NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges
Open accessAbstract
Data on nonbilaterian animals (sponges, cnidarians, and ctenophores) have suggested that Antennapedia (ANTP) class homeobox genes played a crucial role in the early diversification of animal body plans. Estimates of ancestral gene diversity within this important class of developmental regulators have been mostly based on recent analyses of the complete genome of a demosponge species, leading to the proposal that all ANTP families found in nonsponges animals (eumetazoans) derived from an ancestral "proto-NK" six-gene cluster. However, a single sponge species cannot reveal ancestral metazoan traits, in particular because lineage-specific gene duplications or losses are likely to have occurred during the long history of the Porifera. We thus looked for ANTP genes by degenerate polymerase chain reaction search in five species belonging to the Homoscleromorpha, a sponge lineage recently phylogenetically classified outside demosponges and characterized by unique histological features. We identified new genes of the ANTP class called HomoNK. Our phylogenetic analyses placed HomoNK (without significant support) close to the NK6 and NK7 families of cnidarian and bilaterian ANTP genes and did not recover the monophyly of the proposed "proto-NK" cluster. Our expression analyses of the HomoNK gene OlobNK in adult Oscarella lobularis showed that this gene is a strict marker of choanocytes, the most typical sponge cell type characterized by an apical flagellum surrounded by a collar of microvilli. These results are discussed in the light of the predominant neurosensory expression of NK6 and NK7 genes in bilaterians and of the recent proposal that choanocytes could be the sponge homologs of sensory cells.
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The known choanocyte gene expression profile has so far not revealed any similarities with bilaterian gut or enterocyte cell types.
“(iii) The known choanocyte gene expression profile (e.g. piwi, Wnt signalling genes, Sox genes, NK genes) has so far not revealed any similarities with bilaterian gut or enterocyte cell types (Fortunato et al. 2012; Funayama et al. 2010; Gazave et al. 2008; Leininger et al. 2014).”
From A non-bilaterian perspective on the development and evolution of animal digestive systems (2019) · cites this paper as Gazave et al. 2008
Cites
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“In addition to being central in the biology of sponges, choanocytes have recently attracted special attention as the possible sponge homologs of the eumetazoan sensory cells (Jacobs et al. 2007; Nielsen 2008).”
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“Homoscleromorpha could be the sister group of eumetazoans (Borchiellini et al. 2004; Sperling et al. 2007), although conflicting results have been obtained from other data sets (Wang and Lavrov 2007).”
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The NK homeobox gene cluster predates the origin of Hox genes.
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- Authors
- Gazave, E., Lapébie, P., Renard, E., Bézac, C., Boury-Esnault, N., Vacelet, J., Pérez, T., Manuel, M., & Borchiellini, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Borchiellini, Carole
- ORCID
- Venue
- Development Genes and Evolution
- Published
- 2008-08-14
- Volume
- 218
- Issue
- 9
- Pages
- 479-489
- ISSN
- 0043-5546 (ISSN-L)
- 0949-944X
- 1432-041X
- OpenAlex
- W2041100778
- Cited by
- 42
- References
- 13
- Citations by year
- 2025: 1 · 2024: 1 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 2 · 2016: 4 · 2015: 2 · 2013: 6 · 2012: 4
- FWCI
- 4.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Development Genes and Evolution (publishedVersion)
- PubMed (publishedVersion)
- HAL AMU (submittedVersion)
- HAL (submittedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Keywords
- Homoscleromorpha, choanocytes, Oscarella lobularis, sponge evolution, gene duplication and loss, gene expression, sensory cells
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Genes, Homeobox, Phylogeny, Porifera, RNA, Messenger, Species Specificity, Polymerase Chain Reaction, Homeodomain Proteins, Antennapedia Homeodomain Protein
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