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. 2016 Jul 18:6:29949.
doi: 10.1038/srep29949.

Unique sex chromosome systems in Ellobius: How do male XX chromosomes recombine and undergo pachytene chromatin inactivation?

Sergey Matveevsky  1 , Irina Bakloushinskaya  2 , Oxana Kolomiets  1
Affiliations

Unique sex chromosome systems in Ellobius: How do male XX chromosomes recombine and undergo pachytene chromatin inactivation?

Sergey Matveevsky et al. Sci Rep. .

Abstract

Most mammalian species have heteromorphic sex chromosomes in males, except for a few enigmatic groups such as the mole voles Ellobius, which do not have the Y chromosome and Sry gene. The Ellobius (XX ♀♂) system of sex chromosomes has no analogues among other animals. The structure and meiotic behaviour of the two X chromosomes were investigated for males of the sibling species Ellobius talpinus and Ellobius tancrei. Their sex chromosomes, despite their identical G-structure, demonstrate short synaptic fragments and crossover-associated MLH1 foci in both telomeric regions only. The chromatin undergoes modifications in the meiotic sex chromosomes. SUMO-1 marks a small nucleolus-like body of the meiotic XX. ATR and ubiH2A are localized in the asynaptic area and the histone γH2AFX covers the entire XX bivalent. The distribution of some markers of chromatin inactivation differentiates sex chromosomes of mole voles from those of other mammals. Sex chromosomes of both studied species have identical recombination and meiotic inactivation patterns. In Ellobius, similar chromosome morphology masks the functional heteromorphism of the male sex chromosomes, which can be seen at meiosis.

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Figures

Figure 1
Figure 1. Male G- and C-band sex chromosomes of mole voles.
(A) G-band sex chromosomes of E. tancrei (ХХ). For more details concerning G-band E. tancrei/E. talpinus sex chromosomes, see Bakloushinskaya et al. (B) C-band sex chromosomes of E. talpinus. (C) C-band sex chromosomes of E. tancrei.
Figure 2
Figure 2. Morphometric parameters and the frequency of MLH1 foci in sex bivalents of mole voles.
The x-axis shows the average length of sex bivalents in μm; the y-axis shows the relative frequency of MLH1 foci in each 10% of the length of sex bivalent. The arrows point to the central position of MLH1 in Ss2. Axial elements of the XX chromosomes are green, the central element of the SC in areas of synapsis is pink, the centromere is red, and Nlbs are grey. The frequency of MLH1 is presented graphically as blue bars.
Figure 3
Figure 3. Ellobius talpinus pachytene spermatocyte after multiple sequential immunostaining assays.
Bar = 10 μm. Localization of SYCP3 (green), SYCP1 (magenta), CREST (red), SUMO-1 (yellow), ubiH2A (cyan), RNA pol II (blue), γH2AFX (violet), MLH1 (grey) and DAPI (grey). (A–H) The same spermatocyte was stained with different antibodies. (I,J) Sex (XX) bivalent (from A–H). MLH1-signals were observed in telomeric synapsis, proteins of inactivation were localized at the asynaptic zone. SUMO-1 was located within the nucleolus-like body (Nlb) (arrow). Intense RNA pol II signal was detected in the main part of spermatocytes; within the sex bivalent, it was less intense. Co-localisation of SUMO-1, ubiH2A, RNA pol II, and γH2AFX is shown in graphs (a–d) (see I’ and J’).
Figure 4
Figure 4. Pachytene spermatocytes and male sex (XX) chromosomes of Ellobius tancrei.
Bar (A–C, H) = 5 μm; Bar (D–G, J–M) = 2 μm. Axial elements were identified using anti-SYCP3 antibodies (green), and anti-CREST for kinetochores (red). (A–C) Spermatocyte at the pachytene stage. The sex bivalent was displaced to the periphery of the nucleus. (D–G) The sex (XX) bivalent (from Figs A–C) has two regions of synapsis (white arrows) and a wide asynaptic area (asterisk) (see D). SUMO-1 (yellow) immunostained Nlb (yellow arrows) in the form of two large round spots (see E). γH2AFX (violet) surrounded the entire sex bivalent (F). DAPI-signal (grey) surrounded the sex bivalent (see C), with the more intense signal in the Nlb (see G). (H) The RNA pol II signal was intense in the main part of the spermatocyte. RNA pol II had a weak staining signal within the sex bivalent. (I) Co-localization of SUMO-1, γH2AFX, and DAPI is shown in graph (a,b) (see E–G). (J) The sex bivalent at the early pachytene stage was intensely γH2AFX stained (violet) (scheme J’). (K) The asynaptic area of the sex bivalent was intensely ATR stained at the mid pachytene stage (scheme K’). (L) The sex bivalent rolled up into a tangle at the late pachytene stage (scheme L’). Axial elements of the XX bivalent had SYCP3 gaps, which were marked with SUMO-1 (yellow). (M) The sex bivalent underwent reorganization at the early diplotene stage (scheme M’). At the same time, the gaps in the axial elements are interspersed with clusters of SYCP3 along the chromosomes, including the area near the centromere, and were surrounded by ubiH2A (cyan).
Figure 5
Figure 5. Schematic illustration of male Ellobius MSCI.
A pachytene spermatocyte (A) and a sex (XX) bivalent (B) of a mole vole are shown. The sex (XX) chromosomes form a sex body on the periphery of the nucleus. The chromatin of the sex body undergoes reorganization. MSCI markers have different distributions: SUMO-1 (yellow), ATR (black dots), ubiH2A (blue), H2AFX (violet). SUMO-1 marks a small nucleolus-like body of the meiotic XX. ATR and ubiH2A are localized in the asynaptic area of the sex bivalent. γH2AFX covers the entire XX bivalent. The approximate number of autosomal SCs is shown. MLH1 signals are shown only for the sex chromosomes (black balls). The red balls indicate centromeres.
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