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Origin of B chromosomes in the genus Astyanax (Characiformes, Characidae) and the limits of chromosome painting

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Abstract

Eukaryote genomes are frequently burdened with the presence of supernumerary (B) chromosomes. Their origin is frequently investigated by chromosome painting, under the hypothesis that sharing the repetitive DNA sequences contained in the painting probes is a sign of common descent. However, the intragenomic mobility of many anonymous DNA sequences contained in these probes (e.g., transposable elements) adds high uncertainty to this conclusion. Here we test the validity of chromosome painting to investigate B chromosome origin by comparing its results for seven B chromosome types in two fish species genus Astyanax, with those obtained (1) by means of the physical mapping of 18S ribosomal DNA (rDNA), H1 histone genes, the As51 satellite DNA and the (AC)15 microsatellite, and (2) by comparing the nucleotide sequence of one of these families (ITS regions from ribosomal DNA) between genomic DNA from B-lacking individuals in both species and the microdissected DNA from two metacentric B chromosomes found in these same species. Intra- and inter-specific painting suggested that all B chromosomes that were assayed shared homologous DNA sequences among them, as well as with a variable number of A chromosomes in each species. This finding would be consistent with a common origin for all seven B chromosomes analyzed. By contrast, the physical mapping of repetitive DNA sequences failed to give support to this hypothesis, as no more than two B-types shared a given repetitive DNA. Finally, sequence analysis of the ITS regions suggested that at least some of the B chromosomes could have had a common origin.

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Authors and Affiliations

  1. Departamento de Morfologia, Instituto de Biociências, Universidade Estadual Paulista, Distrito de Rubião Junior, s/n, Botucatu, SP, 18618-970, Brazil

    Duílio M. Z. de A. Silva, Ricardo Utsunomia, José Carlos Pansonato-Alves, Claudio Oliveira & Fausto Foresti

  2. Departamento de Ciências Biológicas, Faculdade de Ciências, Universidade Estadual Paulista, Campus de Bauru., Bauru, SP, 17033-360, Brazil

    Sandro Natal Daniel, Manolo Penitente & Fábio Porto-Foresti

  3. Departamento de Genética, Universidad de Granada, 18071, Granada, Spain

    Juan Pedro M. Camacho & Francisco J. Ruiz-Ruano

  4. CAUNESP, Universidade Estadual Paulista, Campus Jaboticabal, Jaboticabal, SP, 14884-900, Brazil

    Diogo Teruo Hashimoto

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  1. Duílio M. Z. de A. Silva
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  2. Sandro Natal Daniel
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  3. Juan Pedro M. Camacho
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  4. Ricardo Utsunomia
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  5. Francisco J. Ruiz-Ruano
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  7. José Carlos Pansonato-Alves
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  8. Diogo Teruo Hashimoto
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  9. Claudio Oliveira
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  10. Fábio Porto-Foresti
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  11. Fausto Foresti
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Correspondence to Duílio M. Z. de A. Silva.

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Funding

This research was funded by grant from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) to DMZA (2011/16825-3), grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to FF and by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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All authors declare that they have no competing interests.

Ethical approval

Samples were collected in accordance with Brazilian environmental protection legislation (collection permission MMA/IBAMA/SISBIO—number 3245), and the procedures for sampling, maintenance and analysis of the samples were performed in compliance with international guidelines for the care and use of animals followed by the Brazilian College of Animal Experimentation (COBEA) and was approved (protocol 405) by the Bioscience Institute/UNESP Ethics Committee on the Use of Animals (CEUA).

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Communicated by J. Cerdá.

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438_2016_1195_MOESM1_ESM.tif

Supplementary material Fig. S1 Metaphases of Astyanax species after FISH with the (AC)15 microsatellite probe. a A. bockmanni – Água da Madalena stream; b A. bockmanni – Alambari river; c A. fasciatus – Água da Madalena stream; d A. fasciatus – Alambari river; e A. fasciatus – Córrego das Araras stream; f A. paranae – Capivara river. Bar = 10 μm (TIFF 7009 kb)

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de A. Silva, D.M.Z., Daniel, S.N., Camacho, J.P.M. et al. Origin of B chromosomes in the genus Astyanax (Characiformes, Characidae) and the limits of chromosome painting. Mol Genet Genomics 291, 1407–1418 (2016). https://doi.org/10.1007/s00438-016-1195-y

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