Expanded Functional Diversity of Shaker K+ Channels in Cnidarians Is Driven by Gene Expansion
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The genome of the cnidarian Nematostella vectensis (starlet sea anemone) provides a molecular genetic view into the first nervous systems, which appeared in a late common ancestor of cnidarians and bilaterians. Nematostella has a surprisingly large and diverse set of neuronal signaling genes including paralogs of most neuronal signaling molecules found in higher metazoans. Several ion channel gene families are highly expanded in the sea anemone, including three subfamilies of the Shaker K(+) channel gene family: Shaker (Kv1), Shaw (Kv3) and Shal (Kv4). In order to better understand the physiological significance of these voltage-gated K(+) channel expansions, we analyzed the function of 18 members of the 20 gene Shaker subfamily in Nematostella. Six of the Nematostella Shaker genes express functional homotetrameric K(+) channels in vitro. These include functional orthologs of bilaterian Shakers and channels with an unusually high threshold for voltage activation. We identified 11 Nematostella Shaker genes with a distinct "silent" or "regulatory" phenotype; these encode subunits that function only in heteromeric channels and serve to further diversify Nematostella Shaker channel gating properties. Subunits with the regulatory phenotype have not previously been found in the Shaker subfamily, but have evolved independently in the Shab (Kv2) family in vertebrates and the Shal family in a cnidarian. Phylogenetic analysis indicates that regulatory subunits were present in ancestral cnidarians, but have continued to diversity at a high rate after the split between anthozoans and hydrozoans. Comparison of Shaker family gene complements from diverse metazoan species reveals frequent, large scale duplication has produced highly unique sets of Shaker channels in the major metazoan lineages.
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Nematostella has a significantly expanded set of 20 voltage-gated K+ channels of the shaker family.
“Nematostella has a significantly expanded set of 20 voltage-gated K+ channels of the shaker family, yet their function in Nematostella is still unclear [80].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [80]
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- Authors
- Jegla, T., Marlow, H. Q., Chen, B., Simmons, D. K., Jacobo, S. M., & Martindale, M. Q.
- Affiliations
- Pennsylvania State University (US)
- University of Hawaiʻi at Mānoa (US)
- Scripps Research Institute (US)
- Corresponding author
- Jegla, Timothy
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-12-10
- Volume
- 7
- Issue
- 12
- Pages
- e51366
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3519636
- OpenAlex
- W1984704872
- Cited by
- 35
- References
- 64
- Citations by year
- 2025: 5 · 2024: 7 · 2023: 1 · 2022: 2 · 2020: 2 · 2018: 5 · 2017: 1 · 2016: 2 · 2015: 8 · 2014: 2
- FWCI
- 1.28
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Science Foundation
- National Aeronautics and Space Administration
- University of Pennsylvania
- Pennsylvania State University
- National Institute of General Medical Sciences (R01GM093116)
- National Institute of Neurological Disorders and Stroke
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Keywords
- Shaker potassium channel, Nematostella vectensis, gene family expansion, gene duplication, voltage-gated potassium channels, cnidarian evolution, Anthozoa, Hydrozoa, ion channel evolution
- MeSH terms
- Animals, Cnidaria, Gene Expression Regulation, Phylogeny, In Situ Hybridization, Shaker Superfamily of Potassium Channels
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