Genome Analysis of the Platypus

Emily SW Wong, University of Sydney, New South Wale, Australia
Mette Lillie, University of Sydney, New South Wale, Australia
Katherine Belov, University of Sydney, New South Wale, Australia

Published online: April 2010

DOI: 10.1002/9780470015902.a0021554

The sequencing of the platypus genome represents a significant milestone in the study of mammalian evolution. The platypus is an egg-laying mammal, a member of the order Monotremata, the most divergent mammalian clade. It is the first monotreme to have its genome sequenced. Its unique evolutionary position, as an offshoot between the early divergence of birds and the later emergence of therian (eutherian and marsupials) mammals, provides an unrivalled opportunity to understand the evolution of all mammals. Much like the physical characteristics of the platypus, the platypus genome shows traces of an amalgamation of mammalian and reptilian traits. Key findings to emerge from the genome project include the complex evolution of mammalian sex chromosomes, the transition from egg-laying to live birth in mammals, and the evolution of immune genes and venom molecules in this unique species.

Key concepts:

  • The platypus genome is the first monotreme genome to be sequenced. The platypus's unique evolutionary position, as an offshoot between the early divergence of birds and the later emergence of therian (eutherian and marsupials) mammals, provides an opportunity to increase our understanding of the evolution of all mammals.
  • The platypus genome shows features of mammalian and reptilian traits.
  • The platypus has 10 sex chromosomes, some of which have homology to chicken Z. The mechanism used by platypuses to determine sex is not known.
  • The density of interspersed repeat elements in the platypus genome is greater than that seen in any other vertebrate genome.
  • The platypus genome contains a high G+C content (45.4%).
  • The platypus possesses a unique class of over 40 000 noncoding RNA known as snoRTE.
  • The platypus contains the largest repertoire of V1R vomeronasal receptors seen in any vertebrate.
  • The platypus genome contains the major egg yolk protein, vitellogenin.
  • Key mammalian milk genes, caseins, are present in the platypus.
  • The platypus genome contains an expansion of antimicrobial peptide genes.
  • Platypus venom molecules evolved independently to snake venom molecules.

Keywords: platypus; genome; mammals; evolution; monotreme

Figure 1. A phylogenetic tree of showing the divergence times of major clades during amniote evolution.
close
 References
    Armstrong JA, Gamble HJ and Goldby F (1953) Observations on the olfactory apparatus and the telencephalon of Anolis, a microsmatic lizard. Journal of Anatomy 87: 288–307.
    Babin PJ (2008) Conservation of a vitellogenin gene cluster in oviparous vertebrates and identification of its traces in the platypus genome. Gene 413: 76–82.
    Bininda-Emonds ORP, Cardillo M, Jones KE et al. (2007) The delayed rise of present-day mammals. Nature 446: 507–512.
    Birney E, Stamatoyannopoulos JA, Dutta A et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799–816.
    Borrelli L, De Stasio R, Filosa S et al. (2006) Evolutionary fate of duplicate genes encoding aspartic proteinases. Nothepsin case study. Gene 368: 101–109.
    Brawand D, Wahli W and Kaessmann H (2008) Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biology 6: e63.
    Daly KA, Digby MR, Lefévre C et al. (2008) Identification, characterization and expression of cathelicidin in the pouch young of tammar wallaby (Macropus eugenii). Comparative Biochemistry and Physiology–Part B: Biochemistry & Molecular Biology 149: 524–533.
    Dohm JC, Tsend-Ayush E, Reinhardt R, Grützner F and Himmelbauer H (2007) Disruption and pseudoautosomal localization of the major histocompatibility complex in monotremes. Genome Biology 8: R175.
    Elkin RG, Freed MB, Danetz SA and Bidwell CA (1995) Proteolysis of Japanese quail and chicken plasma apolipoprotein B and vitellogenin by cathepsin D: similarity of the resulting protein fragments with egg yolk polypeptides. Comparative Biochemistry and Physiology–Part B: Biochemistry & Molecular Biology 112: 191–196.
    El-Mogharbel N, Wakefield M, Deakin JE et al. (2007) DMRT gene cluster analysis in the platypus: new insights into genomic organization and regulatory regions. Genomics 89: 10–21.
    Gilbert N and Labuda D (2000) Evolutionary inventions and continuity of CORE-SINEs in mammals. Journal of Molecular Biology 298: 365–377.
    Goudet G, Mugnier S, Callebaut I and Monget P (2008) Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biology and Reproduction 78: 796–806.
    Grafodatskaya D, Rens W, Wallis MC et al. (2007) Search for the sex-determining switch in monotremes: mapping WT1, SF1, LHX1, LHX2, FGF9, WNT4, RSPO1 and GATA4 in platypus. Chromosome Research 15: 777–785.
    book Grant T (2007) Platypus. Collingwood, VIC: CSIRO Publishing.
    Grus WE, Shi P and Zhang J (2007) Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Molecular Biology and Evolution 24: 2153–2157.
    Grus WE, Shi P, Zhang Y and Zhang J (2005) Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proceedings of the National Academy of Sciences of the USA 102: 5767–5772.
    Keverne EB (1999) The vomeronasal organ. Science 286: 716–720.
    Kirby PJ, Greaves IK, Koina E, Waters PD and Marshall Graves JA (2007) Core-SINE blocks comprise a large fraction of monotreme genomes; implications for vertebrate chromosome evolution. Chromosome Research 15: 975–984.
    Kordis D, Lovsin N and Gubensek F (2006) Phylogenomic analysis of the L1 retrotransposons in deuterostomia. Systems Biology 55: 886–901.
    Luo Y and Li S (2007) Genome-wide analyses of retrogenes derived from the human box H/ACA snoRNAs. Nucleic Acids Research 35: 559–571.
    Mattick JS and Makunin IV (2006) Non-coding RNA. Human Molecular Genetics 15(Spec No 1): R17–R29.
    McMillan D, Miethke P, Alsop AE et al. (2007) Characterizing the chromosomes of the platypus (Ornithorhynchus anatinus). Chromosome Research 15: 961–974.
    Murchison EP, Kheradpour P, Sachidanandam R et al. (2008) Conservation of small RNA pathways in platypus. Genome Research 18: 995–1004.
    Ordoñez GR, Hillier LW, Warren WC et al. (2008) Loss of genes implicated in gastric function during platypus evolution. Genome Biology 9: R81.
    Pask AJ, Papenfuss AT, Ager EI et al. (2009) Analysis of the platypus genome suggests a transposon origin for mammalian imprinting. Genome Biology 10: R1.
    Potrzebowski L, Vinckenbosch N, Marques AC et al. (2008) Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biology 6: e80.
    Riggio M, Scudiero R, Filosa S and Parisi E (2000) Sex- and tissue-specific expression of aspartic proteinases in Danio rerio (zebrafish). Gene 260: 67–75.
    Schmitz J, Zemann A, Churakov G et al. (2008) Retroposed SNOfall: a mammalian-wide comparison of platypus snoRNAs. Genome Research 18: 1005–1010.
    Shao P, Yang J, Zhou H, Guan D and Qu L (2009) Genome-wide analysis of chicken snoRNAs provides unique implications for the evolution of vertebrate snoRNAs. BMC Genomics 10: 86.
    Shekar PC, Goel S, Rani SDS et al. (2006) Kappa-casein-deficient mice fail to lactate. Proceedings of the National Academy of Sciences of the USA 103: 8000–8005.
    Shi P and Zhang J (2007) Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Research 17: 166–174.
    Sinclair AH, Berta P, Palmer MS et al. (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346: 240–244.
    Smith CA, Roeszler KN, Ohnesorg T et al. (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461: 267–271.
    Smith J, Paton IR, Hughes DC and Burt DW (2005) Isolation and mapping the chicken zona pellucida genes: an insight into the evolution of orthologous genes in different species. Molecular Reproduction and Development 70: 133–145.
    Stevanovi M, Lovell-Badge R, Collignon J and Goodfellow PN (1993) SOX3 is an X-linked gene related to SRY. Human Molecular Genetics 2: 2013–2018.
    Torres AM, de Plater GM, Doverskog M et al. (2000) Defensin-like peptide-2 from platypus venom: member of a class of peptides with a distinct structural fold. Biochemical Journal 348(Pt 3): 649–656.
    Torres AM, Wang X, Fletcher JI et al. (1999) Solution structure of a defensin-like peptide from platypus venom. Biochemical Journal 341(Pt 3): 785–794.
    Tsend-Ayush E, Dodge N, Mohr J et al. (2009) Higher-order genome organization in platypus and chicken sperm and repositioning of sex chromosomes during mammalian evolution. Chromosoma 118: 53–69.
    book Tyndale-Biscoe CH and Renfree M (1987) Reproductive Physiology of Marsupials. Cambridge, UK: Cambridge University Press.
    Veyrunes F, Waters PD, Miethke P et al. (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Research 18: 965–973.
    Wallis MC, Waters PD and Graves JAM (2008) Sex determination in mammals: before and after the evolution of SRY. Cellular and Molecular Life Sciences 65: 3182–3195.
    Wallis MC, Waters PD, Delbridge ML et al. (2007) Sex determination in platypus and echidna: autosomal location of SOX3 confirms the absence of SRY from monotremes. Chromosome Research 15: 949–959.
    Warren WC, Hillier LW, Marshall Graves JA et al. (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453: 175–183.
    Weber MJ (2006) Mammalian small nucleolar RNAs are mobile genetic elements. PLoS Genetics 2: e205.
    Whittington C, Sharp J, Papenfuss A and Belov K (2009a) No evidence of expression of two classes of natural antibiotics (cathelicidins and defensins) in a sample of platypus milk. Australian Journal of Zoology 57: 211–217.
    Whittington CM, Koh JMS, Warren WC et al. (2009b) Understanding and utilising mammalian venom via a platypus venom transcriptome. Journal of Proteomics 72: 155–164.
    Whittington CM, Papenfuss AT, Bansal P et al. (2008) Defensins and the convergent evolution of platypus and reptile venom genes. Genome Research 18: 986–994.
    Wong ESW, Papenfuss A, Miller R and Belov K (2009a) Hatching time for monotreme immunology. Australian Journal of Zoology 57: 185–198.
    Wong ESW, Sanderson CE, Deakin JE et al. (2009b) Identification of natural killer cell receptor clusters in the platypus genome reveals an expansion of C-type lectin genes. Immunogenetics 61: 565–579.
 Further Reading
    Daish T and Grützner F (2009) Location, location, location! Monotremes provide unique insights into the evolution of sex chromosome silencing in mammals. DNA Cell Biology 28: 91–100.
    Deakin JE, Chaumeil J, Hore TA and Marshall Graves JA (2009) Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Research 17: 671–685.
    Deakin JE, Hore TA, Koina E and Marshall Graves JA (2008) The status of dosage compensation in the multiple X chromosomes of the platypus. PLoS Genetics 4: e1000140.
    O'Brien SJ (2008) The platypus genome unravelled. Cell 133: 953–955.
    Whittington C and Belov K (2007) Platypus venom: a review. Australian Mammalogy 29: 57–62.

Related Sub-Topics:

Evolutionary Genomics
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Genome Analysis of the Platypus
 
How to Cite close
Wong, Emily SW, Lillie, Mette, and Belov, Katherine(Apr 2010) Genome Analysis of the Platypus. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021554]