Mammalian Genome

, Volume 8, Issue 6, pp 418–422

Comparative chromosome painting between two marsupials: origins of an XX/XY1Y2 sex chromosome system

  • Roland Toder
  • Rachel J. W. O’Neill
  • Johannes Wienberg
  • Patricia C. M. O’Brien
  • Lucille Voullaire
  • Jennifer A. Marshall-Graves
Original Contribution

Abstract

Cross-species chromosome painting was used to investigate genome rearrangements between tammar wallaby Macropus eugenii (2n = 16) and the swamp wallaby Wallabia bicolor (2n = 10♀/11♂), which diverged about 6 million years ago. The swamp wallaby has an XX female:XY1Y2 male sex chromosome system thought to have resulted from a fusion between an autosome and the small original X, not involving the Y. Thus, the small Y1 should represent the original Y and the large Y2 the original autosome. DNA paints were prepared from flow-sorted and micro-dissected chromosomes from the tammar wallaby. Painting swamp wallaby spreads with each tammar chromosome-specific probe gave extremely strong and clear signals in single-, two-, and three-color FISH. These showed that two tammar wallaby autosomes are represented unchanged in the swamp wallaby, two are represented by different centric fusions, and one by a tandem fusion to make the very long arms of swamp wallaby Chromosome (Chr) 1. The large swamp wallaby X comprises the tammar X as its short arm, and a tandemly fused 7 and 2 as the long arm. The acrocentric swamp wallaby Y2 is a 2/7 fusion, homologous with the long arm of the X. The small swamp wallaby Y1 is confirmed as the original Y by its painting with the tammar Y. However, the presence of sequences shared between the microdissected tammar Xp and Y on the swamp wallaby Y2 implies that the formation of the compound sex chromosomes involved addition of autosome(s) to both the original X and Y. We propose that this involved fusion with an ancient pseudoautosomal region followed by fission proximal to this shared region.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ferguson-Smith MA (1995) Gene order by FISH and FACS. In Molecular Biology and Biotechnology. A Comprehensive Desk Reference, R.A. Meyers (ed) (VCH Publishers, Inc.), pp 354–359Google Scholar
  2. Frönicke L, Chowdhary BP, Scherthan H, Gustavsson I (1996) A comparative map of the porcine and human genomes demonstrates ZOO-FISH and gene mapping-based chromosomal homologies. Mamm Genome 7, 285–290PubMedCrossRefGoogle Scholar
  3. Graves JAM, Watson JM (1991) Mammalian sex chromosomes: evolution of organization and function. Chromosoma 101, 63–68PubMedCrossRefGoogle Scholar
  4. Graves JAM, Cooper DW, McKenzie LM, Hope RM, Watson JM (1993) Genetic maps of marsupial and monotreme mammals. In Genetic Maps. Locus Maps of Complex Genomes, S.J. O’Brien (ed) (Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratories Press), pp. 4.282–4.289Google Scholar
  5. Hayman DL, Martin PG (1974) Mammalia I: Monotremata and Marsupialia. In Animal Cyotgenetics, 4 Chordata, B. John (ed) (Berlin, Stuttgart: Gebrüder Borntraeger), pp 000–000Google Scholar
  6. Köhler U, Arnold N, Wienberg J, Tofanelli S, Stanyon R (1995a) Genomic reorganization and disrupted chromosomal synteny in the siamang (Hy-lobates syndactylus) revealed by fluorescence in situ hybridization. Am J Phys Anthropol 97, 37–47CrossRefGoogle Scholar
  7. Köhler U, Bigoni F, Wienberg J, Stanyon R (1995b) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30, 287–292CrossRefGoogle Scholar
  8. Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80, 224–234PubMedCrossRefGoogle Scholar
  9. Meltzer PS, Guan XY, Burgess A, Trent JM (1992) Rapid generation of region specific probes by chromosome microdissection and their application. Nature Genet 1, 24–28PubMedCrossRefGoogle Scholar
  10. Nash WG, O'Brien SJ (1982) Conserved regions of homologous G-banded chromosomes between orders in mammalian evolution: carnivores and primates. Proc Natl Acad Sci USA 79, 6631–6635PubMedCrossRefGoogle Scholar
  11. O’Brien SJ, Seuánez HN, Womack JE (1988) Mammalian genome organization: an evolutionary view. Annu Rev Genet 22, 323–351PubMedCrossRefGoogle Scholar
  12. Raudsepp T, Frönicke L, Scherthan H, Gustavsson I, Chowdhary BP (1996). Zoo-FISH delineates conserved chromosomal segments in horse and man. Chromosome Res 4, 218–225PubMedCrossRefGoogle Scholar
  13. Rettenberger G, Klett C, Zechner U, Bruch J, Just W, Vogel W, Hameister H (1995a) ZOO-FISH analysis: cat and human karyotypes closely resemble the putative ancestral mammalian karyotype. Chromosome Res 3, 479–486PubMedCrossRefGoogle Scholar
  14. Rettenberger G, Klett C, Zechner U, Kunz J, Vogel W, Hameister H (1995b) Visualization of the conversation of synteny between humans and pigs by heterologous chromosomal painting. Genomics 26, 372–378PubMedCrossRefGoogle Scholar
  15. Rofe RH (1978) G-banded chromosomes and the evolution of Macropodidae. Aust Mammal 2, 53–63Google Scholar
  16. Scherthan H, Cremer T, Arnason U, Weier HU, Lima-de-Faria A, Frönicke L (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nature Genet 6, 342–347PubMedCrossRefGoogle Scholar
  17. Solinas-Toldo S, Lengauer C, Fries R (1995) Comparative genome map of human and cattle. Genomics 27, 489–496PubMedCrossRefGoogle Scholar
  18. Telenius H, Pelmear A, Tunnacliffe A, Carter NP, Behmel A, Ferguson-Smith MA, Nordenskjold M, Pfragner R, Ponder B (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flowsorted chromosomes. Genes Chromosomes Cancer 4, 257–263PubMedCrossRefGoogle Scholar
  19. Toder R, Zeitler S, Goodfellow PN, Schempp W (1993) Comparative mapping of SRY in the great apes. Chromosome Res 1, 117–120PubMedCrossRefGoogle Scholar
  20. Toder R, Rappold GA, Schiebel K, Schempp W (1995) ANT3 and STS are autosomal in prosimian lemurs; implications for the evolution of the pseudoautosomal region. Hum Genet 95, 22–28PubMedCrossRefGoogle Scholar
  21. Toder R, Wilcox SA, Smithwick M, Graves JAM (1996) The human-mouse imprinted genes IGF2, H19, SNRPN and ZNF127 map to two conserved autosomal clusters in a marsupial. Chromosome Res 4, 295–300PubMedCrossRefGoogle Scholar
  22. Toder R, Wienberg J, Voullaire L, Maccarone P, Graves JAM (1997) Shared DNA sequences between the X and Y Chromosome in the tammar Wallaby-evidence for independent additions to eutherian and marsupial sex chromosomes. Chromosoma (in press)Google Scholar
  23. Wienberg J, Stanyon R (1995) Chromosome painting in mammals as an approach to comparative genomics. Curr Opin Genet Dev 5, 792–797PubMedCrossRefGoogle Scholar
  24. Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215, 1525–1530PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1997

Authors and Affiliations

  • Roland Toder
    • 1
  • Rachel J. W. O’Neill
    • 1
  • Johannes Wienberg
    • 2
  • Patricia C. M. O’Brien
    • 2
  • Lucille Voullaire
    • 3
  • Jennifer A. Marshall-Graves
    • 1
  1. 1.School of Genetics and Human VariationLa Trobe University, Kingsbury DriveMelbourneAustralia
  2. 2.Department of PathologyCambridge UniversityCambridgeUK
  3. 3.The Murdoch InstituteRoyal Children’s HospitalMelbourneAustralia
  4. 4.Institute of Human Genetics and AnthropologyFreiburg i. Br.Germany

Personalised recommendations