Meiotic Pairing and Segregation of Achiasmate Sex Chromosomes in Eutherian Mammals: The Role of SYCP3 Protein

Abstract

In most eutherian mammals, sex chromosomes synapse and recombine during male meiosis in a small region called pseudoautosomal region. However in some species sex chromosomes do not synapse, and how these chromosomes manage to ensure their proper segregation is under discussion. Here we present a study of the meiotic structure and behavior of sex chromosomes in one of these species, the Mongolian gerbil (Meriones unguiculatus). We have analyzed the location of synaptonemal complex (SC) proteins SYCP1 and SYCP3, as well as three proteins involved in the process of meiotic recombination (RAD51, MLH1, and γ-H2AX). Our results show that although X and Y chromosomes are associated at pachytene and form a sex body, their axial elements (AEs) do not contact, and they never assemble a SC central element. Furthermore, MLH1 is not detected on the AEs of the sex chromosomes, indicating the absence of reciprocal recombination. At diplotene the organization of sex chromosomes changes strikingly, their AEs associate end to end, and SYCP3 forms an intricate network that occupies the Y chromosome and the distal region of the X chromosome long arm. Both the association of sex chromosomes and the SYCP3 structure are maintained until metaphase I. In anaphase I sex chromosomes migrate to opposite poles, but SYCP3 filaments connecting both chromosomes are observed. Hence, one can assume that SYCP3 modifications detected from diplotene onwards are correlated with the maintenance of sex chromosome association. These results demonstrate that some components of the SC may participate in the segregation of achiasmate sex chromosomes in eutherian mammals.

Chromatin Organization and Remodeling of Interstitial Telomeric Sites During Meiosis in the Mongolian Gerbil (Meriones unguiculatus)

“…This protein acts in the repair of DNA doublestrand breaks (DSBs) during early stages of meiotic prophase and may remain associated with unrepaired regions after gH2AX labeling has disappeared (Plug et al 1998). As previously reported (de la Fuente et al 2007), RAD51 is distributed along autosomes and sex chromosomes during zygotene in the Mongolian gerbil ( Figure 6E). We did not observe any accumulation of RAD51 at the pericentromeric regions, indicating that ITSs may not be a preferential location for the action of DNA repair processes.…”

“…Our previous results (de la Fuente et al 2007) and those presented here indicate that centromeric regions of metacentric chromosomes are for the most part not attached to the nuclear envelope during zygotene or pachytene. Likewise, although synapsis has been previously observed to start either from the ends or from the inner positions of the chromosomes in M. unguiculatus, we did not find evidence of a centromeric initiation of synapsis in metacentric chromosomes (de la Fuente et al 2007). However, the amazing finding that some centromere regions can bind SUN1 and attach to the nuclear envelope suggests that ITSs can retain their capability to perform some telomere-associated functions.…”

“…This suggests that, as in voles, telomeric repeats in the Mongolian gerbil are not the only origin of the pericentromeric heterochromatin (Rovatsos et al 2011). Additionally, H3K9Me3 was also detected over a whole bivalent that presented delayed synapsis (de la Fuente et al 2007) and over a large interstitial segment of another bivalent ( Figure 3A). These bivalents retained their histone signal during the entire first meiotic prophase ( Figure 3, A-D).…”

“…We used an antibody against SYCP3 protein, the main component of the SC LEs, to localize meiotic chromosomes during prophase I. Identification of the different stages of the first meiotic prophase was performed on the basis of homologous synapsis and the morphology of the sex chromosomes, as we previously reported (de la Fuente et al 2007).…”

Double-strand break repair on sex chromosomes: challenges during male meiotic prophase

“…However, there are some exception for some mammalian species, whose male sex chromosomes never recombine. 3,4 Crossovers are Generated by Homologous Recombination Repair of DNA Double-Strand Breaks…”