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; Dustin Wcisel; Cristian Cañestro; 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

doi:10.1038/ng.3526

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 FanDustin Wcisel, Cristian Cañestro, 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

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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.

Original language	English
Pages (from-to)	427-437
Number of pages	14
Journal	Nature Genetics
Volume	48
Issue number	4
Early online date	7 Mar 2016
DOIs	https://doi.org/10.1038/ng.3526
Publication status	Published - 1 Apr 2016

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Cite this

Braasch, I., Gehrke, A. R., Smith, J. J., Kawasaki, K., Manousaki, T., Pasquier, J., Amores, A., Desvignes, T., Batzel, P., Catchen, J., Berlin, A. M., Campbell, M. S., Barrell, D., Martin, K. J., Mulley, J. F., Ravi, V., Lee, A. P., Nakamura, T., Chalopin, D., ... 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

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title = "The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons",

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.",

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

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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, Cañestro, 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, J-N, 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

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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

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AU - Nakamura, Tetsuya

AU - Chalopin, Domitille

AU - Fan, Shaohua

AU - Wcisel, Dustin

AU - Cañestro, 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

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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.

AB - 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.

U2 - 10.1038/ng.3526

DO - 10.1038/ng.3526

M3 - Article

VL - 48

SP - 427

EP - 437

JO - Nature Genetics

JF - Nature Genetics

SN - 1061-4036

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