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

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.

[1]  J. Suja,et al.  Squash Procedure for Protein Immunolocalization in Meiotic Cells , 1998, Chromosome Research.

[2]  P. de Boer,et al.  SHORT COMMUNICATIONS A drying-down technique for the spreading of mammalian meiocytes from the male and female germline , 1997, Chromosome Research.

[3]  P. Moens,et al.  Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis , 1995, Chromosoma.

[4]  J. Graves,et al.  Mammalian sex chromosomes: Evolution of organization and function , 1991, Chromosoma.

[5]  S. Berríos,et al.  Nuclear architecture of human pachytene spermatocytes: quantitative analysis of associations between nucleolar and XY bivalents , 1990, Human Genetics.

[6]  R. Wettstein,et al.  The meiotic behaviour of the XY pair in Lutreolina crassicaudata (Marsupialia: Didelphoidea) , 1986, Genetica.

[7]  T. Ashley,et al.  Ultrastructure and behavior of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus) , 1977, Chromosoma.

[8]  C. Murtagh A unique cytogenetic system in monotremes , 1977, Chromosoma.

[9]  N. Bianchi,et al.  The synaptic behaviour of the X and Y chromosomes in the marsupial Monodelphis dimidiata , 1975, Chromosoma.

[10]  P. Burgoyne,et al.  Genetic homology and crossing over in the X and Y chromosomes of mammals , 2004, Human Genetics.

[11]  M. Handel,et al.  Sex chromosomes, recombination, and chromatin conformation , 2004, Chromosoma.

[12]  P. Sharp Sex chromosome pairing during male meiosis in marsupials , 2004, Chromosoma.

[13]  A. Solari The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes , 2004, Chromosoma.

[14]  J. Graves,et al.  The minimal mammalian Y chromosome – the marsupial Y as a model system , 2001, Cytogenetic and Genome Research.

[15]  J. Suja,et al.  Phosphorylated proteins are involved in sister-chromatid arm cohesion during meiosis I. , 1999, Journal of cell science.

[16]  S. Pöggeler,et al.  Spo76p Is a Conserved Chromosome Morphogenesis Protein that Links the Mitotic and Meiotic Programs , 1999, Cell.

[17]  C. Heyting,et al.  SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. , 1998, Nucleic acids research.

[18]  N. Kleckner,et al.  The leptotene-zygotene transition of meiosis. , 1998, Annual review of genetics.

[19]  J. Wienberg,et al.  Shared DNA sequences between the X and Y chromosomes in the tammar wallaby – evidence for independent additions to eutherian and marsupial sex chromosomes , 1997, Chromosoma.

[20]  R. Benavente,et al.  Change of karyoskeleton during mammalian spermatogenesis: expression pattern of nuclear lamin C2 and its regulation. , 1996, Experimental cell research.

[21]  C. Heyting Synaptonemal complexes: structure and function. , 1996, Current opinion in cell biology.

[22]  R. Pearlman,et al.  Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. , 1994, Journal of cell science.

[23]  C. Heyting,et al.  The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes , 1994, Molecular and cellular biology.

[24]  K. Wolf How meiotic cells deal with non‐exchange chromosomes , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[25]  S. Demirel [Opening speech by President Suleyman Demirel for the meeting "Population Issues in Turkey: Policy Priorities"]. , 1994, Nufusbilim dergisi.

[26]  A. Solari Sex Chromosomes and Sex Determination in Vertebrates , 1993 .

[27]  C. Heyting,et al.  A coiled‐coil related protein specific for synapsed regions of meiotic prophase chromosomes. , 1992, The EMBO journal.

[28]  P. Hunt,et al.  Sex‐chromosome pairing and activity during mammalian meiosis , 1992, BioEssays : news and reviews in molecular, cellular and developmental biology.

[29]  A. Solari,et al.  Male meiotic prophase in Didelphis albiventris A comparative cytological and electron microscopical study , 1987 .

[30]  F. M. Davis,et al.  Monoclonal antibodies to mitotic cells. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[31]  S. Pathak,et al.  Asynaptic behavior of X and Y chromosomes in the Virginia oppossum and the southern pygmy mouse. , 1980, Cytogenetics and cell genetics.

[32]  A. Solari The behavior of the XY pair in mammals. , 1974, International review of cytology.

[33]  J. Rattner Nuclear shaping in marsupial spermatids. , 1972, Journal of ultrastructure research.

[34]  O. Reig,et al.  Further Occurrence of a Karyotype of 2N = 14 Chromosomes in two Species of Chilean Didelphoid Marsupiais , 1972 .

[35]  D. Fawcett THE FINE STRUCTURE OF CHROMOSOMES IN THE MEIOTIC PROPHASE OF VERTEBRATE SPERMATOCYTES , 1956, The Journal of biophysical and biochemical cytology.

[36]  M. Moses Chromosomal Structures in Crayfish Spermatocytes , 1956, The Journal of biophysical and biochemical cytology.