Platypus chain reaction: Directional and ordered meiotic pairing of the multiple sex chromosome chain in Ornithorhynchus anatinus

Reproduction, Fertility and Development

Volumn 21, Issue 8, 2009, Pages 976-984

  Daish, Tasman ^a   Casey, Aaron ^a   Grützner, Frank ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Chromosome pairing; Meiosis; Pseudoautosomal regions; Telomeres

Indexed keywords

ARTICLE; ECHIDNA; MALE; MEIOSIS; MEIOTIC PROPHASE I; MONOTREMATE; NONHUMAN; ORNITHORHYNCHUS ANATINUS; PHENOTYPE; PHYLOGENY; PLATYPUS; SEX CHROMOSOME; SPERMATOCYTE; SPERMATOZOON; X CHROMOSOME; Y CHROMOSOME;

ANIMALS; CHROMOSOME PAIRING; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CHROMOSOMES, MAMMALIAN; DNA REPLICATION TIMING; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MEIOSIS; MODELS, BIOLOGICAL; PLATYPUS; SEX CHROMOSOMES; TELOMERE;

ANIMALIA; MONOTREMATA; ORNITHORHYNCHUS ANATINUS;

EID: 71049165323     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09085     Document Type: Article

References (38)

1. 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. doi:10.1089/DNA.2008.0818
2. Davis, L., and Smith, G. R. (2006). The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174, 167-177. doi:10.1534/GENETICS.106.059733 (Pubitemid 44427663)
3. de Boer, E., and Heyting, C. (2006). The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115, 220-234. doi:10.1007/S00412-006-0057-5
4. 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. doi:10.1016/S1534-5807(04)00059-0 (Pubitemid 38364566)
5. 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. doi:10.1016/J.DEVCEL.2007.03.018 (Pubitemid 46805916)
6. 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. doi:10.1186/GB-2007-8-8-R175
7. Gerton, J. L., and Hawley, R. S. (2005). Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat. Rev. Genet. 6, 477-487. doi:10.1038/NRG1614
8. 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. doi:10.1007/S00412-005-0034-4
9. 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. doi:10.1038/NATURE03021 (Pubitemid 40037154)
10. Grützner, F., Nixon, B., and Jones, R. C. (2008). Reproductive biology in egg-laying mammals. Sex Dev. 2, 115-127. doi:10.1159/000143429
11. Harper, L., Golubovskaya, I., and Cande, W. Z. (2004). A bouquet of chromosomes. J. Cell Sci. 117, 4025-4032. doi:10.1242/JCS.01363
12. Hirano, T. (2006). At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7, 311-322. doi:10.1038/NRM1909
13. Johannisson, R., andWinking, H. (1994). Synaptonemal complexes of chains and rings in mice heterozygous for multiple Robertsonian translocations. Chromosome Res. 2, 137-145. doi:10.1007/BF01553492
14. 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. doi:10.1016/S0092-8674(00)80609-1 (Pubitemid 29331199)
15. 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. doi:10.1091/MBC.E03-07-0524 (Pubitemid 38146496)
16. Liebe, B., Petukhova, G., Barchi, M., Bellani, M., 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. doi:10.1016/J.YEXCR.2006.07.019
17. 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. doi:10.1093/EMBOJ/19.14.3831 (Pubitemid 30462140)
18. 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. doi:10.1242/JCS.00252 (Pubitemid 36231293)
19. 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. doi:10.1371/JOURNAL.PGEN. 0020136
20. Penkner, A., Portik-Dobos, Z., Tang, L., Schnabel, R., Novatchkova, M., Jantsch,V., and Loidl, J. (2007).Aconserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J. 26, 5071-5082. doi:10.1038/SJ.EMBOJ.7601916 (Pubitemid 350261279)
21. 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.
22. 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 duckbilled platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc. Natl Acad. Sci. USA 101, 16 257-16 261. doi:10.1073/PNAS. 0405702101
23. Rens,W., O'Brien, P. C., Grützner, F., Clarke, O., 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. doi:10.1186/GB-2007-8-11-R243
24. 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. doi:10.1038/NCB1135
25. Scherthan, H. (2007). Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117-124. doi:10.1007/S00018-006-6463-2
26. 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. (Pubitemid 28434921)
27. 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.
28. 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. (Pubitemid 29441878)
29. 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. doi:10.1007/BF00285785
30. 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. doi:10.1083/JCB.151.1.95 (Pubitemid 30761123)
31. 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. doi:10.1083/JCB.200501042
32. Trelles-Sticken, E., Bonfils, S., Sollier, J., Géli, V., Scherthan, H., and de La Roche Saint-Andŕ, 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. doi:10.1242/10.1242/JCS.02612
33. 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 spermand repositioning of sex chromosomes during mammalian evolution. Chromosoma 118, 53-69. doi:10.1007/S00412-008-0177-1
34. Turner, J. M. (2007). Meiotic sex chromosome inactivation. Development 134, 1823-1831. doi:10.1242/DEV.000018
35. 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. doi:10.1083/JCB.200312061 (Pubitemid 38821966)
36. Veyrunes, F., Waters, P. D., Miethke, P., Rens, W., McMillan, D., et al. (2008). Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965-973. doi:10.1101/GR.7101908 (Pubitemid 351793069)
37. 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. doi:10.1128/MCB.26.10.3683-3694.2006
38. Zickler, D., and Kleckner, N. (1998). The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-697. doi:10.1146/ANNUREV. GENET.32.1.619