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Evolutionary implication of the absence of atrial natriuretic peptide (ANP) in euryhaline Oryzias fishes

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Abstract

The genus Oryzias contains nearly 20 species, including the Japanese medaka (Oryzias latipes). Because each species exhibits different adaptability to environmental salinity, Oryzias fishes offer unique opportunities for comparative studies. To understand the mechanisms of osmotic adaptation, we are studying the functional evolution of the natriuretic peptide (NP) family—a group of small peptide hormones involved in body fluid regulation—by using Oryzias fishes. Analysis of the Japanese medaka genome revealed that 7 NP subtypes, namely, Atrial NP (ANP), B-type NP (BNP), Ventricular NP (VNP), and 4 C-type NPs (CNP-1 through CNP-4) were generated from a CNP-4-like ancestral gene discovered in the cyclostomes before the ray-finned fish/lobe-finned fish divergence. This evolutionary history has been confirmed by the discovery of hidden NP genes in tetrapods. Through analyses of phylogenetic distribution of NP subtypes, we also found that specific losses of subtypes have occurred in each vertebrate lineage. For example, ANP is absent in the Japanese and Indian medaka and the flying fish, suggesting that loss of the ANP gene occurred after the divergence of Beloniformes from Cyprinodontiformes. This fact also supports the inclusion of Oryzias into Beloniformes as suggested by phylogenetic analysis using whole mitochondrial genome sequences. How Oryzias fishes have retained their euryhalinity with a reduced number of NPs is an interesting question. CNP-3, which is functionally flexible, may be a substitute for the lost cardiac NPs.

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Acknowledgements

The authors thanks Yoshitaka Kondo, Yoshiaki Maeda, Akihisa Ohsawa of Kamogawa Sea World for providing us with the flying fish specimen, and Masahiro Aizawa of Coastal Branch of Natural History Museum and Institute, Chiba for identification of the flying fish.

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  1. Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwanoha, Kashiwa, 277–8564, Japan

    Koji Inoue, Hiroshi Miyanishi, Shigenori Nobata & Yoshio Takei

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  1. Koji Inoue
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  2. Hiroshi Miyanishi
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  3. Shigenori Nobata
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  4. Yoshio Takei
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Correspondence to Koji Inoue.

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Inoue, K., Miyanishi, H., Nobata, S. et al. Evolutionary implication of the absence of atrial natriuretic peptide (ANP) in euryhaline Oryzias fishes. Environ Biol Fish 94, 559–566 (2012). https://doi.org/10.1007/s10641-011-9852-9

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