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

M. B. Renfree, Anthony Papenfuss, Janine DEAKIN, James Lindsay, Thomas Heider, Katherine Belov, Willem Rens, Paul Waters, Elizabeth Pharo, Geoff Shaw, Emily Wong, Christophe Lefevre, Kevin R. Nicholas, Yoko Kuroki, Matthew Wakefield, Kyall Zenger, Chenwei Wang, Malcolm Ferguson-Smith, Frank Nicholas, Danielle Hickford & 83 others Hongshi Yu, Kirsty R. Short, Hannah Siddle, Stephen Frankenberg, Keng Chew, Brandon Menzies, Jessica Stringer, Shunsuke Suzuki, Timothy Hore, Margaret L. Delbridge, Amir Mohammadi, Nanette Schneider, Yanqiu Hu, William O'Hara, Shafagh Nadaf, Chen Wu, Zhi-Ping Feng, Benjamin Cocks, Jianghui Wang, Paul Flicek, Stephen Searle, Susan Fairley, Kathryn Beal, Javier Herrero, Dawn Carone, Yutaka Suzuki, Sumio Sugano, Atsushi Toyoda, Yoshiyuki Sakaki, Shinji Kondo, Yuichiro Nishida, Shoji Tatsumoto, Ion Mandiou, Arthur Hsu, Kaighin McColl, Benjamin Lansdell, George Weinstock, Elizabeth Kuczek, Annette McGrath, Peter Wilson, Artem Men, Mehlika Hazar-Rethinam, Allison Hall, John Davis, David Wood, Sarah Williams, Yogi Sundaravadanam, Donna Muzny, Shalini Jhangiani, Lora Lewis, Margaret Morgan, Geoffrey Okwuonu, San Ruiz, Jireh Santibanez, Lynne Nazareth, Andrew Cree, Gerald Fowler, Christie Kovar, Huyen Dinh, Vandita Joshi, Chyn Jing, Fremiet Lara, Rebecca Thornton, Lei Chen, Jixin Deng, Yue Liu, Joshua Shen, Xing-Zhi Song, Janette Edson, Carmen Troon, Daniel Thomas, Amber Stephens, Lankesha Yapa, Tanya Levchenko, Richard A. Gibbs, Desmond Cooper, Terence Speed, Asao Fujiyama, Jennifer A Marshall Graves, Rachel O’Neill, Andrew Pask, Susan Forrest, Kim Worley

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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.
Original languageEnglish
Pages (from-to)1-25
Number of pages25
JournalGenome Biology
Volume12:R81
DOIs
Publication statusPublished - 2011
Externally publishedYes

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Macropus eugenii
Macropodidae
Marsupialia
marsupial
Reproduction
Metatheria
genome
Genome
gene
genes
Genes
Mammals
mammal
mammals
MHC Class I Genes
genome assembly
major histocompatibility complex
X Chromosome Inactivation
Retroelements
germ cell

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Renfree, M. B. ; Papenfuss, Anthony ; DEAKIN, Janine ; Lindsay, James ; Heider, Thomas ; Belov, Katherine ; Rens, Willem ; Waters, Paul ; Pharo, Elizabeth ; Shaw, Geoff ; Wong, Emily ; Lefevre, Christophe ; Nicholas, Kevin R. ; Kuroki, Yoko ; Wakefield, Matthew ; Zenger, Kyall ; Wang, Chenwei ; Ferguson-Smith, Malcolm ; Nicholas, Frank ; Hickford, Danielle ; Yu, Hongshi ; Short, Kirsty R. ; Siddle, Hannah ; Frankenberg, Stephen ; Chew, Keng ; Menzies, Brandon ; Stringer, Jessica ; Suzuki, Shunsuke ; Hore, Timothy ; Delbridge, Margaret L. ; Mohammadi, Amir ; Schneider, Nanette ; Hu, Yanqiu ; O'Hara, William ; Nadaf, Shafagh ; Wu, Chen ; Feng, Zhi-Ping ; Cocks, Benjamin ; Wang, Jianghui ; Flicek, Paul ; Searle, Stephen ; Fairley, Susan ; Beal, Kathryn ; Herrero, Javier ; Carone, Dawn ; Suzuki, Yutaka ; Sugano, Sumio ; Toyoda, Atsushi ; Sakaki, Yoshiyuki ; Kondo, Shinji ; Nishida, Yuichiro ; Tatsumoto, Shoji ; Mandiou, Ion ; Hsu, Arthur ; McColl, Kaighin ; Lansdell, Benjamin ; Weinstock, George ; Kuczek, Elizabeth ; McGrath, Annette ; Wilson, Peter ; Men, Artem ; Hazar-Rethinam, Mehlika ; Hall, Allison ; Davis, John ; Wood, David ; Williams, Sarah ; Sundaravadanam, Yogi ; Muzny, Donna ; Jhangiani, Shalini ; Lewis, Lora ; Morgan, Margaret ; Okwuonu, Geoffrey ; Ruiz, San ; Santibanez, Jireh ; Nazareth, Lynne ; Cree, Andrew ; Fowler, Gerald ; Kovar, Christie ; Dinh, Huyen ; Joshi, Vandita ; Jing, Chyn ; Lara, Fremiet ; Thornton, Rebecca ; Chen, Lei ; Deng, Jixin ; Liu, Yue ; Shen, Joshua ; Song, Xing-Zhi ; Edson, Janette ; Troon, Carmen ; Thomas, Daniel ; Stephens, Amber ; Yapa, Lankesha ; Levchenko, Tanya ; Gibbs, Richard A. ; Cooper, Desmond ; Speed, Terence ; Fujiyama, Asao ; Graves, Jennifer A Marshall ; O’Neill, Rachel ; Pask, Andrew ; Forrest, Susan ; Worley, Kim. / Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. In: Genome Biology. 2011 ; Vol. 12:R81. pp. 1-25.
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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.",
author = "Renfree, {M. B.} and Anthony Papenfuss and Janine DEAKIN and James Lindsay and Thomas Heider and Katherine Belov and Willem Rens and Paul Waters and Elizabeth Pharo and Geoff Shaw and Emily Wong and Christophe Lefevre and Nicholas, {Kevin R.} and Yoko Kuroki and Matthew Wakefield and Kyall Zenger and Chenwei Wang and Malcolm Ferguson-Smith and Frank Nicholas and Danielle Hickford and Hongshi Yu and Short, {Kirsty R.} and Hannah Siddle and Stephen Frankenberg and Keng Chew and Brandon Menzies and Jessica Stringer and Shunsuke Suzuki and Timothy Hore and Delbridge, {Margaret L.} and Amir Mohammadi and Nanette Schneider and Yanqiu Hu and William O'Hara and Shafagh Nadaf and Chen Wu and Zhi-Ping Feng and Benjamin Cocks and Jianghui Wang and Paul Flicek and Stephen Searle and Susan Fairley and Kathryn Beal and Javier Herrero and Dawn Carone and Yutaka Suzuki and Sumio Sugano and Atsushi Toyoda and Yoshiyuki Sakaki and Shinji Kondo and Yuichiro Nishida and Shoji Tatsumoto and Ion Mandiou and Arthur Hsu and Kaighin McColl and Benjamin Lansdell and George Weinstock and Elizabeth Kuczek and Annette McGrath and Peter Wilson and Artem Men and Mehlika Hazar-Rethinam and Allison Hall and John Davis and David Wood and Sarah Williams and Yogi Sundaravadanam and Donna Muzny and Shalini Jhangiani and Lora Lewis and Margaret Morgan and Geoffrey Okwuonu and San Ruiz and Jireh Santibanez and Lynne Nazareth and Andrew Cree and Gerald Fowler and Christie Kovar and Huyen Dinh and Vandita Joshi and Chyn Jing and Fremiet Lara and Rebecca Thornton and Lei Chen and Jixin Deng and Yue Liu and Joshua Shen and Xing-Zhi Song and Janette Edson and Carmen Troon and Daniel Thomas and Amber Stephens and Lankesha Yapa and Tanya Levchenko and Gibbs, {Richard A.} and Desmond Cooper and Terence Speed and Asao Fujiyama and Graves, {Jennifer A Marshall} and Rachel O’Neill and Andrew Pask and Susan Forrest and Kim Worley",
year = "2011",
doi = "10.1186/gb-2011-12-8-r81",
language = "English",
volume = "12:R81",
pages = "1--25",
journal = "Genome Biology",
issn = "1474-7596",
publisher = "BioMed Central",

}

Renfree, MB, Papenfuss, A, DEAKIN, J, Lindsay, J, Heider, T, Belov, K, Rens, W, Waters, P, Pharo, E, Shaw, G, Wong, E, Lefevre, C, Nicholas, KR, Kuroki, Y, Wakefield, M, Zenger, K, Wang, C, Ferguson-Smith, M, Nicholas, F, Hickford, D, Yu, H, Short, KR, Siddle, H, Frankenberg, S, Chew, K, Menzies, B, Stringer, J, Suzuki, S, Hore, T, Delbridge, ML, Mohammadi, A, Schneider, N, Hu, Y, O'Hara, W, Nadaf, S, Wu, C, Feng, Z-P, Cocks, B, Wang, J, Flicek, P, Searle, S, Fairley, S, Beal, K, Herrero, J, Carone, D, Suzuki, Y, Sugano, S, Toyoda, A, Sakaki, Y, Kondo, S, Nishida, Y, Tatsumoto, S, Mandiou, I, Hsu, A, McColl, K, Lansdell, B, Weinstock, G, Kuczek, E, McGrath, A, Wilson, P, Men, A, Hazar-Rethinam, M, Hall, A, Davis, J, Wood, D, Williams, S, Sundaravadanam, Y, Muzny, D, Jhangiani, S, Lewis, L, Morgan, M, Okwuonu, G, Ruiz, S, Santibanez, J, Nazareth, L, Cree, A, Fowler, G, Kovar, C, Dinh, H, Joshi, V, Jing, C, Lara, F, Thornton, R, Chen, L, Deng, J, Liu, Y, Shen, J, Song, X-Z, Edson, J, Troon, C, Thomas, D, Stephens, A, Yapa, L, Levchenko, T, Gibbs, RA, Cooper, D, Speed, T, Fujiyama, A, Graves, JAM, O’Neill, R, Pask, A, Forrest, S & Worley, K 2011, 'Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development', Genome Biology, vol. 12:R81, pp. 1-25. https://doi.org/10.1186/gb-2011-12-8-r81

Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. / Renfree, M. B.; Papenfuss, Anthony; DEAKIN, Janine; Lindsay, James; Heider, Thomas; Belov, Katherine; Rens, Willem; Waters, Paul; Pharo, Elizabeth; Shaw, Geoff; Wong, Emily; Lefevre, Christophe; Nicholas, Kevin R.; Kuroki, Yoko; Wakefield, Matthew; Zenger, Kyall; Wang, Chenwei; Ferguson-Smith, Malcolm; Nicholas, Frank; Hickford, Danielle; Yu, Hongshi; Short, Kirsty R.; Siddle, Hannah; Frankenberg, Stephen; Chew, Keng; Menzies, Brandon; Stringer, Jessica; Suzuki, Shunsuke; Hore, Timothy; Delbridge, Margaret L.; Mohammadi, Amir; Schneider, Nanette; Hu, Yanqiu; O'Hara, William; Nadaf, Shafagh; Wu, Chen; Feng, Zhi-Ping; Cocks, Benjamin; Wang, Jianghui; Flicek, Paul; Searle, Stephen; Fairley, Susan; Beal, Kathryn; Herrero, Javier; Carone, Dawn; Suzuki, Yutaka; Sugano, Sumio; Toyoda, Atsushi; Sakaki, Yoshiyuki; Kondo, Shinji; Nishida, Yuichiro; Tatsumoto, Shoji; Mandiou, Ion; Hsu, Arthur; McColl, Kaighin; Lansdell, Benjamin; Weinstock, George; Kuczek, Elizabeth; McGrath, Annette; Wilson, Peter; Men, Artem; Hazar-Rethinam, Mehlika; Hall, Allison; Davis, John; Wood, David; Williams, Sarah; Sundaravadanam, Yogi; Muzny, Donna; Jhangiani, Shalini; Lewis, Lora; Morgan, Margaret; Okwuonu, Geoffrey; Ruiz, San; Santibanez, Jireh; Nazareth, Lynne; Cree, Andrew; Fowler, Gerald; Kovar, Christie; Dinh, Huyen; Joshi, Vandita; Jing, Chyn; Lara, Fremiet; Thornton, Rebecca; Chen, Lei; Deng, Jixin; Liu, Yue; Shen, Joshua; Song, Xing-Zhi; Edson, Janette; Troon, Carmen; Thomas, Daniel; Stephens, Amber; Yapa, Lankesha; Levchenko, Tanya; Gibbs, Richard A.; Cooper, Desmond; Speed, Terence; Fujiyama, Asao; Graves, Jennifer A Marshall; O’Neill, Rachel; Pask, Andrew; Forrest, Susan; Worley, Kim.

In: Genome Biology, Vol. 12:R81, 2011, p. 1-25.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development

AU - Renfree, M. B.

AU - Papenfuss, Anthony

AU - DEAKIN, Janine

AU - Lindsay, James

AU - Heider, Thomas

AU - Belov, Katherine

AU - Rens, Willem

AU - Waters, Paul

AU - Pharo, Elizabeth

AU - Shaw, Geoff

AU - Wong, Emily

AU - Lefevre, Christophe

AU - Nicholas, Kevin R.

AU - Kuroki, Yoko

AU - Wakefield, Matthew

AU - Zenger, Kyall

AU - Wang, Chenwei

AU - Ferguson-Smith, Malcolm

AU - Nicholas, Frank

AU - Hickford, Danielle

AU - Yu, Hongshi

AU - Short, Kirsty R.

AU - Siddle, Hannah

AU - Frankenberg, Stephen

AU - Chew, Keng

AU - Menzies, Brandon

AU - Stringer, Jessica

AU - Suzuki, Shunsuke

AU - Hore, Timothy

AU - Delbridge, Margaret L.

AU - Mohammadi, Amir

AU - Schneider, Nanette

AU - Hu, Yanqiu

AU - O'Hara, William

AU - Nadaf, Shafagh

AU - Wu, Chen

AU - Feng, Zhi-Ping

AU - Cocks, Benjamin

AU - Wang, Jianghui

AU - Flicek, Paul

AU - Searle, Stephen

AU - Fairley, Susan

AU - Beal, Kathryn

AU - Herrero, Javier

AU - Carone, Dawn

AU - Suzuki, Yutaka

AU - Sugano, Sumio

AU - Toyoda, Atsushi

AU - Sakaki, Yoshiyuki

AU - Kondo, Shinji

AU - Nishida, Yuichiro

AU - Tatsumoto, Shoji

AU - Mandiou, Ion

AU - Hsu, Arthur

AU - McColl, Kaighin

AU - Lansdell, Benjamin

AU - Weinstock, George

AU - Kuczek, Elizabeth

AU - McGrath, Annette

AU - Wilson, Peter

AU - Men, Artem

AU - Hazar-Rethinam, Mehlika

AU - Hall, Allison

AU - Davis, John

AU - Wood, David

AU - Williams, Sarah

AU - Sundaravadanam, Yogi

AU - Muzny, Donna

AU - Jhangiani, Shalini

AU - Lewis, Lora

AU - Morgan, Margaret

AU - Okwuonu, Geoffrey

AU - Ruiz, San

AU - Santibanez, Jireh

AU - Nazareth, Lynne

AU - Cree, Andrew

AU - Fowler, Gerald

AU - Kovar, Christie

AU - Dinh, Huyen

AU - Joshi, Vandita

AU - Jing, Chyn

AU - Lara, Fremiet

AU - Thornton, Rebecca

AU - Chen, Lei

AU - Deng, Jixin

AU - Liu, Yue

AU - Shen, Joshua

AU - Song, Xing-Zhi

AU - Edson, Janette

AU - Troon, Carmen

AU - Thomas, Daniel

AU - Stephens, Amber

AU - Yapa, Lankesha

AU - Levchenko, Tanya

AU - Gibbs, Richard A.

AU - Cooper, Desmond

AU - Speed, Terence

AU - Fujiyama, Asao

AU - Graves, Jennifer A Marshall

AU - O’Neill, Rachel

AU - Pask, Andrew

AU - Forrest, Susan

AU - Worley, Kim

PY - 2011

Y1 - 2011

N2 - 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.

AB - 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.

U2 - 10.1186/gb-2011-12-8-r81

DO - 10.1186/gb-2011-12-8-r81

M3 - Article

VL - 12:R81

SP - 1

EP - 25

JO - Genome Biology

JF - Genome Biology

SN - 1474-7596

ER -