Skip to main content
SpringerLink
Log in

The library model for satellite DNA evolution: a case study with the rodents of the genus Ctenomys (Octodontidae) from the Iberá marsh, Argentina

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

On the basement of the library model of satellite DNA evolution is the differential amplification of subfamilies through lineages diversification. However, this idea has rarely been explored from an experimental point of view. In the present work, we analyzed copy number and sequence variability of RPCS (repetitive PvuII Ctenomys sequence), the major satellite DNA present in the genomes of the rodents of the genus Ctenomys, in a closely related group of species and forms inhabiting the Iberá marsh in Argentina. We studied the dependence of these two parameters at the intrapopulation level because in the case of interbreeding genomes, differences in RPCS copy number are due to recent amplification/contraction events. We found an inverse relationship among RPCS copy number and sequence variability: amplifications lead to a decrease in sequence variability, by means of biased homogenization of the overall satellite DNA, prevailing few variants. On the contrary, the contraction events that involve tandems of homogeneous monomers contribute—by default—minor variants to become “evident”, which otherwise were undetectable. On the other hand, all the RPCS sequence variants are totally or partially shared by all the studied populations. As a whole, these results are comprehensible if these RPCS variants preexisted in the common ancestor of this Ctenomys group.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anderson S, de Bruijn MH, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    Article  CAS  PubMed  Google Scholar 

  • Argüelles CF, Suárez P, Giménez MD, Bidau CJ (2001) Intraspecific chromosome variation between different populations of Ctenomys dorbignyi (Rodentia, Ctenomyidae) from Argentina. Acta Theriol 46(4):363–373

    Article  Google Scholar 

  • Bruvo-Madaric B, Plohl M, Ugarković D (2007) Wide distribution of related satellite DNA families within the genus Pimelia (Tenebrionidae). Genetica 130:35–42

    Article  PubMed  Google Scholar 

  • Capanna E, Castiglia R (2004) Chromosomes and speciation in Mus musculus domesticus. Cytogenet Genome Res 105:375–384

    Article  CAS  PubMed  Google Scholar 

  • Carpentier G (2008) Dot blot analyzer: software development using the macro language of imageJ. ImageJ User and Developer Conference proceedings

  • Castiglia R, Garagna S, Merico V, Oguge N, Corti M (2006) Cytogenetics of a new cytotype of African Mus (subgenus Nannomys) minutoides (Rodentia, Muridae) from Kenya: C- and G- banding and distribution of (TTAGGG)n telomeric sequences. Chromosome Res 14:587–594

    Article  CAS  PubMed  Google Scholar 

  • Dobigny G, Aniskin V, Granjon L, Cornette R, Volobouev V (2005) Recent radiation in West African Taterillus (Rodentia, Gerbillinae): the concerted role of chromosome and climatic changes. Heredity 95:358–368

    Article  CAS  PubMed  Google Scholar 

  • Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Philos Trans R Soc Lond B Biol Sci 312:275–289

    Article  CAS  PubMed  Google Scholar 

  • Ellingsen A, Slamovits CH, Rossi MS (2007) Sequence evolution of the major satellite DNA of the genus Ctenomys (Octodontidae, Rodentia). Gene 392:283–290

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Fronicke L, Scherthan H (1997) Zoo-fluorescence in situ hybridization analysis of human and Indian muntjac karyotypes (Muntiacus muntjak vaginalis) reveals satellite DNA clusters at the margins of conserved syntenic segments. Chromosome Res 5:254–261

    Article  CAS  PubMed  Google Scholar 

  • Fry K, Salser W (1977) Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084

    Article  CAS  PubMed  Google Scholar 

  • García L, Ponsà M, Egozcue J, García M (2000) Cytogenetic variation in Ctenomys perrensi (Rodentia, Octodontidae). Biol J Linn Soc 69:103–120

    Article  Google Scholar 

  • Giménez MD, Mirol PM, Bidau CJ, Searle JB (2002) Molecular analysis of populations of Ctenomys (Caviomorpha, Rodentia) with high karyotypic variability. Cytogenet Genome Res 96:130–136

    Article  PubMed  Google Scholar 

  • Grewal SI, Elgin SC (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447:399–406

    Article  CAS  PubMed  Google Scholar 

  • Hartmann N, Scherthan H (2004) Characterization of ancestral chromosome fusion points in the Indian muntjac deer. Chromosoma 112:213–220

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Dalal Y (2005) Centromeric chromatin: what makes it unique? Curr Opin Genet Dev 15:177–184

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Kiblisky P, Brum-Zorrilla N, Perez G, Saez F (1977) Variabilidad cromosómica entre diversas poblaciones uruguayas del roedor cavador del genero Ctenomys (Rodentia-Octodontidae). Mendeliana 2:85–93

    Google Scholar 

  • Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci USA 103:4186–4191

    Article  CAS  PubMed  Google Scholar 

  • Lanzone C, Bidau CJ, Giménez MD, Santos JL (2002) Synaptic behaviour and morphological modifications of the X and Y chromosomes during pachytene in three species of Ctenomys (Rodentia, Caviomorpha, Ctenomyidae). Genome 45:1110–1115

    Article  CAS  PubMed  Google Scholar 

  • Li YC, Lee C, Sanoudou D, Hseu TH, Li SY, Lin CC (2000) Interstitial colocalization of two cervid satellite DNAs involved in the genesis of the Indian muntjac karyotype. Chromosome Res 8:363–373

    Article  CAS  PubMed  Google Scholar 

  • Luchetti A, Marini M, Mantovani B (2006) Non-concerted evolution of the RET76 satellite DNA family in Reticulitermes taxa (Insecta, Isoptera). Genetica 128:123–132

    Article  Google Scholar 

  • Matsubara K, Yamada K, Umemoto S, Tsuchiya K, Ikeda N, Nishida C, Chijiwa T, Moriwaki K, Matsuda Y (2008) Molecular cloning and characterization of the repetitive DNA sequences that comprise the constitutive heterochromatin of the A and B chromosomes of the Korean field mouse (Apodemus peninsulae, Muridae, Rodentia). Chromosome Res 16:1013–1026

    Article  CAS  PubMed  Google Scholar 

  • Meštrović N, Plohl M, Mravinac B, Ugarković D (1998) Evolution of satellite DNAs from the genus Palorus–experimental evidence for the “library” hypothesis. Mol Biol Evol 15:1062–1068

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ortells MO, Barrantes GE (1994) Genetic distances and variability study in several species of the genus Ctenomys (Rodentia: Octodontidae), with special reference to a probable causal role of chromosomes in speciation. Biol J Linn Soc 53:189–208

    Article  Google Scholar 

  • Ortells MO, Contreras JR, Reig OA (1990) New Ctenomys karyotypes (Rodentia, Octodontidae) from north-eastern Argentina and from Paraguay confirm the extreme chromosomal multiformity of the genus. Genetica 82:189–201

    Article  Google Scholar 

  • Picariello O, Feliciello I, Bellinello R, Chinali G (2002) S1 satellite DNA as a taxonomic marker in brown frogs: molecular evidence that Rana graeca graeca and Rana graeca italica are different species. Genome 45:63–70

    Article  CAS  PubMed  Google Scholar 

  • Plohl M, Luchetti A, Meštrović N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409:72–82

    Article  CAS  PubMed  Google Scholar 

  • Pons J, Gillespie RG (2004) Evolution of satellite DNAs in a radiation of endemic Hawaiian spiders: does concerted evolution of highly repetitive sequences reflect evolutionary history? J Mol Evol 59:632–641

    Article  CAS  PubMed  Google Scholar 

  • Reig OA, Massarini AI, Ortells MO, Barros MA, Tiranti SI, Dyzenchauz FJ (1992) New karyotypes and C-banding patterns of the subterranean rodents of the genus Ctenomys (Caviomorpha, Octodontidae) from Argentina. Mammalia 54:603–623

    Article  Google Scholar 

  • Rossi MS, Reig OA, Zorzopulos J (1990) Evidence for rolling-circle replication in a major satellite DNA from the South American rodents of the genus Ctenomys. Mol Biol Evol 7:340–350

    CAS  PubMed  Google Scholar 

  • Rossi MS, Pesce CG, Reig OA, Kornblihtt AR, Zorzopulos J (1993a) Retroviral-like features in the monomer of the major satellite DNA from the South American rodents of the genus Ctenomys. DNA Seq 3:379–381

    CAS  PubMed  Google Scholar 

  • Rossi MS, Reig OA, Zorzopulos J (1993b) A major satellite DNA from the South American rodents of the genus Ctenomys: quantitative and qualitative differences in species with different geographic distribution. Z Säugetierk 58:244–251

    Google Scholar 

  • Rossi MS, Redi CA, Viale G, Massarini AI, Capanna E (1995) Chromosomal distribution of the major satellite DNA of South American rodents of the genus Ctenomys. Cytogenet Cell Genet 69:179–184

    Article  CAS  PubMed  Google Scholar 

  • Ruedas LA, Cook JA, Yates TL, Bickham JW (1993) Conservative genome size and rapid chromosomal evolution in the South American tuco-tucos (Rodentia: Ctenomyidae). Genome 36:449–458

    Article  CAS  PubMed  Google Scholar 

  • Shestakova EA, Mansuroglu Z, Mokrani H, Ghinea N, Bonnefoy E (2004) Transcription factor YY1 associates with pericentromeric gamma-satellite DNA in cycling but not in quiescent (G0) cells. Nucleic Acids Res 32:4390–4399

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP: phylogenetic analysis using parsimony (and other methods), version 4 Sinauer Associates Inc. Publishers, Sunderland, MA, USA

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

    Article  PubMed  Google Scholar 

  • Woods C, Kilpatrick C (2005) Infraorder hystricognathi brandt, 1855. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. John Hopkins University Press, Baltimore, pp 1538–1600

    Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Agencia Nacional de Investigaciones Científicas y Técnicas (PICT 3836/1) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 5776) from Argentina. D.A.C. is supported by a doctoral fellowship awarded by CONICET. M. S. R. is career investigator of the CONICET. We would like to thank Mercedes Goin and Diana Avedikian, and also three anonymous reviewers for their comments on the first version of the manuscript. We also would like to thank Thales R. de Freitas, María Jimena Gómez Fernandez, Marcelo Kittlien, Fernando Mapelli, Patricia Mirol, Matías Mora, Vanina Raimondi, Verónica Trucco Cano and Laura Wolfenson for assistance at the fieldwork.

Author information

Authors and Affiliations

  1. IFIBYNE-CONICET. Laboratorio de Fisiología y Biología Molecular, Departamento de Fisiología, Biología Molecular y Celular, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, 2do piso, EHA1428, Buenos Aires, Argentina

    Diego A. Caraballo, Pablo M. Belluscio & María Susana Rossi

Authors
  1. Diego A. Caraballo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pablo M. Belluscio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Susana Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Susana Rossi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caraballo, D.A., Belluscio, P.M. & Rossi, M.S. The library model for satellite DNA evolution: a case study with the rodents of the genus Ctenomys (Octodontidae) from the Iberá marsh, Argentina. Genetica 138, 1201–1210 (2010). https://doi.org/10.1007/s10709-010-9516-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-010-9516-2

Keywords

Search

Navigation