Abstract
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.
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Acknowledgements
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»).
Funding
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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Table S1
MLH1 foci in XX, XX* and X*Y pachytene oocytes in each individual mouse (DOCX 38 kb)
Figure S1
Synapsis of the sex-autosome quadrivalents in XX* and X*Y females. (a) Distribution of oocytes from XX, XX* and X*Y females at the indicated prophase I stages. The data from all mice of each genotype are pooled in Fig. 2a. Littermates are indicated by underlined or circled numbers (b) Distribution of pachytene oocytes from XX, XX* and X*Y females in the classes P1, P2, P3 and P4. P1, 1–2 fully asynapsed chromosome arms; P2, one partially asynapsed arm; P3, full synapsis with strong extended γH2AX signal on 1–2 arms; P4, full synapsis with no strong γH2AX signal. The females XX #1 and 2, XX* #2, 3 and 4, and X*Y #3 are littermates, as well as the females XX* #1 and X*Y #1. Data from all mice of each genotype are pooled in Fig. 2b. (c) Centromere signal distribution on the quadrivalent in fully synapsed (P3 and P4) pachytene oocytes from XX* and X*Y females. The data from all mice of each genotype are pooled in Fig. 3g. (PDF 143 kb)
Figure S2
BRCA1 immunostaining during meiotic prophase progression in XX females. (a-d) Chromosome spreads of oocytes from XX females stained with antibodies against centromere proteins (CEN, CREST serum, light blue), a meiotic chromosome axis marker (SYCP3, red) and BRCA1 (white or green). Stages are indicated on the left. Scale bar = 10 μm. (PDF 545 kb)
Figure S3
DMC1 immunostaining on meiotic chromosome spreads in one X*Y female. (a-d) Chromosome spreads of oocytes from one X*Y female (X*Y-1) were stained with antibodies against centromere proteins (CEN, CREST serum, blue), a meiotic chromosome axis marker (SYCP3, red) and DMC1 (green). P1, P3 and P4 classes as defined in the legend to Fig. 2. Enlarged view from each nucleus shows the sex chromosome-containing quadrivalent, with the corresponding drawing on the right panel. Recognizable chromosome arms are indicated by colored arrowheads, with the same color code as in Fig. 1. Scale bars = 10 μm. (e) Distribution of the nuclei with various patterns of DMC1 foci distribution among different classes of pachytene oocytes (P1, P2 and P3/P4). P3 and P4 nuclei were not distinguished due to the absence of γH2AX staining. P2 nuclei displaying DMC1 staining on both unsynapsed and nonhomologously synapsed regions were categorized according to the prevailing staining. (PDF 629 kb)
Figure S4
Numbers of MLH1 foci in XX, XX* and X*Y oocytes. (a) Number of MLH1 foci in pachytene nuclei displaying at least one MLH1 focus on each bivalent. Animals are the same as in Fig. S1, and the females XX #1 and 2, XX* #2, 3 and 4, and X*Y #3 are littermates. The data from all mice of each genotype are pooled in Fig. 5e. Oocyte numbers: XX-1, n = 47; XX-2, n = 58; XX*-2, n = 40; XX*-3, n = 63; XX*-4, n = 61; X*Y-2, n = 47; X*Y-3, n = 45. (PDF 150 kb)
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Baudat, F., de Massy, B. & Veyrunes, F. Sex chromosome quadrivalents in oocytes of the African pygmy mouse Mus minutoides that harbors non-conventional sex chromosomes. Chromosoma 128, 397–411 (2019). https://doi.org/10.1007/s00412-019-00699-4
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DOI: https://doi.org/10.1007/s00412-019-00699-4