Abstract
Recently we characterised TRB1, a protein from a single-myb-histone family, as a structural and functional component of telomeres in Arabidopsis thaliana. TRB proteins, besides their ability to bind specifically to telomeric DNA using their N-terminally positioned myb-like domain of the same type as in human shelterin proteins TRF1 or TRF2, also possess a histone-like domain which is involved in protein–protein interactions e.g., with POT1b. Here we set out to investigate the genome-wide localization pattern of TRB1 to reveal its preferential sites of binding to chromatin in vivo and its potential functional roles in the genome-wide context. Our results demonstrate that TRB1 is preferentially associated with promoter regions of genes involved in ribosome biogenesis, in addition to its roles at telomeres. This preference coincides with the frequent occurrence of telobox motifs in the upstream regions of genes in this category, but it is not restricted to the presence of a telobox. We conclude that TRB1 shows a specific genome-wide distribution pattern which suggests its role in regulation of genes involved in biogenesis of the translational machinery, in addition to its preferential telomeric localization.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alexandrov NN, Troukhan ME, Brover VV, Tatarinova T, Flavell RB, Feldmann KA (2006) Features of Arabidopsis genes and genome discovered using full-length cDNAs. Plant Mol Biol 60:69–85. doi:10.1007/s11103-005-2564-9
Bosco N, de Lange T (2012) A TRF1-controlled common fragile site containing interstitial telomeric sequences. Chromosoma 121:465–474. doi:10.1007/s00412-012-0377-6
Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39:776–789. doi:10.1111/j.1365-313X.2004.02169.x
Bradshaw PS, Stavropoulos DJ, Meyn MS (2005) Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage. Nat Genet 37:193–197. doi:10.1038/ng1506
Brown JW, Shaw PJ, Shaw P, Marshall DF (2005) Arabidopsis nucleolar protein database (AtNoPDB). Nucleic Acids Res 33:D633–D636
Brown JW, Marshall DF, Echeverria M (2008) Intronic noncoding RNAs and splicing. Trends Plant Sci 13:335–342. doi:10.1016/j.tplants.2008.04.010
Chen LY et al (2012) Mitochondrial localization of telomeric protein TIN2 links telomere regulation to metabolic control. Mol Cell 47:839–850. doi:10.1016/j.molcel.2012.07.002
Cifuentes-Rojas C, Kannan K, Tseng L, Shippen DE (2011) Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc Natl Acad Sci USA 108:73–78. doi:10.1073/pnas.1013021107
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. doi:10.1038/sj.embor.7400314
de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100–2110. doi:10.1101/Gad.1346005
Deng Z, Lezina L, Chen CJ, Shtivelband S, So W, Lieberman PM (2002) Telomeric proteins regulate episomal maintenance of Epstein-Barr virus origin of plasmid replication. Mol Cell 9:493–503
Dundr M, Meier UT, Lewis N, Rekosh D, Hammarskjold ML, Olson MO (1997) A class of nonribosomal nucleolar components is located in chromosome periphery and in nucleolus-derived foci during anaphase and telophase. Chromosoma 105:407–417
Dvorackova M, Rossignol P, Shaw PJ, Koroleva OA, Doonan JH, Fajkus J (2010) AtTRB1, a telomeric DNA-binding protein from Arabidopsis, is concentrated in the nucleolus and shows highly dynamic association with chromatin. Plant J 61:637–649. doi:10.1111/j.1365-313X.2009.04094.x
Dvorackova M, Fojtova M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J. doi:10.1111/tpj.12822
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340
Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210. doi:10.1093/Nar/30.1.207
Fajkus J, Sykorova E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13:469–479. doi:10.1007/s10577-005-0997-2
Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA 99:14584–14589. doi:10.1073/pnas.212325299
Gaspin C, Rami JF, Lescure B (2010) Distribution of short interstitial telomere motifs in two plant genomes: putative origin and function. BMC Plant Biol 10:283. doi:10.1186/1471-2229-10-283
Hanaoka S, Nagadoi A, Nishimura Y (2005) Comparison between TRF2 and TRF1 of their telomeric DNA-bound structures and DNA-binding activities. Protein Sci 14:119–130. doi:10.1110/ps.04983705
Hofr C, Sultesova P, Zimmermann M, Mozgova I, Schrumpfova PP, Wimmerova M, Fajkus J (2009) Single-Myb-histone proteins from Arabidopsis thaliana: a quantitative study of telomere-binding specificity and kinetics. Biochem J 419:221–228. doi:10.1042/BJ20082195
Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K (2012) Chromosome end protection by blunt-ended telomeres. Genes Dev 26:1703–1713. doi:10.1101/gad.194944.112
Krutilina RI et al (2003) Protection of internal (TTAGGG)n repeats in Chinese hamster cells by telomeric protein TRF1. Oncogene 22:6690–6698. doi:10.1038/sj.onc.1206745
Kuchar M, Fajkus J (2004) Interactions of putative telomere-binding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Lett 578:311–315. doi:10.1016/j.febslet.2004.11.021
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923
Latrick CM, Cech TR (2010) POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation. EMBO J 29:924–933. doi:10.1038/emboj.2009.409
Liang K, Keles S (2012) Normalization of ChIP-seq data with control. BMC Bioinformatics 13:199. doi:10.1186/1471-2105-13-199
Liboz T, Bardet C, Le Van Thai A, Axelos M, Lescure B (1990) The four members of the gene family encoding the Arabidopsis thaliana translation elongation factor EF-1 alpha are actively transcribed. Plant Mol Biol 14:107–110
Louis EJ, Vershinin AV (2005) Chromosome ends: different sequences may provide conserved functions. BioEssays 27:685–697. doi:10.1002/Bies.20259
Macas J, Neumann P, Novak P, Jiang J (2010) Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinformatics 26:2101–2108. doi:10.1093/bioinformatics/btq343
Majerska J, Sykorova E, Fajkus J (2011) Non-telomeric activities of telomerase. Mol BioSyst 7:1013–1023. doi:10.1039/c0mb00268b
Mandakova T, Lysak MA (2008) Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae). Plant Cell 20:2559–2570. doi:10.1105/tpc.108.062166
Manevski A, Bertoni G, Bardet C, Tremousaygue D, Lescure B (2000) In synergy with various cis-acting elements, plant insterstitial telomere motifs regulate gene expression in Arabidopsis root meristems. FEBS Lett 483:43–46
Marian CO et al (2003) The maize Single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol 133:1336–1350. doi:10.1104/pp.103.026856
Martinez P et al (2010) Mammalian Rap1 controls telomere function and gene expression through binding to telomeric and extratelomeric sites. Nat Cell Biol 12:768–780. doi:10.1038/ncb2081
Mignon-Ravix C, Depetris D, Delobel B, Croquette MF, Mattei MG (2002) A human interstitial telomere associates in vivo with specific TRF2 and TIN2 proteins. Eur J Hum Genet 10:107–112. doi:10.1038/sj.ejhg.5200775
Morse RH (2000) RAP, RAP, open up! New wrinkles for RAP1 in yeast. Trends Genet 16:51–53. doi:10.1016/S0168-9525(99)01936-8
Mozgova I, Schrumpfova PP, Hofr C, Fajkus J (2008) Functional characterization of domains in AtTRB1, a putative telomere-binding protein in Arabidopsis thaliana. Phytochemistry 69:1814–1819. doi:10.1016/j.phytochem.2008.04.001
Nelson AD, Forsythe ES, Gan X, Tsiantis M, Beilstein MA (2014) Extending the model of Arabidopsis telomere length and composition across Brassicaceae. Chromosome Res 22:153–166. doi:10.1007/s10577-014-9423-y
Nishikawa T, Okamura H, Nagadoi A, Konig P, Rhodes D, Nishimura Y (2001) Solution structure of a telomeric DNA complex of human TRF1. Structure 9:1237–1251
Nosek J, Tomaska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44:73–84. doi:10.1007/s00294-003-0426-z
Pendle AF et al (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16:260–269
Peska V, Schrumpfova PP, Fajkus J (2011) Using the telobox to search for plant telomere binding proteins. Curr Protein Pept Sci 12:75–83
Pfaffl MW (2004) Quantification strategies in real-time PCR. International University Line (IUL), La Jolla
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
Roudier F et al (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938. doi:10.1038/emboj.2011.103
Savada RP, Bonham-Smith PC (2014) Differential transcript accumulation and subcellular localization of Arabidopsis ribosomal proteins. Plant Sci 223:134–145. doi:10.1016/j.plantsci.2014.03.011
Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100
Schrumpfova P, Kuchar M, Mikova G, Skrisovska L, Kubicarova T, Fajkus J (2004) Characterization of two Arabidopsis thaliana myb-like proteins showing affinity to telomeric DNA sequence. Genome 47:316–324. doi:10.1139/g03-136
Schrumpfova PP, Kuchar M, Palecek J, Fajkus J (2008) Mapping of interaction domains of putative telomere-binding proteins AtTRB1 and AtPOT1b from Arabidopsis thaliana. FEBS Lett 582:1400–1406. doi:10.1016/j.febslet.2008.03.034
Schrumpfova PP, Vychodilova I, Dvorackova M, Majerska J, Dokladal L, Schorova S, Fajkus J (2014) Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J 77:770–781. doi:10.1111/Tpj.12428
Sequeira-Mendes J et al (2014) The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26:2351–2366. doi:10.1105/tpc.114.124578
Sfeir A, de Lange T (2012) Removal of shelterin reveals the telomere end-protection problem. Science 336:593–597. doi:10.1126/science.1218498
Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138:90–103. doi:10.1016/j.cell.2009.06.021
Shen L, Shao N, Liu X, Nestler E (2014) ngs.plot: quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genom 15:284. doi:10.1186/1471-2164-15-284
Simonet T et al (2011) The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res 21:1028–1038. doi:10.1038/cr.2011.40
Snaar S, Wiesmeijer K, Jochemsen AG, Tanke HJ, Dirks RW (2000) Mutational analysis of fibrillarin and its mobility in living human cells. J Cell Biol 151:653–662
Soudet J, Jolivet P, Teixeira MT (2014) Elucidation of the DNA end-replication problem in Saccharomyces cerevisiae. Mol Cell 53:954–964. doi:10.1016/j.molcel.2014.02.030
Sprague BL, McNally JG (2005) FRAP analysis of binding: proper and fitting. Trends Cell Biol 15:84–91
Teo H et al (2010) Telomere-independent Rap1 is an IKK adaptor and regulates NF-kappaB-dependent gene expression. Nat Cell Biol 12:758–767. doi:10.1038/ncb2080
Tremousaygue D, Manevski A, Bardet C, Lescure N, Lescure B (1999) Plant interstitial telomere motifs participate in the control of gene expression in root meristems. Plant J 20:553–561
Tremousaygue D, Garnier L, Bardet C, Dabos P, Herve C, Lescure B (2003) Internal telomeric repeats and ‘TCP domain’ protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J 33:957–966
Turck F et al (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86. doi:10.1371/journal.pgen.0030086
Uchida W, Matsunaga S, Sugiyama R, Kawano S (2002) Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet Syst 77:63–67
Valach M et al (2011) Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res 39:4202–4219. doi:10.1093/nar/gkq1345
Weaver DT (1998) Telomeres: moonlighting by DNA repair proteins. Curr Biol 8:R492–R494
Zeeberg BR et al (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4:R28
Zeeberg BR et al (2005) High-throughput GoMiner, an ‘industrial-strength’ integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinform 6:168. doi:10.1186/1471-2105-6-168
Zhang P, Pazin MJ, Schwartz CM, Becker KG, Wersto RP, Dilley CM, Mattson MP (2008a) Nontelomeric TRF2-REST interaction modulates neuronal gene silencing and fate of tumor and stem cells. Curr Biol 18:1489–1494. doi:10.1016/j.cub.2008.08.048
Zhang Y et al (2008b) Model-based analysis of ChIP-seq (MACS). Genome Biol 9:R137. doi:10.1186/gb-2008-9-9-r137
Zhang Y, Lin YH, Johnson TD, Rozek LS, Sartor MA (2014) PePr: a peak-calling prioritization pipeline to identify consistent or differential peaks from replicated ChIP-seq data. Bioinformatics 30:2568–2575. doi:10.1093/bioinformatics/btu372
Acknowledgments
We thank Vladimir Benes from the European Molecular Biology Laboratory (EMBL), Genomics Core Facility, Heidelberg, Germany, for valuable comments and recommendations on our ChIP procedure. We also thank Ronald Hancock, Hôtel-Dieu de Québec for critical reading of the manuscript. Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum, provided under the programme “Projects of Large Infrastructure for Research, Development, and Innovations” (LM2010005), is greatly appreciated. This research was supported by the Czech Science Foundation (13-06943S) and by project CEITEC (CZ.1.05/1.1.00/02.0068) of the European Regional Development Fund.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schrumpfová, P.P., Vychodilová, I., Hapala, J. et al. Telomere binding protein TRB1 is associated with promoters of translation machinery genes in vivo. Plant Mol Biol 90, 189–206 (2016). https://doi.org/10.1007/s11103-015-0409-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-015-0409-8