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Physiol. Genomics (May 24, 2005). doi:10.1152/physiolgenomics.00229.2004
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Submitted on October 4, 2004
Accepted on May 13, 2005

Comprehensive analysis of the ascidian genome reveals novel insights into the molecular evolution of ion channel genes

Yasushi Okamura1*, Atsuo Nishino2, Yoshimichi Murata3, Koichi Nakajo4, Hirohide Iwasaki3, Yukio Ohtsuka5, Motoko Tanaka-Kunishima6, Nobuyuki Takahashi4, Yuji Hara2, Takashi Yoshida2, Motohiro Nishida2, Haruo Okado7, Hirofumi Watari2, Ian A Meinertzhagen8, Nori Satoh9, Kunitaro Takahashi6, Yutaka Satou9, Yasunobu Okada10, and Yasuo Mori11

1 National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, Okazaki, Aichi, Japan; National Institutes of Natural Sciences, National Institute of Physiological Science, Okazaki, Aichi, Japan; Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki, Japan
2 National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, Okazaki, Aichi, Japan
3 National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, Okazaki, Aichi, Japan; National Institutes of Natural Sciences, National Institute of Physiological Science, Okazaki, Aichi, Japan
4 National Institutes of Natural Sciences, National Institute of Physiological Science, Okazaki, Aichi, Japan
5 Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki, Japan
6 Department of Medical Physiology, Meiji Pharmaceutical University, Kiyose, Tokyo, Japan
7 Department of Neurobiology, Tokyo Metropolitan Institute for Neuroscience, Fuchu, Tokyo, Japan
8 Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada
9 Department of Zoology, Kyoto University, Kyoto, Kyoto, Japan
10 National Institutes of Natural Sciences, National Institute of Physiological Science, Okazaki, Aichi, Japan; School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi, Japan
11 National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, Okazaki, Aichi, Japan; National Institutes of Natural Sciences, National Institute of Physiological Science, Okazaki, Aichi, Japan; School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi, Japan

* To whom correspondence should be addressed. E-mail: yokamura{at}nips.ac.jp.

Ion fluxes through membrane ion channels play crucial roles both in neuronal signaling and the homeostatic control of body electrolytes. In spite of our knowledge about the respective ion channels, just how diversification of ion channel genes underlies adaptation of animals to the physical environment remains unknown. Here we systematically survey up to 160 putative ion channel genes in the genome of Ciona intestinalis and compare them with corresponding gene sets from the genomes of the nematode Chaenorhabditis elegans, the fruit fly Drosophila melanogaster, and the more closely related genomes of vertebrates. Ciona has a set of so-called "prototype" genes for ion channels regulating neuronal excitability, or for neurotransmitter receptors, suggesting that genes responsible for neuronal signaling in mammals appear to have diversified mainly via gene duplications of the more restricted members of ancestral genomes prior to the ascidian/vertebrate divergence. Most genes responsible for modulation of neuronal excitability and pain sensation are absent from the ascidian genome, suggesting that these genes arose after the divergence of urochordates. In contrast, the divergent genes encoding connexins, TRP-related channels and chloride channels, channels involved rather in homeostatic control, indicate gene duplication events unique to the ascidian lineage. Since several invertebrate-unique channel genes exist in Ciona genome, the crown group of extant vertebrates not only acquired novel channel genes via gene/genome duplications, but also discarded some ancient genes that have persisted in invertebrates. Such genome-wide information of ion channel genes in basal chordates enables us to begin correlating the innovation and remodeling of genes with the adaptation of more recent chordates to their physical environment.




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