As chromatin structures, telomeres undergo epigenetic regulation of their maintenance and function. In plants, these processes are likely of a higher complexity than in animals or yeasts, as exemplified by methylation of cytosines in plant telomeric DNA or reversible developmental regulation of plant telomerase. We highlight the dual role of telomeres from the epigenetic point of view: (i) as chromatin structures that are the subject of epigenetic regulation (e.g. DNA and histone modifications), and (ii) as chromosome domains acting themselves as epigenetic regulatory elements (e.g. in the telomere position effect). Possibly, some molecular tools (e.g. telomeric transcripts) are common to both these aspects of telomere epigenetics. We further discuss the justification for the classical textbook view of telomeres as heterochromatic structures.

1.
Adams SP, Hartman TP, Lim KY, Chase MW, Bennett MD, et al: 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 268:1541-1546 (2001).
[PubMed]
2.
Arnoult N, Van Beneden A, Decottignies A: Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1α. Nat Struct Mol Biol 19:948-956 (2012).
[PubMed]
3.
Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J: Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798-801 (2007).
[PubMed]
4.
Baur JA, Zou Y, Shay JW, Wright WE: Telomere position effect in human cells. Science 292:2075-2077 (2001).
[PubMed]
5.
Benetti R, García-Cao M, Blasco MA: Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet 39:243-250 (2007).
[PubMed]
6.
Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE: Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS One 3:e3156 (2008).
[PubMed]
7.
Blasco MA: The epigenetic regulation of mammalian telomeres. Nat Rev Genet 8:299-309 (2007).
[PubMed]
8.
Bojang P Jr, Ramos KS: The promise and failures of epigenetic therapies for cancer treatment. Cancer Treat Rev 40:153-169 (2013).
[PubMed]
9.
Canudas S, Houghtaling BR, Bhanot M, Sasa G, Savage SA, et al: A role for heterochromatin protein 1γ at human telomeres. Genes Dev 25:1807-1819 (2011).
[PubMed]
10.
Cao F, Li X, Hiew S, Brady H, Liu Y, Dou Y: Dicer independent small RNAs associate with telomeric heterochromatin. RNA 15:1274-1281 (2009).
[PubMed]
11.
Cohanim AB, Kashi Y, Trifonov EN: Three sequence rules for chromatin. J Biomol Struct Dyn 23:559-566 (2006).
[PubMed]
12.
Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, et al: Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215-219 (2008).
[PubMed]
13.
Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC: An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543-553 (2000).
[PubMed]
14.
de Lange T: Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100-2110 (2005).
[PubMed]
15.
de Lange T: How telomeres solve the end-protection problem. Science 326:948-952 (2009).
[PubMed]
16.
Fajkus J, Trifonov EN: Columnar packing of telomeric nucleosomes. Biochem Biophys Res Commun 280:961-963 (2001).
[PubMed]
17.
Fajkus J, Kovarik A, Kralovics R, Bezdek M: Organization of telomeric and subtelomeric chromatin in the higher-plant Nicotiana tabacum. Mol Gen Genet 247:633-638 (1995a).
[PubMed]
18.
Fajkus J, Kralovics R, Kovarik A, Fajkusova L: The telomeric sequence is directly attached to the HRS60 subtelomeric tandem repeat in tobacco chromosomes. FEBS Lett 364:33-35 (1995b).
[PubMed]
19.
Fajkus J, Kovarik A, Kralovics R: Telomerase activity in plant cells. FEBS Lett 391:307-309 (1996).
[PubMed]
20.
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 260:470-474 (1998).
[PubMed]
21.
Farnung BO, Brun CM, Arora R, Lorenzi LE, Azzalin CM: Telomerase efficiently elongates highly transcribing telomeres in human cancer cells. PLoS One 7:e35714 (2012).
[PubMed]
22.
Ferguson BM, Fangman WL: A position effect on the time of replication origin activation in yeast. Cell 68:333-339 (1992).
[PubMed]
23.
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC: Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811 (1998).
[PubMed]
24.
Fransz P, ten Hoopen R, Tessadori F: Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14:71-82 (2006).
[PubMed]
25.
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 4:248-264 (2012).
[PubMed]
26.
Fulneckova J, Sevcikova T, Fajkus J, Lukesova A, Lukes M, et al: A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5:468-483 (2013).
[PubMed]
27.
Galati A, Rossetti L, Pisano S, Chapman L, Rhodes D, et al: The human telomeric protein TRF1 specifically recognizes nucleosomal binding sites and alters nucleosome structure. J Mol Biol 360:377-385 (2006).
[PubMed]
28.
Galati A, Magdinier F, Colasanti V, Bauwens S, Pinte S, et al: TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS One 7:e34386 (2012).
[PubMed]
29.
Gamez-Arjona FM, Lopez-Lopez C, Vaquero-Sedas MI, Vega-Palas MA: On the organization of the nucleosomes associated with telomeric sequences. Biochim Biophys Acta 1803:1058-1061 (2010).
[PubMed]
30.
Gottschling DE, Aparicio OM, Billington BL, Zakian VA: Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751-762 (1990).
[PubMed]
31.
Henderson IR, Deleris A, Wong W, Zhong X, Chin HG, et al: The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 6:e1001182 (2010).
[PubMed]
32.
Henikoff S: Position effect and related phenomena. Curr Opin Genet Dev 2:907-912 (1992).
[PubMed]
33.
Herr AJ, Jensen MB, Dalmay T, Baulcombe DC: RNA polymerase IV directs silencing of endogenous DNA. Science 308:118-120 (2005).
[PubMed]
34.
Iglesias VA, Moscone EA, Papp I, Neuhuber F, Michalowski S, et al: Molecular and cytogenetic analyses of stably and unstably expressed transgene loci in tobacco. Plant Cell 9:1251-1264 (1997).
[PubMed]
35.
Jaske K, Mokros P, Mozgova I, Fojtova M, Fajkus J: A telomerase-independent component of telomere loss in chromatin assembly factor 1 mutants of Arabidopsis thaliana. Chromosoma 122:285-293 (2013).
[PubMed]
36.
Jones AL, Thomas CL, Maule AJ: De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J 17:6385-6393 (1998).
[PubMed]
37.
Jones TI, Chen JCJ, Rahimov F, Homma S, Arashiro P, et al: Facioscapulohumeral muscular dystrophy family studies of DUX4 expression: evidence for disease modifiers and a quantitative model of pathogenesis. Hum Mol Genet 21:4419-4430 (2012).
[PubMed]
38.
Kawasaki H, Taira K: Induction of DNA methylation and gene silencing by short interfering RNAs in human cells. Nature 431:211-217 (2004).
[PubMed]
39.
Koering CE, Pollice A, Zibella MP, Bauwens S, Puisieux A, et al: Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep 3:1055-1061 (2002).
[PubMed]
40.
Lee J, Jang SJ, Benoit N, Hoque MO, Califano JA, et al: Presence of 5-methylcytosine in CpNpG trinucleotides in the human genome. Genomics 96:67-72 (2010).
[PubMed]
41.
Lejnine S, Makarov VL, Langmore JP: Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc Natl Acad Sci USA 92:2393-2397 (1995).
[PubMed]
42.
Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al: Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315-322 (2009).
[PubMed]
43.
Lou ZJ, Wei J, Riethman H, Baur JA, Voglauer R, et al: Telomere length regulates ISG15 expression in human cells. Aging 1:608-621 (2009).
[PubMed]
44.
Maida Y, Yasukawa M, Furuuchi M, Lassmann T, Possemato R, et al: An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 461:230-235 (2009).
[PubMed]
45.
Majerova E, Fojtova M, Mandakova T, Fajkus J: Methylation of plant telomeric DNA: What do the results say? (author reply). Plant Mol Biol 77:533-536 (2011a).
46.
Majerova E, Fojtova M, Mozgova I, Bittova M, Fajkus J: Hypomethylating drugs efficiently decrease cytosine methylation in telomeric DNA and activate telomerase without affecting telomere lengths in tobacco cells. Plant Mol Biol 77:371-380 (2011b).
[PubMed]
47.
Makarov VL, Lejnine S, Bedoyan J, Langmore JP: Nucleosomal organization of telomere-specific chromatin in rat. Cell 73:775-787 (1993).
[PubMed]
48.
Mathieu O, Reinders J, Caikovski M, Smathajitt C, Paszkowski J: Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130:851-862 (2007).
[PubMed]
49.
Mette MF, Aufsatz W, van der Winden J, Matzke MA, Matzke AJ: Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J 19:5194-5201 (2000).
[PubMed]
50.
Morcillo G, Barettino D, Carmona MJ, Carretero MT, Diez JL: Telomeric DNA sequences differentially activated by heat shock in two Chironomus subspecies. Chromosoma 96:139-144 (1988).
[PubMed]
51.
Morris KV, Chan SW, Jacobsen SE, Looney DJ: Small interfering RNA-induced transcriptional gene silencing in human cells. Science 305:1289-1292 (2004).
[PubMed]
52.
Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, et al: ArabidopsisSGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533-542 (2000).
[PubMed]
53.
Mozgova I, Mokros P, Fajkus J: Dysfunction of chromatin assembly factor 1 induces shortening of telomeres and loss of 45S rDNA in Arabidopsis thaliana. Plant Cell 22:2768-2780 (2010).
[PubMed]
54.
Nandakumar J, Bell CF, Weidenfeld I, Zaug AJ, Leinwand LA, Cech TR: The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity. Nature 492:285-289 (2012).
[PubMed]
55.
Napoli C, Lemieux C, Jorgensen R: Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-289 (1990).
[PubMed]
56.
Nebbioso A, Carafa V, Benedetti R, Altucci L: Trials with ‘epigenetic' drugs: an update. Mol Oncol 6:657-682 (2012).
[PubMed]
57.
Nikitina T, Woodcock CL: Closed chromatin loops at the ends of chromosomes. J Cell Biol 166:161-165 (2004).
[PubMed]
58.
Ogrocka A, Polanska P, Majerova E, Janeba Z, Fajkus J, Fojtova M: Compromised telomere maintenance in hypomethylated Arabidopsis thaliana plants. Nucleic Acids Res 42:2919-2931 (2014).
[PubMed]
59.
O'Sullivan RJ, Kubicek S, Schreiber SL, Karlseder J: Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat Struct Mol Biol 17:1218-1225 (2010).
[PubMed]
60.
Ottaviani A, Rival-Gervier S, Boussouar A, Foerster AM, Rondier D, et al: The D4Z4 macrosatellite repeat acts as a CTCF and A-type lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet 5:e1000394 (2009).
[PubMed]
61.
Ottaviani A, Schluth-Bolard C, Gilson E, Magdinier F: D4Z4 as a prototype of CTCF and lamins-dependent insulator in human cells. Nucleus 1:30-36 (2010).
[PubMed]
62.
Palm W, de Lange T: How shelterin protects mammalian telomeres. Annu Rev Genet 42:301-334 (2008).
[PubMed]
63.
Pedram M, Sprung CN, Gao Q, Lo AWI, Reynolds GE, Murnane JP: Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol Cell Biol 26:1865-1878 (2006).
[PubMed]
64.
Peska V, Prochazkova Schrumpfova P, Fajkus J: Using the telobox to search for plant telomere binding proteins. Curr Protein Pept Sci 12:75-83 (2011).
[PubMed]
65.
Pfeiffer V, Lingner J: TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genet 8:e1002747 (2012).
[PubMed]
66.
Pich U, Fuchs J, Schubert I: How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4:207-213 (1996).
[PubMed]
67.
Polanska E, Dobsakova Z, Dvorackova M, Fajkus J, Stros M: HMGB1 gene knockout in mouse embryonic fibroblasts results in reduced telomerase activity and telomere dysfunction. Chromosoma 121:419-431 (2012).
[PubMed]
68.
Postepska-Igielska A, Krunic D, Schmitt N, Greulich-Bode KM, Boukamp P, Grummt I: The chromatin remodelling complex NoRC safeguards genome stability by heterochromatin formation at telomeres and centromeres. EMBO Rep 14:704-710 (2013).
[PubMed]
69.
Prochazkova Schrumpfova P, Fojtova M, Mokros P, Grasser KD, Fajkus J: Role of HMGB proteins in chromatin dynamics and telomere maintenance in Arabidopsis thaliana. Curr Protein Pept Sci 12:105-111 (2011).
[PubMed]
70.
Prochazkova Schrumpfova P, Vychodilova I, Dvorackova M, Majerska J, Dokladal L, et al: Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J 77:770-781 (2014).
[PubMed]
71.
Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R: Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 97:5237-5242 (2000).
[PubMed]
72.
Redon S, Reichenbach P, Lingner J: The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res 38:5797-5806 (2010).
[PubMed]
73.
Redon S, Zemp I, Lingner J: A three-state model for the regulation of telomerase by TERRA and hnRNPA1. Nucleic Acids Res 41:9117-9128 (2013).
[PubMed]
74.
Riha K, Fajkus J, Siroky J, Vyskot B: Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691-1698 (1998).
[PubMed]
75.
Roberts AR, Blewitt ME, Youngson NA, Whitelaw E, Chong S: Reduced dosage of the modifiers of epigenetic reprogramming Dnmt1, Dnmt3L, SmcHD1 and Foxo3a has no detectable effect on mouse telomere length in vivo. Chromosoma 120:377-385 (2011).
[PubMed]
76.
Roberts AR, Huang E, Jones L, Daxinger L, Chong S, Whitelaw E: Non-telomeric epigenetic and genetic changes are associated with the inheritance of shorter telomeres in mice. Chromosoma 122:541-554 (2013).
[PubMed]
77.
Rosenfeld JA, Wang Z, Schones DE, Zhao K, DeSalle R, Zhang MQ: Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics 10:143 (2009).
[PubMed]
78.
Rossetti L, Cacchione S, Fua M, Savino M: Nucleosome assembly on telomeric sequences. Biochemistry 37:6727-6737 (1998).
[PubMed]
79.
Rotkova G, Sykorova E, Fajkus J: Protect and regulate: recent findings on plant POT1-like proteins. Biol Plantarum 53:1-4 (2009).
80.
Rudenko G, Van der Ploeg LH: Transcription of telomere repeats in protozoa. EMBO J 8:2633-2638 (1989).
[PubMed]
81.
Sandell LL, Gottschling DE, Zakian VA: Transcription of a yeast telomere alleviates telomere position effect without affecting chromosome stability. Proc Natl Acad Sci USA 91:12061-12065 (1994).
[PubMed]
82.
Schoeftner S, Blasco MA: Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10:228-236 (2008).
[PubMed]
83.
Sfeir A, de Lange T: Removal of shelterin reveals the telomere end-protection problem. Science 336:593-597 (2012).
[PubMed]
84.
Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, et al: Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138:90-103 (2009).
[PubMed]
85.
Solovei I, Gaginskaya ER, Macgregor HC: The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds. Chromosome Res 2:460-470 (1994).
[PubMed]
86.
Stadler G, Rahimov F, King OD, Chen JCJ, Robin JD, et al: Telomere position effect regulates DUX4 in human facioscapulohumeral muscular dystrophy. Nat Struct Mol Biol 20:671-678 (2013).
[PubMed]
87.
Sykorova E, Fajkus J, Ito M, Fukui K: Transition between two forms of heterochromatin at plant subtelomeres. Chromosome Res 9:309-323 (2001).
[PubMed]
88.
Sykorova E, Cartagena J, Horakova M, Fukui K, Fajkus J: Characterization of telomere-subtelomere junctions in Silene latifolia. Mol Genet Genomics 269:13-20 (2003a).
[PubMed]
89.
Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, et al: 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 (2003b).
[PubMed]
90.
Sykorova E, Lim KY, Kunicka Z, Chase MW, Bennett MD, et al: Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270:1893-1904 (2003c).
[PubMed]
91.
Sykorova E, Fajkus J, Meznikova M, Lim KY, Neplechova K, et al: Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am J Bot 93:814-823 (2006).
[PubMed]
92.
Tommerup H, Dousmanis A, de Lange T: Unusual chromatin in human telomeres. Mol Cell Biol 14:5777-5785 (1994).
[PubMed]
93.
Trifonov EN: Nucleosome positioning by sequence, state of the art and apparent finale. J Biomol Struct Dyn 27:741-746 (2010).
[PubMed]
94.
Uchida W, Matsunaga S, Sugiyama R, Kawano S: Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77:63-67 (2002).
[PubMed]
95.
Vaquero-Sedas MI, Gamez-Arjona FM, Vega-Palas MA: Arabidopsis thaliana telomeres exhibit euchromatic features. Nucleic Acids Res 39:2007-2017 (2011).
[PubMed]
96.
Vaquero-Sedas MI, Luo C, Vega-Palas MA: Analysis of the epigenetic status of telomeres by using ChIP-seq data. Nucleic Acids Res 40:e163 (2012).
[PubMed]
97.
Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA: Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837 (2002).
[PubMed]
98.
Vrbsky J, Akimcheva S, Watson JM, Turner TL, Daxinger L, et al: siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genet 6:e1000986 (2010).
[PubMed]
99.
Waterhouse PM, Graham MW, Wang MB: Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA 95:13959-13964 (1998).
[PubMed]
100.
Weuts A, Voet T, Verbeeck J, Lambrechts N, Wirix E, et al: Telomere length homeostasis and telomere position effect on a linear human artificial chromosome are dictated by the genetic background. Nucleic Acids Res 40:11477-11489 (2012).
[PubMed]
101.
Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ, et al: Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev 26:1825-1836 (2012).
[PubMed]
102.
Yehezkel S, Segev Y, Viegas-Pequignot E, Skorecki K, Selig S: Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum Mol Genet 17:2776-2789 (2008).
[PubMed]
103.
Zhu Y, Dong AW, Shen WH: Histone variants and chromatin assembly in plant abiotic stress responses. Biochim Biophys Acta 1819:343-348 (2012).
[PubMed]
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