Dual mechanism of chromatin remodeling in the common shrew sex trivalent (XY 1Y 2)

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).

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

“…The length of the neo-PAR, the extreme size difference of the non-homologous segments of the X and Y chromosomes and the fact that all chromosome ends remain attached to the nuclear envelope force the X chromosome to bend significantly (see Fig 2F), which may be the cause of the synapsis delay, as has been reported for other chromosomal rearrangements [70,71]. Furthermore, other type of synapsis impairments have been described in other mammalian species with neo-sex chromosomes (e.g., heterologous synapsis, asynapsis, desynapsis) [20,[72][73][74]. Such modifications seem to be the norm following sex-autosome fusions in mammals.…”

“…Furthermore, other type of synapsis impairments have been described in other mammalian species with neo-sex chromosomes ( e . g ., heterologous synapsis, asynapsis, desynapsis) [ 20 , 72 – 74 ]. Such modifications seem to be the norm following sex-autosome fusions in mammals.…”

Chromosomal Analysis in Crotophaga ani (Aves, Cuculiformes) Reveals Extensive Genomic Reorganization and an Unusual Z-Autosome Robertsonian Translocation

“…However, several authors have proposed that repetitive sequences-rich regions, such as heterochromatin blocks, intercalated between the ancestral chromosome fused to the sex chromosomes can act as a barrier to the progression of meiotic sex chromosome inactivation to the autosomal segment in species with these rearrangements [ 10 , 44 , 45 ]. On the other hand, in the common shrew ( Sorex araneus ), the translocated autosomal element onto the X chromosome did not affect the behaviour of the true sex chromosome regions in meiosis and did not affect the process of chromatin transformation at prophase I [ 46 ].…”

Reorganization of the Y Chromosomes Enhances Divergence in Israeli Mole Rats Nannospalax ehrenbergi (Spalacidae, Rodentia): Comparative Analysis of Meiotic and Mitotic Chromosomes

“…For example, mice Mus possess an incredible variability of autosomes and diverse types of sex chromosomes changes, such as displacement of the PAR border [ 84 ], heterochromatin variations [ 95 ], Robertsonian translocations [ 96 , 97 ], whole-arm reciprocal translocation (WART) [ 98 ], and sex-reverse mutation (XY female) [ 5 ]. Considerable chromosomal variations and sex trivalent XY 1 Y 2 have been described in males with different karyotypes of the common shrew Sorex araneus [ 99 , 100 ]. The eastern mole vole has been shown to present unique XX chromosomes in males and females and extreme autosomal variability [ 4 ].…”