The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons

Ingo Braasch, Andrew R. Gehrke, Jeramiah J. Smith, Kazuhiko Kawasaki, Tereza Manousaki, Jeremy Pasquier, Angel Amores, Thomas Desvignes, Peter Batzel, Julian Catchen, Aaron M. Berlin, Michael S. Campbell, Daniel Barrell, Kyle J. Martin, John F. Mulley, Vydianathan Ravi, Alison P. Lee, Tetsuya Nakamura, Domitille Chalopin, Shaohua Fan & 41 others Dustin Wcisel, Cristian Caestro, Jason Sydes, Felix E.G. Beaudry, Yi Sun, Jana Hertel, Michael J. Beam, Mario Fasold, Mikio Ishiyama, Jeremy Johnson, Steffi Kehr, Marcia Lara, John H. Letaw, Gary W. Litman, Ronda T. Litman, Masato Mikami, Tatsuya Ota, Nil Ratan Saha, Louise Williams, Peter F. Stadler, Han Wang, John S. Taylor, Quenton Fontenot, Allyse Ferrara, Stephen M.J. Searle, Bronwen Aken, Mark Yandell, Igor Schneider, Jeffrey A. Yoder, Jean Nicolas Volff, Axel Meyer, Chris T. Amemiya, Byrappa Venkatesh, Peter W.H. Holland, Yann Guiguen, Julien Bobe, Neil H. Shubin, Federica Di Palma, Jessica Alföldi, Kerstin Lindblad-Toh, John H. Postlethwait

Research output: Contribution to journalArticle

178 Citations (Scopus)

Abstract

To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.

Original languageEnglish (US)
Pages (from-to)427-437
Number of pages11
JournalNature Genetics
Volume48
Issue number4
DOIs
StatePublished - Mar 29 2016

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Vertebrates
Genome
Human Genome
Genome-Wide Association Study
MicroRNAs
Genes
Immunity
Fishes
Chromosomes
Gene Expression

All Science Journal Classification (ASJC) codes

  • Genetics

Cite this

Braasch, I., Gehrke, A. R., Smith, J. J., Kawasaki, K., Manousaki, T., Pasquier, J., ... Postlethwait, J. H. (2016). The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nature Genetics, 48(4), 427-437. https://doi.org/10.1038/ng.3526
Braasch, Ingo ; Gehrke, Andrew R. ; Smith, Jeramiah J. ; Kawasaki, Kazuhiko ; Manousaki, Tereza ; Pasquier, Jeremy ; Amores, Angel ; Desvignes, Thomas ; Batzel, Peter ; Catchen, Julian ; Berlin, Aaron M. ; Campbell, Michael S. ; Barrell, Daniel ; Martin, Kyle J. ; Mulley, John F. ; Ravi, Vydianathan ; Lee, Alison P. ; Nakamura, Tetsuya ; Chalopin, Domitille ; Fan, Shaohua ; Wcisel, Dustin ; Caestro, Cristian ; Sydes, Jason ; Beaudry, Felix E.G. ; Sun, Yi ; Hertel, Jana ; Beam, Michael J. ; Fasold, Mario ; Ishiyama, Mikio ; Johnson, Jeremy ; Kehr, Steffi ; Lara, Marcia ; Letaw, John H. ; Litman, Gary W. ; Litman, Ronda T. ; Mikami, Masato ; Ota, Tatsuya ; Saha, Nil Ratan ; Williams, Louise ; Stadler, Peter F. ; Wang, Han ; Taylor, John S. ; Fontenot, Quenton ; Ferrara, Allyse ; Searle, Stephen M.J. ; Aken, Bronwen ; Yandell, Mark ; Schneider, Igor ; Yoder, Jeffrey A. ; Volff, Jean Nicolas ; Meyer, Axel ; Amemiya, Chris T. ; Venkatesh, Byrappa ; Holland, Peter W.H. ; Guiguen, Yann ; Bobe, Julien ; Shubin, Neil H. ; Di Palma, Federica ; Alföldi, Jessica ; Lindblad-Toh, Kerstin ; Postlethwait, John H. / The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. In: Nature Genetics. 2016 ; Vol. 48, No. 4. pp. 427-437.
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abstract = "To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.",
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Braasch, I, Gehrke, AR, Smith, JJ, Kawasaki, K, Manousaki, T, Pasquier, J, Amores, A, Desvignes, T, Batzel, P, Catchen, J, Berlin, AM, Campbell, MS, Barrell, D, Martin, KJ, Mulley, JF, Ravi, V, Lee, AP, Nakamura, T, Chalopin, D, Fan, S, Wcisel, D, Caestro, C, Sydes, J, Beaudry, FEG, Sun, Y, Hertel, J, Beam, MJ, Fasold, M, Ishiyama, M, Johnson, J, Kehr, S, Lara, M, Letaw, JH, Litman, GW, Litman, RT, Mikami, M, Ota, T, Saha, NR, Williams, L, Stadler, PF, Wang, H, Taylor, JS, Fontenot, Q, Ferrara, A, Searle, SMJ, Aken, B, Yandell, M, Schneider, I, Yoder, JA, Volff, JN, Meyer, A, Amemiya, CT, Venkatesh, B, Holland, PWH, Guiguen, Y, Bobe, J, Shubin, NH, Di Palma, F, Alföldi, J, Lindblad-Toh, K & Postlethwait, JH 2016, 'The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons', Nature Genetics, vol. 48, no. 4, pp. 427-437. https://doi.org/10.1038/ng.3526

The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. / Braasch, Ingo; Gehrke, Andrew R.; Smith, Jeramiah J.; Kawasaki, Kazuhiko; Manousaki, Tereza; Pasquier, Jeremy; Amores, Angel; Desvignes, Thomas; Batzel, Peter; Catchen, Julian; Berlin, Aaron M.; Campbell, Michael S.; Barrell, Daniel; Martin, Kyle J.; Mulley, John F.; Ravi, Vydianathan; Lee, Alison P.; Nakamura, Tetsuya; Chalopin, Domitille; Fan, Shaohua; Wcisel, Dustin; Caestro, Cristian; Sydes, Jason; Beaudry, Felix E.G.; Sun, Yi; Hertel, Jana; Beam, Michael J.; Fasold, Mario; Ishiyama, Mikio; Johnson, Jeremy; Kehr, Steffi; Lara, Marcia; Letaw, John H.; Litman, Gary W.; Litman, Ronda T.; Mikami, Masato; Ota, Tatsuya; Saha, Nil Ratan; Williams, Louise; Stadler, Peter F.; Wang, Han; Taylor, John S.; Fontenot, Quenton; Ferrara, Allyse; Searle, Stephen M.J.; Aken, Bronwen; Yandell, Mark; Schneider, Igor; Yoder, Jeffrey A.; Volff, Jean Nicolas; Meyer, Axel; Amemiya, Chris T.; Venkatesh, Byrappa; Holland, Peter W.H.; Guiguen, Yann; Bobe, Julien; Shubin, Neil H.; Di Palma, Federica; Alföldi, Jessica; Lindblad-Toh, Kerstin; Postlethwait, John H.

In: Nature Genetics, Vol. 48, No. 4, 29.03.2016, p. 427-437.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons

AU - Braasch, Ingo

AU - Gehrke, Andrew R.

AU - Smith, Jeramiah J.

AU - Kawasaki, Kazuhiko

AU - Manousaki, Tereza

AU - Pasquier, Jeremy

AU - Amores, Angel

AU - Desvignes, Thomas

AU - Batzel, Peter

AU - Catchen, Julian

AU - Berlin, Aaron M.

AU - Campbell, Michael S.

AU - Barrell, Daniel

AU - Martin, Kyle J.

AU - Mulley, John F.

AU - Ravi, Vydianathan

AU - Lee, Alison P.

AU - Nakamura, Tetsuya

AU - Chalopin, Domitille

AU - Fan, Shaohua

AU - Wcisel, Dustin

AU - Caestro, Cristian

AU - Sydes, Jason

AU - Beaudry, Felix E.G.

AU - Sun, Yi

AU - Hertel, Jana

AU - Beam, Michael J.

AU - Fasold, Mario

AU - Ishiyama, Mikio

AU - Johnson, Jeremy

AU - Kehr, Steffi

AU - Lara, Marcia

AU - Letaw, John H.

AU - Litman, Gary W.

AU - Litman, Ronda T.

AU - Mikami, Masato

AU - Ota, Tatsuya

AU - Saha, Nil Ratan

AU - Williams, Louise

AU - Stadler, Peter F.

AU - Wang, Han

AU - Taylor, John S.

AU - Fontenot, Quenton

AU - Ferrara, Allyse

AU - Searle, Stephen M.J.

AU - Aken, Bronwen

AU - Yandell, Mark

AU - Schneider, Igor

AU - Yoder, Jeffrey A.

AU - Volff, Jean Nicolas

AU - Meyer, Axel

AU - Amemiya, Chris T.

AU - Venkatesh, Byrappa

AU - Holland, Peter W.H.

AU - Guiguen, Yann

AU - Bobe, Julien

AU - Shubin, Neil H.

AU - Di Palma, Federica

AU - Alföldi, Jessica

AU - Lindblad-Toh, Kerstin

AU - Postlethwait, John H.

PY - 2016/3/29

Y1 - 2016/3/29

N2 - To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.

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