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.
Highlights
The proper distribution of chromosomes into daughter cells during meiosis depends on the essential phenomena of pairing, synapsis, recombination, and segregation
Meiosis is a special kind of cell division that leads to the formation of gametes
This is the case in the Mongolian gerbil, a mammal whose sex chromosomes pair and segregate during male meiosis without undergoing meiotic recombination
Summary
The proper distribution of chromosomes into daughter cells during meiosis depends on the essential phenomena of pairing, synapsis, recombination, and segregation. Recombination between homologues along with the existence of mechanisms that maintain sister chromatid cohesion are responsible for ensuring the proper segregation of homologous chromosomes during first meiotic division [5,6]. Homologous recognition, pairing, and synapsis are promoted by the initiation of recombination events involved in the repair of programmed DNA double strand breaks (DSBs) made by SPO11 protein at the very beginning of first meiotic prophase [7,8,9]. At least one chiasma per bivalent is necessary to ensure that homologues remain associated from the disorganization of the SC at diplotene until they segregate at anaphase I
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