Wnt evolution and function shuffling in liberal and conservative chordate genomes

Ildiko M. L. Somorjai; Josep Marti-Solans; Miriam Diaz-Gracia; Hiroki Nishida; Kaoru Imai; Hector Escriva; Cristian Cañestro; Ricard Albalat

doi:10.1186/s13059-018-1468-3

Wnt evolution and function shuffling in liberal and conservative chordate genomes

Ildiko M. L. Somorjai, Josep Marti-Solans, Miriam Diaz-Gracia, Hiroki Nishida, Kaoru Imai, Hector Escriva, Cristian Cañestro, Ricard Albalat

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

Abstract

Background: What impact gene loss has on the evolution of developmental processes, and how function shuffling has affected retained genes driving essential biological processes, remain open questions in the fields of genome evolution and EvoDevo. To investigate these problems, we have analyzed the evolution of the Wnt ligand repertoire in the chordate phylum as a case study.

Results: We conduct an exhaustive survey of Wnt genes in genomic databases, identifying 156 Wnt genes in 13 non-vertebrate chordates. This represents the most complete Wnt gene catalog of the chordate subphyla and has allowed us to resolve previous ambiguities about the orthology of many Wnt genes, including the identification of WntA for the first time in chordates. Moreover, we create the first complete expression atlas for the Wnt family during amphioxus development, providing a useful resource to investigate the evolution of Wnt expression throughout the radiation of chordates.

Conclusions: Our data underscore extraordinary genomic stasis in cephalochordates, which contrasts with the liberal and dynamic evolutionary patterns of gene loss and duplication in urochordate genomes. Our analysis has allowed us to infer ancestral Wnt functions shared among all chordates, several cases of function shuffling among Wnt paralogs, as well as unique expression domains for Wnt genes that likely reflect functional innovations in each chordate lineage. Finally, we propose a potential relationship between the evolution of WntA and the evolution of the mouth in chordates.

Original language	English
Article number	98
Number of pages	17
Journal	Genome Biology
Volume	19
DOIs	https://doi.org/10.1186/s13059-018-1468-3
Publication status	Published - 25 Jul 2018

Keywords

Wnt evolution
Genome stasis
Gene loss
Function shuffling
Chordate WntA
Ascidians
Vertebrates
Amphioxus

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10.1186/s13059-018-1468-3Licence: CC BY

Somorjai_2018_GB_Wntevolution_CC
© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Final published version, 6.01 MBLicence: CC BY

CORBEL: H2020 INFRADEV4
Ferrier, D. E. K. (PI) & Somorjai, I. M. L. (CoI)
European Commission
1/09/15 → 31/05/20
Project: Standard

Ildiko Maureen Lara Somorjai
- imlsst-andrews.acuk
Person: Academic

Wnt evolution and function shuffling in liberal and conservative chordate genomes
Somorjai, I. M. L. (Creator), Marti-Solans, J. (Creator), Diaz-Gracia, M. (Creator), Escriva, H. (Creator), Cañestro, C. (Creator), Nishida, H. (Creator), Imai, K. S. (Creator) & Albalat, R. (Creator), Figshare, 12 Jun 2018
DOI: 10.6084/m9.figshare.6477494.v1
Dataset

Cite this

@article{d076d71be38348a1b1f989f250231c19,

title = "Wnt evolution and function shuffling in liberal and conservative chordate genomes",

abstract = "Background: What impact gene loss has on the evolution of developmental processes, and how function shuffling has affected retained genes driving essential biological processes, remain open questions in the fields of genome evolution and EvoDevo. To investigate these problems, we have analyzed the evolution of the Wnt ligand repertoire in the chordate phylum as a case study.Results: We conduct an exhaustive survey of Wnt genes in genomic databases, identifying 156 Wnt genes in 13 non-vertebrate chordates. This represents the most complete Wnt gene catalog of the chordate subphyla and has allowed us to resolve previous ambiguities about the orthology of many Wnt genes, including the identification of WntA for the first time in chordates. Moreover, we create the first complete expression atlas for the Wnt family during amphioxus development, providing a useful resource to investigate the evolution of Wnt expression throughout the radiation of chordates. Conclusions: Our data underscore extraordinary genomic stasis in cephalochordates, which contrasts with the liberal and dynamic evolutionary patterns of gene loss and duplication in urochordate genomes. Our analysis has allowed us to infer ancestral Wnt functions shared among all chordates, several cases of function shuffling among Wnt paralogs, as well as unique expression domains for Wnt genes that likely reflect functional innovations in each chordate lineage. Finally, we propose a potential relationship between the evolution of WntA and the evolution of the mouth in chordates.",

keywords = "Wnt evolution, Genome stasis, Gene loss, Function shuffling, Chordate WntA, Ascidians, Vertebrates, Amphioxus",

author = "Somorjai, {Ildiko M. L.} and Josep Marti-Solans and Miriam Diaz-Gracia and Hiroki Nishida and Kaoru Imai and Hector Escriva and Cristian Ca{\~n}estro and Ricard Albalat",

note = "IS was supported by the European Union Horizon 2020 research and innovation programme under grant agreement numbers 654428 (“CORBEL”). HN was supported by Grants in Aid from The Japan Society for The Promotion of Science (22370078, 15H04377) and The Ministry of Education, Culture, Sports, Science and Thechnology, Japan (23112714, 25113518). KI was supported by a Grant in Aid from the Japan Society for the Promotion of Science (26711014). HE was supported by ANR-16-CE12-0008-01 grant from Agence Nationale de la Recherche. CC was supported by BFU2016-80601-P. RA was supported by BIO2015-67358-C2-1-P grant from Ministerio de Econom{\'i}a y Competitividad (Spain). CC and RA were also supported by grants BFU2010-14875 from Ministerio de Ciencia e Innovaci{\'o}n (Spain), and SGR2014-290 and SGR2017-1665 from Generalitat de Catalunya.",

year = "2018",

month = jul,

day = "25",

doi = "10.1186/s13059-018-1468-3",

language = "English",

volume = "19",

journal = "Genome Biology",

issn = "1474-760X",

publisher = "BioMed Central",

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TY - JOUR

T1 - Wnt evolution and function shuffling in liberal and conservative chordate genomes

AU - Somorjai, Ildiko M. L.

AU - Marti-Solans, Josep

AU - Diaz-Gracia, Miriam

AU - Nishida, Hiroki

AU - Imai, Kaoru

AU - Escriva, Hector

AU - Cañestro, Cristian

AU - Albalat, Ricard

N1 - IS was supported by the European Union Horizon 2020 research and innovation programme under grant agreement numbers 654428 (“CORBEL”). HN was supported by Grants in Aid from The Japan Society for The Promotion of Science (22370078, 15H04377) and The Ministry of Education, Culture, Sports, Science and Thechnology, Japan (23112714, 25113518). KI was supported by a Grant in Aid from the Japan Society for the Promotion of Science (26711014). HE was supported by ANR-16-CE12-0008-01 grant from Agence Nationale de la Recherche. CC was supported by BFU2016-80601-P. RA was supported by BIO2015-67358-C2-1-P grant from Ministerio de Economía y Competitividad (Spain). CC and RA were also supported by grants BFU2010-14875 from Ministerio de Ciencia e Innovación (Spain), and SGR2014-290 and SGR2017-1665 from Generalitat de Catalunya.

PY - 2018/7/25

Y1 - 2018/7/25

N2 - Background: What impact gene loss has on the evolution of developmental processes, and how function shuffling has affected retained genes driving essential biological processes, remain open questions in the fields of genome evolution and EvoDevo. To investigate these problems, we have analyzed the evolution of the Wnt ligand repertoire in the chordate phylum as a case study.Results: We conduct an exhaustive survey of Wnt genes in genomic databases, identifying 156 Wnt genes in 13 non-vertebrate chordates. This represents the most complete Wnt gene catalog of the chordate subphyla and has allowed us to resolve previous ambiguities about the orthology of many Wnt genes, including the identification of WntA for the first time in chordates. Moreover, we create the first complete expression atlas for the Wnt family during amphioxus development, providing a useful resource to investigate the evolution of Wnt expression throughout the radiation of chordates. Conclusions: Our data underscore extraordinary genomic stasis in cephalochordates, which contrasts with the liberal and dynamic evolutionary patterns of gene loss and duplication in urochordate genomes. Our analysis has allowed us to infer ancestral Wnt functions shared among all chordates, several cases of function shuffling among Wnt paralogs, as well as unique expression domains for Wnt genes that likely reflect functional innovations in each chordate lineage. Finally, we propose a potential relationship between the evolution of WntA and the evolution of the mouth in chordates.

AB - Background: What impact gene loss has on the evolution of developmental processes, and how function shuffling has affected retained genes driving essential biological processes, remain open questions in the fields of genome evolution and EvoDevo. To investigate these problems, we have analyzed the evolution of the Wnt ligand repertoire in the chordate phylum as a case study.Results: We conduct an exhaustive survey of Wnt genes in genomic databases, identifying 156 Wnt genes in 13 non-vertebrate chordates. This represents the most complete Wnt gene catalog of the chordate subphyla and has allowed us to resolve previous ambiguities about the orthology of many Wnt genes, including the identification of WntA for the first time in chordates. Moreover, we create the first complete expression atlas for the Wnt family during amphioxus development, providing a useful resource to investigate the evolution of Wnt expression throughout the radiation of chordates. Conclusions: Our data underscore extraordinary genomic stasis in cephalochordates, which contrasts with the liberal and dynamic evolutionary patterns of gene loss and duplication in urochordate genomes. Our analysis has allowed us to infer ancestral Wnt functions shared among all chordates, several cases of function shuffling among Wnt paralogs, as well as unique expression domains for Wnt genes that likely reflect functional innovations in each chordate lineage. Finally, we propose a potential relationship between the evolution of WntA and the evolution of the mouth in chordates.

KW - Wnt evolution

KW - Genome stasis

KW - Gene loss

KW - Function shuffling

KW - Chordate WntA

KW - Ascidians

KW - Vertebrates

KW - Amphioxus

U2 - 10.1186/s13059-018-1468-3

DO - 10.1186/s13059-018-1468-3

M3 - Article

SN - 1474-760X

VL - 19

JO - Genome Biology

JF - Genome Biology

M1 - 98

ER -

Wnt evolution and function shuffling in liberal and conservative chordate genomes

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Keywords

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Ildiko Maureen Lara Somorjai

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Wnt evolution and function shuffling in liberal and conservative chordate genomes

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