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Flexible selection of diversified Na(+)/K(+)-ATPase ?-subunit isoforms for osmoregulation in teleosts.

ABSTRACT: BACKGROUND AND METHODS:Multiple Na+/K+-ATPase (NKA) ?-subunit isoforms express differentially in response to salinity transfer in teleosts but we observed that the isoform nomenclature is inconsistent with the phylogenetic relationship of NKA ?-genes. We cloned the catalytic NKA ?-subunit isoforms in eels and medaka, analyzed the time course of their expressions in osmoregulatory tissues after transfer from freshwater (FW) to seawater (SW), and performed phylogenetic analyses to deduce an evolutionary scenario that illustrates how various duplication events have led to the current genomic arrangement of NKA ?-genes in teleosts. RESULTS AND DISCUSSION:Five and six ?-subunits were cloned in eels and medaka respectively. In eels, the commonly-reported ?1a and ?1b isoforms were absent while the ?1c isoform was diversified instead (?1c-1, ?1c-2, ?1c-3, ?2, and ?3 in eels). Phylogenetic estimation indicated that the ?1a and ?1b isoforms from salmon, tilapia, and medaka were generated by independent duplication events and thus they are paralogous isoforms. Re-examination of expression changes of known isoforms after salinity challenge revealed that the isoforms selected as predominant SW-types varied among teleost lineages. Diversification of ?1 isoforms occurred by various types of gene duplication, or by alternative transcription among tandem genes to form chimeric transcripts, but there is no trend for more ?1 copies in euryhaline species. Our data suggest that the isoform switching between FW (?1a predominates) and SW (?1b predominates) that occurs in salmonids is not universal in teleosts. Instead, in eels, ?1c-1 was the major ?-subunit upregulated gill, intestine, and kidney in SW. Localization of both NKA mRNA and protein showed consistent upregulation in gill and intestine in SW eels, but not in renal distal and collecting tubules, where low transcript expression levels were accompanied by high protein levels, suggesting a tissue-specific translational regulation that determines and fine-tunes the NKA expression. In medaka, ?1b was upregulated in SW in anterior intestine while most other ?-subunit isoforms were less responsive to salinity changes. CONCLUSION:By integrating gene expression and phylogenetic results, we propose that the major NKA ?-subunits for SW acclimation were not ancestrally selected, but rather were flexibly determined in lineage-specific fashion in teleosts.

SUBMITTER: Wong MK

PROVIDER: S-EPMC4971688 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Flexible selection of diversified Na(+)/K(+)-ATPase α-subunit isoforms for osmoregulation in teleosts.

Wong Marty Kwok-Shing MK Pipil Supriya S Ozaki Haruka H Suzuki Yutaka Y Iwasaki Wataru W Takei Yoshio Y

Zoological letters 20160803

<h4>Background and methods</h4>Multiple Na+/K+-ATPase (NKA) α-subunit isoforms express differentially in response to salinity transfer in teleosts but we observed that the isoform nomenclature is inconsistent with the phylogenetic relationship of NKA α-genes. We cloned the catalytic NKA α-subunit isoforms in eels and medaka, analyzed the time course of their expressions in osmoregulatory tissues after transfer from freshwater (FW) to seawater (SW), and performed phylogenetic analyses to deduce a ...[more]

PMID: 27489726

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Project description:BackgroundNa,K-ATPase is a key protein in maintaining membrane potential that has numerous additional cellular functions. Its catalytic subunit (α), found in a wide range of organisms from prokaryotes to complex eukaryote. Several studies have been done to identify the functions as well as determining the evolutionary relationships of the α-subunit. However, a survey of a larger collection of protein sequences according to sequences similarity and their attributes is very important in revealing deeper evolutionary relationships and identifying specific amino acid differences among evolutionary groups that may have a functional role.ResultsIn this study, 753 protein sequences using phylogenetic tree classification resulted in four groups: prokaryotes (I), fungi and various kinds of Protista and some invertebrates (II), the main group of invertebrates (III), and vertebrates (IV) that was consisted with species tree. The percent of sequences that acquired a specific motif for the α/β subunit assembly increased from group I to group IV. The vertebrate sequences were divided into four groups according to isoforms with each group conforming to the evolutionary path of vertebrates from fish to tetrapods. Data mining was used to identify the most effective attributes in classification of sequences. Using 1252 attributes extracted from the sequences, the decision tree classified them in five groups: Protista, prokaryotes, fungi, invertebrates and vertebrates. Also, vertebrates were divided into four subgroups (isoforms). Generally, the count of different dipeptides and amino acid ratios were the most significant attributes for grouping. Using alignment of sequences identified the effective position of the respective dipeptides in the separation of the groups. So that 208GC is apparently involved in the separation of vertebrates from the four other organism groups, and 41DH, 431FK, and 451KC were involved in separation vertebrate isoform types.ConclusionThe application of phylogenetic and decision tree analysis for Na,K-ATPase, provides a better understanding of the evolutionary changes according to the amino acid sequence and its related properties that could lead to the identification of effective attributes in the separation of sequences in different groups of phylogenetic tree. In this study, key evolution-related dipeptides are identified which can guide future experimental studies.

Dataset Information

Flexible selection of diversified Na(+)/K(+)-ATPase ?-subunit isoforms for osmoregulation in teleosts.

Publications

Flexible selection of diversified Na(+)/K(+)-ATPase α-subunit isoforms for osmoregulation in teleosts.

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