title: The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa.
abstract: Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria.
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Germany.
authors.forename: Andreas
authors.initials: A
authors.lastname: Schüler
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Germany.
authors.forename: Gregor
authors.initials: G
authors.lastname: Schmitz
authors.affiliation: Centre for Organismal Studies, University of Heidelberg, Germany.
authors.forename: Abigail
authors.initials: A
authors.lastname: Reft
authors.affiliation: Centre for Organismal Studies, University of Heidelberg, Germany HEIKA-Heidelberg Karlsruhe Research Partnership, Heidelberg University, Karlsruhe Institute of Technology (KIT), Heidelberg and Karlsruhe, Germany.
authors.forename: Suat
authors.initials: S
authors.lastname: Özbek
authors.affiliation: Institute for Neurobiology and Behavioural Biology, University of Muenster, Germany.
authors.forename: Ulrich
authors.initials: U
authors.lastname: Thurm
authors.affiliation: Institute for Evolution and Biodiversity, University of Muenster, Germany ebb@wwu.de.
authors.forename: Erich
authors.initials: E
authors.lastname: Bornberg-Bauer
mesh_terms: D000818:Animals; D003063:Cnidaria / Q000235:genetics; D019143:Evolution, Molecular; D018628:Gene Dosage; D006829:Hydra / Q000235:genetics; D007473:Ion Channels; D005810:Multigene Family; D010802:Phylogeny; D017434:Protein Structure, Tertiary / Q000235:genetics; D050051:Transient Receptor Potential Channels / Q000737:chemistry / Q000145:classification / Q000235:genetics*
chemical_list: D007473:Ion Channels; D050051:Transient Receptor Potential Channels
keywords: Cnidaria; domain rearrangements; mechanosensation; nematocyst evolution; neurobiology; protein evolution