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Origin of animal epithelia: insights from the sponge genome
Abstract
SUMMARY Epithelial tissues are a key metazoan cell type, providing a basic structural unit for the construction of diverse animal body plans. Historically, an epithelial grade of organization was considered to be restricted to the Eumetazoa, with the majority of cell layers described for Porifera lacking any of the conserved ultrastructural characteristics of epithelia. Now with the use of genomic information from the demosponge, Amphimedon queenslandica, we identify orthologs of bilaterian genes that determine epithelial cell polarity or encode components of specialized epithelial junctions and extracellular matrix structures. Amphimedon possesses orthologs of most bilaterian epithelial polarity and adherens junction genes but few or no tight junction, septate junction, or basal lamina genes. To place this information in an evolutionary context, we extended these analyses to the completed genomes of various fungi, the choanoflagellate, Monosiga brevicollis, the placozoan, Trichoplax adhaerens, and the cnidarian, Nematostella vectensis. The results indicate that the majority of “epithelial” genes originated in metazoan or eumetazoan lineages, with only two genes, Par‐1 and Discs large, antedating the choanoflagellate‐metazoan split. We further explored the mechanism of evolution for each of these genes by tracking the origin of constituent domains and domain combinations. In general, domain configurations found in contemporary bilaterians are inferred to have evolved early in metazoan evolution and are identical or similar to those present in representatives of modern cnidarians, placozoans, and demosponges.
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Sponges have long been considered to lack epithelia, but recent studies have revealed the presence of some typical epithelial components and a capacity to seal their internal space from the environment.
“Sponges have long been considered to lack epithelia, but recent studies have revealed the presence of some typical epithelial components (cell polarity and cell junction genes), and a capacity to seal their internal space from the environment (Adams et al. 2010; Belahbib et al. 2018; Fahey and Degnan 2010; Leys and Hill 2012; Leys et al. 2009; Riesgo et al. 2014).”
From A non-bilaterian perspective on the development and evolution of animal digestive systems (2019) · cites this paper as Fahey and Degnan 2010
Citations
Cites
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The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049
Self-citationThe cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42
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Nelson, W. J. (2003) · Nature · doi:10.1038/nature01602 · Cited by 716
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A Post-Synaptic Scaffold at the Origin of the Animal Kingdom
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The NK homeobox gene cluster predates the origin of Hox genes.
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“In some cases, an in-house trace assembly pipeline was used to derive missing sequence information for local gaps or breaks in the genomic contigs (Larroux et al. 2007).”
MethodSperling, E. A., Peterson, K. J., & Pisani, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp148 · Cited by 172 · cited 5×
“If these sponges are paraphyletic (e.g., Sperling et al. 2009), then these may represent characters that evolved in the clade containing the Calcarea, Homoscleromorpha, and Eumetazoa after it diverged from the lineage comprising the majority of demosponges.”
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Metadata
- Authors
- Fahey, B., & Degnan, B. M.
- Affiliations
- The University of Queensland (AU)
- Corresponding author
- Degnan, Bernard M.
- ORCID
- Degnan, Bernard M.
- Venue
- Evolution & Development
- Publisher
- Wiley
- Published
- 2010-10-29
- Volume
- 12
- Issue
- 6
- Pages
- 601-617
- ISSN
- 1520-541X (ISSN-L)
- 1525-142X
- OpenAlex
- W1876693625
- Cited by
- 109
- References
- 12
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 6 · 2021: 13 · 2020: 7 · 2019: 10 · 2018: 6 · 2017: 5 · 2016: 8 · 2015: 12 · 2014: 8 · 2013: 7 · 2012: 13
- FWCI
- 5.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Evolution & Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Energy
- Joint Genome Institute
- Australian Research Council
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Keywords
- Amphimedon queenslandica, sponge genome, epithelial polarity, adherens junctions, tight junctions, septate junctions, basement membrane, protease-activated receptor 1, Discs large, Monosiga brevicollis, Trichoplax adhaerens, Nematostella vectensis, gene origin, protein domain evolution
- MeSH terms
- Animals, Epithelium, Phylogeny, Porifera, Genome, Cell Polarity, Evolution, Molecular
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