The rise and fall of TRP-N, an ancient family of mechanogated ion channels, in Metazoa
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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.
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Analyses of the opsin gene family and ion-channel proteins involved in mechanoreception are consistent with a close relationship between Ctenophora, Cnidaria, and Bilateria.
“Likewise, analyses of the opsin gene family, which is involved in light detection in animals, as well as ion-channel proteins involved in mechanoreception, are consistent with a close relationship between Ctenophora, Cnidaria, and Bilateria (50, 51).”
From Genomic data do not support comb jellies as the sister group to all other animals (2015) · cites this paper as [51]
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Self-citationFormation and discharge of nematocysts is controlled by a proton gradient across the cyst membrane
Berking, S., & Herrmann, K. (2005) · Helgoland Marine Research · doi:10.1007/s10152-005-0019-y · Cited by 31 · see citing works
Evolutionary Dynamics on Protein Bi-stability Landscapes can Potentially Resolve Adaptive Conflicts
Sikosek, T., Bornberg‐Bauer, E., & Chan, H. S. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002659 · Cited by 25 · see citing works
Self-citationUphill transport of water by electroosmosis
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Self-citationGolz, R. (1994) · Journal of Morphology · doi:10.1002/jmor.1052220106 · Cited by 21 · see citing works
From Structure to Information in Sensory Systems
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Cnidocil regeneration in nematocytes ofHydra
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Self-citationMechanotransduction: The Elusive Hair Cell Transduction Channel Revealed?
Morgan, C. P., & Gillespie, P. G. (2013) · Current Biology · doi:10.1016/j.cub.2013.08.031 · Cited by 8 · see citing works
Signaling pathways in phagocytosis
Kwiatkowska (1999) · doi:10.1002/(sici)1521-1878(199905)21:5
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Genomic data do not support comb jellies as the sister group to all other animals
Pisani, D., Pett, W., Dohrmann, M., Feuda, R., Rota-Stabelli, O., Philippe, H., Lartillot, N., & Wörheide, G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518127112 · Cited by 319 · see citing works
Reafference and the origin of the self in early nervous system evolution
Jékely, G., Godfrey-Smith, P., & Keijzer, F. (2021) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2019.0764 · Cited by 119 · see citing works
A Short History of Nearly Every Sense—The Evolutionary History of Vertebrate Sensory Cell Types
Schlosser, G. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy024 · Cited by 33 · see citing works
- Authors
- Schüler, A., Schmitz, G., Reft, A., Özbek, S., Thurm, U., & Bornberg-Bauer, E.
- Affiliations
- University of Münster (DE)
- Heidelberg University (DE)
- Karlsruhe Institute of Technology (DE)
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-06
- Volume
- 7
- Issue
- 6
- Pages
- 1713-1727
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC4494053
- OpenAlex
- W2203280675
- Cited by
- 51
- References
- 108
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 3 · 2021: 12 · 2020: 9 · 2019: 4 · 2018: 3 · 2017: 3 · 2016: 2 · 2015: 1
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- URN:NBN Resolver for Germany & Switzerland (German National Library) (submittedVersion, cc-by)
- Funders
- National Science Foundation (1306604)
- Deutsche Forschungsgemeinschaft
- Volkswagen Foundation
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- mechanosensitive ion channels, mechanoreception, ankyrin repeat domain, channel gating, ion channel evolution, whole-genome duplication, subfunctionalization, gene family expansion, Cnidaria, Hydra, Nematostella, Ctenophora, Placozoa, sponges, nervous system evolution, metazoan genomes
- MeSH terms
- Animals, Cnidaria, Multigene Family, Hydra, Ion Channels, Phylogeny, Protein Structure, Tertiary, Gene Dosage, Evolution, Molecular, Transient Receptor Potential Channels
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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