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Sex differences in the meiotic behavior of an XX sex chromosome pair in males and females of the mole vole Ellobius tancrei: turning an X into a Y chromosome?

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Abstract

Sex determination in mammals is usually provided by a pair of chromosomes, XX in females and XY in males. Mole voles of the genus Ellobius are exceptions to this rule. In Ellobius tancrei, both males and females have a pair of XX chromosomes that are indistinguishable from each other in somatic cells. Nevertheless, several studies on Ellobius have reported that the two X chromosomes may have a differential organization and behavior during male meiosis. It has not yet been demonstrated if these differences also appear in female meiosis. To test this hypothesis, we have performed a comparative study of chromosome synapsis, recombination, and histone modifications during male and female meiosis in E. tancrei. We observed that synapsis between the two X chromosomes is limited to the short distal (telomeric) regions of the chromosomes in males, leaving the central region completely unsynapsed. This uneven behavior of sex chromosomes during male meiosis is accompanied by structural modifications of one of the X chromosomes, whose axial element tends to appear fragmented, accumulates the heterochromatin mark H3K9me3, and is associated with a specific nuclear body that accumulates epigenetic marks and proteins such as SUMO-1 and centromeric proteins but excludes others such as H3K4me, ubiH2A, and γH2AX. Unexpectedly, sex chromosome synapsis is delayed in female meiosis, leaving the central region unsynapsed during early pachytene. This region accumulates γH2AX up to the stage in which synapsis is completed. However, there are no structural or epigenetic differences similar to those found in males in either of the two X chromosomes. Finally, we observed that recombination in the sex chromosomes is restricted in both sexes. In males, crossover-associated MLH1 foci are located exclusively in the distal regions, indicating incipient differentiation of one of the sex chromosomes into a neo-Y. Notably, in female meiosis, the central region of the X chromosome is also devoid of MLH1 foci, revealing a lack of recombination, possibly due to insufficient homology. Overall, these results reveal new clues about the origin and evolution of sex chromosomes.

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Acknowledgements

This work was supported by grants CGL2014-53106-P from the Ministerio de Economía y Competitividad (Spain) and the Russian Foundation for Basic Research Nos. 20-34-70027 (SM), 20-04-00618 (IB), VIGG RAS State Assignment Contract No. 0112-2019-0002 and No. 0092-2019-0007 (SM, OK), and IDB RAS State Assignment for Basic Research No. 0088-2021-0019 (IB). AG-F was supported by a predoctoral fellowship from the Ministerio de Economía y Competitividad (Spain) and the European Social Fund (European Commission). We are grateful to GN Davidovich and AG Bogdanov of the Electron Microscopy Laboratory of the Biological Faculty of Moscow State University for technical assistance and Dr. C García de la Vega for insightful discussions.

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  1. Ana Gil-Fernández and Sergey Matveevsky contributed equally to this work.

Authors and Affiliations

  1. Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain

    Ana Gil-Fernández, Marta Martín-Ruiz, Marta Ribagorda, María Teresa Parra, Alberto Viera, Julio S. Rufas & Jesús Page

  2. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia

    Sergey Matveevsky & Oxana Kolomiets

  3. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia

    Irina Bakloushinskaya

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  1. Ana Gil-Fernández
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Correspondence to Irina Bakloushinskaya or Jesús Page.

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Supplementary Information

Supplementary Figure 1.

a. Immunolocalization of SYPC3 (green) and centromeres (red) in a E. tancrei spermatocyte at pachytene. The X chromosomes (XX) are indicated. b. Arranged meiotic karyotype from the same spermatocyte. The XX chromosomes from a female oocyte (XX♀) are included for comparison with the male ones (XX♂). Bar represents 10 μm. (PNG 623 kb)

High resolution image (TIF 766 kb)

Supplementary Figure 2.

Immunolocalization of SYPC3 (green) and RNA polymerase-II (red) in E. tancrei spermatocytes. a. Early pachytene. RNA pol-II appears evenly distributed over the nucleus, except in the region where the sex chromosomes (XX) are located. This localization pattern is maintained through mid pachytene (b), late pachytene (c), and early diplotene (d). However, at late diplotene (e), RNA pol-II labeling extends to the sex chromosomes. By prometaphase-I (f), no RNA pol-II signal is detected. Bar represents 10 μm. (PNG 2773 kb)

High resolution image (TIF 2940 kb)

Supplementary Figure 3.

Immunolocalization of SYPC3 (red) and RPA (green) in E. tancrei spermatocytes. a. Leptotene. RPA appears as discrete foci distributed over the forming AEs. During early (b) and late zygotene (c), RPA is located mainly along the chromosomal regions that have completed synapsis. d. Early pachytene. RPA is still abundantly distributed along chromosomes. Sex chromosomes (XX) present RPA foci in both synapsed and unsynapsed regions. e. Mid pachytene. Only a few RPA foci are still present along the chromosomes, while a diffuse staining is covering the unsynapsed regions of sex chromosomes (XX). f. Late pachytene. RPA foci are not detectable. A faint diffuse staining covers sex chromosomes (XX). Bar represents 10 μm. (PNG 761 kb)

High resolution image (TIF 989 kb)

Supplementary Figure 4.

Immunolocalization of SYPC3 (red) and RAD51 (green) in E. tancrei spermatocytes. a. Leptotene. RPA appears as discrete foci distributed over the forming AEs. During early (b) and late zygotene (c), RAD51 is located along both synapsed and unsynapsed AEs. d. Early pachytene. Only a few RAD51 foci are present along the autosomes, but many foci are still visible over the sex chromosomes (XX). A diffuse staining covers the unsynapsed regions of these chromosomes. This diffuse staining and a few RAD51 foci are still detectable during mid (e) and late pachytene (f). Bar represents 10 μm. (PNG 725 kb)

High resolution image (TIF 968 kb)

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Gil-Fernández, A., Matveevsky, S., Martín-Ruiz, M. et al. Sex differences in the meiotic behavior of an XX sex chromosome pair in males and females of the mole vole Ellobius tancrei: turning an X into a Y chromosome?. Chromosoma 130, 113–131 (2021). https://doi.org/10.1007/s00412-021-00755-y

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