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NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

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Abstract

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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Acknowledgments

We thank to the diving staff of the COM (Roland Graille, Frederic Zuberer, and Bernard De Ligondes) and Christophe Lejeusne for their help in sampling. We also thank Alexander Ereskovsky for helpful comments, Christian Marschal for his help in the use of the microscope and binocular magnifier and also Dr Clive Wilkinson and Michael Paul for help with the English revision.

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Authors and Affiliations

  1. Centre d’Océanologie de Marseille, Aix-Marseille Université, CNRS-UMR 6540, Station marine d’Endoume, rue de la batterie des Lions, 13007, Marseille, France

    Eve Gazave, Pascal Lapébie, Emmanuelle Renard, Nicole Boury-Esnault, Jean Vacelet, Thierry Pérez & Carole Borchiellini

  2. Centre d’Océanologie de Marseille, Aix-Marseille Université, CNRS-UMS 2196, Station marine d’Endoume, 13007, Marseille, France

    Chantal Bézac

  3. Université Pierre et Marie Curie-Paris 6, UMR 7138 CNRS UPMC MNHN IRD, Case 05, 7 quai St Bernard, 75005, Paris, France

    Michaël Manuel

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  1. Eve Gazave
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  2. Pascal Lapébie
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Correspondence to Carole Borchiellini.

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Communicated by: M.Q. Martindale

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Supplementary material S1

Sequences of the primers used. (DOC 27.0 KB)

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Supplementary material S3

Homeodomain sequences used for phylogenetic analysis, with accession numbers. (RTF 148 KB)

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Gazave, E., Lapébie, P., Renard, E. et al. NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges. Dev Genes Evol 218, 479–489 (2008). https://doi.org/10.1007/s00427-008-0242-z

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