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Evidence of Positive Selection of Aquaporins Genes from Pontoporia blainvillei during the Evolutionary Process of Cetaceans.

São Pedro SL, Alves JM, Barreto AS, Lima AO - PLoS ONE (2015)

Bottom Line: Marine mammals are well adapted to their hyperosmotic environment.Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance.Many genes have been identified to be involved in osmotic regulation, including the aquaporins.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Genética Molecular, Centro de Ciências Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí, Itajaí, SC, Brazil.

ABSTRACT

Background: Marine mammals are well adapted to their hyperosmotic environment. Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance. However, most previous studies have focused on the unique renal physiology of marine mammals, but the molecular bases of these mechanisms remain poorly explored. Many genes have been identified to be involved in osmotic regulation, including the aquaporins. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals.

Results: Our results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2 (amino acids 23, 83, 107,179, 180, 181, 182), whereas no selection was observed in terrestrial mammalian lineages. We also analyzed the changes in the 3D structure of the aquaporin 2 protein. Signs of strong positive selection in AQP2 sites 179, 180, 181, and 182 were unexpectedly identified only in the baiji lineage, which was the only river dolphin examined in this study. Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater.

Conclusions: Our results suggest that the AQP2 gene might reflect different selective pressures in maintaining water balance in cetaceans, contributing to the passage from the terrestrial environment to the aquatic. Further studies are necessary, especially those including other freshwater dolphins, who exhibit osmoregulatory mechanisms different from those of marine cetaceans for the same essential task of maintaining serum electrolyte balance.

No MeSH data available.


Partial alignment of mammalian AQP2 amino acid sequences.Dots represent residues that are identical to those on the first row of the alignment. A) Alignment showing amino acid substitutions in sites 23 (Leu → Val, Iso), 83 (Val → Iso), and 107 (Ser → His), occurring exclusively in the cetacean lineage. B) Alignment of sites 179, 180, 181, and 182 showing differences only in cetacean Lipotes vexiliffer, the only freshwater dolphin in our sample.
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pone.0134516.g002: Partial alignment of mammalian AQP2 amino acid sequences.Dots represent residues that are identical to those on the first row of the alignment. A) Alignment showing amino acid substitutions in sites 23 (Leu → Val, Iso), 83 (Val → Iso), and 107 (Ser → His), occurring exclusively in the cetacean lineage. B) Alignment of sites 179, 180, 181, and 182 showing differences only in cetacean Lipotes vexiliffer, the only freshwater dolphin in our sample.

Mentions: The branch site model was used to detect positive selection in a small number of sites that are sometimes hard to detect by the site model. The branch site constrained ω to be the same in the whole cetacean clade (ω1) and different for the rest of the mammals (ω0), using the LRT analysis. The selection analysis using the branch sites model suggested several positively selective sites, with seven identified in AQP2 (sites 23, 83, 107, 179, 180, 181, 182), five in AQP3 (20, 36, 103, 248, 256), one in AQP6 (27), and one in AQP9 (97) (Fig 2). These sites were detected only by this method, with overall probabilities greater than 0.9 using the Bayes empirical Bayes (BEB) test. However, the selection analysis using the branch site model showed that only one gene, namely AQP2, was subjected to strong positive selection exclusively in cetacean-specific lineages, whereas no selection was observed in terrestrial mammalian lineages.


Evidence of Positive Selection of Aquaporins Genes from Pontoporia blainvillei during the Evolutionary Process of Cetaceans.

São Pedro SL, Alves JM, Barreto AS, Lima AO - PLoS ONE (2015)

Partial alignment of mammalian AQP2 amino acid sequences.Dots represent residues that are identical to those on the first row of the alignment. A) Alignment showing amino acid substitutions in sites 23 (Leu → Val, Iso), 83 (Val → Iso), and 107 (Ser → His), occurring exclusively in the cetacean lineage. B) Alignment of sites 179, 180, 181, and 182 showing differences only in cetacean Lipotes vexiliffer, the only freshwater dolphin in our sample.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4520692&req=5

pone.0134516.g002: Partial alignment of mammalian AQP2 amino acid sequences.Dots represent residues that are identical to those on the first row of the alignment. A) Alignment showing amino acid substitutions in sites 23 (Leu → Val, Iso), 83 (Val → Iso), and 107 (Ser → His), occurring exclusively in the cetacean lineage. B) Alignment of sites 179, 180, 181, and 182 showing differences only in cetacean Lipotes vexiliffer, the only freshwater dolphin in our sample.
Mentions: The branch site model was used to detect positive selection in a small number of sites that are sometimes hard to detect by the site model. The branch site constrained ω to be the same in the whole cetacean clade (ω1) and different for the rest of the mammals (ω0), using the LRT analysis. The selection analysis using the branch sites model suggested several positively selective sites, with seven identified in AQP2 (sites 23, 83, 107, 179, 180, 181, 182), five in AQP3 (20, 36, 103, 248, 256), one in AQP6 (27), and one in AQP9 (97) (Fig 2). These sites were detected only by this method, with overall probabilities greater than 0.9 using the Bayes empirical Bayes (BEB) test. However, the selection analysis using the branch site model showed that only one gene, namely AQP2, was subjected to strong positive selection exclusively in cetacean-specific lineages, whereas no selection was observed in terrestrial mammalian lineages.

Bottom Line: Marine mammals are well adapted to their hyperosmotic environment.Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance.Many genes have been identified to be involved in osmotic regulation, including the aquaporins.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Genética Molecular, Centro de Ciências Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí, Itajaí, SC, Brazil.

ABSTRACT

Background: Marine mammals are well adapted to their hyperosmotic environment. Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance. However, most previous studies have focused on the unique renal physiology of marine mammals, but the molecular bases of these mechanisms remain poorly explored. Many genes have been identified to be involved in osmotic regulation, including the aquaporins. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals.

Results: Our results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2 (amino acids 23, 83, 107,179, 180, 181, 182), whereas no selection was observed in terrestrial mammalian lineages. We also analyzed the changes in the 3D structure of the aquaporin 2 protein. Signs of strong positive selection in AQP2 sites 179, 180, 181, and 182 were unexpectedly identified only in the baiji lineage, which was the only river dolphin examined in this study. Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater.

Conclusions: Our results suggest that the AQP2 gene might reflect different selective pressures in maintaining water balance in cetaceans, contributing to the passage from the terrestrial environment to the aquatic. Further studies are necessary, especially those including other freshwater dolphins, who exhibit osmoregulatory mechanisms different from those of marine cetaceans for the same essential task of maintaining serum electrolyte balance.

No MeSH data available.