Chromosomal polymorphism in Steindachneridionmelanodermatum Garavello, 2005 (Siluriformes, Pimelodidae): a reappraisal the existence of sex chromosome system in the species

  • Daniele Aparecida Matoso
  • Vera Maria Fonseca de Almeida Val
  • Maelin da  Silva
  • Américo Moraes-Neto
  • Mara Cristina Almeida
  • Marcelo Ricardo Vicari
  • Orlando Moreira-Filho
  • Roberto Ferreira Artoni
Reviews

Abstract

Fifty-five specimens of Steindachneridion melanodermatum were analyzed using molecular and conventional cytogenetic tools. Two polymorphisms were found: one involving the length of nucleolar organizer regions and another involving two submetacentric chromosomes previously identified as sex chromosomes. The polymorphism was confirmed by homogeneity between male and female karyotypes. Nucleotide sequencing and physical chromosome mapping were also used to identify and characterize one class of repetitive DNA, named SmAluI-Rex3. Based on the results and literature the present study offers an update of the occurrence of sex chromosome system in this species.

Keywords

Evolutionary biology Karyotype evolution Sex differentiation Retrotransposon 

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Alves AL (2005) Análise da evolução da família Loricaridae (Teleostei: Siluriformes) com base em caracteres cromossômicos e de sequências de DNA. PhD Thesis. Universidade Estadual PaulistaGoogle Scholar
  3. Alves AL, Oliveira C, Foresti F (2003) Karyotype variability in eight species of the subfamilies Loricarinae and Ancistrinae (Teleostei, Siluriformes, Loricaridae). Caryologia 56:57–63Google Scholar
  4. Artoni RF, Bertollo LAC (2002) Evolutionary aspects of the ZZ/ZW sex chromosome system in the Characidae fish, genus Triportheus. A monophyletic state and NOR location on the W chromosome. Heredity 89:15–19PubMedCrossRefGoogle Scholar
  5. Artoni RF, Falcão JN, Moreira-Filho O, Bertollo LAC (2001) An uncommon condition for a sex chromosome system in Characidae fish. Distribution and differentiation of ZZ/ZW system in Triportheus. Chromosome Res 9:449–456PubMedCrossRefGoogle Scholar
  6. Bellafronte ES (2009) Citogenética Clássica e Molecular em peixes neotropicais. Estudos comparativos entre bacias hidrográficas com ênfase em região de transposição de rio. PhD Thesis. Universidade Federal de São CarlosGoogle Scholar
  7. Bertollo LAC, Mestriner CA (1998) The X1X2Y sex chromosome system in the fish Hoplias malabaricus. II. Meiotic analyses. Chromosome Res 6:141–147PubMedCrossRefGoogle Scholar
  8. Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Brazil J Genet 1:103–120Google Scholar
  9. Bertollo LAC, Takahashi CS, Moreira-Filho O (1979) Karyotypic studies of two allopatric populations of the genus Hoplias (Pisces, Erythrinidae). Brazil J Genet 2:17–37Google Scholar
  10. Bertollo LAC, Fontes MS, Fenocchio AS, Jesus C (1997) The X1X2Y sex chromosome system in the fish Hoplias malabaricus. I. G-, C- and chromosome replication banding. Chromosome Res 5:493–499PubMedCrossRefGoogle Scholar
  11. Born GG, Bertollo LAC (2000) An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res 8:111–118PubMedCrossRefGoogle Scholar
  12. Brum MJI, Galetti PM Jr, Correa MMO, Aguilar CT (1992) Multiple sex chromosomes in South Atlantic ash, Brevoortia aurea, Clupeidae. Brazil J Genet 15:547–553Google Scholar
  13. Capistano TG, Castro ALBP, Júlio-Junior HF (2008) Chromosome divergence and NOR polymorphism in Bryconamericus aff. iheringii (Teleostei, Characidae) in the hydrographic systems of Paranapanema and Ivaí Rivers, Paraná, Brazil. Genet Mol Biol 31:203–207. doi:10.1590/S1415-47572008000200006 CrossRefGoogle Scholar
  14. Carvalho RA, Dias AL (2005) Karyotypic characterization of Iheringichthys labrosus (Pisces, Pimelodidae): C-, G- and restriction endonuclease banding. Genet Mol Res 4:663–667PubMedGoogle Scholar
  15. Carvalho RA, Giuliano-Caetano L, Dias AL (2004) Cytogenetic analysis of A- and B-chromosomes of Iheringichthys labrosus (Pisces, Pimelodidae) from the Tibagi River, Paraná, Brazil. Cytologia 69:381–385CrossRefGoogle Scholar
  16. Centofante L, Bertollo LA, Moreira-Filho O (2006) Cytogenetic characterization and description of na XX/XY1Y2 sex chromosome system in catfish Harttia carvalhoi (Siluriformes, Loricariidae). Cytogenet Genome Res 112:320–324PubMedCrossRefGoogle Scholar
  17. Dimitri P, Junakovic N (1999) Revising the selfish DNA hypotehis. New evidence on accumulation of transposable elements in heterochromatin. Trends Genet 15:123–124. doi:10.1016/S0168-9525(99)01711-4 PubMedCrossRefGoogle Scholar
  18. Feldberg E, Bertollo LAC (1985) Nucleolar organizing regions in species of Neotropical Cichlid fish (Pisces, Perciformes). Caryologia 38:319–324Google Scholar
  19. Fenocchio AS, Bertollo LAC (1992) Karyotype similarities among Pimelodidae (Pisces, Siluriformes) from the Brazilian Amazon region. Cytobios 69:41–46PubMedGoogle Scholar
  20. Fernandes FMC, Albert JS, Daniel-Silva MFZ, Lopes CE, Crampton WGR, Almeida-Toledo LF (2005) A new Gymnotus (Teleostei: Gymnotiformes: Gymnotidae) from the Pantanal Matogrossense of Brazil and adjacent drainages: continued documentation of a cryptic fauna. Zootaxa 933:1–14Google Scholar
  21. Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 978:223–257CrossRefGoogle Scholar
  22. Foresti F, Oliveira C, Galetti PM Jr, Almeida-Toledo LF (1993) Synaptonemal complex analysis in spermatocytes of tilapia, Oreochromis niloticus (Pisces, Cichlidae). Genome 36:1124–1128PubMedCrossRefGoogle Scholar
  23. Galetti PM Jr, Foresti F, Bertollo LAC, Moreira-Filho O (1981) Heteromorphic sex chromosomes in three species of the genus Leporinus (Pisces, Anostomidae). Cytog Cell Genet 29:138–142CrossRefGoogle Scholar
  24. Garavello JC (2005) Revision of genus Steindachneridion (Siluriformes: Pimelodidae). Neotrop Ichthyol 3:607–623. doi:10.1590/S1679-62252005000400018 CrossRefGoogle Scholar
  25. Garcia C, Moreira-Filho O (2005) Cytogenetical analyses in three fish species of the genus Pimelodus (Siluriformes: Pimelodidae) from rio São Francisco: considerations about the karyotypical evolution in the genus. Neotrop Ichthyol 3:285–290. doi:10.1590/S1679-62252005000200006 CrossRefGoogle Scholar
  26. Garcia C, Moreira-Filho O (2008) Localization of ribosomal genes in three Pimelodus species (Siluriformes, Pimelodidae) of the São Francisco River: 5S genes as markers and conservation of the 18S rDNA sites. Genet Mol Biol 31:261–264. doi:10.1590/S1415-47572008000200018 CrossRefGoogle Scholar
  27. Gross MC, Schneider CH, Valente GT, Porto JIR, Martins C, Feldberg E (2009) 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 PubMedCrossRefGoogle Scholar
  28. Hatanaka T, Galetti PM Jr (2004) Mapping of the 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica 122:239–244. doi:10.1007/s10709-004-2039-y PubMedCrossRefGoogle Scholar
  29. Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015. doi:10.1007/BF01953855 PubMedCrossRefGoogle Scholar
  30. Jesus CM, Moreira-Filho O (2000) Cytogenetics studies in some Apareiodon species (Pisces, Parodontidae). Cytologia 65:397–402Google Scholar
  31. Kavalco KF, Pazza R, Bertollo LAC, Moreira-Filho O (2004) Gene mapping of 5S rDNA sites in eight fish species from the Paraíba do Sul river basin, Brazil. Cytogenet Genome Res 106:107–110. doi:10.1159/000078567 PubMedCrossRefGoogle Scholar
  32. Kligerman AD, Blum SE (1977) Rapid chromosome preparations from solid tissues of Fishes. J Fish Res Bd Can 34:266–269CrossRefGoogle Scholar
  33. Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220CrossRefGoogle Scholar
  34. Maistro EL, Mata EP, Oliveira C, Foresti F (1998) Unusual occurrence of a ZZ/ZW sex-chromosome system and supernumerary chromosomes in Characidium cf. fasciatum (Pisces, Characiformes, Characidiinae). Genetica 104:1–7. doi:10.1023/A:1003242020259 PubMedCrossRefGoogle Scholar
  35. Martins C, Galetti PM Jr (1999) Chromosomal localization of 5S rDNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosome Res 7:363–367PubMedCrossRefGoogle Scholar
  36. Martins C, Galetti PM Jr (2001) Organization of 5S rDNA in species of the fish Leporinus: two different genomic location are characterized by distinct nontranscribed spacers. Genome 44:903–910PubMedGoogle Scholar
  37. Martins IC, Portella-Castro ALB, Julio HF Jr (1995) Chromosome analysis of 5 species of the Cichlidae Family (Pisces-Perciformes) from the Paraná river. Cytologia 60:223–231Google Scholar
  38. Mazzuchelli J, Martins C (2009) Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus. Genetic 136:461–469. doi:10.1007/s10709-008-9346-7 CrossRefGoogle Scholar
  39. Mestriner CA, Bertollo LAC, Galetti PM Jr (1995) Chromosome banding and synaptonemal complexes in Leporinus lacustris (Pisces, Anostomidae): analysis of a sex system. Chromosome Res 3:440–443PubMedCrossRefGoogle Scholar
  40. Michele JL, Takahashi CS (1977) Comparative cytology of Tilapia randalli and Geophagus brasiliensis (Cichlidae, Pisces). Cytologia 42:535–537Google Scholar
  41. Moreira-Filho O, Bertollo LAC, Galetti PM Jr (1984) Structure and variability of nucleolar organizing regions in Parodontidae fish. Can J Genet Cytol 26:564–568Google Scholar
  42. Moreira-Filho O, Bertollo LAC, Galetti PM Jr (1985) Karyotypic study of some species of family Parodontidae (Pisces–Cypriniformes). Caryologia 38:47–55Google Scholar
  43. Morelli S, Vicari MR, Bertollo LAC (2007) Evolutionary cytogenetics of the Hoplias lacerdae, Miranda Ribeiro, 1908 group. A particular pathway concerning the other Erythrinidae fish. Brazil J Biol 67:897–903CrossRefGoogle Scholar
  44. Oliveira C, Gosztonyi AEA (2000) Cytogenetic study of Diplomysues mesembrinus (Teleostei, Siluriformes, Diplomystidae) with e discussion of chromosome evolution in Siluriformes. Caryologia 53:31–37Google Scholar
  45. Oliveira C, Almeida-Toledo LF, Foresti F (2005) Karyotypic evolution in Neotropical fishes. In: Pisano E, Ozouf-Costaz C, Foresti F, Kapoor BG (eds) Fish cytogenetics, 1st edn. Science Publisher Inc, Enfield, pp 1–49Google Scholar
  46. Ozouf-Costaz C, Brandt J, Körting C, Pisano E, Bonillo C, Countaceau JP, Volff JN (2004) Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish. Antarct Sci 16:51–57. doi:10.1017/S0954102004001816 CrossRefGoogle Scholar
  47. Pimpinelli S, Berloco M, Fanti L, Dimitri P, Bonaccorsi S, Marchetti E, Caizzi R (1995) Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci USA 92:3804–3808. doi:10.1073/pnas.92.9.3804 PubMedCrossRefGoogle Scholar
  48. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci 83:2934–2938PubMedCrossRefGoogle Scholar
  49. Porto-Foresti F, Oliveira C, Gomes EA, Tabata YA, Rigolino MG, Foresti F (2004) A lethal effect associated with polymorphism of the NOR-bearing chromosomes in rainbow trout (Oncorhyncus mykiss). Genet Mol Biol 27:51–54. doi:10.1590/S1415-47572004000100009 CrossRefGoogle Scholar
  50. Posada D, Crandal KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics Appl Note 14:817–818CrossRefGoogle Scholar
  51. Presting GG, Malysheva L, Fuchs J, Schubert I (1998) A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J 6:721–728. doi:10.1046/j.1365-313x.1998.00341.x CrossRefGoogle Scholar
  52. Ribeiro LB, Matoso DA, Almeida MC, Vicari MR, Moraes-Neto A, Svidnicki MCCM, Artoni RF (2008) Karyotypic variability in Iheringichthys labrosus (Teleostei, Pimelodidae) from the Tibagi River basin (Paraná State, Brazil). Genet Mol Res 7:718–724. doi:10.4238/vol7-3gmr456 PubMedCrossRefGoogle Scholar
  53. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  54. Silva EB, Margarido VP (2005) An X1X1X2X2/X1X2Y multiple sex chromosome system in a new species of the genus Gymnotus (Pisces, Gymnotiformes). Env Biol Fish 73:293–297. doi:10.1007/s10641-005-2144-5 CrossRefGoogle Scholar
  55. Souza L, Giuliano-Caetano L, Dias AL (2003) Karyotypic study of three species of Pimelodus (Pisces, Pimelodidae) from the Paraguai River Basin. Cytologia 4:345–350CrossRefGoogle Scholar
  56. Souza L, Swarça AC, Dias AL (2004) Analysis of the nucleolus organizer regions in 5 species of the genus Pimelodus (Siluriformes, Pimelodidae) using AgNO3, CMA3 and FISH with the 18S rDNA probe. Caryologia 57:145–151Google Scholar
  57. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 74:304–306. doi:10.1016/0014-4827(72)90558-7 CrossRefGoogle Scholar
  58. Swarça AC, Giuliano-Caetano L, Dias AL (1999) Cytogenetic characterization through chromosomic banding of Pinirampus pirinampu (Pisces, Pimelodidae) from the Tibagi river basin Pr/Brazil. Caryologia 1–2:31–35Google Scholar
  59. Swarça AC, Cestari MM, Giuliano-Caetano L, Dias AL (2001) Cytogenetic characterization of the large South American siluriform fish species Zungaro zungaro (Pisces, Pimelodidae). Chromosome Sci 5:51–55Google Scholar
  60. Swarça AC, Fenocchio AS, Cestari MM, Dias AL (2005) First chromosome data on Steindachneridion scripta (Pisces, Siluriformes, Pimelodidae) from Brazilian rivers: Giemsa, CBG, G-, and RE banding. Genet Mol Res 4:734–741PubMedGoogle Scholar
  61. Swarça AC, Fenocchio AS, Cestari MM, Bertollo LAC, Dias AL (2006) Heteromorphic sex chromosome system with an exceptionally large Y chromosome in a catfish Steindachneridion sp. (Pimelodidae). Cytogenet Genome Res 112:325–328. doi:10.1159/000089888 PubMedCrossRefGoogle Scholar
  62. Swarça AC, Fenocchio AS, Dias AL (2007) An update cytogenetic review for species of the families Pseudopimelodidae, Pimelodidade and Heptapteridae (Pisces, Siluriformes). Suggestion of a cytotaxonomical classification. Caryologia 4:338–348Google Scholar
  63. Swarça AC, Fenocchio AS, Cestari MM, Dias AL (2009) Localization and characterization of the 5S rDNA bearing chromosome in two Steindachneridion species by means of different cytogenetic techniques. Cytologia 3:323–327CrossRefGoogle Scholar
  64. Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  65. Teixeira WG, Ferreira IA, Cabral-de-Mello DC, Mazzuchelli J, Valente GT, Pinhal D, Poletto AB, Venere PC, Martins C (2009) Organization of repeated DNA elements in the genome of the cichlid fish Cichla kelberi and its contributions to the knowledge of fish genomes. Cytogenet Genome Res 125:224–239Google Scholar
  66. 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 22:4673–4680PubMedCrossRefGoogle Scholar
  67. Treco FR, Malabarba LR, Giuliano-Caetano L, Dias AL (2008) Cytogenetic study of two species of the family Pimelodidae (Siluriformes) collected in lago Guaíba, Rio Grande do Sul, Brazil. Neotrop Ichthyol 6:87–92. doi:10.1590/S1679-62252008000100010 CrossRefGoogle Scholar
  68. Vasconcelos C, Martins-Santos IC (2000) Chromosome polymorphism in species of the Pimelodidae family (Pisces, Siluriformes). Hereditas 132:103–109CrossRefGoogle Scholar
  69. Venere PC, Ferreira IA, Martins C, Galetti PM Jr (2004) A novel ZZ/ZW sex chromosome system for the genus Leporinus (Pisces, Anostomidae, Characiformes). Genetica 121:75–80. doi:10.1023/B:GENE.0000019936.40970.7a PubMedCrossRefGoogle Scholar
  70. Vicari MR, Moreira-Filho O, Artoni RF, Bertollo LAC (2006) ZZ/ZW sex chromosome system in an undescribed species of the genus Apareiodon (Characiformes, Parodontidae). Cytogenet Genome Res 114:163–168. doi:10.1159/000093333 PubMedCrossRefGoogle Scholar
  71. Vissotto PC (2000) Análise Citogenética no gênero Imparfinis (Pisces, Siluriformes, Pimelodidae). PhD Thesis. Instituto de Biociências da Universidade Estadual PaulistaGoogle Scholar
  72. Vissotto PC, Foresti F, Oliveira C (1997) A ZZ/ZW sex chromosome system in Imparfinis mirini (Pisces, Siluriformes). Cytologia 62:61–66Google Scholar
  73. Volff JN, Körting C, Sweeney K, Schartl M (1999) The non-LTR retrotransposon Rex3 from the fish Xiphophorus is widespread among teleosts. Mol Biol Evol 16:1427–1438PubMedGoogle Scholar
  74. Volff JN, Korting C, Meyer A, Schartl M (2001) Evolution and discontinuous distribution of REX3 retrotransposons in fish. Mol Biol Evol 18:427–431Google Scholar
  75. Volff JN, Bouneau L, Ozouf-Costaz C, Fisher C (2003) Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678. doi:10.1016/j.tig.2003.10.006 PubMedCrossRefGoogle Scholar
  76. Wasko AP, Cesar ACG, Martins C, Galetti PM Jr (2001) A ZZ/ZW sex chromosome system in Cheirodontidae fish. Chromosome Sci 5:145–148Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Daniele Aparecida Matoso
    • 1
  • Vera Maria Fonseca de Almeida Val
    • 1
  • Maelin da  Silva
    • 2
  • Américo Moraes-Neto
    • 2
  • Mara Cristina Almeida
    • 2
  • Marcelo Ricardo Vicari
    • 2
  • Orlando Moreira-Filho
    • 3
  • Roberto Ferreira Artoni
    • 2
  1. 1.Laboratório de Ecofisiologia e Evolução MolecularInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  2. 2.Departamento de Biologia Estrutural, Molecular e GenéticaUniversidade Estadual de Ponta GrossaPonta GrossaBrazil
  3. 3.Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil

Personalised recommendations