The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements

Abstract

Unlike eutherian males, pairing of the sex chromosomes in marsupial males during the first meiotic prophase is not mediated by a synaptonemal complex. Instead, a specific structure, the dense plate, develops during pachytene between the sex chromosomes. We have investigated the development and structural nature of this asynaptic association in males of the marsupial species Thylamys elegans by means of immunolabelling and electron microscopy techniques. Our results show that the behaviour of male marsupial sex chromosomes during first meiotic prophase is complex, involving modifications of their structure and/or composition. Pairing of the sex chromosomes and formation of the dense plate take place in mid pachytene,paralleling morphological changes in the sex chromosomal axial elements. Components of the central element of the synaptonemal complex were not found in the sex body, in agreement with ultrastructural studies that reported the absence of a canonical tripartite synaptonemal complex between male marsupial sex chromosomes. Interestingly, the dense plate is labelled with antibodies against the SCP3 protein of the lateral elements of the synaptonemal complex. Moreover, as sex chromosome axial elements decrease in mass throughout mid-late pachytene, the dense plate increases, suggesting that material moves from the axial elements to the dense plate. Additionally, both sex chromosome axial elements and the dense plate have proteins that are specifically phosphorylated, as revealed by their labelling with the MPM-2 antibody,indicating that they undergo a chromosome-specific regulation process throughout first meiotic prophase. We propose that the unique modifications of the composition and structure of the axial elements of the sex chromosomes in meiotic prophase may result in the proscription of synaptonemal complex formation between male marsupial sex chromosomes, where the dense plate is an extension of the axial elements of sex chromosomes. This replaces synapsis to maintain X and Y association during first meiotic prophase.

Cytogenetic and Molecular Evaluation of Centromere-Associated DNA Sequences From a Marsupial (Macropodidae:Macropus rufogriseus) X Chromosome

“…Unequal crossover has been suggested to explain sex chromosome-specific amplification of constitutive heterochromatin seen in rodents (Nova et al 2002). The marsupial X and Y do not undergo homologous pairing (side to side) at meiosis; however, axial pairing (end to end) does occur (Solari and Bianchi 1975;Sharp 1982;Page et al 2003). Although no pseudoautosomal region has been identified on marsupial sex chromosomes , the X and Y of Macropus eugenii have been shown to possess homologous sequences (Toder et al 1997b).…”

Sex chromosomes, synapsis, and cohesins: a complex affair

“…According to this, the dense plate is mainly formed by the SYCP3 component of the AEs (Fig. 4c,d) (Page et al 2003). It is interesting to note that although the cohesin subunits SMC3 and STAG3 are present along sex chromosomes, they do not follow many of the modifications of the sex chromosomal AEs and, most relevantly, do not participate in the organization of the dense plate .…”

“…The modification of the AEs that originates the dense plate in marsupial males is indicative that the structural elements of the SC may play, in addition to the organization of the canonical LEs, other roles in nonhomologous chromosomes pairing (Page et al 2003) and segregation (Page et al unpublished). These additional roles of the SC elements are not exclusive of marsupial meiosis.…”

An Analysis of Univalent Segregation in Meiotic Mutants ofArabidopsis thaliana: A Possible Role for Synaptonemal Complex

“…In mouse, a meiosis-specific structural protein, Sycp3, which appears in axial and lateral elements of the SC, is involved in the monopolar attachment of sister kinetochores during the first meiotic division (Parra et al 2004). Recently, Page et al (2003Page et al ( , 2005 have reported that in marsupial males the pairing of the achiasmatic X and Y chromosomes during meiotic prophase is maintained by a dense plate developed from their axial elements.…”