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Chromosome Research

, Volume 12, Issue 8, pp 795–804 | Cite as

Molecular characterization and evolution of X and Y-borne ATRX homologues in American marsupials

  • Denise R. Carvalho-SilvaEmail author
  • Rachel J. W. O’Neill
  • Judith D. Brown
  • Kim Huynh
  • Paul D. Waters
  • Andrew J. Pask
  • Margaret L. Delbridge
  • Jennifer A. Marshall Graves
Article

Abstract

In eutherians, the sex-reversing ATRX gene on the X has no homologue on the Y chromosome. However, testis-specific and ubiquitously expressed X-borne genes have been identified in Australian marsupials. We studied nucleotide sequence and chromosomal location of ATRX homologues in two American marsupials, the opossums Didelphis virginiana and Monodelphis domestica. A PCR fragment of M. domestica ATRX was used to probe Southern blots and to screen male genomic libraries. Southern analysis demonstrated ATRX homologues on both X and Y in D. virginiana, and two clones were isolated which hybridized to a single position on the Y chromosome in male-derived cells but to multiple sites of the X in female cells. In M. domestica, there was a single clone that mapped to the X but not to the Y, suggesting that it represents the M. domestica ATRX. However a male-specific band was detected in Southern blots probed with the D. virginiana ATRY and with a mouse ATRX clone, which implies that the Y copy in M. domestica has diverged further from other ATRX homologues. Thus there appears to be a Y-borne copy of ATRY in American, as well as Australian marsupials, although it has diverged in sequence, as have other Y genes that are testis-specific in both eutherian and marsupial lineages.

Key words

ATRY comparative genomics marsupial sex chromosomes Y chromosome evolution 

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References

  1. Amrine-Madsen H, Scally M, Westerman M, Stanhope MJ, Krajewsky C, Springer M (2003) Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials. Mol Phylogenet Evol 28: 186–196.PubMedGoogle Scholar
  2. Charleswort B (1991) The evolution of sex chromosomes. Science 251: 1030–1033.Google Scholar
  3. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995.PubMedGoogle Scholar
  4. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16: 10881–10890.PubMedGoogle Scholar
  5. Delbridge ML, Harry JL, Toder R et al. (1997) A human candidate spermatogenesis gene, RBM1, is conserved and amplified on the marsupial Y chromosome. Nat Genet 15: 131–136.CrossRefPubMedGoogle Scholar
  6. Foster JW, Brennan FE, Hampikian GK et al. (1992) Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature 359: 531–533.CrossRefPubMedGoogle Scholar
  7. Graves JAM (1995) The origin and function of the mammalian Y chromosome and Y-borne genes — an evolving understanding. BioEssays 17: 311–320.CrossRefPubMedGoogle Scholar
  8. Graves JAM (2002a) The rise and fall of SRY. Trends Genet 18: 259–264.Google Scholar
  9. Graves JAM (2002b) Sex chromosomes and sex determination in weird animals. Cytogenet Genome Res 96: 161–168.Google Scholar
  10. Graves JAM, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18: 517–521.PubMedGoogle Scholar
  11. Gibbons RJ, Picketts DJ, Villard L, Higgs DR (1995) Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 80: 837–845.CrossRefPubMedGoogle Scholar
  12. Jegalian K, Page DC (1998) A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature 394: 776–780.PubMedGoogle Scholar
  13. Just W, Rau W, Akhverdian M et al. (1995) Sex determination in Ellobius lutescens and E. tancrei in the absence of the Y chromosome and the Sry gene. Nature Genet 11: 117–118.CrossRefPubMedGoogle Scholar
  14. Lichter P, Cremer T, Borden J, Manuelidis L, Ward D (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80: 224–234.CrossRefPubMedGoogle Scholar
  15. Merry DE, Pathak S, VandeBerg JL (1983) Differential NOR activities in somatic and germ cells of Monodelphis domestica (Marsupialia, Mammalia). Cytogenet Cell Genet 35: 244–251.PubMedGoogle Scholar
  16. Mitchell MJ, Woods DR, Wilcox SA, Graves JAM, Bishop CE (1992) Marsupial Y chromosome encodes a homologue of the mouse Y-linked candidate spermatogenesis gene Ube1y. Nature 359: 528–531.CrossRefPubMedGoogle Scholar
  17. Ohno S (1967) Sex Chromosomes and Sex Linked Genes. New York: Springer-Verlag.Google Scholar
  18. Park DJ, Pask AJ, Huynh K, Renfree MB, Harley VR, Marshall Graves JA (2004) Comparative analysis of ATRX, a chromatin remodeling protein. Gene 339: 39–48.CrossRefPubMedGoogle Scholar
  19. Pask A, Renfree MB, Graves JAM (2000) The human sex-reversing ATRX gene has a homologue on the marsupial Y chromosome, ATRY: implications for the evolution of mammalian sex determination. Proc Natl Acad Sci USA 97: 13198–13202.CrossRefPubMedGoogle Scholar
  20. Pearson WR, Wood T, Zhang Z, Miller W (1997) Comparison of DNA sequences with protein sequences. Genomics 46: 24–36.CrossRefPubMedGoogle Scholar
  21. Picketts DJ, Higgs DR, Bachoo S, Blake DJ, Quarrell OW, Gibbons RJ (1996) ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum Mol Genet 5: 1899–1907.CrossRefPubMedGoogle Scholar
  22. Rens W, O’Brien PC, Yang F et al. (2001) Karyotype relationships between distantly related marsupials from South America and Australia. Chromosome Res 9: 301–308.CrossRefPubMedGoogle Scholar
  23. Robinson ES, Samollow PB, VandeBerg JL, Johnston PG (1994) X-chromosome replication patterns in adult, newborn and prenatal opossums. Reprod Fertil Dev 6: 533–540.CrossRefPubMedGoogle Scholar
  24. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
  25. Shaver EL (1962) The chromosomes of the opossum, Didelphis virginiana. Can J Genet Cytol 4: 62–68.PubMedGoogle Scholar
  26. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ et al. (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825–837.CrossRefPubMedGoogle Scholar
  27. Svartman M, Vianna-Morgante AM (1999) Comparative genome analysis in American marsupials: chromosome banding and in-situ hybridization. Chromosome Res 7: 267–275.CrossRefPubMedGoogle Scholar
  28. Toder R, Wakefield M, Graves JAM (2000) The minimal mammalian Y chromosome—the marsupial Y as a model system. Cytogenet Cell Genet 91: 285–292.CrossRefPubMedGoogle Scholar
  29. Waters P, Duffy B, Frost CJ, Delbridge ML, Graves JAM (2001) The human Y chromosome derives largely from a single autosomal region added 80–130 million years ago. Cytogenet Cell Genet 92: 74–79.CrossRefPubMedGoogle Scholar
  30. Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28: 360–385.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Denise R. Carvalho-Silva
    • 1
    Email author
  • Rachel J. W. O’Neill
    • 2
  • Judith D. Brown
    • 2
  • Kim Huynh
    • 3
  • Paul D. Waters
    • 1
  • Andrew J. Pask
    • 3
  • Margaret L. Delbridge
    • 1
  • Jennifer A. Marshall Graves
    • 1
  1. 1.Research School of Biological ScienceAustralian National UniversityCanberraAustralia
  2. 2.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA
  3. 3.Department of ZoologyUniversity of MelbourneVictoriaAustralia

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