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

    Research output: Contribution to journalArticle

    78 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 languageEnglish
    Pages (from-to)459-465
    Number of pages7
    JournalNature
    Volume527
    Issue number7579
    DOIs
    Publication statusPublished - Nov 26 2015

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    Chordata
    Genome
    Lancelets
    Genes
    Synteny
    Conserved Sequence
    Invertebrates
    Regulator Genes
    Life Style
    Respiration
    Transcription Factors
    Gene Expression

    All Science Journal Classification (ASJC) codes

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    Cite this

    Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J., Koyanagi, R., Mitros, T., ... Gerhart, J. (2015). Hemichordate genomes and deuterostome origins. Nature, 527(7579), 459-465. https://doi.org/10.1038/nature16150

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

    In: Nature, Vol. 527, No. 7579, 26.11.2015, p. 459-465.

    Research output: Contribution to journalArticle

    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
    Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T et al. Hemichordate genomes and deuterostome origins. Nature. 2015 Nov 26;527(7579):459-465. https://doi.org/10.1038/nature16150
    Simakov, Oleg ; Kawashima, Takeshi ; Marlétaz, Ferdinand ; Jenkins, Jerry ; Koyanagi, Ryo ; Mitros, Therese ; Hisata, Kanako ; Bredeson, Jessen ; Shoguchi, Eiichi ; Gyoja, Fuki ; Yue, Jia Xing ; Chen, Yi Chih ; Freeman, Robert M. ; Sasaki, Akane ; Hikosaka-Katayama, Tomoe ; Sato, Atsuko ; Fujie, Manabu ; Baughman, Kenneth W. ; Levine, Judith ; Gonzalez, Paul ; Cameron, Christopher ; Fritzenwanker, Jens H. ; Pani, Ariel M. ; Goto, Hiroki ; Kanda, Miyuki ; Arakaki, Nana ; Yamasaki, Shinichi ; Qu, Jiaxin ; Cree, Andrew ; Ding, Yan ; Dinh, Huyen H. ; Dugan, Shannon ; Holder, Michael ; Jhangiani, Shalini N. ; Kovar, Christie L. ; Lee, Sandra L. ; Lewis, Lora R. ; Morton, Donna ; Nazareth, Lynne V. ; Okwuonu, Geoffrey ; Santibanez, Jireh ; Chen, Rui ; Richards, Stephen ; Muzny, Donna M. ; Gillis, Andrew ; Peshkin, Leonid ; Wu, Michael ; Humphreys, Tom ; Su, Yi Hsien ; Putnam, Nicholas H. ; Schmutz, Jeremy ; Fujiyama, Asao ; Yu, Jr Kai ; Tagawa, Kunifumi ; Worley, Kim C. ; Gibbs, Richard A. ; Kirschner, Marc W. ; Lowe, Christopher J. ; Satoh, Noriyuki ; Rokhsar, Daniel S. ; Gerhart, John. / Hemichordate genomes and deuterostome origins. In: Nature. 2015 ; Vol. 527, No. 7579. pp. 459-465.
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    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.",
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