Skip to main content
SpringerLink
Log in

Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The possible origins and differentiation of a ZZ/ZW sex chromosome system in Semaprochilodus taeniurus, the only species of the family Prochilodontidae known to possess heteromorphic sex chromosomes, were examined by conventional (C-banding) and molecular (cross-species hybridization of W-specific WCP, Fluorescence in situ hybridization (FISH) with telomere (TTAGGG)n, and Rex1 probes) cytogenetic protocols. Several segments obtained by W-specific probe were cloned, and the sequences localized on the W chromosome were identified by DNA sequencing and search of nucleotide collections of the NCBI and GIRI using BLAST and CENSOR, respectively. Blocks of constitutive heterochromatin in chromosomes of S. taeniurus were observed in the centromere of all autosomal chromosomes and in the terminal, interstitial, and pericentromeric regions of the W chromosome, which did not demonstrate interstitial telomeric sites with FISH of the telomere probe. The Rex1 probe displayed a compartmentalized distribution pattern in some chromosomes and showed signs of invasion of the pericentromeric region in the W chromosome. Chromosomal painting with the W-specific WCP of S. taeniurus onto its own chromosomes showed complete staining of the W chromosome, centromeric sites, and the ends of the Z chromosome, as well as other autosomes. However, cross-species painting using this WCP on chromosomes of S. insignis, Prochilodus lineatus, and P. nigricans did not reveal a proto-W element, but instead demonstrated scattered positive signals of repetitive DNAs. Identification of the W-specific repetitive sequences showed high similarity to microsatellites and transposable elements. Classes of repetitive DNA identified in the W chromosome suggested that the genetic degeneration of this chromosome in S. taeniurus occurred through accumulation of these repetitive DNAs.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Genes and Evolution of Genes and Proteins. Sinauer, Sunderland, pp 38–61

    Google Scholar 

  • Artoni RF, Vicari MR, Endler AL, Cavallaro ZI, Jesus CM, Almeida MC, Moreira-Filho O, Bertollo LAC (2006) Banding pattern of A and B chromosomes of Prochilodus lineatus (Characiformes, Prochilodontidae), with comments on B chromosomes evolution. Genetica 127:277–284. doi:10.1007/s10709-005-4846-1

    Article  PubMed  Google Scholar 

  • Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erytrinidae). Braz J Genet 1:103–120

    Google Scholar 

  • Bohne A, Zhou Q, Amandine D, Schmidt C, Schartl M, Galiana-Arnoux D, Volff JN (2012) Zisupton—A novel superfamily of DNA transposable elements recently active in fish. Mol Biol Evol 29(2):631–645. doi:10.1093/molbev/msr208

    Article  PubMed  Google Scholar 

  • Brooks LD (1988) The evolution of recombination rates. In: Michod RE, Levin BR (eds) The Evolution of Sex. Sianauer, Sunderland, pp 87–105

    Google Scholar 

  • Canapa A, Cerioni PN, Barucca M, Olmo E, Caputo V (2002) A centromeric satellite DNA may be involved in heterochromatin compactness in gobiid fishes. Chromosome Res 10:297–304. doi:10.1023/A:1016519708187

    Article  PubMed  CAS  Google Scholar 

  • Caputo V, Giovannotti M, Cerioni PN, Splendiani A, Tagliavini J, Olmo E (2011) Chromosomal study of a lamprey (Lampetra zanandreai Vladykov, 1955) (Petromyzonida: Petromyzontiformes): convencional and FISH analysis. Chromosome Res 19:481–491

    Article  PubMed  CAS  Google Scholar 

  • Carvalho NDM, Gross MC, Schneider CH, Terencio ML, Zuanon J, Feldberg E (2012) Cytogenetics of Synbranchiformes: a comparative analysis of two Synbranchus Bloch, 1795 species from the Amazon. Genetica 140:149–158

    Article  PubMed  CAS  Google Scholar 

  • Castro RMC, Vari RP (2004) Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): A Phylogenetic and Revisionary Study: Smithsonian Contributions and Studies Series. An Imprint of Smithsonian Books, Washington, D. C. N622

    Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128. doi:10.1038/sj.hdy.6800697

    Article  PubMed  CAS  Google Scholar 

  • Cioffi MB, Bertollo LAC (2010) Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group. Heredity 105:554–561. doi:10.1038/hdy.2010.18

    Article  PubMed  CAS  Google Scholar 

  • Cioffi MB, Sanchez A, Marchal JA, Kosyakova N, Liehr T, Trifonov V (2011) Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species. Genetica 8:1065–1072. doi:10.1007/s10709-011-9610-0

    Article  Google Scholar 

  • Dasilva C, Hadji H, Ozouf-Costaz C, Nicaud S, Jaillon O, Weissenbach J, Roest Crollius H (2002) Remarkable compartmentalization of transposable elements and pseudogenes in the heterocromatin of the Tetraodon nigroviridis genome. Proc Natl Acad Sci USA 21:13636–13641

    Article  Google Scholar 

  • Diniz D, Laudicina A, Cioffi MB, Bertollo LAC (2008) Microdissection and whole chromosome painting. Improving sex chromosome analysis in Triportheus (Teleostei, Characiformes). Cytogenet Genome Res 122:163–168. doi:10.1159/000163094

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H (2011) Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12:157–166. doi:10.1038/nrg2948

    Article  PubMed  CAS  Google Scholar 

  • Feldberg E, Bertollo LAC, Almeida-Toledo LF, Foresti F, Moreira-Filho O, Santos AF (1987) Biological aspects of Amazonian fishes. IX. Cytogenetic studies in two species of the genus Semaprochilodus (Pisces, Prochilodontidae). Genome 29:1–4

    Article  Google Scholar 

  • Grewal SIS, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46. doi:10.1038/nrg2008

    Article  PubMed  CAS  Google Scholar 

  • Gross MC, Schneider CH, Valente GT, Porto JIR, Martins C, Feldberg E (2010) Comparative cytogenetic analysis of the genus Symphysodon (Discus Fishes, Cichlidae): chromosomal characteristics of retrotransposons and minor ribosomal DNA. Cytogenet Genome Res 127:43–53. doi:10.1159/000279443

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/96/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hatanaka T, Henrique-Silva F, Galetti PM Jr (2002) A polymorphic, telomeric-like sequence microsatellite in the neotropical fish Prochilodus. Cytogenet Genome Res 98:308–310. doi:10.1159/000071054

    Article  PubMed  CAS  Google Scholar 

  • Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780

    Article  PubMed  CAS  Google Scholar 

  • Jesus CM, Galetti PM Jr, Valentini SR, Moreira-Filho O (2003) Molecular characterization and chromosomal location of two families of satellite DNA in Prochilodus lineatus (Pisces, Prochilodontidae), a species with B chromosomes. Genetica 118:25–32. doi:10.1023/A:1022986816648

    Article  PubMed  Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467

    Article  PubMed  CAS  Google Scholar 

  • Jurka J, Bao W, Kojima KK (2011) Families of transposable elements, population structure and the origin of species. Biol Direct 6:44. doi:10.1186/1745-6150-6-44

    Article  PubMed  CAS  Google Scholar 

  • Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in repbase: repbase submitter and censor. BMC Bioinforma 7:474

    Article  Google Scholar 

  • Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220

    Article  Google Scholar 

  • Machado TC, Pansonato-Alves JC, Pucci MB, Nogaroto V, Almeida MC, Oliveira C, Foresti F, Bertollo LAC, Moreira-Filho O, Artoni RF, Vicari MR (2011) Chromosomal painting and ZW sex chromosomes differentiation in Characidium (Characiformes, Crenuchidae). BMC Genet 12:65. doi:10.1186/1471-2156-12-65

    Article  PubMed  Google Scholar 

  • Mago-Leccia E (1972) Consideraciones sobre la sistematica de la familia prochilodontidae (Osteichthyes, Cypriniformes), con una sinopsia de las especies de Venezuela. Acta Biol Venezuelica 8(Suppl 1):35–96

    Google Scholar 

  • Marreta ME, Faldoni FLC, Parise-Maltempi PP (2012) Cytogenetic mapping of the W chromosome in the genus Leporinus (Teleostei, Anostomidae) using a highly repetitive DNA sequence. J Fish Biol 80:630–637. doi:10.1111/j.1095-8649.2011.03199.x

    Article  PubMed  CAS  Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9

    Article  Google Scholar 

  • Noleto RB, Vicari MR, Cestari MM, Artoni RF (2012) Variable B chromosomes frequencies between males and females of two species of pufferfishes (Tetraodontiformes). Rev Fish Biol Fisheries 22:343–349. doi:10.1007/s11160-011-9231-9

    Article  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex-Linked Genes. Springer, Berlin

    Book  Google Scholar 

  • Oliveira C, Nirchio M, Granado A, Levy S (2003) Karyotypic characterization of Prochilodus mariae, Semaprochilodus kneri and Semaprochilodus laticeps (Teleostei: Prochilodontidae) from caicara del orinoco, Venezuela. Neotrop Ichthyol 1:47–52. doi:10.1590/S1679-62252003000100005

    Article  Google Scholar 

  • Oliver KR, Greene WK (2011) Mobile DNA and the TE-Thrust Hypothesis: supporting evidence from the primates. Mob DNA 2:8. doi:10.1186/1759-8753-2-8

    Article  PubMed  CAS  Google Scholar 

  • Pauls E, Bertollo LAC (1990) Distribution of a supernumerary chromosome system and aspects of karyotypic evolution in the genus Prochilodus (Pisces, Prochilodontidae). Genetica 81:117–123. doi:10.1007/BF00226450

    Article  Google Scholar 

  • Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: A laboratory manual, vol I. Cold Spring Harbor Press, Cold Spring Harbor

    Google Scholar 

  • Schemberger MO, Bellafronte E, Nogaroto V, Almeida MC, Schuhli GS, Artoni RF, Moreira-Filho O, Vicari MR (2011) Differentiation of repetitive DNA sites and sex chromosome systems reveal closely related group in Parodontidae (Actinopterygii: Characiformes). Genetica 139:1499–1508. doi:10.1007/s10709-012-9649-6

    Article  PubMed  Google Scholar 

  • Skipper M (2007) Mysteries of heterochromatic sequences unravelled. Nat Rev Genet 8:567. doi:10.1038/nrg2161

    Article  CAS  Google Scholar 

  • Steinemann S, Steinemann M (2005) Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143. doi:10.1159/000084945

    Article  PubMed  CAS  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  PubMed  CAS  Google Scholar 

  • Takehana Y, Naruse K, Asada Y, Matsuda Y, Shin-I T, Kohara Y, Fujiyama A, Hamaguchi S, Sakaizumi M (2012) Molecular cloning and characterization of the repetitive DNA sequences that comprise the constitutive heterochromoatin of the W chromosomes of the medaka fishes. Chromosome Res 20:71–81. doi:10.1007/s10577-011-9259-7

    Article  PubMed  CAS  Google Scholar 

  • Terencio ML, Schneider CH, Gross MC, Vicari MR, Feldberg E (2012) Stable karyotypes: a general rule for the fish of the family Prochilodontidae? Hydrobiologia 686:147–156. doi:10.1007/s10750-012-1006-3

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Torres GA, Gong Z, Iovene M, Hirsch CD, Buell CR, Bryan GL, Novák P, Macas J, Jiang J (2011) Organization and evolution of subtelomeric satellite repeats in the potato genome. Genes Genomes Genet 1:85–92. doi:10.1534/g3.111.000125

    CAS  Google Scholar 

  • Valente GT, Mazzuchelli J, Ferreira IA, Poletto AB, Fantinatti BEA, Martins C (2011) Cytogenetic mapping of the retroelements Rex1, Rex3 and Rex6 among cichlid fish: new insights on the chromosomal distribution of transposable elements. Cytogenet Genome Res 133:34–42. doi:10.1159/000322888

    Article  PubMed  CAS  Google Scholar 

  • Venere PC, Miyazawa CS, Galetti-Jr PM (1999) New cases of supernumerary chromosomes in characiform fishes. Genet Mol Biol 22:345–349. doi:10.1590/S1415-47572006000400008

    Article  Google Scholar 

  • Vicari MR, Almeida MC, Bertollo LAC, Moreira-Filho O, Artoni RF (2006) Cytogenetic analysis and chromosomal characteristics of the polymorphic 18S rDNA in the fish Prochilodus lineatus (Characiformes, Prochilodontidae). Genet Mol Biol 4:621–625. doi:10.1590/S1415-47572006000400008

    Article  Google Scholar 

  • Vicari MR, Nogaroto V, Noleto RB, Cestari MM, Cioffi MB, Almeida MC, Moreira-Filho O, Bertollo LAC, Artoni RF (2010) Satellite DNA and chromosomes in neotropical fishes: methods, applications and perspectives. J Fish Biol 76:1094–1116. doi:10.1111/j.1095-8649.2010.02564.x

    Article  PubMed  CAS  Google Scholar 

  • Volff JN, Korting C, Schartl M (2000) Multiple lineages of the non-LTR retrotransposons Rex1with varying success in invading fish genomes. Mol Biol Evol 17:1673–1684

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanable M, Kuroiwa A, Hirai H, Hirai Y, Matsuda Y, Okada N (2011) B chromosomes have a functional effect on female sex determination in lake victoria cichlid fishes. PLoS Genet 7(8):e1002203. doi:10.1371/journal.pgen.1002203

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by National Council for Scientific and Technological Development (CNPq—141660/2009-0), National Amazon Research Institute/Genetic, Conservations and Evolutionary Biology (INPA/GCBEV), The State of Amazonas Research Foundation (FAPEAM) and Centre for Studies of Adaptation to Environmental Changes in the Amazon (INCT ADAPTA,FAPEAM/CNPq 573976/2008-2), PRONEX/FAPEAM/CNPQ 003/2009.

Author information

Authors and Affiliations

  1. Laboratório de Genética Animal, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Petrópolis, Manaus, AM, 69011-970, Brazil

    Maria Leandra Terencio, Carlos Henrique Schneider & Eliana Feldberg

  2. Laboratório de Citogenômica Animal, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, AM, Brazil

    Maria Claudia Gross

  3. Laboratório de Citogenética e Evolução, Departamento de Biologia Estrutural, Universidade Estadual de Ponta Grossa, Molecular e Genética, Ponta Grossa, PR, Brazil

    Viviane Nogaroto, Mara Cristina de Almeida, Roberto Ferreira Artoni & Marcelo Ricardo Vicari

Authors
  1. Maria Leandra Terencio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos Henrique Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Claudia Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Viviane Nogaroto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mara Cristina de Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roberto Ferreira Artoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo Ricardo Vicari
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eliana Feldberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Leandra Terencio.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Terencio, M.L., Schneider, C.H., Gross, M.C. et al. Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus . Genetica 140, 505–512 (2012). https://doi.org/10.1007/s10709-013-9699-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-013-9699-4

Keywords

Search

Navigation