Synaptonemal complexes in Gerbillidae: probable role of intercalated heterochromatin in gonosome-autosome translocations

Abstract

A study of sex chromosomes and synaptonemal complexes in male specimens of Gerbillus chiesmaní, G. nigeriae, G. hoogstrali, and Taterillus pygargus is reported. In each of these Gerbillidae species there are two or three translocations of autosomes with X and Y chromosomes. Analysis of mitotic chromosomes consistently shows the presence of constitutive heterochromatin on the der t(X;autosome) at the X-autosome junction and on the der t(Y;autosome). Analysis of the synaptonemal complexes shows the existence of an unusual structure, lightly stained, at the X-autosome junction and at the Y-autosome junction, which is probably heterochromatic in nature, thus corresponding to the mitotic patterns. This heterochromatin separates the autosomal and gonosomal segments, which behave independently and normally. By analogy with findings from humans and other mammals, a general hypothesis is proposed on the role of intercalated heterochromatin between translocated gonosomes and autosomes. This hypothesis explains why the pathological consequences of these translocations may be very different in males and females. The role of intercalated heterochromatin would be to avoid the pathological consequences of gonosome-autosome translocations resulting from inactivation of the sex chromosomes in female somatic cells and male germinal cells.

Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein

“…However, the ends of sex chromosome AEs are distally connected at the beginning of diplotene ( Figure 2D and 2D9). This contact may involve any of the ends of each sex chromosome with the other sex chromosome or even the two tips of each chromosome, as shown for sex chromosomes of other species of Gerbillidae [30,31,33]. Nevertheless, at late diplotene the four chromosome ends are always connected ( Figure 2E and 2E9).…”

“…This situation is especially well characterized in marsupials [24][25][26][27][28], in which we have recently reported that a particular structure formed by SC proteins, called dense plate, is involved in maintaining the association of the X and Y chromosomes from pachytene until they segregate at anaphase I [29]. The lack of synapsis has also been reported in some species of eutherian mammals, especially among gerbils and voles [30][31][32][33][34]. In these species sex chromosomes do not form SC, but they are associated during first meiotic prophase and segregate properly during first meiotic division.…”

“…This is the case of Psamommys obessus [30,33], Gerbillus campestris, M. libycus, M. shawi, and M. crassus [32]. On the other hand, some species present sex chromosomes with synapsis and recombination, as in G. chiesmani, G. nigeriae, G. hoogstrali, and Taterillus pygargus [31]. However, the synapsing regions in these species seem to be originated, as in many other eutherian mammals, by recent translocations of autosomal segments to both the X and Y chromosomes [49,50].…”

“…To shed light on these mechanisms, we have investigated the sequence and the nature of X and Y chromosome association during male meiosis in the Mongolian gerbil (M. unguiculatus), an eutherian mammal that presents asynaptic sex chromosomes [31]. For this purpose we have analyzed the location of SYCP1 and SYCP3 proteins of the SC [35][36][37], as well as RAD51 and MLH1 proteins, which are involved in meiotic recombination [38,39], and c-H2AX, a histone variant related to both DSBs9 repair and meiotic sex chromosome inactivation [40,41].…”

Synaptonemal complex karyotype of the pachytene spermatocytes and oocytes of the Turkish hamster (Mesocricetus brandti)

“…Species with unique chromosomal structure such as Gerbil (WAHRMAN etal. 1983;RATOMPONIRINA et al 1986) and Palearctic hamsters (SPYROPOULOS et al 1982), or the common shrew (BoRODIN 1991) have been of particular value. The latter study which detailed the pairing of a Robertsonian translocation and polymorphic Y chromosomes highlights such an informative examination.…”