Abstract
B chromosomes are additional chromosomes widely studied in a diversity of eukaryotic groups, including fungi, plants and animals, but their origin, evolution and possible functions are not clearly understood. To further understand the genomic content and the evolutionary history of B chromosomes, classical and molecular cytogenetic analyses were conducted in the cichlid fish Astatotilapia latifasciata, which harbor 1–2 B chromosomes. Through cytogenetic mapping of several probes, including transposable elements, rRNA genes, a repeated DNA genomic fraction (C 0 t − 1 DNA), whole genome probes (comparative genomic hybridization), and BAC clones from Oreochromis niloticus, we found similarities between the B chromosome and the 1st chromosome pair and chromosomes harboring rRNA genes. Based on the cytogenetic mapping data, we suggest the B chromosome may have evolved from a small chromosomal fragment followed by the invasion of the proto-B chromosome by several repeated DNA families.
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References
Almeida-Toledo LF, Foresti F, Trajano E, Almeida-Toledo S (1992) Cytogenetic analysis of the Brazilian blind catfish Pimelodella kronei and of its presumed ancestor Pimelodella transitoria. Caryologia 45:255–262
Andreata AA, Almeida-Toledo LF, Oliveira C, Almeida-Toledo S (1993) Chromosome studies in Hypoptopomatinae (Pisces, Siluriformes, Loricariidae) II. ZZ/ZW sex-chromosome system, B chromosomes, and constitutive heterochromatin differentiation in Microlepidogaster leucofrenatus. Cytogenet Cell Genet 63:215–220
Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Citotaxonomic consideration on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 1:103–120
Camacho JP (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
Camacho JP, Sharbel T, Beukeboom L (2000) B-chromosome evolution. Phil Trans R Soc Lond B 355:163–178
Camacho JP, Schmid M, Cabrero J (2011) B chromosomes and sex in animals. Sex Dev 5:155–166
Cnaani A, Lee BY, Zilberman C, Ozouf-Costaz C et al (2008) Genetics of sex determination in tilapiine species. Sex Dev 2:43–54
Dhar MK, Friebe B, Koul AK, Gill BS (2002) Origin of an apparent B chromosome by mutation, chromosome fragmentation and specific DNA sequence amplification. Chromosoma 111:332–340
Feldberg E, Bertollo LAC (1984) Discordance in chromosome number among somatic and gonadal tissue cells of Gymnogeophagus balzanii (Pisces, Cichlidae). Rev Brasil Genet 7:639–645
Feldberg E, Porto JIR, Alves-Brinn MN, Mendonça MNC, Benzaquem DC (2004) B chromosomes in Amazonian cichlid species. Cytogenet Genome Res 106:195–198
Ferreira IA, Martins C (2008) Physical chromosome mapping of repetitive DNA sequences in Nile tilapia Oreochromis niloticus: evidences for a differential distribution of repetitive elements in the sex chromosomes. Micron 39:411–418
Ferreira IA, Poletto AB, Kocher TD, Mota-Velasco JC, Penman DJ, Martins C (2010) Chromosome evolution in African cichlid fish: contributions from the physical mapping of repeated DNAs. Cytogenet Genome Res 129:314–322
Foresti F, Almeida-Toledo LF, Toledo-Filho SA (1989) Supranumerary chromosomes systems, C-banding pattern characterization and multiple nucleolus organizer regions in Moenkhausia sactaefilomenae (Pisces, Characidae). Genetica 79:107–114
Guerra MS (1986) Reviewing the chromosome nomenclature of Leval et al. Braz J Genet 9:741–743
Katagiri T, Kidd C, Tomasino E, Davis JT, Wishon C, Stern JE, Carleton KL, Howe AE, Kocher TD (2005) A BAC-based physical map of the Nile tilapia genome. BMC Genomics 6:89
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
Martins C, GalettiJr PM (1999) Chromosomal localization of 5S rDNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosome Res 7:363–367
Martins-Santos IC, Portela-Castro ALB, Julio HF Jr (1995) Chromosome analysis of 5 species of the Cichlidae family (Pisces, Perciformes) from the Paraná River. Cytologia 60:223–231
Mazzuchelli J, Yang F, Kocher TD, Martins C (2011) Comparative cytogenetic mapping of Sox2 and Sox14 in cichlid fishes and inferences on the genomic organization of both genes in vertebrates. Chromosome Res 19:657–667
McAllister BF, Werren JH (1997) Hybrid origin of a B chromosome (PSR) in the parasitic wasp Nasonia vitripennis. Chromosoma 106:243–253
Ozouf-Costaz C, Brandt J, Körting C, Pisano E, Bonillo C (2004) Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish. Antarctic Sci 16:51–57
Pauls E, Bertollo LAC (1983) Evidence for a system of supernumerary chromosome in Prochilodus scrofa (Pisces, Prochilodontidae). Caryologia 36:307–314
Poletto AB, Ferreira IA, Martins C (2010a) The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genetics 11:1
Poletto AB, Ferreira IA, Cabral-de-Mello DC, Nakajima RT, Mazzuchelli J, Ribeiro HB, Venere PC, Nirchio M, Kocher TD, Martins C (2010b) Chromosome differentiation patterns during cichlid fish evolution. BMC Genetics 11:50
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
Raskina O, Barber JC, Nevo E, Belyayev A (2008) Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res 120:351–357
Sambrook J, Russel DW (2001) Molecular cloning. A laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
Sapre AB, Deshpande DS (1987) Origin of B chromosomes in Coix L. through spontaneous interspecific hybridization. J Hered 78:191–196
Schartl M, Nanda I, Schlupp I, Wilde B, Epplen JT, Schmidt M, Parzefall J (1995) Incorporation of sub genomic amounts of DNA as compensation for mutational load in a gynogenetic fish. Nature 373:68–71
Schmid M, Ziegler CG, Steinlein C, Nanda I, Schartl M (2006) Cytogenetics of the bleak (Alburnus alburnus), with special emphasis on the B chromosomes. Chromosome Res 14:231–242
Schweizer D (1976) Reverse fluorescent chromosome banding with chromomicin and DAPI. Chromosoma 58:307–324
Sumner A (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306
Teixeira WG, Ferreira IA, Cabral-de-Mello DC, Mazzuchelli J, Valente GT, 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 125:224–234
Trifonov VA, Perelman PL, Kawada S-I, Iwasa MA, Oda S-I, Graphodatsky AS (2002) Complex structure of B-chromosomes in two mammalian species: Apodemus penisulae (Rodentia) and Nyctereutes procyonoides (Carnivora). Chromosome Res 10:109–116
Valente GT, Mazzuchelli J, Ferreira IA, Poletto AB, Fantinatti BEA, Martins C (2011) Cytogenetic mapping of the retroelements Rex1, Rex3 and Rex6 among cichlid fish: new insights on the chromosomal distribution of transposable elements. Cytogenetic Genome Res 133:34–42
Venere PC, Miyazawa C, Galetti PM (1999) New cases of supernumerary chromosomes in characiform fishes. Genet Mol Biol 22:345–349
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 16:1427–1438
Volff JN, Körting C, Schartl M (2000) Multiple lineages of the non-LTR retrotransposon Rex1 with varying success in invading fish genomes. Mol Biol Evol 17:1673–1684
Volff JN, Körting C, Froschauer A, Sweeney K, Schartl M (2001) Non-LTR retrotransposons encoding a restriction enzyme-like endonuclease in vertebrates. J Mol Evol 52:351–360
Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A et al (2011) B Chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genetics 7:e1002203
Ziegler CG, Lamatsch DK, Steinlein C, Engel W, Schartl M, Schmid M (2003) The giant B chromosome of the cyprinid fish Alburnus alburnus harbours a retrotransposon-derived repetitive DNA sequence. Chromosome Res 11:23–35
Zwick MS, Hanson RE, McKnight TD, Nurul-Islam-Faridi M, Stelly DM (1997) A rapid procedure for the isolation of C0t–1 DNA from plants. Genome 40:138–142
Acknowledgments
We thank TD Kocher for providing the BAC clones and the critical review of the manuscript, and F Yang for helpful assistance with BACs hybridization. Financial support was provided by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), the Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) from Brazil.
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Fantinatti, B.E.A., Mazzuchelli, J., Valente, G.T. et al. Genomic content and new insights on the origin of the B chromosome of the cichlid fish Astatotilapia latifasciata . Genetica 139, 1273–1282 (2011). https://doi.org/10.1007/s10709-012-9629-x
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DOI: https://doi.org/10.1007/s10709-012-9629-x