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Chromosoma

, Volume 128, Issue 4, pp 547–560 | Cite as

DNA transposon invasion and microsatellite accumulation guide W chromosome differentiation in a Neotropical fish genome

  • Michelle Orane Schemberger
  • Viviane Demetrio Nascimento
  • Rafael Coan
  • Érica Ramos
  • Viviane Nogaroto
  • Kaline Ziemniczak
  • Guilherme Targino Valente
  • Orlando Moreira-Filho
  • Cesar Martins
  • Marcelo Ricardo VicariEmail author
Original Article

Abstract

Sex chromosome differentiation is subject to independent evolutionary processes among different lineages. The accumulation of repetitive DNAs and consequent crossing-over restriction guide the origin of the heteromorphic sex chromosome region. Several Neotropical fish species have emerged as interesting models for understanding evolution and genome diversity, although knowledge of their genomes is scarce. Here, we investigate the content of repetitive DNAs between males and females of Apareiodon sp. based on large-scale genomic data focusing on W sex chromosome differentiation. In Apareiodon, females are the heterogametic sex (ZW) and males are the homogametic sex (ZZ). The genome size estimate for Apareiodon was 1.2 Gb (with ~ 42× and ~ 47× coverage for males and females, respectively). In Apareiodon sp., approximately 36% of the genome was composed of repetitive DNAs and transposable elements (TEs) were the most abundant class. Read coverage analysis revealed different amounts of repetitive DNAs in males and females. The female-enriched clusters were located on the W sex chromosome and were mostly composed of microsatellite expansions and DNA transposons. Landscape analysis of TE contents demonstrated two major waves of invasions of TEs in the Apareiodon genome. Estimation of TE insertion times correlated with in situ locations permitted the inference that helitron, Tc1-mariner, and CMC EnSpm DNA transposons accumulated repeated copies during W chromosome differentiation between 20 and 12 million years ago. DNA transposons and microsatellite expansions appeared to be major players in W chromosome differentiation and to guide modifications in the genome content of the heteromorphic sex chromosomes.

Keywords

Cytogenomics Read coverage analysis Sex chromosomes Tandem repeats Transposable elements W chromosome region 

Notes

Acknowledgments

The authors are grateful to ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (license number 10538-1 to collect specimens). This study was supported by the Fundação Araucária (Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná), FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, grant number: 2015/16661-1), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Finance Code 001), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, grant number: 304166/2016-2).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

412_2019_721_MOESM1_ESM.pdf (449 kb)
ESM 1 (PDF 448 kb)
412_2019_721_MOESM2_ESM.pdf (2.7 mb)
ESM 2 (PDF 2809 kb)
412_2019_721_MOESM3_ESM.html (26 kb)
Supplementary figure 2 Repeat landscape of DNA transposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate the distinct element types described on the right side. (HTML 26 kb)
412_2019_721_MOESM4_ESM.html (26 kb)
Supplementary figure 3 Repeat landscape of DNA transposons in the female Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right side. (HTML 25 kb)
412_2019_721_MOESM5_ESM.html (40 kb)
Supplementary figure 4 Repeat landscape of retrotransposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right. (HTML 40 kb)
412_2019_721_MOESM6_ESM.html (41 kb)
Supplementary figure 5 Repeat landscape of retrotransposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right side. (HTML 40 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Michelle Orane Schemberger
    • 1
  • Viviane Demetrio Nascimento
    • 2
  • Rafael Coan
    • 3
  • Érica Ramos
    • 3
  • Viviane Nogaroto
    • 1
  • Kaline Ziemniczak
    • 4
  • Guilherme Targino Valente
    • 5
  • Orlando Moreira-Filho
    • 4
  • Cesar Martins
    • 3
  • Marcelo Ricardo Vicari
    • 1
    • 2
    Email author
  1. 1.Departamento de Biologia Estrutural, Molecular e GenéticaUniversidade Estadual de Ponta GrossaPonta GrossaBrazil
  2. 2.Programa de Pós-Graduação em Genética, Centro PolitécnicoUniversidade Federal do ParanáCuritibaBrazil
  3. 3.Departamento de Morfologia, Instituto de Biociências de BotucatuUniversidade Estadual PaulistaBotucatuBrazil
  4. 4.Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil
  5. 5.Departamento de Bioprocessos e Biotecnologia, Fazenda LageadoUniversidade Estadual PaulistaBotucatuBrazil

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