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 c-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.

A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals

“…Instead, we found that X and Y chromosomes can interact through conspicuous structural modifications of AEs: we observed SYCP3 filaments connecting sex chromosomes at late stages of prophase I, and some structural modifications are also detected between zygotene and diplotene . This situation resembles the case of the Mongolian gerbil and several species of marsupials in which asynaptic sex chromosomes present striking reorganizations of SYCP3 involved in their interactions (Solari and Bianchi 1975;Sharp 1982;Roche et al 1986;Seluja et al 1987;Page et al 2005;de la Fuente et al 2007). Therefore, our results in M. duodecimcostatus reinforce and extend the idea that SC components may act as common factors for the association of asynaptic sex chromosomes.…”

“…In order to more precisely resolve the position of sex chromosomes during segregation, we used an antibody against γH2AX, a histone variant that is mainly located in the sex chromosomes at the end of prophase I and later on (de la Fuente et al 2007). Thus, we have confirmed the results of the SYCP3 signal in the sex chromosomes during the first meiotic division and the absence of chromatin connections between X and Y chromosomes during segregation (Fig.…”

“…Moreover, asynaptic sex chromosomes are also found in eutherians, particularly in species of the subfamilies Gerbillinae (Rodentia, Muridae) (Solari and Ashley 1977;Ashley and Moses 1980;de la Fuente et al 2007) and Arvicolinae (Wolf et al 1988;Ashley et al 1989a, b;Carnero et al 1991;Jimenez et al 1991;Borodin et al 1991Borodin et al , 1995Borodin et al , 2011Borodin et al , 2012. In arvicolid rodents, species of the genus Microtus show asynaptic sex chromosomes, whereas the vast majority of the genera in this subfamily exhibit synaptic X-Y chromosomes (for a review, see Borodin et al 2012).…”

“…In previous studies, we have characterized synaptonemal complex (SC)-derived structures mediating the pairing and the segregation of sex chromosomes in marsupials (Page et al 2003;2005;2006a) and gerbils (de la Fuente et al 2007). Asynaptic chromosomes are an ancient feature within both groups of animals.…”

The template choice decision in meiosis: is the sister important?

“…At mid-pachytene, the number of dots decreases, it being undetectable at late pachytene. Mlh1, a protein involved in the process of meiotic recombination, is detected at late pachytene on autosomal chromatid SCs, but it is absent on sex chromosomes (de la Fuente et al 2007).…”