Hemichordate genomes and deuterostome origins

Oleg Simakov; Takeshi Kawashima; Ferdinand Marlétaz; Jerry Jenkins; Ryo Koyanagi; Therese Mitros; Kanako Hisata; Jessen Bredeson; Eiichi Shoguchi; Fuki Gyoja; Jia Xing Yue; Yi Chih Chen; Robert M. Freeman; Akane Sasaki; Tomoe Hikosaka-Katayama; Atsuko Sato; Manabu Fujie; Kenneth W. Baughman; Judith Levine; Paul Gonzalez; Christopher Cameron; Jens H. Fritzenwanker; Ariel M. Pani; Hiroki Goto; Miyuki Kanda; Nana Arakaki; Shinichi Yamasaki; Jiaxin Qu; Andrew Cree; Yan Ding; Huyen H. Dinh; Shannon Dugan; Michael Holder; Shalini N. Jhangiani; Christie L. Kovar; Sandra L. Lee; Lora R. Lewis; Donna Morton; Lynne V. Nazareth; Geoffrey Okwuonu; Jireh Santibanez; Rui Chen; Stephen Richards; Donna M. Muzny; Andrew Gillis; Leonid Peshkin; Michael Wu; Tom Humphreys; Yi Hsien Su; Nicholas H. Putnam; Jeremy Schmutz; Asao Fujiyama; Jr Kai Yu; Kunifumi Tagawa; Kim C. Worley; Richard A. Gibbs; Marc W. Kirschner; Christopher J. Lowe; Noriyuki Satoh; Daniel S. Rokhsar; John Gerhart

doi:10.1038/nature16150

Hemichordate genomes and deuterostome origins

Oleg Simakov, Takeshi Kawashima, Ferdinand Marlétaz, Jerry Jenkins, Ryo Koyanagi, Therese Mitros, Kanako Hisata, Jessen Bredeson, Eiichi Shoguchi, Fuki Gyoja, Jia Xing Yue, Yi Chih Chen, Robert M. Freeman, Akane Sasaki, Tomoe Hikosaka-Katayama, Atsuko Sato, Manabu Fujie, Kenneth W. Baughman, Judith Levine, Paul GonzalezChristopher Cameron, Jens H. Fritzenwanker, Ariel M. Pani, Hiroki Goto, Miyuki Kanda, Nana Arakaki, Shinichi Yamasaki, Jiaxin Qu, Andrew Cree, Yan Ding, Huyen H. Dinh, Shannon Dugan, Michael Holder, Shalini N. Jhangiani, Christie L. Kovar, Sandra L. Lee, Lora R. Lewis, Donna Morton, Lynne V. Nazareth, Geoffrey Okwuonu, Jireh Santibanez, Rui Chen, Stephen Richards, Donna M. Muzny, Andrew Gillis, Leonid Peshkin, Michael Wu, Tom Humphreys, Yi Hsien Su, Nicholas H. Putnam, Jeremy Schmutz, Asao Fujiyama, Jr Kai Yu, Kunifumi Tagawa, Kim C. Worley, Richard A. Gibbs, Marc W. Kirschner, Christopher J. Lowe, Noriyuki Satoh, Daniel S. Rokhsar, John Gerhart

LIF - Molecular and Chemical Life Science

Research output: Contribution to journal › Article › peer-review

156 Citations (Scopus)

Abstract

Acorn worms, also known as enteropneust (literally, gut-breathing) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal gill slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

Original language	English
Pages (from-to)	459-465
Number of pages	7
Journal	Nature
Volume	527
Issue number	7579
DOIs	https://doi.org/10.1038/nature16150
Publication status	Published - 2015 Nov 26

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Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J., Koyanagi, R., Mitros, T., Hisata, K., Bredeson, J., Shoguchi, E., Gyoja, F., Yue, J. X., Chen, Y. C., Freeman, R. M., Sasaki, A., Hikosaka-Katayama, T., Sato, A., Fujie, M., Baughman, K. W., Levine, J., ... Gerhart, J. (2015). Hemichordate genomes and deuterostome origins. Nature, 527(7579), 459-465. https://doi.org/10.1038/nature16150

@article{3bcfdbd10cf24a359a1b5269af4861dc,

title = "Hemichordate genomes and deuterostome origins",

abstract = "Acorn worms, also known as enteropneust (literally, gut-breathing) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal gill slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.",

author = "Oleg Simakov and Takeshi Kawashima and Ferdinand Marl{\'e}taz and Jerry Jenkins and Ryo Koyanagi and Therese Mitros and Kanako Hisata and Jessen Bredeson and Eiichi Shoguchi and Fuki Gyoja and Yue, {Jia Xing} and Chen, {Yi Chih} and Freeman, {Robert M.} and Akane Sasaki and Tomoe Hikosaka-Katayama and Atsuko Sato and Manabu Fujie and Baughman, {Kenneth W.} and Judith Levine and Paul Gonzalez and Christopher Cameron and Fritzenwanker, {Jens H.} and Pani, {Ariel M.} and Hiroki Goto and Miyuki Kanda and Nana Arakaki and Shinichi Yamasaki and Jiaxin Qu and Andrew Cree and Yan Ding and Dinh, {Huyen H.} and Shannon Dugan and Michael Holder and Jhangiani, {Shalini N.} and Kovar, {Christie L.} and Lee, {Sandra L.} and Lewis, {Lora R.} and Donna Morton and Nazareth, {Lynne V.} and Geoffrey Okwuonu and Jireh Santibanez and Rui Chen and Stephen Richards and Muzny, {Donna M.} and Andrew Gillis and Leonid Peshkin and Michael Wu and Tom Humphreys and Su, {Yi Hsien} and Putnam, {Nicholas H.} and Jeremy Schmutz and Asao Fujiyama and Yu, {Jr Kai} and Kunifumi Tagawa and Worley, {Kim C.} and Gibbs, {Richard A.} and Kirschner, {Marc W.} and Lowe, {Christopher J.} and Noriyuki Satoh and Rokhsar, {Daniel S.} and John Gerhart",

note = "Funding Information: Acknowledgements The Ptychodera flava genome project was supported by MEXT and OIST, Japan. This research was supported by USPHS grant HD42724 and NASA grant FDNAG2–1605 to J.G.; USPHS grant HD37277 to M.W.K.; NASA - NNX13AI68G to C.L. F.M. was funded by FP7/ERC grant [268513]. O.S. and D.S.R, and T.K. and N.S. were supported by the Molecular Genetics Unit and Marine Genomics Unit of the Okinawa Institute of Science and Technology Graduate University, respectively. Y.-H.S. and J.-K.Y. are supported by Academia Sinica and Ministry of Science and Technology, Taiwan. L.P. was supported by NIH grant R01HD073104. The Saccoglossus kowalevskii genome project was supported by a grant from the National Human Genome Research Institute, National Institutes of Health (U54 HG003273) to R.A.G. Publisher Copyright: {\textcopyright} 2015 Macmillan Publishers Limited. All rights reserved.",

year = "2015",

month = nov,

day = "26",

doi = "10.1038/nature16150",

language = "English",

volume = "527",

pages = "459--465",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7579",

}

Simakov, O, Kawashima, T, Marlétaz, F, Jenkins, J, Koyanagi, R, Mitros, T, Hisata, K, Bredeson, J, Shoguchi, E, Gyoja, F, Yue, JX, Chen, YC, Freeman, RM, Sasaki, A, Hikosaka-Katayama, T, Sato, A, Fujie, M, Baughman, KW, Levine, J, Gonzalez, P, Cameron, C, Fritzenwanker, JH, Pani, AM, Goto, H, Kanda, M, Arakaki, N, Yamasaki, S, Qu, J, Cree, A, Ding, Y, Dinh, HH, Dugan, S, Holder, M, Jhangiani, SN, Kovar, CL, Lee, SL, Lewis, LR, Morton, D, Nazareth, LV, Okwuonu, G, Santibanez, J, Chen, R, Richards, S, Muzny, DM, Gillis, A, Peshkin, L, Wu, M, Humphreys, T, Su, YH, Putnam, NH, Schmutz, J, Fujiyama, A, Yu, JK, Tagawa, K, Worley, KC, Gibbs, RA, Kirschner, MW, Lowe, CJ, Satoh, N, Rokhsar, DS & Gerhart, J 2015, 'Hemichordate genomes and deuterostome origins', Nature, vol. 527, no. 7579, pp. 459-465. https://doi.org/10.1038/nature16150

TY - JOUR

T1 - Hemichordate genomes and deuterostome origins

AU - Simakov, Oleg

AU - Kawashima, Takeshi

AU - Marlétaz, Ferdinand

AU - Jenkins, Jerry

AU - Koyanagi, Ryo

AU - Mitros, Therese

AU - Hisata, Kanako

AU - Bredeson, Jessen

AU - Shoguchi, Eiichi

AU - Gyoja, Fuki

AU - Yue, Jia Xing

AU - Chen, Yi Chih

AU - Freeman, Robert M.

AU - Sasaki, Akane

AU - Hikosaka-Katayama, Tomoe

AU - Sato, Atsuko

AU - Fujie, Manabu

AU - Baughman, Kenneth W.

AU - Levine, Judith

AU - Gonzalez, Paul

AU - Cameron, Christopher

AU - Fritzenwanker, Jens H.

AU - Pani, Ariel M.

AU - Goto, Hiroki

AU - Kanda, Miyuki

AU - Arakaki, Nana

AU - Yamasaki, Shinichi

AU - Qu, Jiaxin

AU - Cree, Andrew

AU - Ding, Yan

AU - Dinh, Huyen H.

AU - Dugan, Shannon

AU - Holder, Michael

AU - Jhangiani, Shalini N.

AU - Kovar, Christie L.

AU - Lee, Sandra L.

AU - Lewis, Lora R.

AU - Morton, Donna

AU - Nazareth, Lynne V.

AU - Okwuonu, Geoffrey

AU - Santibanez, Jireh

AU - Chen, Rui

AU - Richards, Stephen

AU - Muzny, Donna M.

AU - Gillis, Andrew

AU - Peshkin, Leonid

AU - Wu, Michael

AU - Humphreys, Tom

AU - Su, Yi Hsien

AU - Putnam, Nicholas H.

AU - Schmutz, Jeremy

AU - Fujiyama, Asao

AU - Yu, Jr Kai

AU - Tagawa, Kunifumi

AU - Worley, Kim C.

AU - Gibbs, Richard A.

AU - Kirschner, Marc W.

AU - Lowe, Christopher J.

AU - Satoh, Noriyuki

AU - Rokhsar, Daniel S.

AU - Gerhart, John

N1 - Funding Information: Acknowledgements The Ptychodera flava genome project was supported by MEXT and OIST, Japan. This research was supported by USPHS grant HD42724 and NASA grant FDNAG2–1605 to J.G.; USPHS grant HD37277 to M.W.K.; NASA - NNX13AI68G to C.L. F.M. was funded by FP7/ERC grant [268513]. O.S. and D.S.R, and T.K. and N.S. were supported by the Molecular Genetics Unit and Marine Genomics Unit of the Okinawa Institute of Science and Technology Graduate University, respectively. Y.-H.S. and J.-K.Y. are supported by Academia Sinica and Ministry of Science and Technology, Taiwan. L.P. was supported by NIH grant R01HD073104. The Saccoglossus kowalevskii genome project was supported by a grant from the National Human Genome Research Institute, National Institutes of Health (U54 HG003273) to R.A.G. Publisher Copyright: © 2015 Macmillan Publishers Limited. All rights reserved.

PY - 2015/11/26

Y1 - 2015/11/26

N2 - Acorn worms, also known as enteropneust (literally, gut-breathing) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal gill slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

AB - Acorn worms, also known as enteropneust (literally, gut-breathing) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal gill slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

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U2 - 10.1038/nature16150

DO - 10.1038/nature16150

M3 - Article

C2 - 26580012

AN - SCOPUS:84948422617

SN - 0028-0836

VL - 527

SP - 459

EP - 465

JO - Nature

JF - Nature

IS - 7579

ER -

Hemichordate genomes and deuterostome origins

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