Abstract
X and Y chromosomes in mammals are different in size and gene content due to an evolutionary process of differentiation and degeneration of the Y chromosome. Nevertheless, these chromosomes usually share a small region of homology, the pseudoautosomal region (PAR), which allows them to perform a partial synapsis and undergo reciprocal recombination during meiosis, which ensures their segregation. However, in some mammalian species the PAR has been lost, which challenges the pairing and segregation of sex chromosomes in meiosis. The African pygmy mouse Mus mattheyi shows completely differentiated sex chromosomes, representing an uncommon evolutionary situation among mouse species. We have performed a detailed analysis of the location of proteins involved in synaptonemal complex assembly (SYCP3), recombination (RPA, RAD51 and MLH1) and sex chromosome inactivation (γH2AX) in this species. We found that neither synapsis nor chiasmata are found between sex chromosomes and their pairing is notably delayed compared to autosomes. Interestingly, the Y chromosome only incorporates RPA and RAD51 in a reduced fraction of spermatocytes, indicating a particular DNA repair dynamic on this chromosome. The analysis of segregation revealed that sex chromosomes are associated until metaphase-I just by a chromatin contact. Unexpectedly, both sex chromosomes remain labelled with γH2AX during first meiotic division. This chromatin contact is probably enough to maintain sex chromosome association up to anaphase-I and, therefore, could be relevant to ensure their reductional segregation. The results presented suggest that the regulation of both DNA repair and epigenetic modifications in the sex chromosomes can have a great impact on the divergence of sex chromosomes and their proper transmission, widening our understanding on the relationship between meiosis and the evolution of sex chromosomes in mammals.
Highlights
Meiosis is a specialized type of cell division essential for the transmission of chromosomes across generations [1]
The asynaptic nature of sex chromosomes in M. mattheyi poses intriguing questions about the dynamics of double strand breaks (DSBs) repair in the sex chromosomes in. These results indicate that the pairing of sex chromosomes in M. mattheyi is delayed if compared to that of other mammals [14]
Contrary to M. musculus, in which γH2AX labelling in the sex chromosomes is usually lost during prometaphase-I or metaphase-I (Figure S1), we found that in M. mattheyi γH2CAoXnrtreamryaitnosMin.tomluastceurlsutsa,giensw, ahlliocwh iγnHg 2aAdXetlaaibleedlloinbgseirnvtahteiosnexofcthhreocmhorosommaetisniosrugsauna-lly loizsat tdiounrinogf tphreosme ectharpohmaoses-oImoersm
Summary
Meiosis is a specialized type of cell division essential for the transmission of chromosomes across generations [1]. DNA end resection following DSB events produces single stranded DNA overhangs that become protected by RPA protein This is subsequently replaced by recombinases RAD51 and DMC1, which promote the interaction and recognition of homologous chromosomes and, chromosome synapsis. Some of these DSBs are repaired taking the homologous chromosomes as a template, which can eventually lead to the formation of crossovers, whose cytological manifestation are chiasmata. The latter are essential for maintaining the association of homologous chromosomes until the metaphase-I/anaphase-I transition, when these chromosomes segregate to opposite cell poles. The proper segregation of homologous chromosomes during first meiotic division depends on their recognition and association in prophase-I through a homology-based mechanism [6,7]
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