Abstract
Although extant data favour centromere being an epigenetic structure, it is also clear that centromere formation is based on DNA, in particular, tandemly repeated satellite DNA and its transcripts. Presence of conserved structural motifs within satellite DNAs such as periodically distributed AT tracts, protein binding sites, or promoter elements indicate that despite sequence flexibility, there are structural determinants that are prerequisite for centromere function. In addition, existence of functional centromeric DNA transcripts indicates possible importance of structural elements at the level of RNA secondary or tertiary structure. Rapid centromere evolution is explained by homologous recombination followed by extrachromosomal rolling circle replication. This could lead to amplification of different satellite sequences within a genome. However, only those satellites that have inherent centromere-competence in the form of structural requirements necessary for centromere function are after amplification fixed in a population as a new centromere.
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Alexandrov I, Kazakov A, Tumeneva I, Shepelev V, Yurov Y (2001) Alpha-satellite DNA of primates: old and new families. Chromosoma 110:253–266
Alexiadis V, Ballestas ME, Sanchez C, Winokur S, Vedanarayanan V, Warren M, Ehrilch M (2007) RNAPol-ChIP analysis of transcription from FSHD-linked tandem repeats and satellite DNA. Biochim Biophys Acta 1796:29–40
Allshire RC, Nimmo ER, Ekwall K, Javerzat JP, Cranston G (1995) Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev 9:218–233
Amor DJ, Choo KH (2002) Neocentromeres: role in human disease, evolution and centromere studies. Am J Hum Genet 71:695–714
Assum G, Fink T, Steinbeisser T, Fisel KJ (1993) Analysis of human extrachromosomal DNA elements originating from different beta-satellite subfamilies. Hum Genet 91:489–495
Baker RE, Rogers K (2005) Genetic and genomic analysis of the AT-rich centromere DNA element II of Saccharomyces cerevisiae. Genetics 171:1463–1475
Basu J, Stromberg G, Compitello G, Willard HF, Van Bokkelen G (2005) Rapid creation of BAC-based human artificial chromosome vectors by transposition with synthetic alpha-satellite arrays. Nucleic Acids Res 33:587–596
Bensasson D, Zarowiecki M, Burt A, Koufopanou V (2008) Rapid evolution of yeast centromeres in the abscence of drive. Genetics 178:2161–2167
Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 21:2539–2542
Bernstein E, Allis CD (2005) RNA meets heterochromatin. Genes Dev 19:1635–1655
Black BE, Bassett EA (2008) The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 20:91–100
Blower MD, Nachury M, Heald R, Weis K (2005) A Rac-1 containing ribonucleoprotein is required for mitotic spindle assemby. Cell 121:223–234
Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci USA 103:8709–8714
Bruvo-Mad¯arić B, Plohl M, Ugarković Đ (2007) Wide distribution of related satellite DNA families within the genus Pimelia (Tenebrionidae). Genetica 130:35–42
Bulazel KV, Ferreri GC, Eldridge MD, O’ Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:R170
Bühler M, Haas W, Gygi SP, Moazed D (2007) RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129:707–721
Cesari M, Luchetti A, Passamonti M, Scali V, Mantovani B (2003) Polymerase chain reaction amplification of the Bag320 satellite family reveals the ancestral library and past gene conversion events in Bacillus rossius (Insecta Phasmatodea). Gene 312:289–295
Charlesworth B, Langley CH, Stephan W (1986) The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics 112:947–962
Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734–737
Clarke L, Carbon J (1983) Genomic substitutions of centromeres in Saccharomyces cerevisiae. Nature 305:23–28
Coats SR, Zhang Y, Epstein LM (1994) Transcription of satellite 2 DNA from the newt is driven by a snRNA type of promoter. Nucleic Acids Res 22:4697–4704
Cooper JL, Henikoff S (2004) Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol 21:1712–1718
Dalal Y, Furuyama T, Vermaak D, Henikoff S (2007) Structure, dynamics, and evolution of centromeric nucleosomes. Proc Natl Acad Sci USA. 104:15974–15981
Dawe RK, Henikoff S (2006) Centromeres put epigenetics in the driver’s seat. Trends Biochem Sci 31:662–669
Dobie KW, Hari KL, Maggert KA, Karpen GH (1999) Centromere proteins and chromosome inheritance: a complex affair. Curr Opin Genes Dev 9:206–217
Dover GA (1986) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2:159–165
Durajlija žinić S, Ugarković Đ, Cornudella L, Plohl M (2000) A novel interspersed type of organization of satellite DNAs in Tribolium madens heterochromatin. Chromosome Res 8:201–212
Feliciello I, Picariello O, Chinali G (2005) The first characterisation of the overall variability of repetitive units in a species reveals unexpected features of satelite DNA. Gene 349:153–164
Feliciello I, Picariello O, Chinali G (2006) Intra-specific variability and unusual organization of the repetitive units in a satellite DNA from Rana dalmatina: molecular evidence of a new mechanism of DNA repair acting on satellite DNA. Gene 383:81–92
Ferbeyre G, Smith JM, Cedergren R (1998) Schistosome satellite DNA encodes active hammerhead-ribozymes. Mol Cell Biol 18:3880–3888
Fitzgerald DJ, Dryden GL, Bronson EC, Williams JS, Anderson JN (1994) Conserved pattern of bending in satellite and nucleosome positioning DNA. J Biol Chem 269:21303–21314
Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94–97
Frescas D, Guardavaccaro D, Kuchay SM, Kato H, Poleshko A, Basrur V, Elenitoba-Johnson KS, Katz RA, Pagano M (2008) KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle 7(29):3539–3547
Fry K, Salser W (1977) Nucleotide sequences of HS-α satellite DNA from kangaroo rat Dipodomys ordii and characterisation of similar sequences in other rodents. Cell 12:1069–1084
Grewal SI, Elgin SC (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447:399–406
Grimes BR, Rhoades AA, Willard HF (2002) Alpha-satellite DNA and vector composition influence rates of human artificial chromosome formation. Mol Ther 5:798–805
Hall SE, Kettler G, Preuss D (2003) Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res 13:195–205
Harp JM, Uberbacher EC, Roberson AE, Palmer EL, Gewiess A, Bunick GJ (1996) X-ray diffraction analysis of crystals containing twofold symmetric nucleosome core particles. Acta Crystallogr D 52:283–288
Hegemann JH, Fleig UN (1993) The centromere of budding yeast. Bioessays 15:451–460
Henikoff S, Dalal Y (2005) Centromeric heterochromatin: what makes it unique. Curr Opin Genet Dev 15:177–184
Heslop-Harrison JS, Murata M, Ogura Y, Schwarzacher T, Motoyoshi F (1999) Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11:31–42
Huisinga KL, Elgin SCR (2009) Small RNA-directed heterochromatin formation in the context of development: What flies might learn from fission yeast. Biochim Biophys Acta 1789:3–16
Jaco I, Canela A, Vera E, Blasco MA (2008) Centromere mitotic recombination in mammalian cells. J Cell Biol 181:885–92
Jin W, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, Jiang J (2004) Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–581
Jonstrup AT, Thomsen T, Wang Y, Knudsen BR, Koch J, Andersen AH (2008) Hairpin structures formed by alpha satellite DNA of human centromeres are cleaved by human topoisomerase II α. Nucleic Acids Res 36:6165–6175
Kalitsis P (2008) Centromeres. In: Encyclopedia of life sciences (ELS). Wiley, Chichester
Kawabe A, Charlesworth D (2007) Patterns of DNA variation among three centromere satellite families in Arabidopsis halleri and A. lyrata. J Mol Evol 64:237–247
Kellum R, Alberts BM (1995) Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J Cell Sci 108:1419–1431
King K, Jobst J, Hemleben V (1995) Differential homogenisation and amplification of two satellite DNAs in the genus Cucurbita (Cucurbitaceae). J Mol Evol 4:996–1005
Kipling D, Warburton PE (1997) Centromeres, CENP-B and Tigger too. Trends Genet 13:141–145
Kumekawa N, Hosouchi T, Tsuruoka H, Kotani H (2001) The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 4. DNA Res 8:285–290
Lee C, Wevrick R, Fisher RB, Ferguson-Smith MA, Lin CC (1997) Human centromeric DNAs. Hum Genet 100:291–304
Lee HR, Zhang W, Langdon T, Jin W, Yan H, Cheng Z, Jiang J (2005) Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci USA 102:11793–117998
Li YX, Kirby ML (2003) Coordinated and conserved expression of alphoid repeat and alphoid repeat-tagged coding sequences. Dev Dynamics 228:72–81
Lin CC, Li YC (2006) Chromosomal distribution and organization of three cervid satellite DNAs in Chinese water deer (Hydropotes inermis). Cytogenet Genome Res 114:147–154
Lu J, Gilbert DM (2007) Proliferation-dependent and cell cycle-regulated transcription of mouse pericentromeric heterochromatin. J Cell Biol 179:411–421
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8-angstrom resolution. Nature 389:251–260
Ma J, Jackson SA (2006) Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Res 16:251–259
Maddox PS, Oegema K, Desai A, Cheesman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res 12:641–653
Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentromeric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30:329–334
Malik HS, Henikoff S (2002) Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev 12:711–718
Marshall OJ, Chuch AC, Wong LH, Choo KH (2008) Neocentromeres. new insights into centromere structure, disease, development, and karyotype evolution. Am J Hum Genet 82:261–282
Martinez-Balbas A, Rodriguez-Campos A, Gracia-Ramirez M, Sainz J, Carrera P, Aymami J, Azorin F (1990) Satellite DNAs contain sequences that induce curvature. Biochemistry 29:2342–2348
Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromere satellite. J Cell Biol 109:1963–1973
Masumoto H, Nakano M, Ohzeki J (2004) The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres. Chromosome Res 12:543–556
Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7:R23
Meštrović N, Plohl M, Mravinac B, Ugarković, Đ (1998). Evolution of satellite DNAs from the genus Palorus- experimental evidence for the “library” hypothesis. Mol Biol Evol 15:1062–1068
Meštrović N, Castagnone-Sereno P, Plohl M (2006) Interplay of selective pressure and stochastic events directs evolution of the MEL172 satellite DNA library in root-knot nematodes. Mol Biol Evol 23:2316–2325
Metz A, Soret J, Vourc’h C, Tazi J, Jolly C (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558
Mravinac B, Plohl M, Meštrović N, Ugarković Đ (2002) Sequence of PRAT satellite DNA “frozen” in some coleopteran species. J Mol Evol 54:774–783
Mravinac B, Plohl M, Ugarković Đ (2004) Conserved patterns in the evolution of Tribolium satellite DNAs. Gene 332:169–177
Mravinac B, Plohl M, Ugarković Đ (2005) Preservation and high sequence conservation of satellite DNAs suggest functional constraints. J Mol Evol 61:542–550
Murakami H, Goto DB, Toda T, Chen ES, Grewal SI, Martienssen RA, Yanagida M (2007) Ribonuclease Activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS ONE 3:e317
Nasmyth K (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 288:559–565
Navratilova A, Koblizkova A, Macas J (2008) Survey of extrachromosomal circular DNA derived from plant satellite repeats. BMC Plant Biol 8:90
Nijman IJ, Lenstra JA (2001) Mutation and recombination in cattle satellite DNA: a feedback model for the evolution of satellite DNA repeats. J Mol Evol 52:361–371
Ohzeki J, Nakano M, Okada T, Masumoto H (2002) CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J Cell Biol 159:765–775
Okada T, Ohzeki J, Nakano M, Yoda K, Brinkley WR, Larionov V, Masumoto H (2007) CENP-B controls centromere formation depending on the chromatin context. Cell 131:187–1300
Pezer Ž, Ugarković Đ (2008a) RNA Pol II promotes transcription of centromeric satellite DNA in Beetles. PLoS ONE 3:e1594
Pezer Ž, Ugarković Đ (2008b) Role of non-coding RNA and heterochromatin in aneuploidy and cancer. Semin Cancer Biol 18:123–130
Pezer Ž, Ugarković Đ (2009) Transcription of pericentromeric heterochromatin in beetles – satellite DNAs as active regulatory elements. Cytogenet Genome Res (in press)
Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337
Politi V, Perini G, Trazzi S, Pliss A, Raska I, Earnshaw WC, Della Valle G (2002) CENP-C binds the alpha-satellite DNA in vivo at specific centromere domains. J Cell Sci 11:2317–2327
Pons J, Bruvo B, Petitpierre E, Plohl M, Ugarković D, Juan C (2004) Complex structural feature of satellite DNA sequences in the genus Pimelia (Coleoptera: Tenebrionidae): random differential amplification from a common “satellite DNA library”. Heredity 92:418–427
Renault S, Roulex-Bonnin F, Periquet G, Bigot Y (1999) Satellite DNA transcription in Diadromus pulchellus (Hymenoptera). Insect Biochem Mol Biol 29:103–111
Romanova LY, Deriagin GV, Mashkova TG, Tumeneva IG, Mushegian AR, Kisselev LL, Alexandrov IA (1996) Evidence for selection in evolution of alpha satellite DNA: the central role of CENP-B/pJα binding region. J Mol Biol 261:334–340
Rudd MA, Wray GA, Willard HF (2006) The evolutionary dynamics of α-satellite. Genome Res 16:88–96
Sanyal K, Baum M, Carbon J (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci USA 101:1134–11379
Schueler MG, Sullivan B (2006) Structural and functional dynamics of human centromeric heterochromatin. Annu Rev Genomics Hum Genet 7:301–313
Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115
Schueler MG, Dunn JM, Bird CP, Ross MT, Viggiano L; NISC Comparative Sequencing Program, Rocchi M, Willard HF, Green ED (2005) Progressive proximal expansion of the primate X chromosome centromere. Proc Natl Acad Sci USA 102:10563–10568
Slamovits CH, Cook JA, Lessa EP, Rossi MS (2001) Recurrent amplifications and deletions of satellite DNA accompanied chromosomal diversification in South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidae): a phylogenetic approach. Mol Biol Evol 18:1708–1719
Smith PG (1976) Evolution of repeated sequences by unequal crossover. Science 191:528–535
Stephan W (1986) Recombination and the evolution of satellite DNA. Genet Res 47:167–174
Stephan W (2007) Evolution of genome organization. In: Encyclopedia of Life Sciences (ELS). Wiley, Chichester
Sun X, Le HD, Janice M, Wahlstrom JM, Karpen GH (2003) Sequence analysis of a functional Drosophila centromere. Genome Res 13:182–194
Tal M, Shimron F, Yagil G (1994) Unwound regions in yeast centromere IV DNA. J Mol Biol 243:179–189
Talbert PB, Bryson TD, Henikoff S (2004) Adaptive evolution of centromere proteins in plants and animals. J Biol 3:18
Takasuka TE, Cioffi A, Stein A (2008) Sequence information encoded in DNA that may influence long-range chromatin structure correlates with human chromosome functions. PLoS ONE 3:e2643
Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA 101:15986–15991
Ugarković Đ (2005) Functional elements residing within satellite DNAs. EMBO Rep 6:1035–1039
Ugarković Đ (2008a) Evolution of Alpha satellite DNA. In: Encyclopedia of Life Sciences (ELS). Wiley, Chichester
Ugarković Đ (2008b) Satellite DNA libraries and centromere evolution. Open Evol J 2:1–6
Ugarković Đ, Plohl M (2002) Variation in satellite DNA profiles – causes and effects. EMBO J 21:5955–5959
Ugarković Đ, Podnar M, Plohl M (1996a) Satellite DNA of the red flour beetle Tribolium castaneum-comparative study of satellites from the genus Tribolium. Mol Biol Evol 13:1059–1066
Ugarković Đ, Durajlija S, Plohl M (1996b) Evolution of Tribolium madens (Insecta, Coleoptera) satellite DNA through DNA inversion and insertion. J Mol Evol 42:350–358
Ugarković ĐL, Plohl M, Lucijanić-Justić V, Borštnik B (1992) Detection of satellite DNA in Palorus atzeburgii: Analysis of curvature profiles and comparison with Tenebrio molitor satellite DNA. Biochimie 74:1075–1082
Vagnarelli P, Ribeiro SA, Earnshaw WC (2008) Centromeres: old tales and new tools. FEBS Lett 582:1950–1959
Verdel A, Jia S, Gerber S, Suglyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin with the RITS complex. Science 303:672–676
Vershinin AV, Alkhimova EG, Heslop-Harrison JS (1996) Molecular diversification of tandemly organised sequences and heterochromatic chromosome regions in some Triticeae species. Chromosome Res 4:517–525
Vogt P (1990) Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved “chromatin folding code”. Hum Genet 84:301–336
Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837
Wang F, Koyama N, Nishida H, Haraguchi T, Reith W, Tsukamoto T (2006) The assembly and maintenance of heterochromatin initiated by transgene repeats are independent of the RNA interference pathway in mammalian cells. Mol Cell Biol 26:4028–4040
Westermann S, Drubin DG, Barnes G (2007) Structures and functions of yeast kinetochore complexes. Ann Rev Biochem 76:563–592
Win TZ, Stevenson AL, Wang SW (2006) Fission yeast Cid12 has dual functions in chromosome segregation and checkpoint control. Mol Cell Biol 26:4435–4447
Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, Choo KHA (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17:1146–1160
Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251–256
Zhang Y, Huang YC, Zhang L, Li Y, Lu TT, Lu YQ, Feng Q, Zhao Q, Cheng ZK, Xue YB, Wing RA, Han B (2004) Structural features of the rice chromosome 4 centromere. Nucleic Acids Res 32:2023–2030
Zhu L, Chou SH, Reid BR (1996) A single G-to-C change causes human centromere TGGAA repeats to fold back into hairpins. Proc Natl Acad Sci USA 93:12159–12164
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This work was supported by grant 00982604 from the Croatian Ministry of Science and EU FP6 Marie Curie Transfer of Knowledge Grant MTKD-CT-2006-042248. The author is grateful to Josip Brajković for the help with figures.
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Ugarković, Đ. (2009). Centromere-Competent DNA: Structure and Evolution. In: Ugarkovic, D. (eds) Centromere. Progress in Molecular and Subcellular Biology, vol 48. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00182-6_3
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