, Cooper JP, Cech TR (1995) Telomerase and DNA end replication: no longer a lagging strand problem? Science 269: 1533–1534

    Article  PubMed  CAS  Google Scholar 

  • Muntoni A, Reddel RR (2005) The first molecular details of ALT in human tumor cells. Hum Mol Genet 14:191–196

    Article  Google Scholar 

  • Nugent CI, Hughes TR, Lue NF, Lundblad V (1996) Cdc13p: A single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274:249–252

    Article  PubMed  CAS  Google Scholar 

  • Peska V, Fajkus P, Fojtova M, Dvorackova M, Hapala J, Dvoracek V, Polanská P, Leitch AR, Sýkorová E, Fajkus J (2015) Characterization of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J 82:644–654

    Article  PubMed  CAS  Google Scholar 

  • Price CM, Boltz KA, Chaiken MF, Stewart JA, Beilstein MA, Shippen DE (2010) Evolution of CST function in telomere maintenance. Cell Cycle 9:3157–3165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Richard EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53:127–136

    Article  Google Scholar 

  • Riha K, McKnight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291:1797–1800

    Article  PubMed  CAS  Google Scholar 

  • Rossignol P, Collier S, Bush M, Shaw P, Doonan JH (2007) Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J Cell Sci 120:3678–3687

    Article  PubMed  CAS  Google Scholar 

  • Rucková E, Friml J, Procházková Schrumpfová P, Fajkus J (2008) Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol Biol 66:637–646

    Article  PubMed  CAS  Google Scholar 

  • Schrumpfová PP, Vychodilová I, Dvorácková M, Majerská J, Dokládal L, Schorová S, Fajkus J (2014) Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J 77:770–781

    Article  PubMed  CAS  Google Scholar 

  • Sfeir A (2012) Telomeres at a glance. J Cell Sci 125:4173–4178

    Article  PubMed  CAS  Google Scholar 

  • Sfeir A, De Lange T (2012) Removal of shelterin reveals the telomere end-protection problem. Science 336:593–597

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song X, Leehy K, Warrington RT, Lamb JC, Surovtseva YV, Shippen DE (2008) STN1 protects chromosome ends in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:19815–19820

    Article  PubMed  PubMed Central  Google Scholar 

  • Surovtseva YV, Shakirov EV, Vespa L, Osbun N, Song X, Shippen DE (2007) Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J 26: 3653–3661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Surovtseva YV, Churikov D, Boltz KA, Song X, Lamb JC, Warrington R, Leehy K, Heacock M, Price CM, Shippen DE (2009) Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol Cell 36:207–218

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takai KK, Kibe T, Donigian JR, Frescas D, De Lange T (2011) Telomere protection by TPP1/POT1 requires tethering to TIN2. Mol Cell 44:647–659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tran DT, Cao HX, Jovtchev G, Neumann P, Novak P, Fojtova M, Vu GT, Macas J, Fajkus J, Schubert I, Fuchs J (2015) Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J 84:1087–1099

    Article  PubMed  CAS  Google Scholar 

  • Vespa L, Warrington RT, Mokros P, Siroky J, Shippen DE (2007) ATM regulates the length of individual telomere tracts in Arabidopsis. Proc Natl Acad Sci USA 104:18145–18150

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu KS, Tanksley SD (1993) Genetic and physical mapping of telomeres and macrosatellites of rice. Plant Mol Biol 22:861–872

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Zakian VA (2011) The telomeric Cdc13 protein interacts directly with the telomerase subunit Est1 to bring it to telomeric DNA ends in vitro. Proc Natl Acad Sci USA 108:20362–20369

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang SW, Kim DH, Lee JJ, Chun YJ, Lee JH, Kim YJ, Chung IK, Kim WT (2003) Expression of the telomeric repeat binding factor gene NgTRF1 is closely coordinated with the cell division program in tobacco BY-2 suspension culture cells. J Biol Chem 278:21395–21407

    Article  PubMed  CAS  Google Scholar 

  • Yang SW, Kim SK, Kim WT (2004) Perturbation of NgTRF1 expression induces apoptosis-like cell death in tobacco BY-2 cells and implicates NgTRF1 in the control of telomere length and stability. Plant cell 16:3370–3385

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoo HH, Kwon C, Lee MM, Chung IK (2007) Single-stranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J 49:442–451

    Article  PubMed  CAS  Google Scholar 

  • Yoo HH, Kwon C, Lee MM, Chung IK (2010) Characterization of an Arabidopsis single-stranded telomere binding protein. JNBT 7: 46–50

    Google Scholar 

  • Yu EY, Kim SE, Kim JH, Ko JH, Cho MH, Chung IK (2000) Sequence-specific DNA Recognition by the Myb-like Domain of Plant Telomeric Protein RTBP1. J Biol Chem 275:24208–24214

    Article  PubMed  CAS  Google Scholar 

  • Zakian VA (1995) Telomeres: beginning to understand the end. Science 270:1601–1607

    Article  PubMed  CAS  Google Scholar 

  • Zellinger B, Akimcheva S, Puizina J, Schirato M, Riha K (2007) Ku suppresses formation of telomeric circles and alternative telomere lengthening in Arabidopsis. Mol Cell 27:163–169

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Systems Biology, College of Life Science, Yonsei University, Seoul, 03722, Korea

    Mi Kyung Kim & Woo Taek Kim

Authors
  1. Mi Kyung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Woo Taek Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mi Kyung Kim or Woo Taek Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, M.K., Kim, W.T. Telomere Structure, Function, and Maintenance in Plants. J. Plant Biol. 61, 131–136 (2018). https://doi.org/10.1007/s12374-018-0082-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-018-0082-y

Keywords

Search

Navigation