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

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

Research output: Contribution to journalArticleResearchpeer-review

112 Citations (Scopus)

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. RESULTS: The genome has been sequenced to 2 x 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
Article number8
Number of pages25
JournalGenome Biology
Volume12
Issue number8
DOIs
Publication statusPublished - 2011
Externally publishedYes

Cite this

Renfree, Marilyn ; Papenfuss, Anthony ; Deakin, Janine E ; Lindsay, James ; Heider, Thomas ; Belov, Katherine ; Rens, Willem ; Waters, Paul D ; Pharo, Elizabeth ; Shaw, Geoff ; Wong, Emily SW ; Lefevre, Christophe Marc ; Nicholas, Kevin R ; Kuroki, Yuko ; Wakefield, Matthew J ; Zenger, Kyall ; Wang, Chenwei ; Ferguson-Smith, Malcolm ; Nicholas, Frank W ; Hickford, Danielle ; Yu, Hongshi ; Short, Kirsty R ; Siddle, Hannah V ; Frankenberg, Stephen R ; Chew, Keng Yih ; Menzies, Brandon R ; Stringer, Jessica ; Suzuki, Shunsuke ; Hore, Timothy A ; Delbridge, Margaret L ; Mohammadi, Amir ; Schneider, Nanette Y ; Hu, Yanqiu ; O'Hara, William ; Nadaf, Shafagh Al ; Wu, Chen ; Feng, Zhi-Ping ; Cocks, Benjamin G ; Wang, Jianghui ; Flicek, Paul ; Searle, Stephen M J ; Fairley, Susan ; Beal, Kathryn ; Herrero, Javier ; Carone, Dawn M ; Suzuki, Yutaka ; Sugano, Sumio ; Toyoda, Atsushi ; Sakaki, Yoshiyuki ; Kondo, Shinji ; Nishida, Yuichiro ; Tatsumoto, Shoji ; Mandiou, Ion ; Hsu, Arthur L C ; McColl, Kaighin A ; Lansdell, Benjamin ; Weinstock, George ; Kuczek, Elizabeth ; McGrath, Annette ; Wilson, Peter ; Men, Artem ; Hazar-Rethinam, Mehlike ; Hall, Allison ; Davis, John ; Wood, Dav ; Williams, Sarah ; Sundaravadanam, Yogi ; Muzny, Donna M ; Jhangiani, Shalini N ; Lewis, Lora R ; Morgan, Margaret B ; Okwuonu, Geoffrey O ; Ruiz, San Juana ; Santibanez, Jireh ; Nazareth, Lynne ; Cree, Andrew ; Fowler, Gerald ; Kovar, Christie L ; Dinh, Huyen ; Joshi, Vandita ; Jing, Chyn ; Lara, F ; Thornton, Rebecca ; Chen, Lei ; Deng, Jixin ; Liu, Yue ; Shen, Joshua Y ; Song, Xing-Zhi ; Edson, Janette ; Troon, Carmen ; Thomas, Daniel ; Stephens, Amber ; Yapa, Lankesha ; Levchenko, Tanya ; Gibbs, Richard A ; Cooper, Desmond W ; Speed, Terence P ; Fujiyama, Asao ; Graves, Jennifer A M ; O'Neill, Rachel J ; Pask, Andrew ; Forrest, Susan M ; Worley, Kim C. / Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. In: Genome Biology. 2011 ; Vol. 12, No. 8.
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title = "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. RESULTS: The genome has been sequenced to 2 x 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 = "Marilyn Renfree and Anthony Papenfuss and Deakin, {Janine E} and James Lindsay and Thomas Heider and Katherine Belov and Willem Rens and Waters, {Paul D} and Elizabeth Pharo and Geoff Shaw and Wong, {Emily SW} and Lefevre, {Christophe Marc} and Nicholas, {Kevin R} and Yuko Kuroki and Wakefield, {Matthew J} and Kyall Zenger and Chenwei Wang and Malcolm Ferguson-Smith and Nicholas, {Frank W} and Danielle Hickford and Hongshi Yu and Short, {Kirsty R} and Siddle, {Hannah V} and Frankenberg, {Stephen R} and Chew, {Keng Yih} and Menzies, {Brandon R} and Jessica Stringer and Shunsuke Suzuki and Hore, {Timothy A} and Delbridge, {Margaret L} and Amir Mohammadi and Schneider, {Nanette Y} and Yanqiu Hu and William O'Hara and Nadaf, {Shafagh Al} and Chen Wu and Zhi-Ping Feng and Cocks, {Benjamin G} and Jianghui Wang and Paul Flicek and Searle, {Stephen M J} and Susan Fairley and Kathryn Beal and Javier Herrero and Carone, {Dawn M} 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 Hsu, {Arthur L C} and McColl, {Kaighin A} and Benjamin Lansdell and George Weinstock and Elizabeth Kuczek and Annette McGrath and Peter Wilson and Artem Men and Mehlike Hazar-Rethinam and Allison Hall and John Davis and Dav Wood and Sarah Williams and Yogi Sundaravadanam and Muzny, {Donna M} and Jhangiani, {Shalini N} and Lewis, {Lora R} and Morgan, {Margaret B} and Okwuonu, {Geoffrey O} and Ruiz, {San Juana} and Jireh Santibanez and Lynne Nazareth and Andrew Cree and Gerald Fowler and Kovar, {Christie L} and Huyen Dinh and Vandita Joshi and Chyn Jing and F Lara and Rebecca Thornton and Lei Chen and Jixin Deng and Yue Liu and Shen, {Joshua Y} 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 Cooper, {Desmond W} and Speed, {Terence P} and Asao Fujiyama and Graves, {Jennifer A M} and O'Neill, {Rachel J} and Andrew Pask and Forrest, {Susan M} and Worley, {Kim C}",
year = "2011",
doi = "10.1186/gb-2011-12-8-r81",
language = "English",
volume = "12",
journal = "Genome Biology",
issn = "1474-760X",
publisher = "BioMed Central",
number = "8",

}

Renfree, M, Papenfuss, A, Deakin, JE, Lindsay, J, Heider, T, Belov, K, Rens, W, Waters, PD, Pharo, E, Shaw, G, Wong, ESW, Lefevre, CM, Nicholas, KR, Kuroki, Y, Wakefield, MJ, Zenger, K, Wang, C, Ferguson-Smith, M, Nicholas, FW, Hickford, D, Yu, H, Short, KR, Siddle, HV, Frankenberg, SR, Chew, KY, Menzies, BR, Stringer, J, Suzuki, S, Hore, TA, Delbridge, ML, Mohammadi, A, Schneider, NY, Hu, Y, O'Hara, W, Nadaf, SA, Wu, C, Feng, Z-P, Cocks, BG, Wang, J, Flicek, P, Searle, SMJ, Fairley, S, Beal, K, Herrero, J, Carone, DM, Suzuki, Y, Sugano, S, Toyoda, A, Sakaki, Y, Kondo, S, Nishida, Y, Tatsumoto, S, Mandiou, I, Hsu, ALC, McColl, KA, 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, DM, Jhangiani, SN, Lewis, LR, Morgan, MB, Okwuonu, GO, Ruiz, SJ, Santibanez, J, Nazareth, L, Cree, A, Fowler, G, Kovar, CL, Dinh, H, Joshi, V, Jing, C, Lara, F, Thornton, R, Chen, L, Deng, J, Liu, Y, Shen, JY, Song, X-Z, Edson, J, Troon, C, Thomas, D, Stephens, A, Yapa, L, Levchenko, T, Gibbs, RA, Cooper, DW, Speed, TP, Fujiyama, A, Graves, JAM, O'Neill, RJ, Pask, A, Forrest, SM & Worley, KC 2011, 'Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development', Genome Biology, vol. 12, no. 8, 8. 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, Marilyn; Papenfuss, Anthony; Deakin, Janine E; Lindsay, James; Heider, Thomas; Belov, Katherine; Rens, Willem; Waters, Paul D; Pharo, Elizabeth; Shaw, Geoff; Wong, Emily SW; Lefevre, Christophe Marc; Nicholas, Kevin R; Kuroki, Yuko; Wakefield, Matthew J; Zenger, Kyall; Wang, Chenwei; Ferguson-Smith, Malcolm; Nicholas, Frank W; Hickford, Danielle; Yu, Hongshi; Short, Kirsty R; Siddle, Hannah V; Frankenberg, Stephen R; Chew, Keng Yih; Menzies, Brandon R; Stringer, Jessica; Suzuki, Shunsuke; Hore, Timothy A; Delbridge, Margaret L; Mohammadi, Amir; Schneider, Nanette Y; Hu, Yanqiu; O'Hara, William; Nadaf, Shafagh Al; Wu, Chen; Feng, Zhi-Ping; Cocks, Benjamin G; Wang, Jianghui; Flicek, Paul; Searle, Stephen M J; Fairley, Susan; Beal, Kathryn; Herrero, Javier; Carone, Dawn M; Suzuki, Yutaka; Sugano, Sumio; Toyoda, Atsushi; Sakaki, Yoshiyuki; Kondo, Shinji; Nishida, Yuichiro; Tatsumoto, Shoji; Mandiou, Ion; Hsu, Arthur L C; McColl, Kaighin A; Lansdell, Benjamin; Weinstock, George; Kuczek, Elizabeth; McGrath, Annette; Wilson, Peter; Men, Artem; Hazar-Rethinam, Mehlike; Hall, Allison; Davis, John; Wood, Dav; Williams, Sarah; Sundaravadanam, Yogi; Muzny, Donna M; Jhangiani, Shalini N; Lewis, Lora R; Morgan, Margaret B; Okwuonu, Geoffrey O; Ruiz, San Juana; Santibanez, Jireh; Nazareth, Lynne; Cree, Andrew; Fowler, Gerald; Kovar, Christie L; Dinh, Huyen; Joshi, Vandita; Jing, Chyn; Lara, F; Thornton, Rebecca; Chen, Lei; Deng, Jixin; Liu, Yue; Shen, Joshua Y; Song, Xing-Zhi; Edson, Janette; Troon, Carmen; Thomas, Daniel; Stephens, Amber; Yapa, Lankesha; Levchenko, Tanya; Gibbs, Richard A; Cooper, Desmond W; Speed, Terence P; Fujiyama, Asao; Graves, Jennifer A M; O'Neill, Rachel J; Pask, Andrew; Forrest, Susan M; Worley, Kim C.

In: Genome Biology, Vol. 12, No. 8, 8, 2011.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

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

AU - Renfree, Marilyn

AU - Papenfuss, Anthony

AU - Deakin, Janine E

AU - Lindsay, James

AU - Heider, Thomas

AU - Belov, Katherine

AU - Rens, Willem

AU - Waters, Paul D

AU - Pharo, Elizabeth

AU - Shaw, Geoff

AU - Wong, Emily SW

AU - Lefevre, Christophe Marc

AU - Nicholas, Kevin R

AU - Kuroki, Yuko

AU - Wakefield, Matthew J

AU - Zenger, Kyall

AU - Wang, Chenwei

AU - Ferguson-Smith, Malcolm

AU - Nicholas, Frank W

AU - Hickford, Danielle

AU - Yu, Hongshi

AU - Short, Kirsty R

AU - Siddle, Hannah V

AU - Frankenberg, Stephen R

AU - Chew, Keng Yih

AU - Menzies, Brandon R

AU - Stringer, Jessica

AU - Suzuki, Shunsuke

AU - Hore, Timothy A

AU - Delbridge, Margaret L

AU - Mohammadi, Amir

AU - Schneider, Nanette Y

AU - Hu, Yanqiu

AU - O'Hara, William

AU - Nadaf, Shafagh Al

AU - Wu, Chen

AU - Feng, Zhi-Ping

AU - Cocks, Benjamin G

AU - Wang, Jianghui

AU - Flicek, Paul

AU - Searle, Stephen M J

AU - Fairley, Susan

AU - Beal, Kathryn

AU - Herrero, Javier

AU - Carone, Dawn M

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 L C

AU - McColl, Kaighin A

AU - Lansdell, Benjamin

AU - Weinstock, George

AU - Kuczek, Elizabeth

AU - McGrath, Annette

AU - Wilson, Peter

AU - Men, Artem

AU - Hazar-Rethinam, Mehlike

AU - Hall, Allison

AU - Davis, John

AU - Wood, Dav

AU - Williams, Sarah

AU - Sundaravadanam, Yogi

AU - Muzny, Donna M

AU - Jhangiani, Shalini N

AU - Lewis, Lora R

AU - Morgan, Margaret B

AU - Okwuonu, Geoffrey O

AU - Ruiz, San Juana

AU - Santibanez, Jireh

AU - Nazareth, Lynne

AU - Cree, Andrew

AU - Fowler, Gerald

AU - Kovar, Christie L

AU - Dinh, Huyen

AU - Joshi, Vandita

AU - Jing, Chyn

AU - Lara, F

AU - Thornton, Rebecca

AU - Chen, Lei

AU - Deng, Jixin

AU - Liu, Yue

AU - Shen, Joshua Y

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 W

AU - Speed, Terence P

AU - Fujiyama, Asao

AU - Graves, Jennifer A M

AU - O'Neill, Rachel J

AU - Pask, Andrew

AU - Forrest, Susan M

AU - Worley, Kim C

PY - 2011

Y1 - 2011

N2 - 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 x 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 - 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 x 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.

UR - http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21854559

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

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

M3 - Article

VL - 12

JO - Genome Biology

JF - Genome Biology

SN - 1474-760X

IS - 8

M1 - 8

ER -