Abstract
The identification of the sex chromosomes in the three extant species of Prototherian mammals (the monotremes) is complicated by their involvement in a multivalent translocation chain at the first division of male meiosis. The platypus X chromosome, identified by the presence of two copies in females and one in males, has been found to possess a suite of genes that have been mapped to the X chromosomes of all eutherian and metatherian mammals. We have extended gene mapping studies to a member of the only other extant monotreme family, the echidna, which has a G-band equivalent X1 chromosome, as well as a smaller X2. We find that the five human X-linked genes (G6PD, GDX, F9, AR and MCF2) map to the echidna X1 chromosome in locations equivalent to those on the platypus X. These results confirm that the echidna X1 is the original X chromosome in this species, and identify a conserved ancestral monotreme X chromosome.
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References
Bick YAE, Sharman GB (1975) The chromosomes of the platypus (Ornhthorhynchus: Monotremata). Cytobios 14: 17–28
Bick YAE, Murtagh C, Sharman GB (1973) The chromosomes of an egglaying mammal Tachyglossus aculeatus (the echidna). Cytobios 14: 233–243
Choo KH, Gould KG, Rees DJG, Brownlee GG (1982) Molecular cloning of the gene for human antihaemophilic factor IX. Nature 299: 178–180
Dutrillaux B (1979) Chromosomal evolution in primates: tentative phylogeny from Microcebus Mirinus (Prosimian) to man. Hum Genet 48: 251–314
Ewens WJ, Griffiths RC, Ethier SN, Wilcox SA, Graves JAM (1992) Statistical analysis of in situ hybridization data: derivation and use of the Zmax test. Genomics (in press)
Fredga K (1970) Unusual sex chromosome inheritance in mammals. Philos Trans R Soc Lond [Biol] 259: 15–36
Ford CE, Miller OJ, Polani PE, deAlmeida JC, Briggs JH (1959) A sex-chromosome anomaly in case of gonadal dysgenesis (Turners Syndrome). Lancet 1: 711
Graves JAM, Watson JM (1991) Mammalian sex chromosomes: evolution of organization and function. Chromosoma 101: 63–68
Hayman DL (1990) Marsupial cytogenetics. Aust J Zool 37: 331–349
Hope RM, Cooper S, Wainwright B (1990) Globin macromolecular sequences in marsupials and monotremes. Aust J Zool 37: 289–313
Jacobs PA, Strong JA (1959) A case of human intersexuality having a possible XXY sex determining mechanism. Nature 183: 302–303
Kemp TS (1982) Mammal-like reptile and the origin of mammals. Academic Press, London
Lewis RR, John B (1968) The chromosomal basis of sex determination. Int Rev Cytol 23: 277–379
Lubahn DB, Joseph DR, Sullivan PM, Willard HF, French FS, Wilson EM (1988) Cloning of the human androgen receptor complementary DNA and localization to the X chromosome. Science 240: 327–330
Murtagh C (1977) A unique cytogenetic system in the monotremes. Chromosoma 65: 37–57
Murtagh CE, Sharman GB (1977) Chromosomal sex determination in monotremes. In: Calaby JH, Tyndale-Biscoe CH (eds) Reproduction and evolution. Australian Academy of Science, pp 61–66
Nash WG, O'Brien SJ (1982) Conserved subregions of homologous G-banded chromosomes between orders in mammalian evolution: Carnivores and primates. Proc Natl Acad Sci USA 76: 6631–6635
Noguchi T, Mattei MG, Oberle I, Planche J, Imbart J, Pellassy C, Birg F, Eirnbaum D (1987) Localization of the MCF2 transforming sequence to the X chromosome. EMBO J 6: 1301–1307
O'Brien SJ, Graves JAM (1991) Report of the committee on comparative gene mapping. Human Gene Mapping 11. Cytogenet Cell Genet 58: 1124–1151
O'Brien SJ, Seuanez HN, Womak JE (1985) On the evolution of genome organization in mammals. In: McIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 519–589
Persico MG, Uiglietto G, Martini G, Toniolo D, Paonessa G, Museatell C, Deno R, Villiamy T, Lazzatto L, D'Urso (1986) Isolation of human glucose-6-phosphate dehydrogenase (G6PD) cDNA clones: primary structure of the protein and unusual 5′ noncoding region. Nucleic Acids Res 14: 2511–2522
Reed K, Mann D (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 13: 7207–7221
Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in the marsupialia. Cytogenet Cell Genet 39: 40–50
Sharman GB, Hughes RL, Cooper DW (1990) The chromosomal basis for sex determination in marsupials. Aust J Zool 37: 451–466
Sinclair AM, Wrigley JM, Graves JAM (1987) Autosomal assignment of OTC in marsupials and monotremes: implications for the evolution of sex chromosomes. Genet Res 50: 131–136
Spencer JA, Watson JM, Graves JAM (1991a) The X chromosome of marsupials shares a highly conservative region with eutherians. Genomics 9: 598–604
Spencer JA, Watson JM, Lubahn DB, Joseph DR, French FS, Wilson EM, Graves JAM (1991b) The androgen receptor gene is located on a highly conserved region of the X chromosomes of marsupials and monotreme as well as eutherian mammals. J Hered 82: 134–139
Toniolo D, Perisco M, Alcalay M (1988) A “housekeeping” gene on the X chromosome encodes a protein similar to ubiquitin. Proc Natl Acad Sci USA 85: 851–855
Trapman J, Klaassen P, Kuiper GG, VanDer Korput JA, Faber PW, VanRooij JH, VanKessel AG, Voorhosst MM, Mulder E, Brinkman AO (1988) Cloning, structure and expression of a cDNA encoding the human androgen receptor. Biochem Biophys Res Commun 153: 241–248
Watson JM (1990) Monotreme genetics and cytology and a model for sex chromosome evolution. Aust J Zool 37: 385–406
Watson JM, Spencer JA, Riggs AD, Graves JAM (1990) The X chromosome of monotremes shares a highly conserved region with the eutherian and marsupial X chromosomes despite the absence of X chromosome inactivation. Proc Natl Acad Sci USA 87: 7125–7129
Watson JM, Spencer JA, Riggs AD, Graves JAM (1991) Sex chromosome evolution; platypus gene mapping suggests that part of the human X was originally autosomal. Proc Natl Acad Sci USA 88: 11256–11260
Watson JM, Meyne J, Graves JAM (1992) Chromosomal composition and position in the echidna meiotic translocation chain. In: Augee ML (ed) Platypus and echidnas. The Royal Zoological Society of New South Wales, Sydney, pp 53–63
Westerman M, Edwards D (1991) The divergence between echidna and platypus — new data from DNA studies. Aust Mammal 14: 115–120
Wrigley JM, Graves JAM (1984) Two monotreme cell lines derived from female platypuses (Ornithorhynchus anatinus: monotremata, mammalia). In Vitro 20: 321–328
Wrigley JM, Graves JAM (1988) Karyotypic conservation in the mammalian order monotremata (subclass Prototheria). Chromosoma 96: 231–247
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Watson, J.M., Riggs, A. & Marshall Graves, J.A. Gene mapping studies confirm the homology between the platypus X and echidna X1 chromosomes and identify a conserved ancestral monotreme X chromosome. Chromosoma 101, 596–601 (1992). https://doi.org/10.1007/BF00360536
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DOI: https://doi.org/10.1007/BF00360536
