Polar Biology

, Volume 28, Issue 1, pp 47–55 | Cite as

Chromosomal patterns of major and 5S ribosomal DNA in six icefish species (Perciformes, Notothenioidei, Channichthyidae)

  • F. Mazzei
  • L. Ghigliotti
  • C. Bonillo
  • J-P. Coutanceau
  • C. Ozouf-Costaz
  • E. Pisano
Original Paper


Comparative chromosomal mapping of major and 5S ribosomal genes in six species of the family Channichthyidae, namely Champsocephalus gunnari, Channichthys rhinoceratus, Chionodraco hamatus, Cryodraco atkinsoni, Pagetopsis macropterus and Neopagetopsis ionah, was performed by fluorescence in-situ hybridization, and using 28S and 5S ribosomal gene (rDNA) sequences as probes. Clusters of major and 5S ribosomal genes co-localize and likely compose the entire arm of a single pair of submetacentric chromosomes in all the species. In one species, P. macropterus, a second pair of chromosomes bears an additional common locus for both the two families of ribosomal genes. In all species, except N. ionah, additional copies of 5S rDNA sequences are also present on two other chromosome pairs, including the Y-chromosome in the males of Chionodraco hamatus. The pattern of ribosomal DNAs contributes to species-specific characterization in this fish family, and to our general knowledge and understanding of the chromosomal organization and evolution of the icefish genome.


Chromosome Pair Ribosomal Gene Acrocentric Chromosome Antarctic Fish Submetacentric Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The Italian National Programme for Antarctic Research (PNRA), the Muséum National d’Histoire Naturelle of Paris and IPEV (ICOTA Project) provided financial support. The Australian Antarctic Division supported the participation of E. Pisano in the 1993 cruise on board the RSV Aurora Australis (Anare project N.728). This research contributes to the “Adaptive Evolution of Antarctic Marine Organisms” (Evolanta) SCAR Programme. We are grateful to P.A. Hulley for kindly reviewing this paper and to E. Le Guilloux for technical assistance in Adélie Land.


  1. Almeida-Toledo LF, Ozouf-Costaz C, Foresti F, Bonillo C, Porto-Foresti F, Daniel-Silva MFZ (2002) Conservation of the 5S-bearing chromosome pair and co-localization with major rDNA clusters in five species of Astyanax (Pisces, Characidae). Cytogenet Genome Res 97:229–233CrossRefPubMedGoogle Scholar
  2. Caputo V, Nisi Cerioni P, Splendiani A, Capriglione T, Odierna G, Olmo E (2002) Chromosomal studies on ten species of notothenioid fishes (Notothenioidei: Bathydraconidae, Channichthyidae, Nototheniidae). Cytogenet Genome Res 98:285–290CrossRefPubMedGoogle Scholar
  3. Centofante L, Bertollo LAC, Miyazawa CS, Moreira Filho O (2003) Chromosomal differentiation among populations of Hyphessobrycon anisitsi (Pisces, Tetragonopteridae). Cytologia 68(3):283–288CrossRefGoogle Scholar
  4. Chen W-J, Bonillo C, Lecointre G (1998) Phylogeny of the Channichthyidae (Notothenioidei, Teleostei) based on two mitochondrial genes. In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer, Berlin Heidelberg New York, pp 287–298Google Scholar
  5. De Lucchini S, Nardi I, Barsacchi G, Batistoni R, Andronico F (1993) Molecular cytogenetics of the ribosomal (18S–28S and 5S) DNA loci in primitive and advanced urodele amphibians. Genome 36:762–773Google Scholar
  6. de Marco Ferro DA, Neo DM, Moreira-Filho O, Bertollo LA (2001) Nucleolar organizing regions 18S and 5S rDNA in Astyanax scabripinnis (Pisces, Characide): population distribution and functional diversity. Genetica 110:55–62Google Scholar
  7. di Prisco G, Cocca E, Parker SK, Detrich HW III (2002) Tracking the evolutionary loss of haemoglobin expression by the white-blooded Antarctic icefishes. Gene 295:185–191CrossRefPubMedGoogle Scholar
  8. Doussau De Bazignan M, Ozouf-Costaz C (1985) Une technique rapide d’analyse chromosomique appliquée à sept espèces de poissons antarctiques. Cybium 9(1):5–74Google Scholar
  9. Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Philos Trans R Soc Lond B 312:275–289Google Scholar
  10. Eastman JT, Eakin RR (2000) An updates species list for notothenioid fish (Perciformes; Notothenioidei), with comments on Antarctic species. Arc Fish Man Res 48:11–20Google Scholar
  11. Fischer C, Ozouf-Costaz C, Roest Crollius H, Dasilva C, Jaillon O, Bouneau L, Bonillo C, Weissenbach J, Bernot A (2000) Karyotype and chromosome location of characteristic tandem repeats in the pufferfish Tetraodon nigroviridis. Cytogenet Cell Genet 88(1–2):50–55Google Scholar
  12. Fontana F, Lanfredi M, Congiu L, Leis M, Chicca M, Rossi R (2003) Chromosomal mapping of 18S–28S and 5S rRNA genes by two-colour fluorescent in situ hybridization in six sturgeon species. Genome 46(3):473–477CrossRefPubMedGoogle Scholar
  13. Foresti de Almeida Toledo L, Stocker AJ, Foresti F, de Almeida Toledo-Filho S (1996) Fluorescence in situ hybridization with rDNA probes on chromosomes of two nucleolus organizer region phenothypes of a species of Eigenmannia (Pisces, Gymnotoidei, Stenopygidae). Chromosome Res 4:301–305PubMedGoogle Scholar
  14. Frederiksen S, Cao H, Lomholt B, Levan G, Hallemberg C (1997) The rat 5S rRNA bona fide gene repeat maps to chromosome 19q12→qter and the pseudogene repeat maps to 12q12. Cytogenet Cell Genet 76:101–106PubMedGoogle Scholar
  15. Fujiwara A, Syuiti A, Yamaha E, Yamazaki F, Yoshida MC (1998) Chromosomal localization and heterochromatin association of ribosomal RNA gene loci and silver-stained nucleolar organizer regions in salmonid fishes. Chromosome Res 6:463–471CrossRefPubMedGoogle Scholar
  16. Galetti PM, Mestrinier CA, Monaco PJ, Rasch EM (1995) Post-zygotic modifications and intra-inter individual nucleolar organizing region variations in fish. Report of a case involving Leporinus friderici. Chromosome Res 3:285–290PubMedGoogle Scholar
  17. Hallemberg C, Nederby-Nielsen J, Frederiksen S (1994) Characterization of 5S rDNA genes from mause. Gene 142:291–295CrossRefPubMedGoogle Scholar
  18. Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rDNA genes. Implications for the process of size increase of large subunit rDNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583PubMedGoogle Scholar
  19. Inafuku J, Nabeyama M, Kikuma Y, Saitoh J, Kubota S, Kohono S (2000) Chromosomal location and nucleotide sequences of 5S ribosomal DNA of two cyprinid species (Osteichthyes, Pisces). Chromosome Res 8:193–199CrossRefPubMedGoogle Scholar
  20. Kock KH (1992) Antarctic fish and fisheries, Cambridge University Press, CambridgeGoogle Scholar
  21. Le HLV, Lecointre G, Perasso R (1993) A 28S rRNA-based phylogeny of the gnathostomes: first step in the analysis of conflict and congruence with morphologically based cladograms. Mol Phylogenet Evol 2:35–51Google Scholar
  22. Martins C, Galetti PM (2001) Two 5S rDNA arrays in Neotropical fish species: is it a general rule for fishes? Genetica 111:439–446CrossRefPubMedGoogle Scholar
  23. Martins C, Galletti PM (1999) Chromosomal localization of 5S rDNA genes in Leporinus fish (Anastomidae, Characiformes). Chrom Res 7:363–367CrossRefPubMedGoogle Scholar
  24. Martins C, Wasco AP, Oliveira C, Wright JM (2000) Nucleotide sequence of 5S rDNA and localization of the ribosomal RNA genes to metaphase chromosomes of the tiilapiine cichlid fish, Oreochromis niloticus. Hereditas 133:39–46CrossRefPubMedGoogle Scholar
  25. Medrano L, Bernardi G, Couturier J, Dutrillaux B, Bernardi G (1988) Chromosome banding and genome compartmentalization in fishes. Chromosoma 96:178–183Google Scholar
  26. Mòran P, Martìnez E, Garcia-Vàsquez E, Pendàs AM (1996) Sex chromosome linkage of 5S rDNA in rainbow trout (Oncorhynchus mykiss). Cytogenet Cell Genet 75:145–150PubMedGoogle Scholar
  27. Morescalchi A, Hureau J-C, Olmo E, Ozouf-Costaz C, Pisano E, Stanyon R (1992) A multiple sex chromosome system in Antarctic icefishes. Polar Biol 11:655–661Google Scholar
  28. Moylan TJ, Siddell BD (2000) Concentration of myoglobin and myoglobin mRNA in heart ventricles from Antarctic fishes. J Exp Biol 203:1277–1286PubMedGoogle Scholar
  29. Murakami M, Fujitani H (1998) Characterization of repetitive DNA sequences carrying 5S rDNA of the triploid gimbuna (Japanese silver crucian carp, Carassius auratus langsdorfi). Genes Genet Syst 73:9–20CrossRefPubMedGoogle Scholar
  30. Near TJ, Pesavento J, Cheng C-HC (2003) Mitochondrial DNA, morphology and the phylogenetic relationships of antarctic icefishes (Notothenioidei, Channichthyidae). Mol Phylogenet Evol 28:87–98CrossRefPubMedGoogle Scholar
  31. Negi MS, Rajagopal J, Chauhan N, Cronn R, Lakshmikumaran M (2002) Length and sequence heterogeneity in 5S rDNA of Populus deltoides Genome 45(6):1181–1188CrossRefGoogle Scholar
  32. Ozouf-Costaz C, Hureau JC, Beaunier M (1991) Chromosome studies on fish of the suborder Notothenioidei collected in the Weddell Sea during Epos 3 cruise. Cybium 15:271–289Google Scholar
  33. Ozouf-Costaz C, Pisano E, Bonillo C, Williams R (1996) Ribosomal DNA location in the Antarctic fish Champsocephalus gunnari (Notothenioidei, Channichthyidae) by banding and fluorescence in situ hybridization. Chrom Res 4:557–561PubMedGoogle Scholar
  34. Pendàs AM, Mòran P, Freije JP, Garcia-Vàsquez E (1994) Chromosomal mapping and nucleotide sequence of two tandem repeats of Atlantic salmon 5S rDNA. Cytogenet Cell Genet 67:31–36PubMedGoogle Scholar
  35. Phillips RB, Reed KM (2000) Localization of repetitive DNAs to zebrafish (Danio rerio) chromosomes using multicolor fluorescence in situ hybridization (FISH). Chromosome Res 8:27–35CrossRefPubMedGoogle Scholar
  36. Pisano E, Ozouf-Costaz C (2003) Cytogenetics and evolution in extreme environment: the case of Antarctic fishes. In: Val AL, Kapoor BG (eds) Fish adaptations. Science Publishers Inc, Enfield, pp 309–330Google Scholar
  37. Pisano E, Ozouf-Costaz C, Bonillo C, Caimo A, Rossetti S, Williams R (1997a) Cytogenetics of the Antarctic icefish Champsocephalus gunnari Lonnberg, 1905 (Channichthyidae, Notothenioidei). Comp Biochem Physiol 118A (49):1087–1094CrossRefGoogle Scholar
  38. Pisano E, Ozouf-Costaz C, Bonillo C, Williams R (1997b) Cytogenetic characterization of the Antarctic icefish Channichthys rhinoceratus (Notothenioidei, Channichthyidae) by banding and FISH. In: Ninth international congress of European ichthyologists, “Fish Biodiversity” (Abstract)Google Scholar
  39. Pisano E, Mazzei F, Derome N, Ozouf-Costaz C, Hureau J-C, di Prisco G (2001a) Cytogenetics of the bathydraconid fish Gymnodraco acuticeps (Perciformes, Notothenioidei) from Terra Nova Bay, Ross Sea. Polar Biol 24:846–852CrossRefGoogle Scholar
  40. Pisano E, Ozouf-Costaz C, Ghigliotti L, Mazzei F, Bonillo C (2001b). Chromosomal distribution of 5S and 28S ribosomal DNAs in five species of Channichthyidae (Perciformes, Notothenioidei) and sex-linked chromosomes. In: Tenth European congress of ichthyology, ECIX, Prague (Abstract)Google Scholar
  41. Pisano E, Ghigliotti L, Mazzei F, Ozouf-Costaz C, Bonillo C, Coutanceau J-P (2003) Mapping of 5S ribosomal genes revealed indipendent evolution of sex linked heterochromosomes in two closely related teleostean species, Pagetopsis macropterus and Chionodraco hamatus (suborder Notothenioidei, family Channichthyidae). Ann Genet 46(2–3):98Google Scholar
  42. Pisano E, Cheng C-HC, Ozouf-Costaz C, Ghigliotti L, Mazzei F, Williams R (2004) Cytogenetic differences between the Patagonian (Dissostichus eleginoides) and the Antarctic toothfish (Dissostichus mawsoni). In: XXVIII SCAR Open Science Conference, Bremen (Abstract)Google Scholar
  43. Prirodina VP (1997) The direction of the karyotype specialization in the suborder Notothenioidei (Pisces, Perciformes). Cybium 21(4):393–398Google Scholar
  44. Rabova M, Rab P, Ozouf-Costaz C (2001) Extensive polymorphism and chromosomal characteristics of ribosomal DNA in a loach fish, Cobitis vardarensis (Ostaryophysi, Cobitidae) detected by different banding techniques and fluorescence in situ hybridization (FISH). Genetica 111(1–3):413–422Google Scholar
  45. Rocco L, Costagliola D, Liguori I, Stingo V (2003) Cytogenetic and molecular studies in the nurse shark Gynglimostoma cirratum (Galeomorphii, Heterodontiformes). Ann Genet 46(2–3):98Google Scholar
  46. Sajdak SL, Reed KM, Phillips RB (1998) Intraindividual and interspecies variation in the 5S rDNA of coregonid fish. J Mol Evol 46:680–688PubMedGoogle Scholar
  47. Suzuki H, Moriwaki K, Sakurai K (1994) Sequences and evolutionary analysis of mouse rDNAs. Mol Biol Evol 11:704–710PubMedGoogle Scholar
  48. Vinas A, Gomez C, Martinez P, Sanchez L (1996) Localization of rDNA genes in european eel (Anguilla anguilla) by FISH. Genome 39:1220–1223PubMedGoogle Scholar
  49. Wasko AP, Martins C, Wright JM, Galetti PM Jr (2001) Molecular organization of 5S rDNA in fishes of the genus Brycon. Genome 44:893–902CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • F. Mazzei
    • 1
  • L. Ghigliotti
    • 1
  • C. Bonillo
    • 2
  • J-P. Coutanceau
    • 2
  • C. Ozouf-Costaz
    • 2
  • E. Pisano
    • 1
  1. 1.Department of BiologyUniversity of GenoaGenoaItaly
  2. 2.Département de Systématique, Service de Systématique moléculaireMNHNParis Cedex 05France

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