Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
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Author
Chauvigné, François
Vlasova, Anna
Norberg, Birgitta
Bargelloni, Luca
Guigó, Roderic
Publication date
2023-03-22ISSN
0737-4038
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.
Document Type
Article
Document version
Published version
Language
English
Subject (CDU)
637 - Produce of domestic (farmyard) animals and game
Pages
20
Publisher
Oxford University Press
Is part of
Molecular Biology and Evolution
Citation
Ferré, Alba, François Chauvigné, Anna Vlasova, Birgitta Norberg, Luca Bargelloni, Roderic Guigó, Roderick Nigel Finn, and Joan Cerdà. 2023. "Functional Evolution Of Clustered Aquaporin Genes Reveals Insights Into The Oceanic Success Of Teleost Eggs". Molecular Biology And Evolution 40 (4). doi:10.1093/molbev/msad071.
Grant agreement number
MINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORIN
FEDER/ / /EU/ /
MINECO/Programa Estatal de promoción del talento y su empleabilidad en I+D+I/RYC-2015-17103/ES/ /
Program
Aqüicultura
This item appears in the following Collection(s)
- ARTICLES CIENTÍFICS [2555]
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Except where otherwise noted, this item's license is described as http://creativecommons.org/licenses/by-nc/4.0/