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

Abstract

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.

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

“…To determine the molecular basis for neuromuscular transmission, we characterized the nAChR subunits expressed in the larval muscle. In an earlier (13) and subsequent surveys of the Ciona genome, we identified 10 nAChR subunit genes and a rapsyn homolog gene ( Fig. 2A, Fig.…”

“…These cholinergic neurons project axons down the tail and innervate a part of the (mainly dorsal) muscle cells, whereas others receive excitation via gap junctions (8-11). Despite such knowledge, how the Ciona larva swims like fish using such simplified motor units remains unknown.Recent research on the Ciona genome provides an opportunity to examine the molecular mechanisms underlying the physiology of this animal (12,13). Given the correspondence between the body plans yet nevertheless the extreme contrast between their body complexities (minimal ascidian larva vs. much larger vertebrates), detailed comparison of their apparently similar swimming dynamics could uncover some novel control mechanisms.…”

“…Recent research on the Ciona genome provides an opportunity to examine the molecular mechanisms underlying the physiology of this animal (12,13). Given the correspondence between the body plans yet nevertheless the extreme contrast between their body complexities (minimal ascidian larva vs. much larger vertebrates), detailed comparison of their apparently similar swimming dynamics could uncover some novel control mechanisms.…”

Genomic Organization of Purinergic P2X Receptors

“…Several lines of evidence have suggested that whole genome duplications occurred before the vertebrate/ascidian divergence [39] and, later on, in the lineage of teleostheus after tetrapod divergence where only one set of these duplicated genes were maintained [40]- [43]. This is supported by the existence of several duplicated segments in zebrafish chromosomes [44].…”

AMPA glutamate receptors are required for sensory-organ formation and morphogenesis in the basal chordate

“…Here, we instead used the ascidian chordate Ciona intestinalis, the closest living relative to vertebrates (16), which is thought to have just a single gluA gene (17). Ciona larvae are transparent, enabling easy identification of cells expressing a target gene and detection of morphological phenotypes in the tissues and organs.…”