Skip to main content

First report on classical and molecular cytogenetics of archerfish, Toxotes chatareus (Perciformes: Toxotidae)

Abstract

A detailed account of liner delineation of chromosomes of archerfish, Toxotes chatareus (Perciformes: Toxotidae) employing conventional staining, NOR banding and molecular cytogenetics with fluorescence in situ hybridization (FISH) using 5S, 18S rDNAs and microsatellite d(CA)15, d(GA)15, d(CAA)10, d(CGG)10, and retrotransposonable Rex6 probes, is presented for the first time. The specimens were collected from the Chao Phraya River, Thailand. The mitotic chromosome preparations were directly carried out from kidney tissues of eight male and female fish each. The results revealed that the diploid chromosome number of T. chatareus was 2n = 48, the fundamental numbers (NF) were 50 in both male and female. The karyotype composed of two metacentric and 46 telocentric chromosomes. No irregularly sized chromosomes related to sex were observed. The nucleolar organizer regions (NORs) were detected by Ag-NOR banding and 18S rDNA probe mapping. Both techniques revealed the presence NORs located on the long arm adjacent to the centromere of the single pair of the largest telomeric chromosome pair. The 5S rDNA sequences were located in two large telocentric pairs. One of them is coincident with 18S rDNA sites and another is found at interstitial subcentromeric region of the second telomeric pair. FISH with d(CA)15 and d(GA)15 probes showed that hybridization signals are abundantly distributed in all chromosomes, mostly in telomeric regions while d(CAA)10 and d(CGG)10 repeats are distributed in all chromosomes with high accumulation throughout the chromosomes in some pairs. Chromosomal mapping of the Rex 6 sequences, indicate a weak distribution in all chromosomes, with preferential accumulation at the centromere of the chromosome pair 7.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Allen GR. A review of the archerfishes (family Toxotidae). Rec West Aust Mus. 1978;6:354–78.

    Google Scholar 

  2. Affonso PRAM, Galetti PM Jr. Chromosomal diversification of reef fishes from genus Centropyge (Perciformes, Pomacanthidae). Genetica. 2005;123:227–33.

    CAS  Article  PubMed  Google Scholar 

  3. Almeida-Toledo LF, Ozouf-Costaz C, Foresti F, Bonillo C, Porto-Foresti F, Daniel-Silva MFZ. Conservation of the 5S-bearing chromosome pair and co-localization with major rDNA clusters in five species of Astyanax (Pisces, Characidae). Cytogenet Genome Res. 2002;97:229–33.

    CAS  Article  PubMed  Google Scholar 

  4. Arai R. Fish karyotypes a check list. Tokyo: Springer Press; 2011.

    Book  Google Scholar 

  5. Arthington A, McKenzie F. Review of impacts of displaced/introduced fauna associated with inland waters. In: Environment Australia: state of the environment technical paper series (inland waters), Series 1; 1997.

  6. Chaiyasut K. Cytogenetics and cytotaxonomy of the family Zephyranthes. Bangkok: Department of Botany, Faculty of Science, Chulalongkorn University; 1989.

    Google Scholar 

  7. Cioffi MB, Bertollo LAC. Distribution and evolution of repetitive DNAs in fish. In: Garrido–Ramos MA, editor. Repetitive DNA, volume 7. Karger: Genome dyn, Basel; 2012. p. 197–221.

  8. Cioffi MB, Martins C. Bertollo LAC. Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish, Hoplias malabaricus. BMC Genet. 2009;10:34.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Cioffi MB, Martins C. Bertollo, L.A.C. 2010. Chromosomal spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol. 2010;10:271.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cioffi MB, Kejnovsky E, Bertollo LAC. The chromosomal distribution of microsatellite repeats in the wolf fish genome Hoplias malabaricus, focusing on the sex chromosomes. Cytogenet Genome Res. 2011;132:289–96.

    CAS  Article  PubMed  Google Scholar 

  11. Cross I, Merlo A, Manchado M, Infante C, Cañavate JP, Rebordinos L. Cytogenetic characterization of the Solea senegalensis (Teleostei: Pleurenectiformes. Soleidae): Ag-NOR, (GATA)n, (TTAGGG)n and ribosomal genes by one-color and two-color FISH. Genetica. 2006;128:253–9.

    Article  PubMed  Google Scholar 

  12. Diniz D, Moreira-Filho O, Bertollo LAC. Molecular cytogenetics and characterization of a ZZ/ZW sex chromosome system in Triportheus nemaratus (Characiformes, Characidae). Genetica. 2008;133:85–91.

    CAS  Article  PubMed  Google Scholar 

  13. Donsakul T. Chromosome study of four teleostean fishes, Microphis boaja, Xenentodon candila, Acanthophthalmus kuhlii and Chanda sianemsis, from Thailand. In: Proceedings of the 36th Kasetsart University Annual Conference. Bangkok, Thailand; 1998.

  14. Fontana F, Lanfredi M, Congiu L, Leis M, Chicca M, Rossi R. Chromosomal mapping of 18S–28S and 5S rRNA genes by two-colour fluorescent in situ hybridization in six sturgeon species. Genome. 2003;46:473–7.

    CAS  Article  PubMed  Google Scholar 

  15. Galetti PM Jr, Aguilar CT, Molina WF. An overview on marine fish cytogenetics. Hydrobiologia. 2000;420:55–62.

    Article  Google Scholar 

  16. Galetti PM Jr, Molina WF, Affonso PRAM, Aguilar CT. Assessing genetic diversity of Brazilian reef fishes by chromosomal and DNA markers. Genetica. 2006;126:161–77.

    Article  PubMed  Google Scholar 

  17. Hatanaka T, Galetti PM Jr. Mapping of the 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica. 2004;122:239–44.

    CAS  Article  PubMed  Google Scholar 

  18. Howell WM, Black DA. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia. 1980;36:1014–5.

    CAS  Article  PubMed  Google Scholar 

  19. Hsu TC, Patak S, Chen TR. The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations. Cytogenet Cell Genet. 1975;15:41–9.

    CAS  Article  PubMed  Google Scholar 

  20. Jesus CM, Moreira-Filho O. Chromosomal location of 5S and 18S rRNA genes in Prochilodus lineatus (Characiformes, Prochilodontidae). Caryologia. 2003;56(3):281–7.

    Article  Google Scholar 

  21. Khuda-Bukhsh AR, Chattopadhyay GK, Das SK. Karyomorphology of two species of freshwater fishes Chanda (Ambassis) nama (fam: Centropomidae) and Trichogaster lalius (fam. Osphronemidae). Perspect Cytol Genet. 1981;3:141–4.

    Google Scholar 

  22. Khuda-Bukhsh AR, Das JK. Karyomorphology and evolution in some Indian hillstream fishes with particular reference to polyploidy in some species. In: Uyeno T, Arai R, Taniuchi T, Matsuura K, editors. Indo-Pacifific fish biology. Tokyo: Ichthyological Society of Japan; 1986. p. 886–98.

    Google Scholar 

  23. Khuda-Bukhsh AR, Das JK. Cytogenetic analyses in eight species of teleostean fishes (Pisces): karyotypes, multiple Ag-NORs, sex chromosomes. Res Rev BioSci (India). 2007;1:47–52.

    Google Scholar 

  24. Khuda-Bukhsh AR, Rahman A, Chanda T, Nayak K, Khuda-Bukhsh A. Diploid numbers and chromosome formulae of some 29 species of Indian teleosts (Pisces). Chromosome Inf Serv. 1995;58:38–9.

    Google Scholar 

  25. Kidwell MG. Transposable elements. In: Gregory T, editor. The evolution of the genome. Burlington: Elsevier Academic Press; 2005. p. 165–223.

    Chapter  Google Scholar 

  26. Kidwell MG, Lisch DR. Transposable elements and host genome evolution. Trends Ecol Evol. 2000;15:95–9.

    CAS  Article  PubMed  Google Scholar 

  27. Kongpetchsak P. Karyotypes of tiger fishes, Coius microlepis, C. undecimradiatus and C. quadrifasciatus (Family Coiidae). Master thesis, M. Ed. (Biology). Graduate School. Srinakharinwirot University. Bangkok, Thailand; 2007.

  28. Kubat Z, Hobza R, Vyskot B, Kejnovsky E. Microsatellite accumulation in the Y chromosome of Silene latifolia. Genome. 2008;51:350–6.

    CAS  Article  PubMed  Google Scholar 

  29. Kumar R, Kushwaha B, Nagpure NS. Characterization and physical mapping of 18S and 5S ribosomal genes in Indian major carps (Pisces, Cyprinidae). Micron. 2013;49:40–5.

    Article  Google Scholar 

  30. Long EO, Dawid IB. Repeated genes in eukaryotes. Ann Rev Plant Physiol Plant Mol Biol. 1980;49:727–64.

    CAS  Google Scholar 

  31. Maneechot N, Yano CF, Bertollo LAC, Getlekha N, Molina WF, Ditcharoen S, et al. Genomic organization of repetitive DNAs highlights chromosomal evolution in the genus Clarias (Clariidae, Siluriformes). Mol Cytogenet. 2016;9:4.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Manna GK, Prasad R. Chromosome analysis in five species of fresh water fishes. Nucleus. 1977;20:264–71.

    Google Scholar 

  33. Martins C, Galetti PM Jr. Chromosomal localization of 5S rDNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosome Res. 1999;7:363–7.

    CAS  Article  PubMed  Google Scholar 

  34. Martins C, Galetti PM Jr. Two 5S arrays in Neotropical fish species: is it a general rule for fishes. Genetica. 2001;111:439–46.

    CAS  Article  PubMed  Google Scholar 

  35. Martins C, Galetti PM Jr. Organization of 5S rDNA in species of the fish Leporinus: two different genomic locations are characterized by distinct non transcribed spacers. Genome. 2001;44:903–10.

    CAS  Article  PubMed  Google Scholar 

  36. Martins C, Wasko AP, Oliveira C, Porto-Foresti F, Parise-Maltempi PP, Wright JM, Foresti F. Dynamics of 5S rDNA in the tilapia (Oreochromis niloticus) genome: repeat units, inverted sequences, pseudogenes and chromosome loci. Cytogenet Genome Res. 2002;2002(98):78–85.

    Article  Google Scholar 

  37. Martins C, Ferreira IA, Oliveira C, Foresti F, Galetti PM Jr. A tandemly repetitive centromeric DNA sequence of the fish Hoplias malabaricus (Characiformes: Erythrinidae) is derived from 5S rDNA. Genetica. 2006;127:133–41.

    CAS  Article  PubMed  Google Scholar 

  38. Mingkhwan J, Tanomtong A. Cytogenetics of black shark (Morulius chrysophekadion) and black tiger fish (Nandus oxyrhynchus). Thai J Genet. 2013;1:338–42.

    Google Scholar 

  39. Molina WF, Bacurau TOF. Structural and numerical chromosome diversification in marine Perciformes (Priacanthidae and Gerreidae). Cytologia. 2006;71:237–42.

    Article  Google Scholar 

  40. Morán P, Martίnez JL, Garcia-Vásquez E, Pendás AM. Sex linkage of 5S rDNA in rainbow trout (Oncorhynchus mykiss). Cytogenet Cell Genet. 1996;75:145–50.

    Article  PubMed  Google Scholar 

  41. Nagpure NS, Kumar R, Verma MS, Srivastava SK, Anna Mercy TV, Gopalakrishnan A, Basheer VS. Characterization of fish, Pristolepis marginata Jerdon using cytogenetic markers. J Cytol Genet. 2004;5:167–72.

    Google Scholar 

  42. Nakajima RT, Cabral de Mello DC, Valente GT, Venere PC, Martins C. Evolutionary dynamics of rRNA gene clusters in cichlid fish. BMC Evol Biol. 2012;12:198.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Nayak K, Khuda-Bukhsh AR. Karyotypes of two species of fishes. J Environ Ecol. 1987;5:318–20.

    Google Scholar 

  44. Nelson JS. Fishes of the world. 4th ed. New York: Wiley; 2006.

    Google Scholar 

  45. Ojima Y, Ueda T, Hayashi M. A review of the chromosome number in fishes. La Kromosomo. 1976;30:19–47.

    Google Scholar 

  46. Ozouf-Costaz C, Brandt J, Körting C, Pisavo E, Bonillo C, Coutanceau JP, Volff JN. Genome dynamics and chromosomal localization of the non–LTR retrotransposons Rex 1 and Rex 3 in Antarctic fish. Antarct Sci. 2004;16:51–7.

    Article  Google Scholar 

  47. Pendás AM, Morán P, Garcia-Vázquez E. Ribosomal RNA genes are interspersed throughout a heterochromatic chromosome arm in Atlantic salmon. Cytogenet Cell Genet. 1993;63:128–30.

    Article  PubMed  Google Scholar 

  48. Pendás AM, Móran P, Freije JP, Garcia-Vásquez E. Chromosomal location and nucleotide sequence of two tandem repeats of the Atlantic salmon 5S rDNA. Cytogenet Cell Genet. 1994;67:31–6.

    Article  PubMed  Google Scholar 

  49. Pinkel D, Straume T, Gray J. Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA. 1986;83:2934–8.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Poleto AB, Ferreira IA, Martins C. The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genet. 2010;11:1.

    Article  Google Scholar 

  51. Rao SR, Trivedi S, Emmanue D, Merita K, Hynniewta M. DNA repetitive sequences-types, distribution and function: a review. J Cell Mol Biol. 2010;7(2)&8(1):1–11.

  52. Rocco L, Costagliola D, Fiorillo M, Tinti F, Stingo V. Molecular and chromosomal analysis of ribosomal cistrons in two cartilaginous fish, Taeniura lymma and Raja montagui (Chondrichthyes, Batoidea). Genetica. 2005;123:245–53.

    CAS  Article  PubMed  Google Scholar 

  53. Rosa R, Bellafronte E, Moreira-Filho O, Margarido VP. Constitutive heterochromatin, 5S and 18S rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica. 2006;128:159–66.

    Article  PubMed  Google Scholar 

  54. Rooney DE. Human cytogenetics: constutitional analysis: a practical approach. 3rd ed. London: Oxford University Press; 2001.

    Google Scholar 

  55. Schmidt M. Chromosome banding in Amphibia. II. Constitutive heterochromatin and nucleolus organizer regions in Ranidae, Microhylidae and Racophoridae. Chromosoma. 1978;68:131–48.

    Article  Google Scholar 

  56. Sharma OP, Tripathi NK. Studies on the chromosomes of Nandus nandus and Badis badis from the J and K State, India. Cytologia. 1984;49:73–9.

    Article  Google Scholar 

  57. Sharma OP, Tripathi NK, Sharma KK. A review of chromosome banding in fishes. In: Sobti RC, editor. Some aspects of chromosome structure and functions. New Delhi: Narosa Publishing House; 2002.

    Google Scholar 

  58. Shimoda N, Knapik EW, Ziniti J, Sim C, Yamada E, Kaplan S, Jackson D, de Sauvage F, Jacob H, Fishman MC. Zebrafish genetic map with 200 microsatellite markers. Genomics. 1999;58:219–32.

    CAS  Article  PubMed  Google Scholar 

  59. Supiwong W, Jearranaiprepame P, Tanomtong A. A new report of karyotype in the chevron snakehead fish, Channa striata (Channidae, Pisces) from Northeast Thailand. Cytologia. 2009;74(3):317–22.

    Article  Google Scholar 

  60. Supiwong W, Liehr T, Cioffi MB, Chaveerach A, Kosyakova N, Pinthong K, Tanee T, Tanomtong A. Karyotype description and cytogenetic mapping of 9 classes of repetitive DNAs on the Thailand catfish Mystus bocourti. Mol Cytogenet. 2013;6:51.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Supiwong W, Liehr T, Cioffi MB, Chaveerach A, Kosyakova N, Fan X, Tanee T, Tanomtong A. Comparative cytogenetic mapping of rRNA genes among naked catfishes: implications for genomic evolution in the Bagridae family. Genet Mol Res. 2014;13(4):9533–42.

    CAS  Article  PubMed  Google Scholar 

  62. Supiwong W, Liehr T, Cioffi MB, Chaveerach A, Kosyakova N, Pinthong K, Tanee T, Tanomtong A. Chromosomal evolution in naked catfishes (Bagridae, Siluriformes): a comparative chromosome mapping study. Zoologischer Anzeiger. 2014;253:316–20.

    Article  Google Scholar 

  63. Tripathi NK, Das CC. Karyotypes of five Indian perciform fishes. Copeia. 1988;1:231–3.

    Article  Google Scholar 

  64. Turpin R, Lejeune J. Les chromosomes humains. Paris: Gauthier-Pillars; 1965.

    Google Scholar 

  65. Úbeda-Manzanaro M, Merlo MA, Palazón JL, Cross I, Sarasquete C, Rebordinos L. Chromosomal mapping of the major and minor ribosomal genes, (GATA)n and U2 snRNA gene by double-colour FISH in species of the Batrachoididae family. Genetica. 2010;138:787–94.

    Article  PubMed  Google Scholar 

  66. Vanzela ALL, Swarça AC, Dias AL, Stolf R, Ruas PM, Ruas CF, Sbalqueiro IJ, Giuliano-Caetano L. Differential distribution of (GA)9+ C microsatellite on chromosomes of some animal and plant species. Cytologia. 2002;67:9–13.

    CAS  Article  Google Scholar 

  67. Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC. Colocalization of repetitive DNAs and silencing of major rRNA genes: a case report of the fish Astyanax janeiroensis. Cytogenet Genome Res. 2008;122(1):67–72.

    CAS  Article  PubMed  Google Scholar 

  68. Vidthayanon C, Kanasuta J, Nabhitabhata J. Diversity of freshwater fishes in Thailand. Bangkok: Integrated Promotion Technology Company ltd; 1997.

    Google Scholar 

  69. Vitturi R, Catalano E, Colomba MS, Montagnino L, Pellerito L. Karyotype analysis of Aphanius fasciatus (Pisces: Cyprinodontiformes): Ag-NORs and C-band polymorphism in four populations from Sicily. Biol Zent. 1995;114:392–402.

    Google Scholar 

  70. Wasko AP, Galetti PM Jr. Mapping 18S ribosomal genes in fish of the genus Brycon (Characidae) by fluorescence in situ hybridization (FISH). Genet Mol Biol. 2000;23(1):135–8.

    CAS  Article  Google Scholar 

  71. Yüksel E, Gaffaroğlu M. The analysis of nucleolar organizer regions in Chalcalburnus mossulensis (Pisces: Cyprinidae). J Fish Sci. 2008;2:587–91.

    Google Scholar 

  72. Zhang SM. Karyotypic studies in two species of Chanda (Centropomidae: Pisces). Chromosome Inf Serv. 1990;49:7–8.

    Google Scholar 

Download references

Acknowledgements

This work was financially supported by Toxic Substances in Livestock and Aquatic Animals Research Group, Khon Kaen University, Royal Thai Government Scholarship National Science and Technology Development Agency (NSTDA), Thailand Toray Science Foundation (Science and Technology Research Grant), and Faculty of Applied Science and Engineering Grant, Khon Kaen University, Nong Khai Campus.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Tanomtong.

Additional information

figure a

In Honour of Prof AK Sharma, the Founder and Editor-in-Chief of the Nucleus

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Supiwong, W., Jiwyam, W., Sreeputhorn, K. et al. First report on classical and molecular cytogenetics of archerfish, Toxotes chatareus (Perciformes: Toxotidae). Nucleus 60, 349–359 (2017). https://doi.org/10.1007/s13237-017-0216-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-017-0216-5

Keywords

  • Chromosome
  • Karyotype
  • Toxotes chatareus
  • FISH