Skip to main content
Log in

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

  • Published:
Chromosome Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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.

    PubMed  CAS  Google Scholar 

  • Charleswort B (1991) The evolution of sex chromosomes. Science 251: 1030–1033.

    Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995.

    PubMed  CAS  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16: 10881–10890.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Graves JAM (1995) The origin and function of the mammalian Y chromosome and Y-borne genes — an evolving understanding. BioEssays 17: 311–320.

    Article  PubMed  CAS  Google Scholar 

  • Graves JAM (2002a) The rise and fall of SRY. Trends Genet 18: 259–264.

    CAS  Google Scholar 

  • Graves JAM (2002b) Sex chromosomes and sex determination in weird animals. Cytogenet Genome Res 96: 161–168.

    Google Scholar 

  • Graves JAM, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18: 517–521.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex Linked Genes. New York: Springer-Verlag.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pearson WR, Wood T, Zhang Z, Miller W (1997) Comparison of DNA sequences with protein sequences. Genomics 46: 24–36.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Shaver EL (1962) The chromosomes of the opossum, Didelphis virginiana. Can J Genet Cytol 4: 62–68.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Svartman M, Vianna-Morgante AM (1999) Comparative genome analysis in American marsupials: chromosome banding and in-situ hybridization. Chromosome Res 7: 267–275.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28: 360–385.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Denise R. Carvalho-Silva.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carvalho-Silva, D.R., O’Neill, R.J.W., Brown, J.D. et al. Molecular characterization and evolution of X and Y-borne ATRX homologues in American marsupials. Chromosome Res 12, 795–804 (2004). https://doi.org/10.1007/s10577-005-5376-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-005-5376-5

Key words

Navigation