ZFIN ID: ZDB-PUB-110613-30
Dual neofunctionalization of a rapidly evolving aquaporin-1 paralog resulted in constrained and relaxed traits controlling channel function during meiosis resumption in teleosts
Zapater, C., Chauvigné, F., Norberg, B., Finn, R.N., and Cerdà, J.
Date: 2011
Source: Mol. Biol. Evol.   28(11): 3151-69 (Journal)
Registered Authors: Cerdà, Joan
Keywords: aquaporin, oocyte, meiosis, hydration, yolk, neofunctionalization
MeSH Terms:
  • Analysis of Variance
  • Animals
  • Aquaporin 1/genetics*
  • Aquaporin 1/physiology
  • Base Sequence
  • Bayes Theorem
  • Biological Transport/genetics
  • Biological Transport/physiology
  • Cloning, Molecular
  • DNA Primers/genetics
  • Electrophoresis, Polyacrylamide Gel
  • Evolution, Molecular*
  • Flounder/genetics*
  • Flounder/physiology
  • Genes, Duplicate/genetics*
  • Genes, Duplicate/physiology
  • Immunoblotting
  • Meiosis/physiology*
  • Microscopy, Fluorescence
  • Microscopy, Immunoelectron
  • Models, Genetic
  • Molecular Sequence Data
  • Norway
  • Oocytes/physiology*
  • Phylogeny
  • Real-Time Polymerase Chain Reaction
  • Regulatory Elements, Transcriptional/genetics
  • Sequence Analysis, DNA
  • Synteny/genetics
  • Xenopus laevis
  • Zebrafish
PubMed: 21653921 Full text @ Mol. Biol. Evol.
ABSTRACT
The pre-ovulatory hydration of marine teleost oocytes is a unique process among vertebrates. The hydration mechanism is most pronounced in modern acanthomorph teleosts that spawn pelagic (floating) eggs, however the molecular pathway for water influx remains poorly understood. Recently, we revealed that whole genome duplication (WGD) resulted in teleosts harbouring the largest repertoire of molecular water channels in the vertebrate lineage, and that a duplicated aquaporin-1 paralog is implicated in the oocyte hydration process. However, the origin and function of the aquaporin-1 paralogs remains equivocal. By integrating the molecular phylogeny with synteny and structural analyses we show here that the teleost aqp1aa and -1ab paralogs (previously annotated as aqp1a and -1b, respectively) arose by tandem duplication rather than WGD, and that the Aqp1ab C-terminus is the most rapidly evolving subdomain within the vertebrate aquaporin superfamily. The functional role of Aqp1ab was investigated in Atlantic halibut, a marine acanthomorph teleost that spawns one of the largest pelagic eggs known. We demonstrate that Aqp1ab is required for full hydration of oocytes undergoing meiotic maturation. We further show that the rapid structural divergence of the C-terminal regulatory domain causes ex vivo loss of function of halibut Aqp1ab when expressed in amphibian oocytes, but not in zebrafish or native oocytes. However, by using chimeric constructs of halibut Aqp1aa and -1ab, and antisera specifically raised against the C-terminus of Aqp1ab, we found that this cytoplasmic domain regulates in vivo trafficking to the microvillar portion of the oocyte plasma membrane when intra-oocytic osmotic pressure is at a maximum. Interestingly, by co-injecting polyA(+) mRNA from post-vitellogenic halibut follicles, ex vivo intracellular trafficking of Aqp1ab is rescued in amphibian oocytes. These data reveal that the physiological role of Aqp1ab during meiosis resumption is conserved in teleosts, but the remarkable degeneracy of the cytoplasmic domain has resulted in alternative regulation of the trafficking mechanism.
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