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

ABSTRACT: 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.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.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.

SUBMITTER: Renfree MB

PROVIDER: S-EPMC3277949 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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

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

Genome biology 20110829 8

<h4>Background</h4>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 b ...[more]

PMID: 21854559

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Project description:BackgroundThe tammar wallaby, Macropus eugenii, a small kangaroo used for decades for studies of reproduction and metabolism, is the model Australian marsupial for genome sequencing and genetic investigations. The production of a more comprehensive cytogenetically-anchored genetic linkage map will significantly contribute to the deciphering of the tammar wallaby genome. It has great value as a resource to identify novel genes and for comparative studies, and is vital for the ongoing genome sequence assembly and gene ordering in this species.ResultsA second-generation anchored tammar wallaby genetic linkage map has been constructed based on a total of 148 loci. The linkage map contains the original 64 loci included in the first-generation map, plus an additional 84 microsatellite loci that were chosen specifically to increase coverage and assist with the anchoring and orientation of linkage groups to chromosomes. These additional loci were derived from (a) sequenced BAC clones that had been previously mapped to tammar wallaby chromosomes by fluorescence in situ hybridization (FISH), (b) End sequence from BACs subsequently FISH-mapped to tammar wallaby chromosomes, and (c) tammar wallaby genes orthologous to opossum genes predicted to fill gaps in the tammar wallaby linkage map as well as three X-linked markers from a published study. Based on these 148 loci, eight linkage groups were formed. These linkage groups were assigned (via FISH-mapped markers) to all seven autosomes and the X chromosome. The sex-pooled map size is 1402.4 cM, which is estimated to provide 82.6% total coverage of the genome, with an average interval distance of 10.9 cM between adjacent markers. The overall ratio of female/male map length is 0.84, which is comparable to the ratio of 0.78 obtained for the first-generation map.ConclusionsConstruction of this second-generation genetic linkage map is a significant step towards complete coverage of the tammar wallaby genome and considerably extends that of the first-generation map. It will be a valuable resource for ongoing tammar wallaby genetic research and assembling the genome sequence. The sex-pooled map is available online at http://compldb.angis.org.au/.

Project description:BACKGROUND:Kangaroos and wallabies have specialised limbs that allow for their hopping mode of locomotion. The hindlimbs differentiate much later in development but become much larger than the forelimbs. The hindlimb autopod has only four digits, the fourth of which is greatly elongated, while digits two and three are syndactylous. We investigated the expression of two genes, HOXA13 and HOXD13, that are crucial for digit patterning in mice during formation of the limbs of the tammar wallaby. RESULTS:We describe the development of the tammar limbs at key stages before birth. There was marked heterochrony and the hindlimb developed more slowly than the forelimb. Both tammar HOXA13 and HOXD13 have two exons as in humans, mice and chickens. HOXA13 had an early and distal mRNA distribution in the tammar limb bud as in the mouse, but forelimb expression preceded that in the hindlimb. HOXD13 mRNA was expressed earlier in the forelimb than the hindlimb and was predominantly detected in the interdigital tissues of the forelimb. In contrast, the hindlimb had a more restricted expression pattern that appeared to be expressed at discrete points at both posterior and anterior margins of the limb bud, and was unlike expression seen in the mouse and the chicken. CONCLUSIONS:This is the first examination of HOXA and HOXD gene expression in a marsupial. The gene structure and predicted proteins were highly conserved with their eutherian orthologues. Interestingly, despite the morphological differences in hindlimb patterning, there were no modifications to the polyalanine tract of either HOXA13 or HOXD13 when compared to those of the mouse and bat but there was a marked difference between the tammar and the other mammals in the region of the first polyserine tract of HOXD13. There were also altered expression domains for both genes in the developing tammar limbs compared to the chicken and mouse. Together these findings suggest that the timing of HOX gene expression may contribute to the heterochrony of the forelimb and hindlimb and that alteration to HOX domains may influence phenotypic differences that lead to the development of marsupial syndactylous digits.

Dataset Information

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

Publications

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

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