Homeobox Gene Diversification in the Calcareous Sponge, Sycon raphanus

Manuel, Michaël; Parco, Yannick Le

doi:10.1006/mpev.2000.0822

Cited by 72 publications

(36 citation statements)

References 59 publications

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“…2), the precise affinities among the ANTP class are unclear. HomoNK genes are not closely related to any NK family previously identified from calcareous sponges (Manuel and Le Parco 2000) or demosponges (Richelle-Maurer and Van de Vyver 1999;Hill et al 2004;Richelle-Maurer et al 2006;Larroux et al 2006Larroux et al , 2007, in particular from the fully sequenced genome of A. queenslandica (Larroux et al 2007). This observation suggests that the homoscleromorph ANTP class gene complement is divergent from that of demosponges, in consistence with the hypothesis that Homoscleromorpha constitute a lineage distinct from Demospongiae (Borchiellini et al 2004;Sperling et al 2007).…”

Section: Antp Class Genes Identified From Homoscleromorph Spongesmentioning

confidence: 93%

NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

et al. 2008

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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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Section: Antp Class Genes Identified From Homoscleromorph Spongesmentioning

confidence: 93%

NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

et al. 2008

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“…There is a clear polarity in the skeletal organization from the choanosome to the ectosome in most sponge species, and a clear radial symmetry can be seen in the skeleton of subspherical sponges (Uriz, 2002). Homeoboxes have been identified in Demosponges (Coutinho et al, 1994;Kruse et al, 1994;Seimyia et al, 1994;Degnan et al, 1995;Richelle-Maurer et al, 1998 and calcareous sponges (Manuel and Le Parco, 2000) and their temporal and spatial expression has been shown both in adults (Seimyia et al, 1997;Richelle-Maurer et al, 1999;Larroux and Degnan, 1999) and in embryos (Leys et al, 1999). These homeobox genes may be responsible for the establishment of polarity during the sponges' life cycle.…”

Section: Spicules Arrangement: How They Get the Right Place And Orienmentioning

confidence: 94%

Siliceous spicules and skeleton frameworks in sponges: Origin, diversity, ultrastructural patterns, and biological functions

Uriz

Turon

Becerro

et al. 2003

Microscopy Res & Technique

216

161

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Silica deposition is a fundamental process in sponges. Most sponges in the Classes Demospongiae and Hexactinellida secrete siliceous elements, which can subsequently fuse, interlock with each other, or form three-dimensional structures connected by spongin. The resulting skeletal frameworks allow sponges to grow upwards and facilitate water exchange with minimal metabolic cost. Several studies on sponge skeletogenesis have been published. We are beginning to understand the mechanisms of spicule secretion and the role of spicules and skeletal frameworks in the biology, ecology, and evolution of sponges. Molecular techniques and ecological experiments have demonstrated the genetic control of the process and the contribution of environmental factors to the expression of a sponge spicule, respectively. However, other classic topics such as the role of membranes in silicon transport or whether spicules are formed in situ or secreted anywhere in the sponge mesohyl and then transported to the skeletal framework require further investigation. We review the process of silica deposition in sponges at the molecular and cellular levels, as well as the biological and ecological functions of spicules and skeletons. The genetic control of spicule shapes makes them useful in the reconstruction of sponge phylogeny, although recent experiments have demonstrated the influence of environmental factors in modulating spicule size, shape, and the presence or absence of one or more spicule types. The implications of such variations in sponge taxonomy may be important. Besides supporting sponge cells, spicules can help larvae stay buoyant while in the plankton or reach the bottom at settlement, enhance reproduction success, or catch prey. Conversely, the role of spicules and skeletons in deterring predation has not been demonstrated. Knowledge of several aspects is still based on a single or a few species and extrapolations should be made only with caution. With the advent of new molecular techniques, new lines of research are presently open and active in this field.

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“…These genes function during development ofbilaterians to cause regionalization of the antero-posterior axis into an anterior head and posterior trunk and tail regions (see Knoll and Carroll 1999). Recently, the homeobox genes in sponges have been summarized (Manuel and Le Parco 2000) and it was concluded that true homologous developmental genes have not yet been identified in sponges in spite of the obvious axial symmetry of most of those species (Vacelet and Boury-Esnault 1995). However, considering the advancement especially in the elucidation of the homeobox genes of the calcareous sponge Sycon raphanus (Manuel and Le Parco 2000), it appears to be premature to conclude a lack of homeobox genes in sponges which could be involved in the antero-posterior or dorso-ventral polarity.…”

Section: Conclusion: Contribution To the Origin Of The Metazoan Body mentioning

confidence: 99%

“…Recently, the homeobox genes in sponges have been summarized (Manuel and Le Parco 2000) and it was concluded that true homologous developmental genes have not yet been identified in sponges in spite of the obvious axial symmetry of most of those species (Vacelet and Boury-Esnault 1995). However, considering the advancement especially in the elucidation of the homeobox genes of the calcareous sponge Sycon raphanus (Manuel and Le Parco 2000), it appears to be premature to conclude a lack of homeobox genes in sponges which could be involved in the antero-posterior or dorso-ventral polarity. The afore-mentioned experiments and expression studies of the Iroquois gene in S. domuncula during the canal formation point in the direction that also in sponges gene products might be involved in the execution of regional morphogenetic program(s).…”

Section: Conclusion: Contribution To the Origin Of The Metazoan Body mentioning

confidence: 99%

Analysis of the Sponge [Porifera] Gene Repertoire: Implications for the Evolution of the Metazoan Body Plan

Müller¹,

Müller²

2003

Sponges (Porifera)

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Abstract. Sponges [phylum Porifera] form the basis of the metazoan kingdom and represent the evolutionary earliest phylum still extant. Hence, as living fossils, they are the taxon closest related to the hypothetical ancestor of all Metazoa, the Urmetazoa. Until recently, it was still unclear whether sponges are provided with a defined body plan. Only after the cloning, expression and functional studies of characteristic metazoan genes, could it be demonstrated that these animals comprise the structural elements which allow the sponge cells to organize themselves according to a body plan. Adhesion molecules involved in cell-cell and cell-matrix interactions have been identified. Among the cell-cell adhesion molecules the aggregation factor (AF) is the prominent particle. It is composed of a core protein that is associated with the adhesion molecules, a 36 kDa as well as a 86 kDa polypeptide. A galee tin functions as a linker of the AF to the cell-membrane-associated receptor, the aggregation receptor (AR). The most important extracellular matrix molecules are collagen-and fibronectin-like molecules. These proteins interact with the cellmembrane receptors, the integrins. In addition, a neuronal receptor has been identified, which -together with the identified neuroactive molecules -indicate the existence of a primordial neuronal network already in Porifera. The primmorph system, aggregated cells that retain the capacity to proliferate and differentiate, has been used to demonstrate that a homeobox-containing gene, Iroquois, is expressed during canal formation in primmorphs. The formation of a body plan in sponges is supported by skeletal elements, the spicules, which are composed in Demospongiae as well as in Hexactinellida of amorphous, noncrystalline silica. In Demospongiae the spicule formation is under enzymic control of silicatein. Already at least one morphogen has been identified in sponges, myotrophin, which is likely to be involved in the axis formation. Taken together, these elements support the recent conclusions that sponges are not merely non organized cell aggregates, but already complex animals provided with a defined body plan.

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Homeobox Gene Diversification in the Calcareous Sponge, Sycon raphanus

Cited by 72 publications

References 59 publications

NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges

Siliceous spicules and skeleton frameworks in sponges: Origin, diversity, ultrastructural patterns, and biological functions

Analysis of the Sponge [Porifera] Gene Repertoire: Implications for the Evolution of the Metazoan Body Plan

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