TheRiseandFallofTRP-N,anAncientFamilyofMechanogated Ion Channels, in Metazoa

Mechanoreception, the sensingofmechanical forces, is anancientmeansoforientationandcommunicationand 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 bywhichmechanical energy induces channel gating.We analyzed the evolutionary origins and possible diversificationof TRP-N.Using a custom-made set of highly discriminative sequence profileswe scanneda representative set ofmetazoangenomesand subsequently corrected several genemodels.Wefind that, contrary toother ionchannel families, TRP-N is remarkably conserved in itsdomainarrangementsandcopynumber (1) inall Bilateriaexcept foramniotes, even in thewakeof several whole-genomeduplications.TRP-N isabsent inPoriferabutpresent inCtenophoraandPlacozoa.ExceptionalmultiplicationsofTRP-N occurred in Cnidaria, independently along the Hydra and theNematostella 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.