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

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• dc.contributor.author Ferré Baños, Alba
• dc.contributor.author Chauvigné, François
• dc.contributor.author Vlasova, Anna
• dc.contributor.author Norberg, Birgitta
• dc.contributor.author Bargelloni, Luca
• dc.contributor.author Guigó Serra, Roderic
• dc.contributor.author Finn, Roderick Nigel
• dc.contributor.author Cerdà, Joan
• dc.date.accessioned 2023-06-12T06:32:25Z
• dc.date.available 2023-06-12T06:32:25Z
• dc.date.issued 2023
• dc.description.abstract 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.
• dc.description.sponsorship 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).
• dc.format.mimetype application/pdf
• dc.identifier.citation Ferré A, Chauvigné F, Vlasova A, Norberg B, Bargelloni L, Guigó R, Finn RN, Cerdà J. Functional evolution of clustered aquaporin genes reveals insights into the oceanic success of teleost eggs. Mol Biol Evol. 2023 Apr 4;40(4):msad071. DOI: 10.1093/molbev/msad071
• dc.identifier.doi http://dx.doi.org/10.1093/molbev/msad071
• dc.identifier.issn 0737-4038
• dc.identifier.uri http://hdl.handle.net/10230/57156
• dc.language.iso eng
• dc.publisher Oxford University Press
• dc.relation.ispartof Mol Biol Evol. 2023 Apr 4;40(4):msad071
• dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/AGL2016-76802-R
• dc.rights © 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.com
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by-nc/4.0/
• dc.subject.keyword 14-3-3 proteins
• dc.subject.keyword Aquaporin
• dc.subject.keyword Functional evolution
• dc.subject.keyword Oocyte hydration
• dc.subject.keyword Teleosts
• dc.subject.keyword Trafficking
• dc.title Functional evolution of clustered aquaporin genes reveals insights into the oceanic success of teleost eggs
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion