Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz; Panos Firbas; Ignacio Maeso; Juan Tena; Ozren Bogdanovic; Malcolm Perry; Chris Wyatt; Elisa de la Calle-Mustienes; Stephanie Bertrand; Demian Burguera; Rafael Acemel; Simon van Heeringen; Silvia Naranjo; Carlos Herrera-Ubeda; Ksenia Skvortsova; Sandra Jimenez-Gancedo; Daniel Aldea; Yamile Marquez; Lorena Buono; Iryna Kozmikova; Jon Permanyer; Alexandra Louis; Beatriz Albuixech-Crespo; Yann Le Petillon; Anthony Leon Florian; Lucie Subirana; Piotr J. Balwierz; Paul Duckett; Ensieh Farahani; Jean Marc Aury; Sophie Mangenot; Patrick Wincker; Ricard Albalat; Elia Benito-Gutierrez; Cristian Canestro; Filipe Castro; Salvatore D'Aniello; David Ellard Keith Ferrier; Shengfeng Huang; Vincent Laudet; Gabriel Marais; Pierre Pontarotti; Michael Schubert; Herve Seitz; Ildiko Maureen Lara Somorjai; Tokiharu Takahashi; Olivier Mirabeau; Anlong Xu; Jr-Kai Yu; Piero Carninci; Juan Martinez-Morales; Hugues Crollius; Zbynek Kozmik; Matt Weirauch; Jordi Garcia-Fernandez; Ryan Lister; Boris Lenhard; Peter Holland; Hector Escriva; Jose Luis Gomez-Skarmeta; Manuel Irimia

doi:10.1038/s41586-018-0734-6

Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz, Panos Firbas, Ignacio Maeso, Juan Tena, Ozren Bogdanovic, Malcolm Perry, Chris Wyatt, Elisa de la Calle-Mustienes, Stephanie Bertrand, Demian Burguera, Rafael Acemel, Simon van Heeringen, Silvia Naranjo, Carlos Herrera-Ubeda, Ksenia Skvortsova, Sandra Jimenez-Gancedo, Daniel Aldea, Yamile Marquez, Lorena Buono, Iryna KozmikovaJon Permanyer, Alexandra Louis, Beatriz Albuixech-Crespo, Yann Le Petillon, Anthony Leon Florian, Lucie Subirana, Piotr J. Balwierz, Paul Duckett, Ensieh Farahani, Jean Marc Aury, Sophie Mangenot, Patrick Wincker, Ricard Albalat, Elia Benito-Gutierrez, Cristian Canestro, Filipe Castro, Salvatore D'Aniello, David Ellard Keith Ferrier, Shengfeng Huang, Vincent Laudet, Gabriel Marais, Pierre Pontarotti, Michael Schubert, Herve Seitz, Ildiko Maureen Lara Somorjai, Tokiharu Takahashi, Olivier Mirabeau, Anlong Xu, Jr-Kai Yu, Piero Carninci, Juan Martinez-Morales, Hugues Crollius, Zbynek Kozmik, Matt Weirauch, Jordi Garcia-Fernandez, Ryan Lister, Boris Lenhard, Peter Holland, Hector Escriva, Jose Luis Gomez-Skarmeta, Manuel Irimia

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

Abstract

Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.

Original language	English
Pages (from-to)	64-70
Number of pages	29
Journal	Nature
Volume	564
Issue number	7734
DOIs	https://doi.org/10.1038/s41586-018-0734-6
Publication status	Published - 21 Nov 2018

Access to Document

10.1038/s41586-018-0734-6Licence: CC BY

Marletaz_2018_Nature_Amphioxus_CC
Copyright © 2018 The Author(s). Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Final published version, 28.3 MBLicence: CC BY

ParaHox gene cluster: Determining major general regulatory mechanisms in the ParaHox gene cluster
Ferrier, D. E. K. (PI)
The Leverhulme Trust
5/06/17 → 4/06/20
Project: Standard
CORBEL: H2020 INFRADEV4
Ferrier, D. E. K. (PI) & Somorjai, I. M. L. (CoI)
European Commission
1/09/15 → 31/05/20
Project: Standard

Amphioxus functional genomics and the origins of vertebrate gene regulation (next-generation sequencing data)
Marletaz, F. (Creator), Firbas, P. (Creator), Maeso, I. (Creator), Tena, J. (Creator), Bogdanovic, O. (Creator), Perry, M. (Creator), Wyatt, C. (Creator), de la Calle-Mustienes, E. (Creator), Bertrand, S. (Creator), Burguera, D. (Creator), Acemel, R. (Creator), van Heeringen, S. (Creator), Naranjo, S. (Creator), Herrera-Ubeda, C. (Creator), Skvortsova, K. (Creator), Jimenez-Gancedo, S. (Creator), Aldea, D. (Creator), Marquez, Y. (Creator), Buono, L. (Creator), Kozmikova, I. (Creator), Permanyer, J. (Creator), Louis, A. (Creator), Albuixech-Crespo, B. (Creator), Le Petillon, Y. (Creator), Leon Florian, A. (Creator), Subirana, L. (Creator), Balwierz, P. J. (Creator), Duckett, P. (Creator), Farahani, E. (Creator), Aury, J. M. (Creator), Mangenot, S. (Creator), Wincker, P. (Creator), Albalat, R. (Creator), Benito-Gutierrez, E. (Creator), Canestro, C. (Creator), Castro, F. (Creator), D'Aniello, S. (Creator), Ferrier, D. E. K. (Creator), Huang, S. (Creator), Laudet, V. (Creator), Marais, G. (Creator), Pontarotti, P. (Creator), Schubert, M. (Creator), Seitz, H. (Creator), Somorjai, I. M. L. (Creator), Takahashi, T. (Creator), Mirabeau, O. (Creator), Xu, A. (Creator), Yu, J.-K. (Creator), Carninci, P. (Creator), Martinez-Morales, J. (Creator), Crollius, H. (Creator), Kozmik, Z. (Creator), Weirauch, M. (Creator), Garcia-Fernandez, J. (Creator), Lister, R. (Creator), Lenhard, B. (Creator), Holland, P. (Creator), Escriva, H. (Creator), Gomez-Skarmeta, J. L. (Creator) & Irimia, M. (Creator), Gene Expression Omnibus (GEO), 15 Aug 2018
http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106372 and 5 more links, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106428, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106429, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106430, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE102144, http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE115945 (show fewer)
Dataset
Amphioxus functional genomics and the origins of vertebrate gene regulation (Raw genome sequencing data)
Marletaz, F. (Creator), Firbas, P. (Creator), Maeso, I. (Creator), Tena, J. (Creator), Bogdanovic, O. (Creator), Perry, M. (Creator), Wyatt, C. (Creator), de la Calle-Mustienes, E. (Creator), Bertrand, S. (Creator), Burguera, D. (Creator), Acemel, R. (Creator), van Heeringen, S. (Creator), Naranjo, S. (Creator), Herrera-Ubeda, C. (Creator), Skvortsova, K. (Creator), Jimenez-Gancedo, S. (Creator), Aldea, D. (Creator), Marquez, Y. (Creator), Buono, L. (Creator), Kozmikova, I. (Creator), Permanyer, J. (Creator), Louis, A. (Creator), Albuixech-Crespo, B. (Creator), Le Petillon, Y. (Creator), Leon Florian, A. (Creator), Subirana, L. (Creator), Balwierz, P. J. (Creator), Duckett, P. (Creator), Farahani, E. (Creator), Aury, J. M. (Creator), Mangenot, S. (Creator), Wincker, P. (Creator), Albalat, R. (Creator), Benito-Gutierrez, E. (Creator), Canestro, C. (Creator), Castro, F. (Creator), D'Aniello, S. (Creator), Ferrier, D. E. K. (Creator), Huang, S. (Creator), Laudet, V. (Creator), Marais, G. (Creator), Pontarotti, P. (Creator), Schubert, M. (Creator), Seitz, H. (Creator), Somorjai, I. M. L. (Creator), Takahashi, T. (Creator), Mirabeau, O. (Creator), Xu, A. (Creator), Yu, J.-K. (Creator), Carninci, P. (Creator), Martinez-Morales, J. (Creator), Crollius, H. (Creator), Kozmik, Z. (Creator), Weirauch, M. (Creator), Garcia-Fernandez, J. (Creator), Lister, R. (Creator), Lenhard, B. (Creator), Holland, P. (Creator), Escriva, H. (Creator), Gomez-Skarmeta, J. L. (Creator) & Irimia, M. (Creator), European Nucleotide Archive (ENA), 2018
https://www.ebi.ac.uk/ena/data/search?query=PRJEB13665
Dataset

Cite this

Marletaz, F., Firbas, P., Maeso, I., Tena, J., Bogdanovic, O., Perry, M., Wyatt, C., de la Calle-Mustienes, E., Bertrand, S., Burguera, D., Acemel, R., van Heeringen, S., Naranjo, S., Herrera-Ubeda, C., Skvortsova, K., Jimenez-Gancedo, S., Aldea, D., Marquez, Y., Buono, L., ... Irimia, M. (2018). Amphioxus functional genomics and the origins of vertebrate gene regulation. Nature, 564(7734), 64-70. https://doi.org/10.1038/s41586-018-0734-6

@article{da3789bec51549c1a1db2a3fec7625e2,

title = "Amphioxus functional genomics and the origins of vertebrate gene regulation",

abstract = "Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.",

author = "Ferdinand Marletaz and Panos Firbas and Ignacio Maeso and Juan Tena and Ozren Bogdanovic and Malcolm Perry and Chris Wyatt and {de la Calle-Mustienes}, Elisa and Stephanie Bertrand and Demian Burguera and Rafael Acemel and {van Heeringen}, Simon and Silvia Naranjo and Carlos Herrera-Ubeda and Ksenia Skvortsova and Sandra Jimenez-Gancedo and Daniel Aldea and Yamile Marquez and Lorena Buono and Iryna Kozmikova and Jon Permanyer and Alexandra Louis and Beatriz Albuixech-Crespo and {Le Petillon}, Yann and {Leon Florian}, Anthony and Lucie Subirana and Balwierz, {Piotr J.} and Paul Duckett and Ensieh Farahani and Aury, {Jean Marc} and Sophie Mangenot and Patrick Wincker and Ricard Albalat and Elia Benito-Gutierrez and Cristian Canestro and Filipe Castro and Salvatore D'Aniello and Ferrier, {David Ellard Keith} and Shengfeng Huang and Vincent Laudet and Gabriel Marais and Pierre Pontarotti and Michael Schubert and Herve Seitz and Somorjai, {Ildiko Maureen Lara} and Tokiharu Takahashi and Olivier Mirabeau and Anlong Xu and Jr-Kai Yu and Piero Carninci and Juan Martinez-Morales and Hugues Crollius and Zbynek Kozmik and Matt Weirauch and Jordi Garcia-Fernandez and Ryan Lister and Boris Lenhard and Peter Holland and Hector Escriva and Gomez-Skarmeta, {Jose Luis} and Manuel Irimia",

note = "This research was funded primarily by the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Econom{\'i}a y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the {\textquoteleft}Centro de Excelencia Severo Ochoa 2013-2017{\textquoteright}(SEV-2012-0208), the {\textquoteleft}Unidad de Excelencia Mar{\'i}a de Maetzu 2017-2021{\textquoteright}(MDM-2016-0687), the People Program (Marie Curie Actions) of the European Union{\textquoteright}s Seventh Framework Program FP7 under REA grant agreement number 607142 (DevCom) to J.L.G.-S., and the CNRS and the ANR (ANR16-CE12-0008-01) to H.E. O.B. was supported by an Australian Research Council Discovery Early Career Researcher Award (DECRA; DE140101962). We acknowledge the support of the CERCA Programme/Generalitat de Catalunya and of the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership. Additional sources of funding for all authors are listed in Supplementary Information.",

year = "2018",

month = nov,

day = "21",

doi = "10.1038/s41586-018-0734-6",

language = "English",

volume = "564",

pages = "64--70",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature publishing group",

number = "7734",

}

Marletaz, F, Firbas, P, Maeso, I, Tena, J, Bogdanovic, O, Perry, M, Wyatt, C, de la Calle-Mustienes, E, Bertrand, S, Burguera, D, Acemel, R, van Heeringen, S, Naranjo, S, Herrera-Ubeda, C, Skvortsova, K, Jimenez-Gancedo, S, Aldea, D, Marquez, Y, Buono, L, Kozmikova, I, Permanyer, J, Louis, A, Albuixech-Crespo, B, Le Petillon, Y, Leon Florian, A, Subirana, L, Balwierz, PJ, Duckett, P, Farahani, E, Aury, JM, Mangenot, S, Wincker, P, Albalat, R, Benito-Gutierrez, E, Canestro, C, Castro, F, D'Aniello, S, Ferrier, DEK, Huang, S, Laudet, V, Marais, G, Pontarotti, P, Schubert, M, Seitz, H, Somorjai, IML, Takahashi, T, Mirabeau, O, Xu, A, Yu, J-K, Carninci, P, Martinez-Morales, J, Crollius, H, Kozmik, Z, Weirauch, M, Garcia-Fernandez, J, Lister, R, Lenhard, B, Holland, P, Escriva, H, Gomez-Skarmeta, JL & Irimia, M 2018, 'Amphioxus functional genomics and the origins of vertebrate gene regulation', Nature, vol. 564, no. 7734, pp. 64-70. https://doi.org/10.1038/s41586-018-0734-6

TY - JOUR

T1 - Amphioxus functional genomics and the origins of vertebrate gene regulation

AU - Marletaz, Ferdinand

AU - Firbas, Panos

AU - Maeso, Ignacio

AU - Tena, Juan

AU - Bogdanovic, Ozren

AU - Perry, Malcolm

AU - Wyatt, Chris

AU - de la Calle-Mustienes, Elisa

AU - Bertrand, Stephanie

AU - Burguera, Demian

AU - Acemel, Rafael

AU - van Heeringen, Simon

AU - Naranjo, Silvia

AU - Herrera-Ubeda, Carlos

AU - Skvortsova, Ksenia

AU - Jimenez-Gancedo, Sandra

AU - Aldea, Daniel

AU - Marquez, Yamile

AU - Buono, Lorena

AU - Kozmikova, Iryna

AU - Permanyer, Jon

AU - Louis, Alexandra

AU - Albuixech-Crespo, Beatriz

AU - Le Petillon, Yann

AU - Leon Florian, Anthony

AU - Subirana, Lucie

AU - Balwierz, Piotr J.

AU - Duckett, Paul

AU - Farahani, Ensieh

AU - Aury, Jean Marc

AU - Mangenot, Sophie

AU - Wincker, Patrick

AU - Albalat, Ricard

AU - Benito-Gutierrez, Elia

AU - Canestro, Cristian

AU - Castro, Filipe

AU - D'Aniello, Salvatore

AU - Ferrier, David Ellard Keith

AU - Huang, Shengfeng

AU - Laudet, Vincent

AU - Marais, Gabriel

AU - Pontarotti, Pierre

AU - Schubert, Michael

AU - Seitz, Herve

AU - Somorjai, Ildiko Maureen Lara

AU - Takahashi, Tokiharu

AU - Mirabeau, Olivier

AU - Xu, Anlong

AU - Yu, Jr-Kai

AU - Carninci, Piero

AU - Martinez-Morales, Juan

AU - Crollius, Hugues

AU - Kozmik, Zbynek

AU - Weirauch, Matt

AU - Garcia-Fernandez, Jordi

AU - Lister, Ryan

AU - Lenhard, Boris

AU - Holland, Peter

AU - Escriva, Hector

AU - Gomez-Skarmeta, Jose Luis

AU - Irimia, Manuel

N1 - This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016-0687), the People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program FP7 under REA grant agreement number 607142 (DevCom) to J.L.G.-S., and the CNRS and the ANR (ANR16-CE12-0008-01) to H.E. O.B. was supported by an Australian Research Council Discovery Early Career Researcher Award (DECRA; DE140101962). We acknowledge the support of the CERCA Programme/Generalitat de Catalunya and of the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership. Additional sources of funding for all authors are listed in Supplementary Information.

PY - 2018/11/21

Y1 - 2018/11/21

N2 - Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.

AB - Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.

U2 - 10.1038/s41586-018-0734-6

DO - 10.1038/s41586-018-0734-6

M3 - Article

SN - 0028-0836

VL - 564

SP - 64

EP - 70

JO - Nature

JF - Nature

IS - 7734

ER -

Amphioxus functional genomics and the origins of vertebrate gene regulation

Abstract

Access to Document

Fingerprint

Projects

ParaHox gene cluster: Determining major general regulatory mechanisms in the ParaHox gene cluster

CORBEL: H2020 INFRADEV4

Datasets

Amphioxus functional genomics and the origins of vertebrate gene regulation (next-generation sequencing data)

Amphioxus functional genomics and the origins of vertebrate gene regulation (Raw genome sequencing data)

Cite this