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Tribe-specific satellite DNA in non-domestic Bovidae

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An Erratum to this article was published on 11 March 2014

Abstract

Satellite sequences present in the centromeric and pericentric regions of chromosomes represent useful source of information. Changes in satellite DNA composition may coincide with the speciation and serve as valuable markers of phylogenetic relationships. Here, we examined satellite DNA clones isolated by laser microdissection of centromeric regions of 38 bovid species and categorized them into three types. Sat I sequences from members of Bovini/Tragelaphini/Boselaphini are similar to the well-documented 1.715 sat I DNA family. Sat I DNA from Caprini/Alcelaphini/Hippotragini/Reduncini/Aepycerotini/Cephalophini/Antilopini/Neotragini/Oreotragini form the second group homologous to the common 1.714 sat I DNA. The analysis of sat II DNAs isolated in our study confirmed conservativeness of these sequences within Bovidae. Newly described centromeric clones from Madoqua kirkii and Strepsiceros strepsiceros were similar in length and repetitive tandem arrangement but showed no similarity to any other satellite DNA in the GenBank database. Phylogenetic analysis of sat I sequences isolated in our study from 38 bovid species enabled the description of relationships at the subfamily and tribal levels. The maximum likelihood and Bayesian inference analyses showed a basal position of sequences from Oreotragini in the subfamily Antilopinae. According to the Bayesian inference analysis based on the indels in a partitioned mixed model, Antilopinae satellite DNA split into two groups with those from Neotragini as a basal tribe, followed by a stepwise, successive branching of Cephalophini, Aepycerotini and Antilopini sequences. In the second group, Reduncini sequences were basal followed by Caprini, Alcelaphini and Hippotragini.

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Abbreviations

BAC:

Bacterial artificial chromosome

BI:

Bayesian inference

BRU-PCR:

Basic repeat unit obtained by PCR

DOP-PCR:

Degenerate oligonucleotide primed polymerase chain reaction

FISH:

Fluorescence in situ hybridization

LINE:

Long interspersed nuclear element

LTR:

Long terminal repeat

MCMC:

Markov chains Monte Carlo

ML:

Maximum likelihood

NCBI:

National Center for Biotechnology Information

NFA:

Numbers of autosomal arms

RFLP:

Restriction fragment length polymorphism

sat:

Satellite

SINE:

Short interspersed nuclear element

SNP:

Single nucleotide polymorphism

References

  • Adega F, Chaves R, Guedes-Pinto H, Heslop-Harrison JS (2006) Physical organization of the 1.709 satellite IV DNA family in Bovini and Tragelaphini tribes of the Bovidae: sequence and chromosomal evolution. Cytogenet Genome Res 114:140–146

    CAS  PubMed  Google Scholar 

  • Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166

    PubMed Central  PubMed  Google Scholar 

  • Buckland RA (1985) Sequence and evolution of related bovine and caprine satellite DNAs. J Mol Biol 186:25–30

    CAS  PubMed  Google Scholar 

  • Buckland RA, Evans HJ (1978) Cytogenetic aspects of phylogeny in the Bovidae. I. G-banding. Cytogenet Cell Genet 21:42–63

    CAS  PubMed  Google Scholar 

  • Cabelova K, Kubickova S, Cernohorska H, Rubes J (2012) Male-specific repeats in wild Bovidae. J Appl Genet 53:423–433

    PubMed  Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Robinson TJ, Rubes J (2011) Cytotypes of Kirk’s dik-dik (Madoqua kirkii, Bovidae) show multiple tandem fusions. Cytogenet Genome Res 132:255–263

    CAS  PubMed  Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Rubes J (2012) Molecular insights into X; BTA5 chromosome rearrangements in the tribe Antilopini (Bovidae). Cytogenet Genome Res 136:188–198

    CAS  PubMed  Google Scholar 

  • Chaves R, Guedes-Pinto H, Heslop-Harrison J, Schwarzacher T (2000) The species and chromosomal distribution of the centromeric alpha-satellite I sequence from sheep in the tribe Caprini and other Bovidae. Cytogenet Cell Genet 91:62–66

    CAS  PubMed  Google Scholar 

  • Chaves R, Guedes-Pinto H, Heslop-Harrison JS (2005) Phylogenetic relationships and the primitive X chromosome inferred from chromosomal and satellite DNA analysis in Bovidae. Proc Biol Sci 272:2009–2016

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng YM, Li TS, Hsieh LJ, Hsu PC, Li YC, Lin CC (2009) Complex genomic organization of Indian muntjac centromeric DNA. Chromosome Res 17:1051–1062

    CAS  PubMed  Google Scholar 

  • D’Aiuto L, Barsanti P, Mauro S, Cserpan I, Lanave C, Ciccarese S (1997) Physical relationship between satellite I and II DNA in centromeric regions of sheep chromosomes. Chromosome Res 5:375–381

    PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    CAS  PubMed  Google Scholar 

  • Decker JE, Pires JC, Conant GC et al (2009) Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci U S A 106:18644–18649

    CAS  PubMed Central  PubMed  Google Scholar 

  • Di Meo GP, Perucatti A, Chaves R, Adega F, De Lorenzi L, Molteni L, De Giovanni A, Incarnato D, Guedes-Pinto H, Eggen A, Iannuzzi L (2006) Cattle rob(1;29) originating from complex chromosome rearrangements as revealed by both banding and FISH-mapping techniques. Chromosome Res 14:649–655

    CAS  PubMed  Google Scholar 

  • Gallagher DS Jr, Womack JE (1992) Chromosome conservation in the Bovidae. J Hered 83:287–298

    PubMed  Google Scholar 

  • Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:W695–W699

    CAS  PubMed Central  PubMed  Google Scholar 

  • Groves C, Grubb P (2011) Ungulate taxonomy. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    PubMed  Google Scholar 

  • Hassanin A, Douzery EJ (1999) Evolutionary affinities of the enigmatic saola (Pseudoryx nghetinhensis) in the context of the molecular phylogeny of Bovidae. Proc Biol Sci 7:893–900

    Google Scholar 

  • Hassanin A, Douzery EJ (2003) Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst Biol 52:206–228

    PubMed  Google Scholar 

  • Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen van Vuuren B, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335:32–50

    PubMed  Google Scholar 

  • Iannuzzi L, Di Berardino D, Gustavsson I, Ferrara L, Di Meo GP (1987) Centromeric loss in translocations of centric fusion type in cattle and water buffalo. Hereditas 106:73–81

    CAS  PubMed  Google Scholar 

  • Jobse C, Buntjer JB, Haagsma N, Breukelman HJ, Beintema JJ, Lenstra JA (1995) Evolution and recombination of bovine DNA repeats. J Mol Evol 41:277–283

    CAS  PubMed  Google Scholar 

  • Kopecna O, Kubickova S, Cernohorska H, Cabelova K, Vahala J, Rubes J (2012) Isolation and comparison of tribe-specific centromeric repeats within Bovidae. J Appl Genet 53:193–202

    PubMed  Google Scholar 

  • Kubickova S, Cernohorska H, Musilova P, Rubes J (2002) The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res 10:571–577

    CAS  PubMed  Google Scholar 

  • Lee C, Wevrick R, Fisher RB, Ferguson-Smith MA, Lin CC (1997) Human centromeric DNA. Hum Genet 100:291–304

    CAS  PubMed  Google Scholar 

  • Louzada S, Paço A, Kubickova S, Adega F, Guedes-Pinto H, Rubes J, Chaves R (2008) Different evolutionary trails in the related genomes Cricetus cricetus and Peromyscus eremicus (Rodentia, Cricetidae) uncovered by orthologous satellite DNA repositioning. Micron 39:1149–1155

    CAS  PubMed  Google Scholar 

  • Macaya G, Cortadas J, Bernardi G (1978) An analysis of the bovine genome by density-gradient centrifugation. Preparation of the dG + dC-rich DNA components. Eur J Biochem 84:179–188

    CAS  PubMed  Google Scholar 

  • Matthee CA, Davis SK (2001) Molecular insights into the evolution of the family Bovidae: a nuclear DNA perspective. Mol Biol Evol 18:1220–1230

    CAS  PubMed  Google Scholar 

  • Modi WS, Gallagher DS, Womack JE (1996) Evolutionary histories of highly repeated DNA families among the Artiodactyla (Mammalia). J Mol Evol 42:337–349

    CAS  PubMed  Google Scholar 

  • Modi WS, Ivanov S, Gallagher DS (2004) Concerted evolution and higher-order repeat structure of the 1.709 (satellite IV) family in bovids. J Mol Evol 58:460–465

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nowak RM (1999) Order Artiodactyla. In: Walker’s Mammals of the World, vol 2, 6th edn. The Johns Hopkins University Press, Baltimore, 1051–1238

  • Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354

    CAS  PubMed  Google Scholar 

  • Pauciullo A, Kubickova S, Cernohorska H, Petrova K, Di Berardino D, Ramunno L, Rubes J (2006) Isolation and physical localization of new chromosome-specific centromeric repeats in farm animals. Vet Med 51

  • Qureshi SA, Blake RD (1995) Sequence characteristics of a cervid DNA repeat family. J Mol Evol 40:400–404

    CAS  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer

  • Robinson TJ, Ropiquet A (2011) Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst Biol 60:439–450

    PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    PubMed Central  PubMed  Google Scholar 

  • Ropiquet A, Li B, Hassanin A (2009) SuperTRI: a new approach based on branch support analyses of multiple independent data sets for assessing reliability of phylogenetic inferences. C R Biol 332:832–847

    CAS  PubMed  Google Scholar 

  • Rubes J, Kubickova S, Pagacova E, Cernohorska H, Di Berardino D, Antoninova M, Vahala J, Robinson TJ (2008) Phylogenomic study of spiral-horned antelope by cross-species chromosome painting. Chromosome Res 16:935–947

    CAS  PubMed  Google Scholar 

  • Saffery R, Earle E, Irvine DV, Kalitsis P, Choo KH (1999) Conservation of centromere protein in vertebrates. Chromosome Res 7:261–265

    CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins D (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    PubMed Central  PubMed  Google Scholar 

  • Skowronski J, Plucienniczak A, Bednarek A, Jaworski J, Bovine 1.709 satellite (1984) Recombination hotspots and dispersed repeated sequences. J Mol Biol 177:399–416

    CAS  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    CAS  PubMed  Google Scholar 

  • Tanaka K, Matsuda Y, Masangkay JS, Solis CD, Anunciado RVP, Namikawa T (1999) Characterization and chromosomal distribution of satellite DNA sequences of the water buffalo (Bubalus bubalis). J Hered 90:418–422

    CAS  PubMed  Google Scholar 

  • Tanaka K, Matsuda Y, Masangkay JS, Solis CD, Anunciado RV, Kuro-o M, Namikawa T (2000) Cytogenetic analysis of the tamaraw (Bubalus mindorensis): a comparison of R-banded karyotype and chromosomal distribution of centromeric satellite DNAs, telomeric sequence, and 18S-28S rRNA genes with domestic water buffaloes. J Hered 91:117–121

    CAS  PubMed  Google Scholar 

  • Ugarković D, Plohl M (2002) Variation in satellite DNA profiles-causes and effects. EMBO J 21:5955–5959

    PubMed  Google Scholar 

  • Vaiman D, Billault A, Tabet-Aoul K, Schibler L, Vilette D, Oustry-Vaiman A, Soravito C, Cribiu EP (1999) Construction and characterization of a sheep BAC library of three genome equivalents. Mamm Genome 10:585–587

    CAS  PubMed  Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Wurster DH, Benirschke K (1968) Chromosome studies in the superfamily Bovoidea. Chromosoma 25:152–171

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Terence J. Robinson and Anne Ropiquet for kindly providing several samples and for useful comments on a draft of the manuscript. This work was supported by the Ministry of Agriculture of the Czech Republic (project MZE 0002716202), the Grant Agency of the Czech Republic (grant P506/10/0421) and by the project “CEITEC—Central European Institute of Technology” (CZ.1.05/1.1.00/02.0068) from European Regional Development Funds.

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Correspondence to Olga Kopecna.

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Responsible editor: Walther Traut

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Kopecna, O., Kubickova, S., Cernohorska, H. et al. Tribe-specific satellite DNA in non-domestic Bovidae. Chromosome Res 22, 277–291 (2014). https://doi.org/10.1007/s10577-014-9401-4

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