Abstract
The cyprinid fish Alburnus alburnus possesses one of the largest supernumerary chromosomes in all vertebrates. In the present study, amplified fragment length polymorphism analyses (AFLP) and fluorescence in-situ hybridization (FISH) were performed in order to characterize these extraordinary chromosomes in detail. Sequence analysis of the B chromosome-specific DNA revealed a strong homology to a Drosophila Gypsy/Ty3 retrotransposon and also to a medaka (Oryzias latipes) one. The sequence is highly abundant on the B chromosome but undetectable in the normal A chromosome complement. It is also absent from the B chromosome of the closely related species, Rutilus rutilus, suggesting a specific spreading of the mobile element during evolution of the giant supernumerary chromosome within A. alburnus. Meitotic chromosomes were in-situ hybridized with the B chromosome-specific probe, documenting that the additional chromosome behaves as an autopaired ring chromosome in diakineses. Our results suggest that the supernumerary chromosome of A. alburnus is not derived from the normal chromosome complement but has evolved independently.
Similar content being viewed by others
References
Beukeboom LW(1994) Bewildering Bs: an impression of the 1st B-Chromosome-Conference. Heredity 73: 328-336.
Berend SA, Hale DW, Enstrom MD, Greenbaum IF (2001) Cytogenetics of collared lemmings (Dicrostonyx groenlandicus). II. Meiotic behaviour of B chromosomes suggests a Y-chromosome origin of supernumerary chromosomes. Cytogenet Cell Genet 95: 85-91.
Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3: 2303-2308.
Cabrero J, Lopez-Leon MD, Gomez R, Castro AJ, Martin-Alganza A, Camacho JPM (1997) Geographical distribution of B chromosomes in the grasshopper Eyprepocnemis plorans, along a river basin, is mainly shaped by non-selective historical events. Chromosome Res 5: 194-198.
Camacho JPM, Carballo AR, Cabrero J (1980) The B chromosome system of the grasshopper Eyprepocnemis plorans subsp. Plorans (Carpentier). Chromosoma 80: 163-166.
Camacho JPM, Sharbel TF, Beukeboom LW (2000) B chromosome evolution. Phil TransR Soc Lond Biol Sci 355: 163-178.
Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6-13.
Fenocchio AS, Bertollo LA (1990) Supernumerary chromosome in a Rhamdia hilarii population (Pisces, Pimelodidae). Genetica 81: 193-198.
Foresti F, Almeida-Toledo LF, Toledo FS (1989) Supernumerary chromosome system C-banding pattern characterization and multiple nucleolus organizer regions in Moenkausia sanctaclomenae (Pisces, Characidae). Genetica 79: 107-114.
Franks A, Houben A, Leach CR, Timmis JN (1996) The molecular organisation of a B chromosome tandem repeat sequence from Brachycome dichromosomatica. Chromosoma 105: 223-230.
Green DM (1990) Muller's ratchet and the evolution of supernumerary chromosomes. Genome 33: 818-824.
Green DM, Zeyl CW, Sharbel TF (1993) The evolution of hypervariable sex and supernumerary chromosomes in the relict New Zealand frog, Leiopelma hochstteri. J Evol Biol 6: 417-441.
Gutknecht L, Sperlich D, Bachmann L (1995) A species specific satellite DNA family of Drosophila subsilvestris appearing predominantly in B chromosomes. Chromosoma 103: 539-544.
Hafez R, Labat R, Quiller R (1978) Aneuploidie observee chez les populations de gardons (Rutilus rutilus L.) et d'ablettes (Alburnus alburnus L.) de la region Midi-Pyrenees. Bull Soc Nat Toulouse 114 (1—2): 85-92.
Hafez R, Labat R, Quiller R (1981) Reserches sur les chromosomes supernumeraires de l'ablette (Alburnus alburnus L.). Cybium 5: 81-87.
Holmes DS, Bougard SM (1989) B-chromosome selection in Allium schoenoprasum. II. Natural populations. Heredity 63: 83-87.
Jamilena M, Garrido-Ramos M, Ruiz Rejon M, Ruiz Rejon C, Parker JS (1995) Characterisation of repeated sequences from microdissected B chromosomes of Crepis capillaris. Chromosoma 104: 113-120.
Jones RN (1991) B-chromosome drive. Am Nat 137: 430-442.
Jones RN, Rees H (1982) B Chromosomes. New York: Academic Press.
Klinkhardt M, Tesche M, Greven H (1995) Database of Fish Chromosomes. Westarp Wissenschaften: Magdeburg.
Langdon T, Seago C, Jones RN et al. (2000) De novo evolution of satellite DNA on the rye B chromosome. Genetics 154: 869-884.
Lyttle TW (1991) Segregation disorders. Ann Rev Genet 25 511-557.
Salvador LB, Moreira-Filho O (1992) B chromosomes in Astyanax scabripinnis (Pisces, Characidae). Heredity 69: 50-56.
Maistro EL, Foresti F, Oliveira C, Almeida-Toledo LF (1992) Occurence of macro B chromosomes in Astyanax scabripinnis paranae (Pisces, Characiformes, Characidae). Genetica 87: 101-106.
McAllister BF (1995) Isolation and characterization of a retroelement from B chromosome (PSR) in the parasitic wasp Nasonia vitripennis. Insect Mol Biol 4(4): 253-262.
Mestriner CA, Galetti Jr PM, Valentinis SR et al. (2000) Structural and functional evidence that a B chromosome in characid fish Astyanax scabripinnis is an isochromosome. Heredity 85: 1-9.
Nanda I, Schartl M, Feichtinger W, Schlupp I, Parzefall J, Schmid M (1995) Chromosomal evidence for laboratory synthesis of a triploid hybrid between the gynogenetic teleost Poecilia formosa and its host species. J Fish Biol 47: 619-623.
Neo DM, Moreira-Filho O, Camacho JPM (2000) Altitudial variation for B chromosome frequency in the characid fish Astyanax scabripinnis. Heredity 85: 136-141.
Pauls E, Bertollo LAC (1983) Evidence for a system of supernumerary chromosomes in Prochilodus scrofa Steindacher, 1881 (Pisces, Prochilodontidae). Caryologia 36: 307-314.
Rab P, Roth P (1989) Chromosome studies in European leuciscine fishes (Pisces, Cyprinidae). Aneuploidy due to a B-chromosome in Rutilus rutilus. Folia Zool 38: 333-337.
Schartl M, Nanda I, Schlupp I et al. (1995) Incorporation of subgenomic amounts of DNA as compensation for mutational load in a gynogenetic fish. Nature 373: 68-71.
Sharbel TF, Green DM, Houben A (1998) B chromosome origin in the endemic New Zealand frog Leiopelma hochstteri through sex chromosome devolution. Genome 41: 14-22.
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. JMol Biol 98: 503-517.
Vicente VE, Moreira-Filho O, Camacho JPM (1996) Sex-ratio distortion associated with the presence of a B chromosome in Astyanax scabripinnis (Teleostei, Characidae). Cytogenet Cell Genet 74: 70-75.
Vos P, Hogers R, Bleeker M et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407-4414.
Zeyl CW, Bell G (1996) Symbiotic DNA in eukaryotic genomes. Trends Ecol Evol 11: 10-14.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ziegler, C.G., Lamatsch, D.K., Steinlein, C. et al. The giant B chromosome of the cyprinid fish Alburnus alburnus harbours a retrotransposon-derived repetitive DNA sequence. Chromosome Res 11, 23–35 (2003). https://doi.org/10.1023/A:1022053931308
Issue Date:
DOI: https://doi.org/10.1023/A:1022053931308