NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

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.

WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella

“…O: Ostium. Positive and negative controls for these techniques under the same conditions have been performed and gived same results as previously on both whole mounted and sectioned material [5].…”

“…The sponges are widely accepted as one of the oldest metazoan lineages, with the unicellular choanoflagellates forming a sister group to the metazoa as a whole [1], [2], [3], [4]. Since sponge choanocytes and choanoflagellates show many similarities, the first step of animal evolution has been proposed to have been the acquisition of multicellularity from a choanoflagellate-like ancestor, with early metazoans comprising epithelial-type cell layer containing feeding choanocytes and non-feeding cells [1], [5], [6]. Such multicellular epithelia are considered as a fundamental metazoan innovation, enabling a range of morphogenetic processes and leading to body plan diversification [7].…”

Origin of the neuro‐sensory system: new and expected insights from sponges

“…We hope that the expression patterns of these genes under various conditions, in both larvae and adults, will give us insights into the cells concerned. Concerning the body plan patterning genes, several genes known to play a role in nervous system differentiation have been reported in sponges: Frizzled (Adell et al 2003); Sox (Jager et al 2006); Pax (for review see Kozmik 2008); NK 6,7 (Gazave et al 2008;Larroux et al 2006);bHLH (Richard et al 2008;Simionato et al 2007); and Tlx apparented genes (Coutinho et al 2003;Larroux et al 2006;Richelle-Maurer et al 2006). Nevertheless, expression data remain scarce and are not always easy to compare to data from eumetazoans.…”

“…2. A NK 6,7 -related gene has been shown to be expressed strictly in choanocytes of the Homoscleromorpha Oscarella lobularis Schmidt, 1862 (Gazave et al 2008). The authors draw our attention to the fact that NK 6 and NK 7 families have a predominantly neural expression pattern in bilaterians (Fig.…”

Molecular Phylogeny Restores the Supra-Generic Subdivision of Homoscleromorph Sponges (Porifera, Homoscleromorpha)

“…Because the Homoscleromorpha were only recently recognized as a separate, major sponge clade [7], [8], [9], [11], [12], [23], [24], their internal relationships have not yet been investigated using molecular markers. However, such investigation is necessary, given both the potential usefulness of Homoscleromorpha in pharmacological research [40] and the recent emergence of two Oscarella species ( O. lobularis and O. carmela ) as models in the Evo-Devo field [15], [41], [42], [43]. Here we present a thorough investigation of homoscleromorph phylogeny using morphology, 18S rDNA, 28S rDNA and complete mitochondrial genome sequence data.…”