Abstract
The meiotic sex chromosomes of the American marsupials Monodelphis dimidiata and Didelphis albiventris were studied with electron microscopy (EM) and with immunofluorescence localization of meiotic proteins SYCP1 and SYCP3, and proteins essential for meiotic sex chromosome inactivation (MSCI), γ-H2AX and BRCA1. The chromatin of the non-synaptic X and Y chromosomes contains γ-H2AX, first as foci and then as homogeneous staining at late stages. The thick and split X and Y axes are labelled with BRCA1 except at one terminus. The bulgings of the axes contain SYCP1 as well as the inner side of the dense plate. The evenly spaced and highly packed chromatin fibres of the conjoined XY body in these species have the same behaviour and the same components (γ-H2AX in the chromatin, BRCA1 in the axes) as in the XY body of eutherian species. These observations and recent data from the literature suggest that XY body formation is ancestral to the metatherian–eutherian divergence.
Similar content being viewed by others
References
Baker SM, Plug AW, Prolla TA, et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336–342.
Barlow AL, Hulten MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6: 350–358.
Bellani MA, Romanienko PJ, Cairatti DA, Camerini-Otero D (2005) SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of ATM−/− spermatocyes. J Cell Sci 118: 3233–3245.
Chen J, Silver DP, Walpita D, et al. (1998) Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol Cell 2: 317–328.
Davidow LS, Breen M, Duke SE, Samollow PB, McCarrey JR, Lee JT (2007) The search for a marsupial XIC reveals a break with vertebrate synteny. Chromosome Res 15: 137–146.
Durant ST, Nickoloff JA (2005) Good timing in the cell cycle for precise DNA repair by BRCA1. Cell Cycle 4: 1216–1222.
Duret L, Chureau C, Samain S, Weissenbach J, Avner P (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312: 1653–1655.
Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, et al. (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4: 497–506.
Graves JAM, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18: 517–521.
Graves JAM, Waters PD (2004) Mammalian sex chromosome evolution. The rise and fall of the Y chromosome. In: Schmid M, Nanda I, eds. Chromosomes Today. Dordrecht: Kluwer Academic, vol. 14, 3–14.
Grutzner F, Graves JAM (2004) A platypus’ eye view of the mammalian genome. Curr Opin Genet Dev 14: 642–649.
Handel MA (2004) The XY body: a specialized meiotic chromatin domain. Exp Cell Res 296: 57–63.
Hore TA, Koina E, Wakefield MJ, Graves JAM (2007) The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res 15: 147–161.
Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392: 917–920.
Mahadevaiah SK, Turner JMA, Baudat F, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapis. Nat Genet 27: 271–276.
Marcon E, Moens PB (2005) The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27: 795–808.
McCarrey JR, Watson C, Atencio J, et al. (2002) X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse. Genesis 34: 257–266.
McKee BD, Handel MA (1993) Sex chromosomes, recombination and chromatin conformation. Chromosoma 102: 71–80.
Moens PB, Marcon E, Shore JS, Kochakpour N, Spyropoulos B (2007) Initiation and resolution of interhomolog connections: crossover and noncrossover sites along mouse synaptonemal complexes. J Cell Sci 120: 1017–1027.
Monesi V (1975) Synthetic activities during spermatogenesis in the mouse. Exp Cell Res 39: 197–224.
Namekawa SH, Park PJ, Zhang L-F, et al. (2006) Postmeiotic sex chromatin in the male germline of mice. Curr Biol 16: 660–667.
Namekawa SH, Vandeberg JL, McCarrey JR, Lee JT (2007) Sex chromosome silencing in the marsupial male germ line. Proc Natl Acad Sci USA 104(23): 9730–9735.
Ollinger R, Alsheimer M, Benavente R (2005) Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell 16: 212–217.
Page J, Berrios S, Rufas JS, et al. (2003) The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamis elegans is maintained by a dense plate developed from their axial elements. J Cell Sci 116: 551–560.
Page J, Viera A, Parra MT, et al. (2006) Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genetics 2: 1240–1253.
Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W (2002) Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 12: 162–169.
Richardson BJ, Czuppon AB, Sharman GB (1971) Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos. Nat New Biol 230: 154–155.
Sciurano RB, Rahn MI, Pigozzi MI, Brugo Olmedo S, Solari AJ (2006) An azoospermic man with a double-strand DNA break-processing deficiency in the spermatocyte nuclei: case report. Hum Reprod 21: 1194–1203.
Sciurano RB, Rahn M, Rey-Valzacchi G, Solari AJ (2007) The asynaptic chromatin in spermatocytes of translocation carriers contains the histone variant γ-H2AX and associates with the XY body. Hum Reprod 22: 142–150.
Seluja GA, Roche L, Solari AJ (1987) Male meiotic prophase in Didelphis albiventris. J Hered 78: 218–222.
Sharp P (1982) Sex chromosome pairing during male meiosis in marsupials. Chromosoma 86: 27–47.
Solari AJ (1969) The evolution of the ultrastructure of the sex chromosomes (sex vesicle) during meiotic prophase in mouse spermatocytes. J Ultrastruct Res 27: 289–305.
Solari AJ (1970) The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes. Chromosoma 29: 217–236.
Solari AJ (1974) The behavior of the XY pair in mammals. Int Rev Cytol 38: 273–317.
Solari AJ (1993) Sex Chromosomes and Sex Determination in Vertebrates. Boca Raton, FL: CRC Press.
Solari AJ, Bianchi NO (1975) The synaptic behavior of the X and Y chromosomes in the marsupial Monodelphis dimidiata. Chromosoma 52: 11–25.
Turner JM (2007) Meiotic sex chromosome inactivation. Development 134: 1823–1831.
Turner JM, Mahadevaiah SK, Elliot DJ, et al. (2002) Meiotic sex chromosome inactivation in male mice with targeted disruption of Xist. J Cell Sci 115: 4097–4105.
Turner JM, Aprelikova O, Xu X, et al. (2004) BRCA1, histone H2AX phosphorylation and male meiotic sex chromosome inactivation. Curr Biol 14: 2135–2142.
Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, et al. (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37: 41–47.
Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS (2006) Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 10: 521–529.
Venkitaraman AR (2002) Functions of BRCA1 and BRCA2 in the biological response to DNA damage. J Cell Sci 114: 3591–3598.
Wettstein D von, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18: 331–413.
Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28: 360–385.
Xu X, Aprelikova O, Moens PJ, Deng C-X, Furth PA (2003) Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice. Develoment 130: 2001–2012.
Xu H, Beasley MD, Warren WD, van der Horst GTJ, McKay MJ (2005) Absence of mouse Rec8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8: 949–961.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Franco, M.J., Sciurano, R.B. & Solari, A.J. Protein immunolocalization supports the presence of identical mechanisms of XY body formation in eutherians and marsupials. Chromosome Res 15, 815–824 (2007). https://doi.org/10.1007/s10577-007-1165-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-007-1165-7