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Reviews in Fish Biology and Fisheries

, Volume 22, Issue 3, pp 739–749 | Cite as

Numeric and structural chromosome polymorphism in Rineloricaria lima (Siluriformes: Loricariidae): fusion points carrying 5S rDNA or telomere sequence vestiges

  • Kamila Oliveira Rosa
  • Kaline Ziemniczak
  • Alain Victor de Barros
  • Viviane Nogaroto
  • Mara Cristina Almeida
  • Marta Margarete Cestari
  • Roberto Ferreira Artoni
  • Marcelo Ricardo Vicari
Research Paper

Abstract

The karyotypes and chromosome polymorphism in Rineloricaria lima have been examined using both conventional (Giemsa-staining, C-banding and silver impregnation) and fluorescence in situ hybridization with 18S rDNA, 5S rDNA and telomeric (TTAGGG)n probes protocols. A variation in chromosome number of 2n = 70–66 was detected in the analyzed populations, with the fundamental number (FN) ranging from 72 to 74. The 2n = 70 chromosomes and karyotypic formula 2st + 68a (NF = 72) was establish the start point of the current polymorphism. Based on this karyotype, seven fusioned and/or inverted chromosomes types (without vestiges of interstitial telomeric sites—ITS; with ITS and; carrying 5S rDNA fusion points) were described and eight karyotypes were established. It was hypothesized that one Rineloricaria branch, originally having a diploid number of 2n = 54 which appears the ancestral 2n for Loricariidae, diversified through centric fissions generating unstable sites at the break points. These unstable sites may have triggered Robertsonian fusions generating the currently observed polymorphism of 70–66 chromosomes. The formation of the chromosomes variants could have possibly led to the formation of different gametic combinations (balanced and unbalanced), which may have generated alterations in the FN above 72. These results demonstrate an important case that ITS and 5S rDNA were observed in fused chromosomes, implying that rDNA could serve as breakpoint for the fusion in Rinelocaria. Thus, all these mechanisms promote an increase in variability and assist in the maintenance of the observed polymorphism.

Keywords

Fish cytogenetic Robertsonian rearrangements Interstitial telomeric sites Chromosome banding FISH 

Notes

Acknowledgments

The authors are grateful to the IBAMA (Instituto Brasileiro do Meio Ambiente) for authorizing the capture of specimens (IBAMA/MMA/SISBIO license number: 15117). This work was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and Fundação Araucária (Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná). We also thank Dr. Cláudio Henrique Zawadzki for the taxonomy identification, professor Juan Pedro M. Camacho for the suggestions in this work, and Mr. Miguel Airton Carvalho for his collaboration in the field work and in the laboratory.

References

  1. Alves AL, Oliveira C, Foresti F (2003) Karyotype variability in eight species of the subfamilies Loricariinae and Ancistrinae (Teleostei, Siluriformes, Loricariidae). Caryologia 56:57–63Google Scholar
  2. Armbruster JW (2004) Phylogenetic relationships of the suckermouth armoured catfishes (Loricariidae) with emphasis on the Hypostominae and the Ancistrinae. Zool J Linn Soc 141:1–80. doi: 10.1111/j.1096-3642.2004.00109.x CrossRefGoogle Scholar
  3. Artoni RF, Bertollo LAC (2001) Trends in the karyotype evolution of Loricariidae fish (Siluriformes). Hereditas 134:201–210. doi: 10.1111/j.1601-5223.2001.00201.x PubMedCrossRefGoogle Scholar
  4. Artoni RF, Vicari MR, Almeida MC, Moreira-Filho O, Bertollo LAC (2009) Karyotype diversity and fish conservation of southern field from South Brazil. Rev Fish Biol Fish 19:393–401. doi: 10.1007/s11160-009-9109-2 CrossRefGoogle Scholar
  5. Bellafronte E, Schemberger MO, Moreira-Filho O, Almeida MC, Artoni RF, Margarido VP, Vicari MR (2011) Chromosomal markers and phylogenetic inferences among species of Parodontidae. Rev Fish Biol Fish 21:559–570. doi: 10.1007/s11160-010-9177-3 CrossRefGoogle Scholar
  6. Beridze R (1986) Satellite DNA. Springer, BerlinCrossRefGoogle Scholar
  7. Bertollo LAC, Takahashi CS, Moreira Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 1:103–120Google Scholar
  8. Blanco DR, Lui RL, Bertollo LAC, Diniz D, Moreira-Filho O (2010) Characterization of invasive fish species in a river transposition region: evolutionary chromosome studies in the genus Hoplias (Characiformes, Erythrinidae). Rev Fish Biol Fish 20:1–8. doi: 10.1007/s11160-009-9116-3 CrossRefGoogle Scholar
  9. Blanco DR, Lui RL, Vicari MR, Bertollo LAC, Moreira-Filho O (2011) Comparative cytogenetics of giant trahiras Hoplias aimara and H. intermedius (Characiformes, Erythrinidae): chromosomal characteristics of minor and major ribosomal DNA and cross-species repetitive centromeric sequences mapping differ among morphologically identical karyotypes. Cytogenet Genome Res 132:171–178. doi: 10.1159/000320923 CrossRefGoogle Scholar
  10. Bouffler S, Silver A, Papworth D, Coates J, Cox R (1993) Murine radiation myeloid leukaemogenesis: relationship between interstitial telomere-like sequences and chromosome 2 fragile sites. Genes Chromosom Cancer 6:98–106. doi: 10.1002/gcc.2870060206 PubMedCrossRefGoogle Scholar
  11. Bueno V, Zawadzki CH, Margarido VP (2011) Trends in chromosome evolution in the genus Hypostomus Lacépède, 1803 (Osteichthyes, Loricariidae): a new perspective about the correlation between diploid number and chromosomes types. Rev Fish Biol Fish. doi: 10.1007/s11160-011-9215-9
  12. Charlesworth B, Snlegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220. doi: 10.1038/371215a0 PubMedCrossRefGoogle Scholar
  13. Cramer CA, Bonatto SL, Reis RE (2011) Molecular phylogeny of the Neoplecostominae and Hypoptopomatinae (Siluriformes: Loricariidae) using multiple genes. Mol Phylogenet Evol 59:43–52. doi: 10.1016/j.ympev.2011.01.002 PubMedCrossRefGoogle Scholar
  14. Day JP, Limoli CL, Morgan WF (1998) Recombination involving interstitial telomere repeat-like sequences promotes chromosomal instability in Chinese hamster cells. Carcinogenesis 19:259–265PubMedCrossRefGoogle Scholar
  15. Desmaze C, Alberti C, Martins L, Pottier G, Sprung CN, Murnane JP, Sabatier L (1999) The influence of interstitial telomeric sequences on chromosome instability in human cells. Cytogenet Cell Genet 86:288–295. doi: 10.1159/000015321 PubMedCrossRefGoogle Scholar
  16. Dunham MA, Neumann AA, Fasching CL, Reddel RR (2000) Telomere maintenance by recombination in human cells. Nat Genet 26:447–450. doi: 10.1038/82586 PubMedCrossRefGoogle Scholar
  17. Gardner RJM, Sutherland GR (2004) Chromosome abnormalities and genetic counselling. Oxford University Press, New YorkGoogle Scholar
  18. Giuliano-Caetano L (1998) Polimorfismo cromossômico Robertosiano em populações de Rineloricaria latirostris (Pisces, Loricariidae). Dissertation, Universidade Federal de São CarlosGoogle Scholar
  19. Hatanaka T, Galetti PM Jr (2004) Mapping 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
  20. Holmquist GP, Ashley T (2006) Chromosome organization and chromatin modification: influence on genome function and evolution. Cytogenet Genome Res 114:96–125. doi: 10.1159/000093326 PubMedCrossRefGoogle Scholar
  21. Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a I-step method. Experientia 36:1014–1015PubMedCrossRefGoogle Scholar
  22. 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 19:4780PubMedCrossRefGoogle Scholar
  23. Kavalco KF, Pazza R, Bertollo LAC, Moreira-Filho O (2005) Karyotypic diversity and evolution of Loricariidae (Pisces, Siluriformes). Heredity 94:180–186. doi: 10.1038/sj.hdy.6800595 PubMedCrossRefGoogle Scholar
  24. Kilburn AE, Shea MJ, Sargent RG, Wilson JH (2001) Insertion of a telomere repeat sequence into a mammalian gene causes chromosome instability. Mol Cell Biol 21:126–135. doi: 10.1128/MCB.21.1.126-135.2001 PubMedCrossRefGoogle Scholar
  25. King M (1993) Species evolution: the role of chromosome change. Cambridge University Press, New YorkGoogle Scholar
  26. Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x CrossRefGoogle Scholar
  27. 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
  28. Martins C, Galetti PM Jr (1999) Chromosomal localization of 5S rDNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosome Res 7:363–367. doi: 10.1023/A:1009216030316 PubMedCrossRefGoogle Scholar
  29. Matoso DA, Almeida Val VMF, Silva M, Moraes-Neto A, Almeida MC, Vicari MR, Moreira-Filho O, Artoni RF (2011) Chromosomal polymorphism in Steindachneridion melanodermatum Garavello, 2005 (Siluriformes, Pimelodidae): a reappraisal the existence of sex chromosome system in the species. Rev Fish Biol Fish 21:497–508. doi: 10.1007/s11160-011-9201-2 CrossRefGoogle Scholar
  30. Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, Ward OG, Wiley JE, Wurster-Hill DH, Yates TL, Moyzis RK (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99:3–10PubMedCrossRefGoogle Scholar
  31. Peitl P, Mello SS, Camparoto ML, Passos GAS, Hande MP, Cardoso RS, Sakamoto-Hojo ET (2002) Chromosomal rearrangements involving telomeric DNA sequences in Balb/3t3 cells transfected with the Ha-ras oncogene. Mutagenesis 17:67–72. doi: 10.1093/mutage/17.1.67 PubMedCrossRefGoogle Scholar
  32. Perry JO, Slater HR, Choo KHA (2004) Centric fission—simple and complex mechanisms. Chromosome Res 12:627–640. doi: 10.1023/B:CHRO.0000036594.38997.59 PubMedCrossRefGoogle Scholar
  33. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938PubMedCrossRefGoogle Scholar
  34. Reis RE, Pereira EHL, Armbruster JW (2006) Delturinae, a new loricariid catfish subfamily (Teleostei, Siluriformes), with revisions of Delturus and Hemipsilichthys. Zool J Linn Soc 147:277–299. doi: 10.1111/j.1096-3642.2006.00229.x CrossRefGoogle Scholar
  35. Richards EJ, Goodman HM, Ausubel FM (1991) The centromere region of Arabidopsis thaliana chromosome 1 contains telomere-similar sequences. Nucleic Acids Res 19:3351–3357. doi: 10.1093/nar/19.12.3351 PubMedCrossRefGoogle Scholar
  36. Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E (2008) Telomeric repeats far from the ends: mechanisms of origin and role evolution. Cytogenet Genome Res 122:219–228. doi: 10.1159/000167807 PubMedCrossRefGoogle Scholar
  37. Shampay J, Schmitt M, Bassham S (1995) A novel minisatellite at a cloned hamster telomere. Chromosoma 104:29–38. doi: 10.1007/s004120050089 PubMedCrossRefGoogle Scholar
  38. Slijepcevic P (1998) Telomeres and mechanisms of Robertsonian fusion. Chromosoma 107:136–140. doi: 10.1007/s004120050289 PubMedCrossRefGoogle Scholar
  39. Slijepcevic P, Xiao Y, Natarajan AT, Bryant PE (1997) Instability of CHO chromosomes containing interstitial telomeric sequences originating from Chinese hamster chromosome 10. Cytogenet Cell Genet 76:58–60. doi: 10.1159/000134516 PubMedCrossRefGoogle Scholar
  40. Sumner AT (1972) A simple technique for demonstrating centromeric heterocromatin. Exp Cell Res 75:304–306. doi: 10.1016/0014-4827(72)90558-7 PubMedCrossRefGoogle Scholar
  41. Sumner AT (2003) Chromosomes—organization and function. Blackwell Publishing, MaldenGoogle Scholar
  42. Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC (2008) Co-localization of repetitive DNAs and silencing of major rDNA genes. A case report in the fish, Astyanax janeiroensis. Cytogenet Genome Res 122:67–72. doi: 10.1159/000151318 PubMedCrossRefGoogle Scholar
  43. 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 PubMedCrossRefGoogle Scholar
  44. Weitzman SH, Menezes NA, Weitzman MJ (1988) Phylogenetic biogeography of the Glandulocaudini (Teleostei: Characiformes: Characidae) with comments on the distributions of other freshwater fishes in eastern and southeastern Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a workshop on Neotropical distribution patterns, 1st edn. Academia Brasileira de Ciências, Rio de Janeiro, pp 379–427Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Kamila Oliveira Rosa
    • 1
  • Kaline Ziemniczak
    • 2
  • Alain Victor de Barros
    • 1
  • Viviane Nogaroto
    • 1
  • Mara Cristina Almeida
    • 1
  • Marta Margarete Cestari
    • 2
  • Roberto Ferreira Artoni
    • 1
  • Marcelo Ricardo Vicari
    • 1
  1. 1.Programa de Pós-Graduação em Biologia Evolutiva, Laboratório de Citogenética e Evolução, Departamento de Biologia Estrutural, Molecular e GenéticaUniversidade Estadual de Ponta GrossaPonta GrossaBrazil
  2. 2.Programa de Pós-Graduação em Genética, Departamento de GenéticaUniversidade Federal do Paraná, Setor de Ciências BiológicasCuritibaBrazil

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