Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development

BackgroundWe present the genome sequence of the tammar wallaby, Macropus eugenii, which is a member of the kangaroo family and the first representative of the iconic hopping mammals that symbolize Australia to be sequenced. The tammar has many unusual biological characteristics, including the longest period of embryonic diapause of any mammal, extremely synchronized seasonal breeding and prolonged and sophisticated lactation within a well-defined pouch. Like other marsupials, it gives birth to highly altricial young, and has a small number of very large chromosomes, making it a valuable model for genomics, reproduction and development.ResultsThe genome has been sequenced to 2 × coverage using Sanger sequencing, enhanced with additional next generation sequencing and the integration of extensive physical and linkage maps to build the genome assembly. We also sequenced the tammar transcriptome across many tissues and developmental time points. Our analyses of these data shed light on mammalian reproduction, development and genome evolution: there is innovation in reproductive and lactational genes, rapid evolution of germ cell genes, and incomplete, locus-specific X inactivation. We also observe novel retrotransposons and a highly rearranged major histocompatibility complex, with many class I genes located outside the complex. Novel microRNAs in the tammar HOX clusters uncover new potential mammalian HOX regulatory elements.ConclusionsAnalyses of these resources enhance our understanding of marsupial gene evolution, identify marsupial-specific conserved non-coding elements and critical genes across a range of biological systems, including reproduction, development and immunity, and provide new insight into marsupial and mammalian biology and genome evolution.

Yoshiyuki Sakaki | Sumio Sugano | Anthony T Papenfuss | Kathryn Beal | Terence P Speed | Katherine Belov | Paul Flicek | Chen Wu | Atsushi Toyoda | Asao Fujiyama | Susan Fairley | Annette McGrath | Vandita Joshi | Jireh Santibanez | Kim C Worley | Jixin Deng | Christie L Kovar | Richard A Gibbs | John Davis | Timothy A Hore | Zhi-Ping Feng | Willem Rens | Matthew J Wakefield | Yanqiu Hu | Andrew Cree | Benjamin Lansdell | George Weinstock | Javier Herrero | Yoko Kuroki | Donna M Muzny | Janette Edson | S. Searle | G. Weinstock | P. Flicek | R. Gibbs | T. Speed | Y. Sakaki | D. Muzny | M. Morgan | L. Nazareth | S. Jhangiani | G. Fowler | C. Kovar | A. Cree | H. Dinh | J. Santibanez | V. Joshi | R. O’Neill | K. Worley | S. Sugano | Yutaka Suzuki | L. Lewis | A. Fujiyama | A. Toyoda | Xing-zhi Song | Yue Liu | Kathryn Beal | Javier Herrero | S. Kondo | Geoffrey O. Okwuonu | S. Ruiz | M. Ferguson-Smith | F. Nicholas | Y. Kuroki | S. Fairley | Chyn Jing | F. Lara | Zhi-Ping Feng | A. Papenfuss | B. Cocks | M. Wakefield | A. McGrath | E. Kuczek | John Davis | K. Nicholas | G. Shaw | A. Pask | Hongshi Yu | M. Renfree | J. Edson | D. Carone | Emily S. Wong | B. Lansdell | K. R. Short | J. Deng | Amber Stephens | J. Deakin | James Lindsay | Thomas Heider | K. Belov | W. Rens | P. Waters | E. Pharo | C. Lefèvre | K. Zenger | Chenwei Wang | D. Hickford | H. Siddle | S. Frankenberg | K. Y. Chew | B. Menzies | J. Stringer | Shunsuke Suzuki | T. Hore | M. Delbridge | A. Mohammadi | Nanette Schneider | Yanqiu Hu | William O'Hara | Shafagh Al Nadaf | Chen Wu | Jianghui Wang | Yuichiro Nishida | Shoji Tatsumoto | Ion Mandiou | A. Hsu | K. McColl | Peter J. Wilson | A. Men | M. Hazar-Rethinam | Allison Hall | David L. A. Wood | Sarah Williams | Y. Sundaravadanam | R. Thornton | Lei Chen | J. Y. Shen | Carmen Troon | Daniela Thomas | L. Yapa | T. Levchenko | D. Cooper | Jennifer A M Graves | S. Forrest | Shinji Kondo | Yutaka Suzuki | Shunsuke Suzuki | Gerald Fowler | San Juana Ruiz | Sarah Williams | Mehlika Hazar-Rethinam | Marilyn B Renfree | Janine E Deakin | James Lindsay | Thomas Heider | Paul D Waters | Elizabeth A Pharo | Geoff Shaw | Emily SW Wong | Christophe M Lefèvre | Kevin R Nicholas | Kyall R Zenger | Chenwei Wang | Malcolm Ferguson-Smith | Frank W Nicholas | Danielle Hickford | Hongshi Yu | Kirsty R Short | Hannah V Siddle | Stephen R Frankenberg | Keng Yih Chew | Brandon R Menzies | Jessica M Stringer | Margaret L Delbridge | Amir Mohammadi | Nanette Y Schneider | William O'Hara | Shafagh Al Nadaf | Benjamin G Cocks | Jianghui Wang | Stephen MJ Searle | Dawn M Carone | Yuichiro Nishida | Shoji Tatsumoto | Ion Mandiou | Arthur Hsu | Kaighin A McColl | Elizabeth Kuczek | Peter Wilson | Artem Men | Allison Hall | David Wood | Yogi Sundaravadanam | Shalini N Jhangiani | Lora R Lewis | Margaret B Morgan | Geoffrey O Okwuonu | Lynne Nazareth | Huyen H Dinh | Chyn Jing | Fremiet Lara | Rebecca Thornton | Lei Chen | Yue Liu | Joshua Y Shen | Xing-Zhi Song | Carmen Troon | Daniel Thomas | Amber Stephens | Lankesha Yapa | Tanya Levchenko | Desmond W Cooper | Rachel J O'Neill | Andrew J Pask | Susan M Forrest | Dawn M. Carone | Amber E Stephens | Vandita Joshi | K. Chew | Jixin Deng | Kathryn M Beal | Rebecca L. Thornton | D. Muzny | Andrew Cree | Xing-Zhi Song

[1]  A. Clark,et al.  Human STELLAR, NANOG, and GDF3 Genes Are Expressed in Pluripotent Cells and Map to Chromosome 12p13, a Hotspot for Teratocarcinoma , 2004, Stem cells.

[2]  S. Schlafke Maternal Recognition of Pregnancy , 2022 .

[3]  B. Stonehouse,et al.  The biology of marsupials , 1977 .

[4]  Reproductive physiology of marsupials , 1987 .

[5]  B. Green,et al.  The Composition of Marsupial Milk , 1988 .

[6]  Sam Griffiths-Jones,et al.  The microRNA Registry , 2004, Nucleic Acids Res..

[7]  R. O’Neill,et al.  Marsupial Centomeres and Telomeres: Dynamic Chromosome Domains , 2010 .

[8]  J. Brosius,et al.  Tracking Marsupial Evolution Using Archaic Genomic Retroposon Insertions , 2010, PLoS biology.

[9]  Manolis Kellis,et al.  Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila , 2007, Cell.

[10]  J. Graves,et al.  The origin and evolution of the pseudoautosomal regions of human sex chromosomes. , 1998, Human molecular genetics.

[11]  J. Graves,et al.  Evolution of genomic imprinting: insights from marsupials and monotremes. , 2009, Annual review of genomics and human genetics.

[12]  J. Deakin,et al.  Part VIII: Marsupial genes and gene evolution: The Evolutionary History of Globin Genes: Insights from Marsupials and Monotremes , 2010 .

[13]  A. Papenfuss,et al.  Immunome database for marsupials and monotremes , 2011, BMC Immunology.

[14]  Zhao Xu,et al.  LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons , 2007, Nucleic Acids Res..

[15]  J. Graves DNA synthesis in chromosomes of cultured leucocytes from two marsupial species. , 1967, Experimental cell research.

[16]  M. Springer,et al.  A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes : Marsupialia) based on nuclear DNA sequences , 2008 .

[17]  Hong-Seog Park,et al.  Construction and Analysis of a Human-Chimpanzee Comparative Clone Map , 2002, Science.

[18]  N. Carter,et al.  Chromosome-specific paints from a high-resolution flow karyotype of the dog , 1996, Chromosome Research.

[19]  M. Ferguson-Smith,et al.  Reversal and convergence in marsupial chromosome evolution , 2004, Cytogenetic and Genome Research.

[20]  R. O’Neill,et al.  Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid , 1998, Nature.

[21]  P. Johnston,et al.  Sex-chromosome elimination in the bandicoot Isoodon macrourus using Y-linked markers , 1998, Cytogenetic and Genome Research.

[22]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[23]  R. Sachidanandam,et al.  An Epigenetic Role for Maternally Inherited piRNAs in Transposon Silencing , 2008, Science.

[24]  M. Springer,et al.  Intergeneric Relationships Among Macropodoidea (Metatheria: Diprotodontia) and The Chronicle of Kangaroo Evolution , 2000, Journal of Mammalian Evolution.

[25]  G. Wessel,et al.  Vasa genes: Emerging roles in the germ line and in multipotent cells , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[26]  György Abrusán,et al.  TEclass - a tool for automated classification of unknown eukaryotic transposable elements , 2009, Bioinform..

[27]  R A Gibbs,et al.  A "double adaptor" method for improved shotgun library construction. , 1996, Analytical biochemistry.

[28]  R. O’Neill,et al.  Recent Amplification of the Kangaroo Endogenous Retrovirus, KERV, Limited to the Centromere , 2011, Journal of Virology.

[29]  H. Tyndale-Biscoe Life of marsupials , 1973 .

[30]  G. Shaw,et al.  Kallmann Syndrome 1 Gene Is Expressed in the Marsupial Gonad1 , 2011, Biology of reproduction.

[31]  M. Ferguson-Smith,et al.  Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation , 2010, Proceedings of the National Academy of Sciences.

[32]  K. Nicholas,et al.  Evolution of lactation: ancient origin and extreme adaptations of the lactation system. , 2010, Annual review of genomics and human genetics.

[33]  J. Harrow,et al.  MHC-linked and un-linked class I genes in the wallaby , 2009, BMC Genomics.

[34]  L. Holm,et al.  The Pfam protein families database , 2005, Nucleic Acids Res..

[35]  Y Sakaki,et al.  The DNA sequence of human chromosome 21. , 2000, Nature.

[36]  Anthony K. Lee,et al.  Evolutionary Ecology of Marsupials , 1985 .

[37]  J. Graves,et al.  ATRX has a critical and conserved role in mammalian sexual differentiation , 2011, BMC Developmental Biology.

[38]  G. Karpen,et al.  Epigenetic regulation of centromeric chromatin: old dogs, new tricks? , 2008, Nature Reviews Genetics.

[39]  J. Graves,et al.  Chromosome evolution in kangaroos (Marsupialia: Macropodidae): cross species chromosome painting between the tammar wallaby and rock wallaby spp. with the 2n = 22 ancestral macropodid karyotype. , 1999, Genome.

[40]  Fengtang Yang,et al.  Karyotype Relationships Between Four Distantly Related Marsupials Revealed by Reciprocal Chromosome Painting , 2004, Chromosome Research.

[41]  O. Oftedal The Mammary Gland and Its Origin During Synapsid Evolution , 2002, Journal of Mammary Gland Biology and Neoplasia.

[42]  Janine E. Deakin,et al.  The Evolution of Epigenetic Regulators CTCF and BORIS/CTCFL in Amniotes , 2008, PLoS genetics.

[43]  P. Chardon,et al.  Ruminants genome no longer contains Whey Acidic Protein gene but only a pseudogene. , 2006, Gene.

[44]  Stijn van Dongen,et al.  miRBase: microRNA sequences, targets and gene nomenclature , 2005, Nucleic Acids Res..

[45]  K. Gräf,et al.  Hormonal control of sexual development. , 1974, Advances in the biosciences.

[46]  Gary H. Karpen,et al.  Determining centromere identity: cyclical stories and forking paths , 2001, Nature Reviews Genetics.

[47]  M. Hattori,et al.  The DNA sequence of human chromosome 21 , 2000, Nature.

[48]  K. Nicholas,et al.  Lactation transcriptomics in the Australian marsupial, Macropus eugenii: transcript sequencing and quantification , 2007, BMC Genomics.

[49]  J. Graves,et al.  Class I genes have split from the MHC in the tammar wallaby , 2007, Cytogenetic and Genome Research.

[50]  Eric B. Keverne,et al.  Epigenetics, brain evolution and behaviour , 2008, Frontiers in Neuroendocrinology.

[51]  R. O’Neill,et al.  A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres , 2009, Chromosoma.

[52]  Jonathan Perreault,et al.  RTAnalyzer: a web application for finding new retrotransposons and detecting L1 retrotransposition signatures , 2007, Nucleic Acids Res..

[53]  Sumio Sugano,et al.  Construction of a full-length enriched and a 5'-end enriched cDNA library using the oligo-capping method. , 2003, Methods in molecular biology.

[54]  J. Graves,et al.  The Olfactory Receptor Gene Family of Marsupials , 2010 .

[55]  H. Hameister,et al.  Evolution of the human X – a smart and sexy chromosome that controls speciation and development , 2003, Cytogenetic and Genome Research.

[56]  R. Kingston,et al.  HOTAIR Lifts Noncoding RNAs to New Levels , 2007, Cell.

[57]  J. Graves,et al.  Sex Chromosome Specialization and Degeneration in Mammals , 2006, Cell.

[58]  S. Pathak,et al.  A high-resolution banding pattern idiogram of Monodelphis domestica chromosomes (Marsupialia, Mammalia). , 1993, Cytogenetics and cell genetics.

[59]  F. Zhou,et al.  MUST: a system for identification of miniature inverted-repeat transposable elements and applications to Anabaena variabilis and Haloquadratum walsbyi. , 2009, Gene.

[60]  B. Trask,et al.  Quantification of the DNA content of structurally abnormal X chromosomes and X chromosome aneuploidy using high resolution bivariate flow karyotyping. , 1990, Cytometry.

[61]  J. Graves The origin and function of the mammalian Y chromosome and Y‐borne genes – an evolving understanding , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[62]  J. Deakin,et al.  Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic , 2010, Genome Biology.

[63]  Howard Y. Chang,et al.  Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis , 2010, Nature.

[64]  Ana Kozomara,et al.  miRBase: integrating microRNA annotation and deep-sequencing data , 2010, Nucleic Acids Res..

[65]  Zhe‐Xi Luo,et al.  An Early Cretaceous Tribosphenic Mammal and Metatherian Evolution , 2003, Science.

[66]  Harjinder Singh,et al.  Milk proteins : from expression to food , 2009 .

[67]  M. Wakefield,et al.  The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals , 2007, Chromosome Research.

[68]  C. Tyndale-Biscoe,et al.  The Developing Marsupial: Models for Biomedical Research , 1988 .

[69]  G. Shaw,et al.  Identification of two distinct genes at the vertebrate TRPC2 locus and their characterisation in a marsupial and a monotreme , 2011, BMC Molecular Biology.

[70]  M. Ichikawa,et al.  Morphological evidence for two types of Mammalian vomeronasal system. , 2004, Chemical senses.

[71]  Y. Kohara,et al.  Retrotransposon Silencing by DNA Methylation Can Drive Mammalian Genomic Imprinting , 2007, PLoS genetics.

[72]  R. O’Neill,et al.  Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages , 2007, Genome Biology.

[73]  K. Dziegielewska,et al.  Postnatal development of the telencephalon of the tammar wallaby (Macropus eugenii) , 2004, Anatomy and Embryology.

[74]  Roles and regulation , 2006, Veterinary Record.

[75]  G. Shaw,et al.  The olfactory system of the tammar wallaby is developed at birth and directs the neonate to its mother's pouch odours. , 2009, Reproduction.

[76]  R. Behringer,et al.  Hoxd13 expression in the developing limbs of the short‐tailed fruit bat, Carollia perspicillata , 2005, Evolution & development.

[77]  G. Shaw,et al.  The marsupial male: a role model for sexual development. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[78]  A. J. Hulbert,et al.  Developmental profile of thyroid hormone distributor proteins in a marsupial, the tammar wallaby Macropus eugenii. , 2002, General and comparative endocrinology.

[79]  Eun-Joon Lee,et al.  Exceptional conservation of horse-human gene order on X chromosome revealed by high-resolution radiation hybrid mapping. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[80]  J. Deakin,et al.  Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby) , 2005, Chromosome Research.

[81]  Howard Y. Chang,et al.  Long Noncoding RNA as Modular Scaffold of Histone Modification Complexes , 2010, Science.

[82]  A. Pask,et al.  Molecular Regulation of Marsupial Reproduction and Development , 2010 .

[83]  Eugene W. Myers,et al.  The greedy path-merging algorithm for contig scaffolding , 2002, JACM.

[84]  G. Weinstock,et al.  The Atlas genome assembly system. , 2004, Genome research.

[85]  P. G. Martin,et al.  Sex chromosome mosaicism in the marsupial genera Isoodon and Perameles. , 1965, Genetics.

[86]  J. Graves,et al.  Physical mapping of the elephant X chromosome: conservation of gene order over 105 million years , 2009, Chromosome Research.

[87]  K. Caldecott XRCC1 and DNA strand break repair. , 2003, DNA repair.

[88]  G. Shaw,et al.  Early onset of ghrelin production in a marsupial , 2009, Molecular and Cellular Endocrinology.

[89]  Kenji Nakamura,et al.  Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta , 2008, Nature Genetics.

[90]  J. Wienberg,et al.  Shared DNA sequences between the X and Y chromosomes in the tammar wallaby – evidence for independent additions to eutherian and marsupial sex chromosomes , 1997, Chromosoma.

[91]  J. Graves,et al.  Chromosome Painting in Marsupials: Genome Conservation in the Kangaroo Family , 2004, Chromosome Research.

[92]  C. Gilbert,et al.  Evolution from XIST-Independent to XIST-Controlled X-Chromosome Inactivation: Epigenetic Modifications in Distantly Related Mammals , 2011, PloS one.

[93]  R. O’Neill,et al.  Enhancing genome assemblies by integrating non-sequence based data , 2011, BMC proceedings.

[94]  G. Shaw,et al.  The vomeronasal organ of the tammar wallaby , 2008, Journal of anatomy.

[95]  R. O’Neill,et al.  Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids , 2001, Mammalian Genome.

[96]  J. Graves,et al.  Bmc Evolutionary Biology the Evolution of Imprinting: Chromosomal Mapping of Orthologues of Mammalian Imprinted Domains in Monotreme and Marsupial Mammals , 2007 .

[97]  S. Salzberg,et al.  Hierarchical scaffolding with Bambus. , 2003, Genome research.

[98]  M. Renfree,et al.  The tammar wallaby, Macropus eugenii: a model kangaroo for the study of developmental and reproductive biology. , 2009, Cold Spring Harbor protocols.

[99]  B. Green,et al.  Qualitative and Quantitative Changes in Milk Fat during Lactation in the Tammar Wallaby (Macro pus eugenii) , 1983 .

[100]  A. Pask,et al.  The human sex-reversing ATRX gene has a homologue on the marsupial Y chromosome, ATRY: implications for the evolution of mammalian sex determination. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[101]  L. Matthews,et al.  Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians , 2008, Nature Genetics.

[102]  Hugh S Taylor,et al.  HOXA11 silencing and endogenous HOXA11 antisense ribonucleic acid in the uterine endometrium. , 2002, The Journal of clinical endocrinology and metabolism.

[103]  D. Hartl,et al.  Evidence for maternally transmitted small interfering RNA in the repression of transposition in Drosophila virilis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[104]  P. Lowry,et al.  Hybrids in Marsupial Research , 1989 .

[105]  M. Shen Nodal signaling: developmental roles and regulation , 2007, Development.

[106]  G. Shaw,et al.  Characterisation of marsupial PHLDA2 reveals eutherian specific acquisition of imprinting , 2011, BMC Evolutionary Biology.

[107]  Gregory Butler,et al.  OrfPredictor: predicting protein-coding regions in EST-derived sequences , 2005, Nucleic Acids Res..

[108]  L. K. Schneider 2 – Marsupial Chromosomes, Cell Cycles, and Cytogenetics , 1977 .

[109]  M. Renfree Maternal recognition of pregnancy in marsupials. , 2000, Reviews of reproduction.

[110]  S. Ranganathan,et al.  The Gene for a Novel Member of the Whey Acidic Protein Family Encodes Three Four-disulfide Core Domains and Is Asynchronously Expressed during Lactation* , 2000, The Journal of Biological Chemistry.

[111]  D. Haussler,et al.  Human-mouse alignments with BLASTZ. , 2003, Genome research.

[112]  M. Surani,et al.  Normal Germ Line Establishment in Mice Carrying a Deletion of the Ifitm/Fragilis Gene Family Cluster , 2008, Molecular and Cellular Biology.

[113]  M. Molloy,et al.  A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii). , 2009, Developmental and comparative immunology.

[114]  S. Batzoglou,et al.  Whole-Genome Sequencing and Assembly with High-Throughput, Short-Read Technologies , 2007, PloS one.

[115]  M. Gerstein,et al.  Annotating non-coding regions of the genome , 2010, Nature Reviews Genetics.

[116]  Laurent Duret,et al.  The Xist RNA Gene Evolved in Eutherians by Pseudogenization of a Protein-Coding Gene , 2006, Science.

[117]  J. Graves,et al.  The Evolution of Genomic Imprinting – A Marsupial Perspective , 2010 .

[118]  A. Pingoud,et al.  Validation of an algorithm for automatic quantification of nucleic acid copy numbers by real-time polymerase chain reaction. , 2003, Analytical biochemistry.

[119]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[120]  M. Renfree Endocrinology of Pregnancy, Parturition and Lactation in Marsupials , 1994 .

[121]  J. Graves,et al.  Karyotype relationships between distantly related marsupials from South America and Australia , 2004, Chromosome Research.

[122]  Y. Matsui,et al.  Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells , 2002, Mechanisms of Development.

[123]  Robert S. Harris,et al.  Improved pairwise alignment of genomic dna , 2007 .

[124]  K. Nicholas,et al.  Characterization of the tammar wallaby (Macropus eugenii) whey acidic protein gene; new insights into the function of the protein , 2009, Evolution & development.

[125]  B. Cocks,et al.  Ancient Antimicrobial Peptides Kill Antibiotic-Resistant Pathogens: Australian Mammals Provide New Options , 2011, PloS one.

[126]  M. Wakefield,et al.  Physical map of two tammar wallaby chromosomes: A strategy for mapping in non-model mammals , 2008, Chromosome Research.

[127]  G. Hannon,et al.  The Piwi-piRNA Pathway Provides an Adaptive Defense in the Transposon Arms Race , 2007, Science.

[128]  H. Niwa,et al.  Platypus Pou5f1 reveals the first steps in the evolution of trophectoderm differentiation and pluripotency in mammals , 2008, Evolution & development.

[129]  D R Bentley,et al.  The DNA sequence and comparative analysis of human chromosome 20 , 2004, Nature.

[130]  Denis Duboule,et al.  The role of Hox genes during vertebrate limb development. , 2007, Current opinion in genetics & development.

[131]  P. Waters,et al.  Mammalian sex--Origin and evolution of the Y chromosome and SRY. , 2007, Seminars in cell & developmental biology.

[132]  P. Tam,et al.  IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. , 2005, Developmental cell.

[133]  D. Hayman,et al.  G-banding evidence for a conserved complement in the Marsupialia. , 1985, Cytogenetics and cell genetics.

[134]  J. Graves,et al.  Recent Assembly of an Imprinted Domain from Non-Imprinted Components , 2006, PLoS genetics.

[135]  François Chevenet,et al.  OligoHeatMap (OHM): an online tool to estimate and display hybridizations of oligonucleotides onto DNA sequences , 2008, Nucleic Acids Res..

[136]  G. Church,et al.  Computational and experimental identification of C. elegans microRNAs. , 2003, Molecular cell.

[137]  Y. Sakaki,et al.  Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes , 2008, Nature.

[138]  F. Nicholas,et al.  A first-generation integrated tammar wallaby map and its use in creating a tammar wallaby first-generation virtual genome map , 2011, BMC Genomics.

[139]  David Haig,et al.  Sex-Specific Parent-of-Origin Allelic Expression in the Mouse Brain , 2010, Science.

[140]  K. Nicholas,et al.  Tammar wallaby mammary cathelicidins are differentially expressed during lactation and exhibit antimicrobial and cell proliferative activity. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[141]  G. Shaw,et al.  Exon 3 of the growth hormone receptor (GH-R) is specific to eutherian mammals , 2008, Molecular and Cellular Endocrinology.

[142]  A. Pask,et al.  Fibroblast Growth Factor-9 in Marsupial Testicular Development , 2011, Sexual Development.

[143]  F. Nicholas,et al.  A second-generation anchored genetic linkage map of the tammar wallaby (Macropus eugenii) , 2011, BMC Genetics.

[144]  J. Graves,et al.  X-inactivation in marsupials and monotremes , 1993 .

[145]  K. Nicholas,et al.  The Tammar Wallaby: A Model to Study Putative Autocrine-Induced Changes in Milk Composition , 1997, Journal of Mammary Gland Biology and Neoplasia.

[146]  E. Lander,et al.  Genomic mapping by fingerprinting random clones: a mathematical analysis. , 1988, Genomics.

[147]  J. N. Baker,et al.  Voyage to Disaster , 2000 .

[148]  A. Fujiyama,et al.  Identification of tammar wallaby SIRH12, derived from a marsupial-specific retrotransposition event , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[149]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[150]  E. Birney,et al.  Velvet: algorithms for de novo short read assembly using de Bruijn graphs. , 2008, Genome research.

[151]  D. A. O’Brien,et al.  A-kinase anchoring protein 4 has a conserved role in mammalian spermatogenesis. , 2009, Reproduction.

[152]  A. Taylor,et al.  The DNA sequence and comparative analysis of human chromosome 10 , 2004, Nature.

[153]  J. Aten,et al.  Bivariate flow karyotyping of human chromosomes: evaluation of variation in Hoechst 33258 fluorescence, chromomycin A3 fluorescence, and relative chromosomal DNA content. , 1991, Cytometry.

[154]  K. Nicholas,et al.  Marsupial Milk – Identifying Signals for Regulating Mammary Function and Development of the Young , 2010 .

[155]  R. O’Neill,et al.  A human candidate spermatogenesis gene, RBM1, is conserved and amplified on the marsupial Y chromosome , 1997, Nature Genetics.

[156]  G. Shaw,et al.  Sexual differentiation of the urogenital system of the fetal and neonatal tammar wallaby, Macropus eugenii , 1996, Anatomy and Embryology.

[157]  E. Mardis,et al.  Transcriptome-Wide Identification of Novel Imprinted Genes in Neonatal Mouse Brain , 2008, PloS one.

[158]  A. Pask,et al.  Sex determining genes and sexual differentiation in a marsupial. , 2001, The Journal of experimental zoology.

[159]  J. Turner,et al.  Key Features of the X Inactivation Process Are Conserved between Marsupials and Eutherians , 2009, Current Biology.

[160]  C. Ponting,et al.  Transcriptomic analysis supports similar functional roles for the two thymuses of the tammar wallaby , 2011, BMC Genomics.

[161]  M. Surani,et al.  A molecular programme for the specification of germ cell fate in mice , 2002, Nature.

[162]  M. Renfree,et al.  Review: Marsupials: placental mammals with a difference. , 2010, Placenta.

[163]  M. Surani,et al.  stella Is a Maternal Effect Gene Required for Normal Early Development in Mice , 2003, Current Biology.

[164]  K. Kinzler,et al.  The Xist RNA Gene Evolved in Eutherians by Pseudogenization of a Protein-Coding Gene , 2006 .

[165]  L. Selwood Development of early cell lineages in marsupial embryos: an overview. , 1994, Reproduction, fertility, and development.

[166]  Jennifer Harrow,et al.  The tammar wallaby major histocompatibility complex shows evidence of past genomic instability , 2011, BMC Genomics.

[167]  A. E. Sippel,et al.  Characterization and cloning of the mRNAs specific for the lactating mouse mammary gland. , 1982, European journal of biochemistry.

[168]  Toshiaki Watanabe,et al.  Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. , 2006, Genes & development.

[169]  G. Shaw,et al.  Differential roles of TGIF family genes in mammalian reproduction , 2011, BMC Developmental Biology.

[170]  Stijn van Dongen,et al.  miRBase: tools for microRNA genomics , 2007, Nucleic Acids Res..

[171]  K. Nicholas Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus eugenii). , 1988, Biochemical and biophysical research communications.

[172]  G. Grigg,et al.  Kangaroos, wallabies and rat-kangaroos , 1989 .

[173]  J. Graves,et al.  Marsupial genetics and genomics. , 2002, Trends in genetics : TIG.

[174]  Howard Y. Chang,et al.  Functional Demarcation of Active and Silent Chromatin Domains in Human HOX Loci by Noncoding RNAs , 2007, Cell.

[175]  W. Thatcher,et al.  Maternal recognition of pregnancy. , 2019, Journal of reproduction and fertility. Supplement.

[176]  Bronwen L. Aken,et al.  Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences , 2007, Nature.

[177]  A. Brennan,et al.  The comparative genomics of tammar wallaby and Cape fur seal lactation models to examine function of milk proteins , 2009 .

[178]  K. Nicholas,et al.  Cross-fostering of the tammar wallaby (Macropus eugenii) pouch young accelerates fore-stomach maturation , 2009, Mechanisms of Development.

[179]  B. Green,et al.  Qualitative and quantitative changes in milk fat during lactation in the tammar wallaby (Macropus eugenii). , 1983, Australian journal of biological sciences.

[180]  John F. McDonald,et al.  LTR_STRUC: a novel search and identification program for LTR retrotransposons , 2003, Bioinform..

[181]  L. Matthews,et al.  The Evolution of the DLK1-DIO3 Imprinted Domain in Mammals , 2008, PLoS biology.

[182]  G. Shaw,et al.  DDX4 (VASA) Is Conserved in Germ Cell Development in Marsupials and Monotremes1 , 2011, Biology of reproduction.

[183]  M. Renfree,et al.  The marsupial placenta: a phylogenetic analysis. , 2003, Journal of experimental zoology. Part A, Comparative experimental biology.

[184]  Clifford A. Meyer,et al.  Model-based Analysis of ChIP-Seq (MACS) , 2008, Genome Biology.

[185]  M. Scott,et al.  Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. , 1996, Genes & development.

[186]  C. Tabin,et al.  Analysis of Hox gene expression in the chick limb bud. , 1996, Development.

[187]  A. Pask,et al.  The evolution of class V POU domain transcription factors in vertebrates and their characterisation in a marsupial. , 2010, Developmental biology.

[188]  C. Tyndale-Biscoe,et al.  The Developing Marsupial , 1988, Springer Berlin Heidelberg.

[189]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.