Functional evolution of clustered aquaporin genes reveals insights into the oceanic success of teleost eggs

Aquaporin-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...

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Autores: Ferré Baños, Alba, Chauvigné, François, Vlasova, Anna, Norberg, Birgitta, Bargelloni, Luca, Guigó Serra, Roderic, Finn, Roderick Nigel, Cerdà, Joan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/57156
Acceso en línea:http://hdl.handle.net/10230/57156
http://dx.doi.org/10.1093/molbev/msad071
Access Level:acceso abierto
Palabra clave:14-3-3 proteins
Aquaporin
Functional evolution
Oocyte hydration
Teleosts
Trafficking
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spelling Functional evolution of clustered aquaporin genes reveals insights into the oceanic success of teleost eggsFerré Baños, AlbaChauvigné, FrançoisVlasova, AnnaNorberg, BirgittaBargelloni, LucaGuigó Serra, RodericFinn, Roderick NigelCerdà, Joan14-3-3 proteinsAquaporinFunctional evolutionOocyte hydrationTeleostsTraffickingAquaporin-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 currents.This 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).Oxford University Press202320232023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/57156http://dx.doi.org/10.1093/molbev/msad071reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésMol Biol Evol. 2023 Apr 4;40(4):msad071info:eu-repo/grantAgreement/ES/1PE/AGL2016-76802-R© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.comhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/571562026-05-29T05:05:01Z
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 Baños, Alba
14-3-3 proteins
Aquaporin
Functional evolution
Oocyte hydration
Teleosts
Trafficking
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 Baños, Alba
Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó Serra, Roderic
Finn, Roderick Nigel
Cerdà, Joan
author Ferré Baños, Alba
author_facet Ferré Baños, Alba
Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó Serra, Roderic
Finn, Roderick Nigel
Cerdà, Joan
author_role author
author2 Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó Serra, Roderic
Finn, Roderick Nigel
Cerdà, Joan
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv 14-3-3 proteins
Aquaporin
Functional evolution
Oocyte hydration
Teleosts
Trafficking
topic 14-3-3 proteins
Aquaporin
Functional evolution
Oocyte hydration
Teleosts
Trafficking
description Aquaporin-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 currents.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/57156
http://dx.doi.org/10.1093/molbev/msad071
url http://hdl.handle.net/10230/57156
http://dx.doi.org/10.1093/molbev/msad071
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Mol Biol Evol. 2023 Apr 4;40(4):msad071
info:eu-repo/grantAgreement/ES/1PE/AGL2016-76802-R
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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