Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs

20 pages, 8 figures, supplementary material https://doi.org/10.1093/molbev/msad071.-- Data Availability: Data underlying this article are available in the article and in its online Supplementary material

Detalles Bibliográficos
Autores: Ferré, Alba, Chauvigné, François, Vlasova, Anna, Norberg, Birgitta, Bargelloni, Luca, Guigó, Roderic, Finn, Roderick N., Cerdà, Joan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/305824
Acceso en línea:http://hdl.handle.net/10261/305824
Access Level:acceso abierto
Palabra clave:Functional evolution
Teleosts
Aquaporin
Trafficking
14-3-3 proteins
Oocyte hydration
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
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spelling Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost EggsFerré, AlbaChauvigné, FrançoisVlasova, AnnaNorberg, BirgittaBargelloni, LucaGuigó, RodericFinn, Roderick N.Cerdà, JoanFunctional evolutionTeleostsAquaporinTrafficking14-3-3 proteinsOocyte hydrationhttp://metadata.un.org/sdg/14Conserve and sustainably use the oceans, seas and marine resources for sustainable development20 pages, 8 figures, supplementary material https://doi.org/10.1093/molbev/msad071.-- Data Availability: Data underlying this article are available in the article and in its online Supplementary materialAquaporin-mediated oocyte hydration is considered important for the evolution of pelagic eggs and the radiative success of marine teleosts. However, the molecular regulatory mechanisms controlling this vital process are not fully understood. Here, we analyzed >400 piscine genomes to uncover a previously unknown teleost-specific aquaporin-1 cluster (TSA1C) comprised of tandemly arranged aqp1aa-aqp1ab2-aqp1ab1 genes. Functional evolutionary analysis of the TSA1C reveals a ∼300-million-year history of downstream aqp1ab-type gene loss, neofunctionalization, and subfunctionalization, but with marine species that spawn highly hydrated pelagic eggs almost exclusively retaining at least one of the downstream paralogs. Unexpectedly, one-third of the modern marine euacanthomorph teleosts selectively retain both aqp1ab-type channels and co-evolved protein kinase-mediated phosphorylation sites in the intracellular subdomains together with teleost-specific Ywhaz-like (14-3-3ζ-like) binding proteins for co-operative membrane trafficking regulation. To understand the selective evolutionary advantages of these mechanisms, we show that a two-step regulated channel shunt avoids competitive occupancy of the same plasma membrane space in the oocyte and accelerates hydration. These data suggest that the evolution of the adaptive molecular regulatory features of the TSA1C facilitated the rise of pelagic eggs and their subsequent geodispersal in the oceanic currentsThis work was supported by the Spanish Ministry of Science and Innovation (MCIN/AEI/10.13039/501100011033), the European Regional Development Fund (ERDF) “A way of making Europe” (European Union), Grant no. AGL2016-76802-R (to J.C.), and the Norwegian Research Council (RCN) Grant no. 294768/E40 (to R.N.F). F.C. and A.F. were supported, respectively, by the “Ramon y Cajal” programe (RYC-2015-17103) and a predoctoral (BES-2014-068745) contract from Spanish MCIN. R.N.F. was also supported by the University of Bergen (Norway)With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewedOxford University PressMinisterio de Ciencia, Innovación y Universidades (España)European CommissionMinisterio de Economía y Competitividad (España)Norwegian Research CouncilUniversity of BergenAgencia Estatal de Investigación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/305824reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI//AGL2016-76802-Rinfo:eu-repo/grantAgreement/MINECO//RYC-2015-17103https://doi.org/10.1093/molbev/msad071Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3058242026-05-22T06:33:51Z
dc.title.none.fl_str_mv Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
title Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
spellingShingle Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
Ferré, Alba
Functional evolution
Teleosts
Aquaporin
Trafficking
14-3-3 proteins
Oocyte hydration
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
title_short Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
title_full Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
title_fullStr Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
title_full_unstemmed Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
title_sort Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
dc.creator.none.fl_str_mv Ferré, Alba
Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó, Roderic
Finn, Roderick N.
Cerdà, Joan
author Ferré, Alba
author_facet Ferré, Alba
Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó, Roderic
Finn, Roderick N.
Cerdà, Joan
author_role author
author2 Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó, Roderic
Finn, Roderick N.
Cerdà, Joan
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
European Commission
Ministerio de Economía y Competitividad (España)
Norwegian Research Council
University of Bergen
Agencia Estatal de Investigación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Functional evolution
Teleosts
Aquaporin
Trafficking
14-3-3 proteins
Oocyte hydration
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
topic Functional evolution
Teleosts
Aquaporin
Trafficking
14-3-3 proteins
Oocyte hydration
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
description 20 pages, 8 figures, supplementary material https://doi.org/10.1093/molbev/msad071.-- Data Availability: Data underlying this article are available in the article and in its online Supplementary material
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/305824
url http://hdl.handle.net/10261/305824
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI//AGL2016-76802-R
info:eu-repo/grantAgreement/MINECO//RYC-2015-17103
https://doi.org/10.1093/molbev/msad071
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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