Sex chromosome quadrivalents in oocytes of the African pygmy mouse Mus minutoides that harbors non-conventional sex chromosomes
Eutherian mammals have an extremely conserved sex-determining system controlled by highly differentiated sex chromosomes. Females are XX and males XY, and any deviation generally leads to infertility, mainly due to meiosis disruption. The African pygmy mouse (Mus minutoides) presents an atypical sex determination system with three sex chromosomes: the classical X and Y chromosomes and a feminizing X chromosome variant, called X*. Thus, three types of females coexist (XX, XX*, and X*Y) that all show normal fertility. Moreover, the three chromosomes (X and Y on one side and X* on the other side) are fused to different autosomes, which results in the inclusion of the sex chromosomes in a quadrivalent in XX* and X*Y females at meiotic prophase. Here, we characterized the configurations adopted by these sex chromosome quadrivalents during meiotic prophase. The XX* quadrivalent displayed a closed structure in which all homologous chromosome arms were fully synapsed and with sufficient crossovers to ensure the reductional segregation of all chromosomes at the first meiotic division. Conversely, the X*Y quadrivalents adopted either a closed configuration with non-homologous synapsis of the X* and Y chromosomes or an open chain configuration in which X* and Y remained asynapsed and possibly transcriptionally silenced. Moreover, the number of crossovers was insufficient to ensure chromosome segregation in a significant fraction of nuclei. Together, these findings raise questions about the mechanisms allowing X*Y females to have a level of fertility as good as that of XX and XX* females, if not higher.
KeywordsAfrican pygmy mouse Sex chromosome quadrivalent Non-homologous synapsis MLH1 Meiotic recombination XY female
We thank Satoshi Namekawa for the anti-BRCA1 antibody, Marie Challe for her help in maintaining the breeding colony, and Julie Perez for genotyping some animals. We are especially indebted to the animal breeding facility of the University of Montpellier (CECEMA), the CytoEvol facilities of ISEM (labex CeMEB) and the imaging facility MRI, member of the national infrastructure France-BioImaging infrastructure supported by the French National Research Agency (ANR-10-INBS-04, «Investments for the future»).
This work was supported by grants from the Centre National pour la Recherche Scientifique (CNRS) and by the European Research Council (ERC) Executive Agency under the European Community’s Seventh Framework Programme (FP7/2007–2013 grant agreement no. 322788) to B.d.M. F.V. was funded by the French National Research Agency (ANR grant “SEXYMUS,” no. 10-JCJC-1605) and the Del Duca Foundation from Institut de France.
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