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

Marilyn B Renfree12*, Anthony T Papenfuss134*, Janine E Deakin15, James Lindsay6, Thomas Heider6, Katherine Belov17, Willem Rens8, Paul D Waters15, Elizabeth A Pharo2, Geoff Shaw12, Emily SW Wong17, Christophe M Lefèvre9, Kevin R Nicholas9, Yoko Kuroki10, Matthew J Wakefield13, Kyall R Zenger1117, Chenwei Wang17, Malcolm Ferguson-Smith8, Frank W Nicholas7, Danielle Hickford12, Hongshi Yu12, Kirsty R Short12, Hannah V Siddle17, Stephen R Frankenberg12, Keng Yih Chew12, Brandon R Menzies1132, Jessica M Stringer12, Shunsuke Suzuki12, Timothy A Hore114, Margaret L Delbridge15, Amir Mohammadi15, Nanette Y Schneider1152, Yanqiu Hu12, William O'Hara6, Shafagh Al Nadaf15, Chen Wu7, Zhi-Ping Feng163, Benjamin G Cocks17, Jianghui Wang17, Paul Flicek18, Stephen MJ Searle19, Susan Fairley19, Kathryn Beal18, Javier Herrero18, Dawn M Carone206, Yutaka Suzuki21, Sumio Sugano21, Atsushi Toyoda22, Yoshiyuki Sakaki10, Shinji Kondo10, Yuichiro Nishida10, Shoji Tatsumoto10, Ion Mandiou23, Arthur Hsu163, Kaighin A McColl3, Benjamin Lansdell3, George Weinstock24, Elizabeth Kuczek12526, Annette McGrath25, Peter Wilson25, Artem Men25, Mehlika Hazar-Rethinam25, Allison Hall25, John Davis25, David Wood25, Sarah Williams25, Yogi Sundaravadanam25, Donna M Muzny24, Shalini N Jhangiani24, Lora R Lewis24, Margaret B Morgan24, Geoffrey O Okwuonu24, San Juana Ruiz24, Jireh Santibanez24, Lynne Nazareth24, Andrew Cree24, Gerald Fowler24, Christie L Kovar24, Huyen H Dinh24, Vandita Joshi24, Chyn Jing24, Fremiet Lara24, Rebecca Thornton24, Lei Chen24, Jixin Deng24, Yue Liu24, Joshua Y Shen24, Xing-Zhi Song24, Janette Edson25, Carmen Troon25, Daniel Thomas25, Amber Stephens25, Lankesha Yapa25, Tanya Levchenko25, Richard A Gibbs24, Desmond W Cooper128, Terence P Speed13, Asao Fujiyama2227, Jennifer A M Graves15, Rachel J O'Neill6, Andrew J Pask126, Susan M Forrest125 and Kim C Worley24

Author Affiliations

1 The Australian Research Council Centre of Excellence in Kangaroo Genomics, Australia

2 Department of Zoology, The University of Melbourne, Melbourne, Victoria 3010, Australia

3 Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3052, Australia

4 Department of Mathematics and Statistics, The University of Melbourne, Melbourne, Victoria 3010, Australia

5 Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia

6 Department of Molecular and Cell Biology, Center for Applied Genetics and Technology, University of Connecticut, Storrs, CT 06269, USA

7 Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia

8 Department of Veterinary Medicine, University of Cambridge, Madingley Rd, Cambridge, CB3 0ES, UK

9 Institute for Technology Research and Innovation, Deakin University, Geelong, Victoria, 3214, Australia

10 RIKEN Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

11 School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia

12 Department of Microbiology and Immunology, The University of Melbourne, Melbourne, Victoria 3010, Australia

13 Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, Berlin 10315, Germany

14 Laboratory of Developmental Genetics and Imprinting, The Babraham Institute, Cambridge, CB22 3AT, UK

15 Department of Molecular Genetics, German Institute of Human Nutrition, Potsdam-Rehbruecke, Arthur-Scheunert-Allee 114-116, 14558 Nuthetal, Germany

16 Department of Medical Biology, The University of Melbourne, Melbourne, Victoria 3010, Australia

17 Biosciences Research Division, Department of Primary Industries, Victoria, 1 Park Drive, Bundoora 3083, Australia

18 European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SD, UK

19 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SD, UK

20 Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01655, USA

21 Graduate School of Frontier Sciences, The University of Tokyo, Chiba 277-8560, Japan

22 National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan

23 Department of Computer Science and Engineering, University of Connecticut, Storrs, CT 06269, USA

24 Human Genome Sequencing Center, Department of Molecular and Human Genetics Baylor College of Medicine, Houston, TX 77030, USA

25 Australian Genome Research Facility, Melbourne, Victoria, 3052 and the University of Queensland, St Lucia, Queensland 4072, Australia

26 Westmead Institute for Cancer Research, University of Sydney, Westmead, New South Wales 2145, Australia

27 National Institute of Informatics, 2-1-2 Hitotsubashi, Chiyoda-ku, Tokyo 101-8430, Japan

28 Department of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW 2052, Australia

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Genome Biology 2011, 12:R81  doi:10.1186/gb-2011-12-8-r81

Published: 19 August 2011

Abstract

Background

We 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.

Results

The 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.

Conclusions

Analyses 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.