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. 2017 Nov 3;11(4):727-745.
doi: 10.3897/CompCytogen.v11i4.13870. eCollection 2017.

Dual Mechanism of Chromatin Remodeling in the Common Shrew Sex Trivalent (XY 1 Y 2)

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Free PMC article

Dual Mechanism of Chromatin Remodeling in the Common Shrew Sex Trivalent (XY 1 Y 2)

Sergey N Matveevsky et al. Comp Cytogenet. .
Free PMC article

Abstract

Here we focus on the XY1Y2 condition in male common shrew Sorex araneus Linnaeus, 1758, applying electron microscopy and immunocytochemistry for a comprehensive analysis of structure, synapsis and behaviour of the sex trivalent in pachytene spermatocytes. The pachytene sex trivalent consists of three distinct parts: short and long synaptic SC fragments (between the X and Y1 and between the X and Y2, respectively) and a long asynaptic region of the X in-between. Chromatin inactivation was revealed in the XY1 synaptic region, the asynaptic region of the X and a very small asynaptic part of the Y2. This inactive part of the sex trivalent, that we named the 'head', forms a typical sex body and is located at the periphery of the meiotic nucleus at mid pachytene. The second part or 'tail', a long region of synapsis between the X and Y2 chromosomes, is directed from the periphery into the nucleus. Based on the distribution patterns of four proteins involved in chromatin inactivation, we propose a model of meiotic silencing in shrew sex chromosomes. Thus, we conclude that pachytene sex chromosomes are structurally and functionally two different chromatin domains with specific nuclear topology: the peripheral inactivated 'true' sex chromosome regions (part of the X and the Y1) and more centrally located transcriptionally active autosomal segments (part of the X and the Y2).

Keywords: ATR; MSCI; SUMO-1; Sex body; Sorex araneus; synaptonemal complex; ubiH2A; γH2AFX.

Figures

Figure 1.
Figure 1.
a G-banded sex chromosomes in the male common shrew (left) and ideogram with chromosome arms labelled according to the alphabetic nomenclature of Searle et al. (1991) b Schematic diagram of the shrew pachytene sex trivalent, based on Pack et al. (1993) and our data c Electron micrograph of a shrew sex trivalent, XY1Y2 at late pachytene. The true X region and the Y1 are surrounded by electron-dense material. Scale bar: 5µm. d Diagram of the XY1Y2 configuration as represented in Fig. 1c.
Figure 2.
Figure 2.
Mid-pachytene spermatocytes and male sex (XY1Y2) chromosomes of Sorex araneus. Bar = 5µm. The axial elements of the SC and the kinetochores were localised using anti-SYCP3 (green) and anti-CREST (red) antibodies, respectively. a–e ATR (magenta) has a discontinuous localisation within the chromatin of the true sex chromosome regions (part of the X and the Y1). The co-localisation of ATR, γH2AFX (violet), DAPI (grey) is shown in graph a-b (see c and c’) f–j SUMO-1 (yellow) is localised on the chromatin of true sex chromosome regions. The co-localisation of SUMO-1, γH2AFX (violet) and DAPI (grey) is shown in graph c-d (see h and h’) k–o ubiH2A (cyan) is localised on the chromatin of the true sex chromosome regions. The co-localisation of ubiH2A, γH2AFX (violet) and DAPI (grey) is shown in graph e-f (see m and m’) d, i, n Diagrams of the sex trivalents p, p’, p’’ SYCP1 (magenta) is located on the area of chromosome synapsis of the autosomal part of the XY1Y2 (from a-c) q XY1Y2 has two MLH1 signals (yellow). The MLH1 signal within the PAR synaptic site is marked by an asterisk. The arrowhead indicates the centromeres of the autosomal part of sex trivalent (part of the X and the Y2) which are not co-oriented with each other (red).
Figure 3.
Figure 3.
Mid-pachytene spermatocytes of Sorex araneus. Double immunostaining with antibodies: a–c anti-SYCP3 (green)/anti-ubiH2A (cyan) d–f anti-SYCP3 (green)/anti-SUMO-1 (yellow) g–i anti-SYCP3 (green)/anti-RNA Pol II (blue) j–l anti-SYCP3 (green)/anti-γH2AFX (violet). The true sex chromosome region is designated as XY1. Scale bars: 5 µm.
Figure 4.
Figure 4.
Intensity correlation analysis (ICA) represented by scatter plots showing the paired intensities of two channels (a γH2AFX - ATR, Fig. 2a–c b γH2AFX - SUMO-1, Fig. 2f–h c γH2AFX - ubiH2A Fig. 2k-m). rp - Pearson correlation coefficient. See more details in the text. Degree of co-localisation for signals in sex trivalents of common shrew (d). On the y-axis, the percentage of co-localised signals are shown according to overlap correlation coefficients (r) and the Pearson correlation coefficient (rp).
Figure 5.
Figure 5.
Schematic illustration of male common shrew MSCI. A mid-pachytene spermatocyte (a) and a sex (XY1Y2) trivalent (b) of a shrew are shown. An electron micrograph of the sex trivalent is shown at the top of the b. The true sex chromosome regions (part of the X and the Y1) form a sex body on the periphery of the nucleus. The chromatin of the sex body undergoes reorganisation. MSCI markers have different distributions: SUMO-1 (yellow), ATR (black dots), ubiH2A (blue), γH2AFX (violet). ATR is localised on the true sex chromosome regions, and is especially intense on the asynaptic region with a smaller amount where there is synapsis. SUMO-1 and ubiH2A are localised on both the asynaptic and synaptic regions of the true sex chromosome regions. γH2AFX overlays all the true sex chromosome regions and the unpaired part of the Y2 axial element. Representative autosomal SCs are shown. MLH1 signals are shown as black balls. The red balls indicate centromeres.

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