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

• Published in: Physiological genomics Vol. 22; no. 3; pp. 269 - 282
• Main Authors: Okamura, Yasushi, Nishino, Atsuo, Murata, Yoshimichi, Nakajo, Koichi, Iwasaki, Hirohide, Ohtsuka, Yukio, Tanaka-Kunishima, Motoko, Takahashi, Nobuyuki, Hara, Yuji, Yoshida, Takashi, Nishida, Motohiro, Okado, Haruo, Watari, Hirofumi, Meinertzhagen, Ian A, Satoh, Nori, Takahashi, Kunitaro, Satou, Yutaka, Okada, Yasunobu, Mori, Yasuo
• Format: Journal Article
• Language: English
• Published: United States Am Physiological Soc 11.08.2005
• Subjects: Animals; Caenorhabditis elegans; Chordata; Ciona intestinalis; Databases, Genetic; Drosophila melanogaster; Drosophila melanogaster - metabolism; Electrolytes; Evolution, Molecular; Gap Junctions; Gene Expression Regulation, Developmental; Genome; Genomics; Humans; Ion Channels - metabolism; Ions - chemistry; Ions - metabolism; Models, Biological; Models, Genetic; Nematoda; Phylogeny; Potassium Channels - chemistry; Receptors, Glutamate - metabolism; Receptors, Nicotinic - metabolism; Ryanodine Receptor Calcium Release Channel - metabolism; Urochordata; Water - chemistry
• DOI: 10.1152/physiolgenomics.00229.2004
• ISSN: 1094-8341

1 Section of Developmental Neurophysiology, Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Okazaki, Aichi 2 National Institutes for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Aichi 3 Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 4 Department of Medical Physiology, Meiji Pharmaceutical University, Kiyose, Tokyo, Japan 5 Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada 6 Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 7 Department of Neurobiology, Tokyo Metropolitan Institute for Neuroscience, Fuchu, Tokyo 8 School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi, Japan Ion fluxes through membrane ion channels play crucial roles both in neuronal signaling and the homeostatic control of body electrolytes. Despite 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 before 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, transient receptor potential-related channels and chloride channels, channels involved rather in homeostatic control, indicate gene duplication events unique to the ascidian lineage. Because 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. ascidian; homeostasis; embryogenesis