Skip to main content
Log in

Low rates of homogenization of the DBC-150 satellite DNA family restricted to a single pair of microchromosomes in species from the Drosophila buzzatii cluster

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

A satellite DNA family, termed DBC-150, comprises slightly GC-rich repeat units of approximately 150 bp that were isolated (by DNA digestions or PCR) from the genome of all seven Drosophila species from the buzzatii cluster (repleta group). The presence of subrepeats suggests that part of the extant DBC-150 monomer originated by the duplication of small sequence motifs. The DBC-150 family is compared to the previously described pBuM satDNA family, an abundant component of the genome of five species of the cluster. The two families are different in several aspects, including primary structure, A+T content, intraspecific and interspecific variability and rates of homogenization (or nucleotide spread). The data indicate a lower rate of homogenization (and absence of complete concerted evolution) of the DBC-150 compared to the pBuM family. FISH on metaphase chromosomes revealed that the DBC-150 family is located exclusively in the microchromosomes. To our knowledge this is the first record of a complex Drosophila satDNA restricted to a single pair of microchromosomes. The observed low rates of homogenization of the DBC-150 family might be related to a presumed reduction or suppression of meiotic recombination in the microchromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abel LDS, Mantovani M, Moreira-Filho O (2006) Chromosomal distribution of the As51 satellite DNA in two species complexes of the genus Astyanax (Pisces, Characidae). Genet Mol Biol 29: 448-52.

    Article  Google Scholar 

  • Adams MD, Celniker SE, Holt RA et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-195.

    Article  PubMed  Google Scholar 

  • Bachmann L, Sperlich D (1993) Gradual evolution of a specific satellite DNA family in Drosophila ambigua, D. tristis and D. obscura. Mol Biol Evol 10: 647-59.

    CAS  PubMed  Google Scholar 

  • Bachmann L, Venazetti F, Sbordoni V (1996). Tandemly repeated satellite DNA of Dolichopoda schiavazzi: a test for models on the evolution of highly repetitive DNA. J Mol Evol 43: 135-44.

    Article  CAS  PubMed  Google Scholar 

  • Baimai V (1977) Chromosomal polymorphisms of constitutive heterochromatin and inversions in Drosophila. Genetics 85: 85-3.

    Google Scholar 

  • Baimai V, Sene FM, Pereira MAQR (1983) Heterochromatin and karyotypic differentiation of some neotropical cactus-breeding species of the Drosophila repleta group. Genetica 67: 81-2.

    Article  Google Scholar 

  • Barragán MJL, Martínez S, Marchal JA et al. (2002) Highly repeated DNA sequences in three species of the genus Pteropus (Megachiroptera, Mammalia). Heredity 88: 366-70.

    Article  PubMed  Google Scholar 

  • Bartolomé C, Maside X (2004) The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster. Genet Res Camb 83: 91-00.

    Article  Google Scholar 

  • Bridges CB (1935) The mutants and linkage data of chromosome four of Drosophila melanogaster. Biol Zh (Moscow) 4: 401–420.

    Google Scholar 

  • Casals F, Cáceres M, Manfrin MH, González J, Ruiz A (2005) Molecular characterization and chromosomal distribution of Galileo, Kepler and Newton, three foldback transposable elements of the Drosophila buzzatii species complex. Genetics 169: 2047-059.

    Article  CAS  PubMed  Google Scholar 

  • Casals F, González J, Ruiz A (2006) Abundance and chromosomal distribution of six Drosophila buzzatii transposons: BuT1, BuT2, BuT3, BuT4, BuT5, and BuT6. Chromosoma 115: 403-12.

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215-20.

    Article  CAS  PubMed  Google Scholar 

  • de Brito RA, Manfrin MH, Sene FM (2002) Nested cladistic analysis of Brazilian populations of Drosophila serido. Mol Phyl Evol 22: 131-43.

    Article  Google Scholar 

  • de la Herrán, R, Robles F, Cuñado N et al. (2001). A heterochromatic satellite DNA is highly amplified in a single chromosome of Muscari (Hyacinthaceae). Chromosoma 110: 197-02.

    Article  PubMed  Google Scholar 

  • Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 199: 111-17.

    Article  Google Scholar 

  • Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Phil Trans R Soc Lond B 312: 272-89.

    Article  Google Scholar 

  • Fernández R, Barragán MJL, Bullejos M et al. (2001) Molecular and cytogenetic characterization of highly repeated DNA sequences in the vole Microtus cabrerae. Heredity 87: 637-46.

    Article  PubMed  Google Scholar 

  • Franco FF, Kuhn GCS, Sene FM, Manfrin MH (2006) Conservation of pBuM-2 satellite DNA sequences among geographically isolated Drosophila gouveai populations. Genetica 128: 287-95.

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Dalal Y (2005) Centromeric heterochromatin: what makes it unique? Curr Opin Genet Dev 15: 177-84.

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098-102.

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison JS, Brandes A, Schwarzacher T (2003) Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res 11: 241-53.

    Article  CAS  PubMed  Google Scholar 

  • Hochman B (1976) The fourth chromosome of Drosophila melanogaster. In Ashburner M, Novitski E, eds., The Genetics and Biology of Drosophila, Vol. 1b. New York: Academic Press, pp. 903–928.

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16: 111-20.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn GCS, Sene FM (2004) Characterisation and interpopulation variability of a complex Hpa I satellite DNA of Drosophila seriema (repleta group). Genetica 121: 241-49.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn GCS, Sene FM (2005) Evolutionary turnover of two pBuM satellite DNA subfamilies in the Drosophila buzzatii cluster (repleta group): from alpha to alpha/beta arrays. Gene 349: 77-5.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn GCS, Ruiz A, Alves MAR, Sene FM (1996) The metaphase and polytene chromosomes of Drosophila seriema (repleta group; mulleri subgroup). Brazil J Genet 19: 209-16.

    Google Scholar 

  • Kuhn GCS, Franco FF, Silva WA Jr, Martinez-Rossi NM, Sene FM (2003) On the pBuM189 satellite DNA variability among South American populations of Drosophila buzzatii. Hereditas 139: 161-66.

    Article  PubMed  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular evolutionary genetics analysis software. Tempe, Arizona: Arizona State University.

    Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4: 203-21.

    CAS  PubMed  Google Scholar 

  • Manfrin MH, Sene FM (2006) Cactophilic Drosophila in South America: a model for evolutionary studies. Genetica 126: 1-9.

    Article  Google Scholar 

  • Mantovani B, Tinti F, Bachmann L, Scali V (1997) The Bag320 satellite DNA family in Bacillus stick insects (Phasmatodea): different rates of molecular evolution of highly repetitive DNA in bisexual and parthenogenetic taxa. Mol Biol Evol 14: 1197-205.

    CAS  PubMed  Google Scholar 

  • Navajas-Pérez R, de la Herrán R, Jamilena M et al. (2005) Reduced rates of sequence evolution of Y-linked satellite DNA in Rumex (Polygonaceae). J Mol Evol 60: 391-99.

    Article  PubMed  Google Scholar 

  • Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative high-sensivity, fluorescence hybridisation. Proc Natl Acad Sci USA 83: 2934-938.

    Article  CAS  PubMed  Google Scholar 

  • Powell JR (1997) Progress and Prospects in Evolutionary Biology: The Drosophila Model. New York: Oxford University Press.

    Google Scholar 

  • Renault S, Rouleux-Bonnin F, Periquet G, Bigot Y (1999) Satellite DNA transcription in Diadromus pulchellus (Hymenoptera). Insect Biochem Mol Biol 29: 103-11.

    Article  CAS  Google Scholar 

  • Riddle NC, Elgin SCR (2006) The dot chromosome of Drosophila: insights into chromatin states and their change over evolutionary time. Chromosome Res 14: 405-16.

    Article  CAS  PubMed  Google Scholar 

  • Rojas AA, Vazquez-Tello A, Ferbeyre G et al. (2000) Hammerhead-mediated processing of satellite pDo500 family transcripts from Dolichopoda cave crickets. Nucl Acids Res 28: 4037-043.

    Article  CAS  PubMed  Google Scholar 

  • Ruiz A, Cansian AM, Kuhn GCS, Alves MAR, Sene FM (2000) The Drosophila serido speciation puzzle: putting new pieces together. Genetica 108: 217-27.

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-25.

    CAS  PubMed  Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191: 528-35.

    Article  CAS  PubMed  Google Scholar 

  • Stephan W (1989) Tandem-repetitive noncoding DNA: forms and forces. Mol Biol Evol 6: 198-12.

    CAS  PubMed  Google Scholar 

  • Stephan W, Cho S (1994) Possible role of natural selection in the formation of tandem-repetitive noncoding DNA. Genetics 136: 333-41.

    CAS  PubMed  Google Scholar 

  • Strachan T, Webb D, Dover G (1985) Transition stages of molecular drive in multiple-copy DNA families in Drosophila. EMBO J 4: 1701-708.

    CAS  PubMed  Google Scholar 

  • Sun FL, Cuaycong MH, Craig CA, Wallrath LL, Locke J (2000) The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc Natl Acad Sci USA 97: 5340-345.

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-680.

    Article  CAS  PubMed  Google Scholar 

  • Ugarkovic D (2005) Functional elements residing within satellite DNAs. EMBO J 6: 1035-039.

    Article  CAS  Google Scholar 

  • Ugarkovic D, Plohl M (2002) Variation in satellite DNA profiles–causes and effects. EMBO J 21: 5955-959.

    Article  CAS  PubMed  Google Scholar 

  • Vermaak D, Hayden HS, Henikoff S (2002) Centromere targeting element within the histone fold domain of Cid. Mol Cell Biol 22: 7553-561.

    Article  CAS  PubMed  Google Scholar 

  • Wheeler LL, Arrighi F, Cordeiro-Stone M, Lee CS (1978) Localization of Drosophila nasutoides satellite DNAs in metaphase chromosomes. Chromosoma 70: 41-0.

    Article  CAS  PubMed  Google Scholar 

  • Yamada K, Nishida-Umehara C, Matsuda Y (2004) A new family of satellite DNA sequences as a major component of centromeric heterochromatin in owls (Strigiformes). Chromosoma 112: 277-87.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gustavo C. S. Kuhn.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuhn, G.C.S., Franco, F.F., Manfrin, M.H. et al. Low rates of homogenization of the DBC-150 satellite DNA family restricted to a single pair of microchromosomes in species from the Drosophila buzzatii cluster. Chromosome Res 15, 457–470 (2007). https://doi.org/10.1007/s10577-007-1138-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-007-1138-x

Key words

Navigation