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Satellite DNA content of B chromosomes in the characid fish Characidium gomesi supports their origin from sex chromosomes

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Abstract

The origin of supernumerary (B) chromosomes is clearly conditioned by their ancestry from the standard (A) chromosomes. Sequence similarity between A and B chromosomes is thus crucial to determine B chromosome origin. For this purpose, we compare here the DNA sequences from A and B chromosomes in the characid fish Characidium gomesi using two main approaches. First, we found 59 satellite DNA (satDNA) families constituting the satellitome of this species and performed FISH analysis for 18 of them. This showed the presence of six satDNAs on the B chromosome: one shared with sex chromosomes and autosomes, two shared with sex chromosomes, one shared with autosomes and two being B-specific. This indicated that B chromosomes most likely arose from the sex chromosomes. Our second approach consisted of the analysis of five repetitive DNA families: 18S and 5S ribosomal DNA (rDNA), the H3 histone gene, U2 snDNA and the most abundant satDNA (CgoSat01-184) on DNA obtained from microdissected B chromosomes and from B-lacking genomes. PCR and sequence analysis of these repetitive sequences was successful for three of them (5S rDNA, H3 histone gene and CgoSat01-184), and sequence comparison revealed that DNA sequences obtained from the B chromosomes displayed higher identity with C. gomesi genomic DNA than with those obtained from other Characidium species. Taken together, our results support the intraspecific origin of B chromosomes in C. gomesi and point to sex chromosomes as B chromosome ancestors, which raises interesting prospects for future joint research on the genetic content of sex and B chromosomes in this species.

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Data availability

We deposited the 0B and + B genomic libraries in the Sequence Read Archive (SRA) database with accession numbers SRR9613702 and SRR9613703, respectively.

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Acknowledgements

We are thankful Renato Devidé for his technical assistance and reviewers for the very helpful suggestions and corrections for improving the paper.

Funding

This study was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grant Number 2013/02143-3) and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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Author notes

  1. Érica A. Serrano-Freitas and Duílio M. Z. A. Silva contributed equally to this study.

Authors and Affiliations

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

    Érica A. Serrano-Freitas, Duílio M. Z. A. Silva, Claudio Oliveira & Fausto Foresti

  2. Centro de Ciências Biológicas e da Saúde, Fundação Educacional de Penápolis, Funepe, Penápolis, SP, 16303-180, Brazil

    Érica A. Serrano-Freitas

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

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

  4. Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, 75236, Uppsala, Sweden

    Francisco J. Ruiz-Ruano

  5. Departamento de Genética, Instituto de Ciências Biológicas e da Saúde, ICBS, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, 23897-000, Brazil

    Ricardo Utsunomia

  6. Instituto de Investigación Multidisciplinar en Ciencia y Tecnología, Universidad de La Serena, 1720256, La Serena, Chile

    Cristian Araya-Jaime

  7. Laboratorio de Genética y Citogenética Vegetal, Departamento de Biología, Universidad de La Serena, 1720256, La Serena, Chile

    Cristian Araya-Jaime

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  1. Érica A. Serrano-Freitas
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  2. Duílio M. Z. A. Silva
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  3. Francisco J. Ruiz-Ruano
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  6. Claudio Oliveira
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Corresponding author

Correspondence to Duílio M. Z. A. Silva.

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All the authors declare that they have no conflict of interest.

Ethical approval

The animals were collected in accordance with Brazilian environmental protection legislation (Collection Permission MMA/IBAMA/SISBIO—number 3245), and the procedures for fish sampling, maintenance and analysis were performed in compliance with the Brazilian College of Animal Experimentation (COBEA) and approved (protocol 504) by the Bioscience Institute/Unesp Ethics Committee on the Use of Animals (CEUA).

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Communicated by Stefan Hohmann.

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Supplementary material 1 Agarose gel showing the ladder pattern for a satDNA of C. gomesi (JPEG 683 kb)

438_2019_1615_MOESM2_ESM.tif

Supplementary material 2 Karyotypes of C. gomesi after FISH with 18S (red) and 5S rDNA (green) (a), U2 snDNA (b) and H3 histone (c) probes and metaphases of C. gomesi after chromosome painting with the probe from the microdissected B chromosome of the same species (d). Bar = 10 µm (TIFF 43 kb)

438_2019_1615_MOESM3_ESM.jpg

Supplementary material 3 Metaphases of C. gomesi after FISH with satDNAs (a, c, e) and C-banding (b, d, f). Bar = 10 µm (JPEG 461 kb)

Supplementary material 4 Metaphases of C. gomesi after FISH with satDNAs. Bar = 10 µm (JPEG 713 kb)

Supplementary material 5 (DOCX 16 kb)

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Serrano-Freitas, É.A., Silva, D.M.Z.A., Ruiz-Ruano, F.J. et al. Satellite DNA content of B chromosomes in the characid fish Characidium gomesi supports their origin from sex chromosomes. Mol Genet Genomics 295, 195–207 (2020). https://doi.org/10.1007/s00438-019-01615-2

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