Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs
Ferré, Alba (Universitat Autònoma de Barcelona. Institut de Biotecnologia i de Biomedicina "Vicent Villar Palasí")
Chauvigné, François (Instituto de Ciencias del Mar - CSIC)
Vlasova, Anna (Institut de Ciència i Tecnologia de Barcelona. Institut de Recerca en Biomedicina)
Norberg, Birgitta (Austevoll Research Station. Institute of Marine Research)
Bargelloni, Luca (Università di Padova. Dipartimento di Biomedicina Comparata e Scienza dell'Alimentazione)
Guigó, Roderic (Institut de Ciència i Tecnologia de Barcelona. Institut de Recerca en Biomedicina)
Finn, Roderick Nigel (Universitat Autònoma de Barcelona. Institut de Biotecnologia i de Biomedicina "Vicent Villar Palasí")
Cerdà, Joan (Universitat Autònoma de Barcelona. Institut de Biotecnologia i de Biomedicina "Vicent Villar Palasí")

Date:	2023
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.
Grants:	Ministerio de Ciencia e Innovación AGL2016-76802-R Ministerio de Economía y Competitividad RYC-2015-17103 Ministerio de Economía y Competitividad BES-2014-068745
Rights:	Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original.
Language:	Anglès
Document:	Article ; recerca ; Versió publicada
Subject:	Functional evolution ; Teleosts ; Aquaporin ; Trafficking ; 14-3-3 proteins ; Oocyte hydration
Published in:	Molecular biology and evolution, Vol. 40, Issue 4 (April 2023) , art. msad071, ISSN 1537-1719

DOI: 10.1093/molbev/msad071
PMID: 36947084

20 p, 2.5 MB

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Research literature > UAB research groups literature > Research Centres and Groups (research output) > Health sciences and biosciences > Institut de Biotecnologia i de Biomedicina (IBB)
Articles > Research articles
Articles > Published articles