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Chromosoma

, Volume 128, Issue 2, pp 149–163 | Cite as

Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics

  • Marta Ribagorda
  • Soledad Berríos
  • Emanuela Solano
  • Eliana Ayarza
  • Marta Martín-Ruiz
  • Ana Gil-Fernández
  • María Teresa Parra
  • Alberto Viera
  • Julio S. Rufas
  • Ernesto Capanna
  • Riccardo Castiglia
  • Raúl Fernández-Donoso
  • Jesús PageEmail author
Original Article

Abstract

Natural populations of the house mouse Mus musculus domesticus show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile hybrid individuals due to impaired meiotic development. In this study, we have analyzed prophase-I spermatocytes of hybrids formed by crossing mice from Vulcano and Lipari island populations. Both populations have a 2n = 26 karyotype but different combinations of Robertsonian translocations. We studied the progress of synapsis, recombination, and meiotic silencing of unsynapsed chromosomes during prophase-I through the immunolocalization of the proteins SYCP3, SYCP1, γH2AX, RAD51, and MLH1. In these hybrids, a hexavalent is formed that, depending on the degree of synapsis between chromosomes, can adopt an open chain, a ring, or a closed configuration. The frequency of these configurations varies throughout meiosis, with the maximum degree of synapsis occurring at mid pachytene. In addition, we observed the appearance of heterologous synapsis between telocentric and metacentric chromosomes; however, this synapsis seems to be transient and unstable and unsynapsed regions are frequently observed in mid-late pachytene. Interestingly, we found that chiasmata are frequently located at the boundaries of unsynapsed chromosomal regions in the hexavalent during late pachytene. These results provide new clues about synapsis dynamics during meiosis. We propose that mechanical forces generated along chromosomes may induce premature desynapsis, which, in turn, might be counteracted by the location of chiasmata. Despite these and additional meiotic features, such as the accumulation of γH2AX on unsynapsed chromosome regions, we observed a large number of cells that progressed to late stages of prophase-I, indicating that synapsis defects may not trigger a meiotic crisis in these hybrids.

Keywords

Chromosome synapsis Meiosis Robertsonian translocation 

Notes

Acknowledgments

This work was supported by grants CGL2014-53106-P from the Ministerio de Economía y Competitividad (Spain), grant A/017762/08 from Agencia Española de Cooperación Internacional para el Desarrollo (Spain), VID Universidad de Chile (Chile), and Research Projects Funds (protocol no. RM116154CABB8B0B) of the University of Rome “La Sapienza” (Italy). The mice survey was funded by ES’ PhD project.

Supplementary material

412_2019_695_Fig8_ESM.png (53 kb)
Supplementary Fig. 1

Dot plot representing the number of RAD51 foci present on the hexavalent and the total number of foci on the autosomes in 40 spermatocytes. (PNG 53 kb)

412_2019_695_MOESM1_ESM.tif (107 kb)
High Resolution Image (TIF 106 kb)

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Copyright information

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

Authors and Affiliations

  • Marta Ribagorda
    • 1
  • Soledad Berríos
    • 2
  • Emanuela Solano
    • 3
  • Eliana Ayarza
    • 4
  • Marta Martín-Ruiz
    • 1
  • Ana Gil-Fernández
    • 1
  • María Teresa Parra
    • 1
  • Alberto Viera
    • 1
  • Julio S. Rufas
    • 1
  • Ernesto Capanna
    • 3
  • Riccardo Castiglia
    • 3
  • Raúl Fernández-Donoso
    • 2
  • Jesús Page
    • 1
    Email author
  1. 1.Departamento de Biología, Facultad de CienciasUniversidad Autónoma de MadridMadridSpain
  2. 2.Programa de Genética Humana, Facultad de MedicinaUniversidad de ChileSantiagoChile
  3. 3.Dipartimento di Biologia e Biotecnologie “Charles Darwin”Università degli Studi di Roma La SapienzaRomeItaly
  4. 4.Departamento de Tecnología Médica, Facultad de MedicinaUniversidad de ChileSantiagoChile

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