Platypus chain reaction: directional and ordered meiotic pairing of the multiple sex chromosome chain in Ornithorhynchus anatinus
Tasman Daish A , Aaron Casey A and Frank Grützner A BA Discipline of Genetics, School of Molecular and Biomedical Science, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia.
B Corresponding author. Email: frank.grutzner@adelaide.edu.au
Reproduction, Fertility and Development 21(8) 976-984 https://doi.org/10.1071/RD09085
Submitted: 6 April 2009 Accepted: 25 June 2009 Published: 30 October 2009
Abstract
Monotremes are phylogenetically and phenotypically unique animals with an unusually complex sex chromosome system that is composed of ten chromosomes in platypus and nine in echidna. These chromosomes are alternately linked (X1Y1, X2Y2, …) at meiosis via pseudoautosomal regions and segregate to form spermatozoa containing either X or Y chromosomes. The physical and epigenetic mechanisms involved in pairing and assembly of the complex sex chromosome chain in early meiotic prophase I are completely unknown. We have analysed the pairing dynamics of specific sex chromosome pseudoautosomal regions in platypus spermatocytes during prophase of meiosis I. Our data show a highly coordinated pairing process that begins at the terminal Y5 chromosome and completes with the union of sex chromosomes X1Y1. The consistency of this ordered assembly of the chain is remarkable and raises questions about the mechanisms and factors that regulate the differential pairing of sex chromosomes and how this relates to potential meiotic silencing mechanisms and alternate segregation.
Additional keywords: chromosome pairing, meiosis, pseudoautosomal regions, telomeres.
Acknowledgements
This work was funded by the Australian Research Council (DP0664267). F.G. is an ARC Australian Research Fellow. A.C. is supported by an Australian Postgraduate Award.
Daish, T. , and Grützner, F. (2009). Location, location, location! Monotremes provide unique insights into the evolution of sex chromosome silencing in mammals. DNA Cell Biol. 28, 91–100.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Davis, L. , and Smith, G. R. (2006). The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174, 167–177.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
de Boer, E. , and Heyting, C. (2006). The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115, 220–234.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ding, D. Q. , Yamamoto, A. , Haraguchi, T. , and Hiraoka, Y. (2004). Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev. Cell 6, 329–341.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ding, X. , Xu, R. , Yu, J. , Xu, T. , Zhuang, Y. , and Han, M. (2007). SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12, 863–872.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Dohm, J. C. , Tsend-Ayush, E. , Reinhardt, R. , Grützner, F. , and Himmelbauer, H. (2007). Disruption and pseudoautosomal localization of the major histocompatibility complex in monotremes. Genome Biol. 8, R175.1–R175.16.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gerton, J. L. , and Hawley, R. S. (2005). Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat. Rev. Genet. 6, 477–487.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Grützner, F. , Ashley, T. , Rowell, D. M. , and Graves, J. A. M. (2006). How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals. Chromosoma 115, 75–88.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grützner, F. , Rens, W. , Tsend-Ayush, E. , El-Mogharbel, N. , O’Brien, P. C. , Jones, R. C. , Ferguson-Smith, M. A. , and Graves, J. A. M. (2004). In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432, 913–917.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grützner, F. , Nixon, B. , and Jones, R. C. (2008). Reproductive biology in egg-laying mammals. Sex Dev. 2, 115–127.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harper, L. , Golubovskaya, I. , and Cande, W. Z. (2004). A bouquet of chromosomes. J. Cell Sci. 117, 4025–4032.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hirano, T. (2006). At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7, 311–322.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Johannisson, R. , and Winking, H. (1994). Synaptonemal complexes of chains and rings in mice heterozygous for multiple Robertsonian translocations. Chromosome Res. 2, 137–145.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Klein, F. , Mahr, P. , Galova, M. , Buonomo, S. B. , Michaelis, C. , Nairz, K. , and Nasmyth, K. (1999). A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98, 91–103.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Liebe, B. , Alsheimer, M. , Hoog, C. , Benavente, R. , and Scherthan, H. (2004). Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell 15, 827–837.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Liebe, B. , Petukhova, G. , Barchi, M. , Bellani, M. , and Braselmann, H. , et al. (2006). Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp. Cell Res. 312, 3768–3781.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Niwa, O. , Shimanuki, M. , and Miki, F. (2000). Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19, 3831–3840.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Page, J. , Berrios, S. , Rufas, J. S. , Parra, M. T. , Suja, J. A. , Heyting, C. , and Fernandez-Donoso, R. (2003). 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. J. Cell Sci. 116, 551–560.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Page, J. , Viera, A. , Parra, M. T. , de la Fuente, R. , Suja, J. A. , Prieto, I. , Barbero, J. L. , Rufas, J. S. , Berrios, S. , and Fernandez-Donoso, R. (2006). Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet. 2, e136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Penkner, A. , Portik-Dobos, Z. , Tang, L. , Schnabel, R. , Novatchkova, M. , Jantsch, V. , and Loidl, J. (2007). A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J. 26, 5071–5082.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Peters, A. H. , Plug, A. W. , van Vugt, M. J. , and de Boer, P. (1997). A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5, 66–68.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Rens, W. , Grützner, F. , O’Brien, P. C. , Fairclough, H. , Graves, J. A. M. , and Ferguson-Smith, M. A. (2004). Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc. Natl Acad. Sci. USA 101, 16 257–16 261.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Rens, W. , O’Brien, P. C. , Grützner, F. , Clarke, O. , and Graphodatskaya, D. , et al. (2007). The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z. Genome Biol. 8, R243.1–R243.21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Revenkova, E. , Eijpe, M. , Heyting, C. , Hodges, C. A. , Hunt, P. A. , Liebe, B. , Scherthan, H. , and Jessberger, R. (2004). Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat. Cell Biol. 6, 555–562.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Scherthan, H. (2007). Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117–124.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Scherthan, H. , Eils, R. , Trelles-Sticken, E. , Dietzel, S. , Cremer, T. , Walt, H. , and Jauch, A. (1998). Aspects of three-dimensional chromosome reorganization during the onset of human male meiotic prophase. J. Cell Sci. 111, 2337–2351.
| PubMed | CAS |
Scherthan, H. , Jerratsch, M. , Li, B. , Smith, S. , Hulten, M. , Lock, T. , and de Lange, T. (2000). Mammalian meiotic telomeres: protein composition and redistribution in relation to nuclear pores. Mol. Biol. Cell 11, 4189–4203.
| PubMed | CAS |
Smilenov, L. B. , Dhar, S. , and Pandita, T. K. (1999). Altered telomere nuclear matrix interactions and nucleosomal periodicity in ataxia telangiectasia cells before and after ionizing radiation treatment. Mol. Cell. Biol. 19, 6963–6971.
| PubMed | CAS |
Solari, A. J. , and Bianchi, N. O. (1975). The synaptic behaviour of the X and Y chromosomes in the marsupial Monodelphis dimidiata. Chromosoma 52, 11–25.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Trelles-Sticken, E. , Dresser, M. E. , and Scherthan, H. (2000). Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151, 95–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Trelles-Sticken, E. , Adelfalk, C. , Loidl, J. , and Scherthan, H. (2005a). Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol. 170, 213–223.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Trelles-Sticken, E. , Bonfils, S. , Sollier, J. , Géli, V. , Scherthan, H. , and de La Roche Saint-André, C. (2005b). Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis. J. Cell Sci. 118, 4985–4994.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Tsend-Ayush, E. , Dodge, N. , Mohr, J. , Casey, A. , Himmelbauer, H. , Kremitzki, C. L. , Schatzkamer, K. , Graves, T. , Warren, W. C. , and Grützner, F. (2009). Higher-order genome organization in platypus and chicken sperm and repositioning of sex chromosomes during mammalian evolution. Chromosoma 118, 53–69.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Turner, J. M. (2007). Meiotic sex chromosome inactivation. Development 134, 1823–1831.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tuzon, C. T. , Borgstrom, B. , Weilguny, D. , Egel, R. , Cooper, J. P. , and Nielsen, O. (2004). The fission yeast heterochromatin protein Rik1 is required for telomere clustering during meiosis. J. Cell Biol. 165, 759–765.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Veyrunes, F. , Waters, P. D. , Miethke, P. , Rens, W. , and McMillan, D. , et al. (2008). Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965–973.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wu, H. Y. , and Burgess, S. M. (2006). Ndj1, a telomere-associated protein, promotes meiotic recombination in budding yeast. Mol. Cell. Biol. 26, 3683–3694.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zickler, D. , and Kleckner, N. (1998). The leptotene–zygotene transition of meiosis. Annu. Rev. Genet. 32, 619–697.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |