Structural and functional divergence of two fish aquaporin-1 water channels following teleost-specific gene duplication.
BACKGROUND
Teleost radiation in the oceans required specific physiological adaptations in eggs and early embryos to survive in the hyper-osmotic seawater. Investigating the evolution of aquaporins (AQPs) in these vertebrates should help to elucidate how mechanisms for water homeostasis evolved. The marine teleost gilthead sea bream (Sparus aurata) has a mammalian aquaporin-1 (AQP1)-related channel, termed AQP1o, with a specialized physiological role in mediating egg hydration. However, teleosts have an additional AQP isoform structurally more similar to AQP1, though its relationship with AQP1o is unclear.


RESULTS
By using phylogenetic and genomic analyses we show here that teleosts, unlike tetrapods, have two closely linked AQP1 paralogous genes, termed aqp1a and aqp1b (formerly AQP1o). In marine teleosts that produce hydrated eggs, aqp1b is highly expressed in the ovary, whereas in freshwater species that produce non-hydrated eggs, aqp1b has a completely different expression pattern or is not found in the genome. Both Aqp1a and Aqp1b are functional water-selective channels when expressed in Xenopus laevis oocytes. However, expression of chimeric and mutated proteins in oocytes revealed that the sea bream Aqp1b C-terminus, unlike that of Aqp1a, contains specific residues involved in the control of Aqp1b intracellular trafficking through phosphorylation-independent and -dependent mechanisms.


CONCLUSIONS
We propose that 1) Aqp1a and Aqp1b are encoded by distinct genes that probably originated specifically in the teleost lineage by duplication of a common ancestor soon after divergence from tetrapods, 2) Aqp1b possibly represents a neofunctionalized AQP adapted to oocytes of marine and catadromous teleosts, thereby contributing to a water reservoir in eggs and early embryos that increases their survival in the ocean, and 3) Aqp1b independently acquired regulatory domains in the cytoplasmatic C-terminal tail for the specific control of Aqp1b expression in the plasma membrane.
Tingaud-Sequeira
Angèle
A
Laboratory of Institut de Recerca i Tecnologia Agroalimentàries-Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas, 08003 Barcelona, Spain. angela.tingaud@u-bordeaux1.fr
Chauvigné
François
F
Fabra
Mercedes
M
Lozano
Juanjo
J
Raldúa
Demetrio
D
Cerdà
Joan
J
D000595:Amino Acid Sequence; D000818:Animals; D051398:Aquaporin 1 / Q000235:genetics*; D001499:Bayes Theorem; D003001:Cloning, Molecular; D018076:DNA, Complementary / Q000235:genetics; D019143:Evolution, Molecular; D005260:Female; D029941:Fish Proteins / Q000235:genetics*; D020440:Gene Duplication; D023281:Genomics; D006801:Humans; D016013:Likelihood Functions; D008969:Molecular Sequence Data; D009865:Oocytes / Q000502:physiology; D010802:Phylogeny; D021541:Sea Bream / Q000235:genetics*; D016415:Sequence Alignment; D020539:Sequence Analysis, Protein
D018076:DNA, Complementary; D029941:Fish Proteins; D051398:Aquaporin 1