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Hemichordate genomes and deuterostome origins

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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·2015·Nature

Abstract

Sequencing the genomes of two enteropneusts reveals complex genomic organization and developmental innovation in the ancestor of deuterostomes, a group of animals including echinoderms (starfish and their relatives) and chordates (which includes humans). 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. Acorn worms or enteropneusts are flaccid sightless sea creatures found burrowing in soft mud and sand. Their genomes hold the key to the evolution of the deuterostomes, an extensive group that encompasses echinoderms (starfishes and their relatives), as well as chordates (including ourselves). Oleg Simakov et al. present genome sequences of two enteropneusts — one a direct-developer, the other with a planktonic larva. Comparison with other animal genomes reveals extensive regions of synteny with the amphioxus (a primitive chordate) and other bilaterians. The authors identify a cassette of genes specifically associated with the development of pharyngeal slits, which are serial perforations of the body wall found at least primitively in all deuterostomes and increasingly thought to be a defining feature of the group as a whole.

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Metadata

Authors
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., Gonzalez, P., Cameron, C., Fritzenwanker, J. H., Pani, A. M., Goto, H., Kanda, M., Arakaki, N., Yamasaki, S., Qu, J., Cree, A., Ding, Y., Dinh, H. H., Dugan, S., Holder, M., Jhangiani, S. N., Kovar, C. L., Lee, S. L., Lewis, L. R., Morton, D., Nazareth, L. V., Okwuonu, G., Santibanez, J., Chen, R., Richards, S., Muzny, D. M., Gillis, A., Peshkin, L., Wu, M., Humphreys, T., Su, Y.-H., Putnam, N. H., Schmutz, J., Fujiyama, A., Yu, J.-K., Tagawa, K., Worley, K. C., Gibbs, R. A., Kirschner, M. W., Lowe, C. J., Satoh, N., Rokhsar, D. S., & Gerhart, J.
Venue
Nature
Published
2015-11
Volume
527
Issue
7579
Pages
459-465
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2187842183
Cited by
255
References
8
FWCI
9.39
Type
journal article
Language
en
Open access
hybrid
Licence
creativecommons.org/licenses/by-nc-sa/3.0/ (tdm)

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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. https://doi.org/10.1038/nature16150

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