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ABSTRACT: The emergence of multicellularity is regarded as one of the major evolutionary events of life. This transition unicellularity/pluricellularity was acquired independently several times (King 2004). The acquisition of multicellularity implies the emergence of cellular cohesion and means of communication, as well as molecular mechanisms enabling the control of morphogenesis and body plan patterning. Some of these molecular tools seem to have predated the acquisition of multicellularity while others are regarded as the acquisition of specific lineages. Morphogenesis consists in the spatial migration of cells or cell layers during embryonic development, metamorphosis, asexual reproduction, growth, and regeneration, resulting in the formation and patterning of a body. In this paper, our aim is to review what is currently known concerning basal metazoans-sponges' morphogenesis from the tissular, cellular, and molecular points of view-and what remains to elucidate. Our review attempts to show that morphogenetic processes found in sponges are as diverse and complex as those found in other animals. In true epithelial sponges (Homoscleromorpha), as well as in others, we find similar cell/layer movements, cellular shape changes involved in major morphogenetic processes such as embryogenesis or larval metamorphosis. Thus, sponges can provide information enabling us to better understand early animal evolution at the molecular level but also at the cell/cell layer level. Indeed, comparison of molecular tools will only be of value if accompanied by functional data and expression studies during morphogenetic processes.
Archiv für Entwickelungsmechanik der Organismen 04/2012; · 1.77 Impact Factor
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ABSTRACT: Over the past few years, there has been
growing interest among the sponge community in the
phylogenetic position of the Homoscleromorpha (i.e.
within or outside the class Demospongiae). Recent
molecular analyses clearly show that the Homoscleromorpha
forms a distinct clade separated from the
Demospongiae and is composed of two families,
Oscarellidae and Plakinidae. Within the currently
more widely accepted hypothesis of a monophyletic
Porifera, we formally propose here to raise Homoscleromorpha
to the class rank (the fourth one). We,
therefore, provide a definition and a formal diagnosis.
In the supplementary materials, we also present an
alternative classification of the Homoscleromorpha,
following the PhyloCode.
Hydrobiologia 01/2012; 687(687):3-10. · 1.78 Impact Factor
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ABSTRACT: Planar cell polarity (PCP), the alignment of cells within 2D tissue planes, involves a set of core molecular regulators highly conserved between animals and cell types. These include the transmembrane proteins Frizzled (Fz) and VanGogh and the cytoplasmic regulators Dishevelled (Dsh) and Prickle. It is widely accepted that this core forms part of a 'PCP pathway' for signal transduction, which can affect cell morphology through activation of an evolutionary ancient regulatory module involving Rho family GTPases and Myosin II, and/or the JNK kinase cascade. We have re-examined the evidence for interactions between the proposed PCP pathway components, and question the placing of the cell morphology regulators in the same pathway as the PCP core. While Fz and Dsh are clearly involved in both PCP and Rho-based cell morphology regulation, available evidence cannot currently discriminate whether these processes are linked mechanistically by a shared Fz/Dsh population, or pass by two distinct pathways.
BioEssays 10/2011; 33(10):759-68. · 4.95 Impact Factor
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BioEssays 08/2011; 33(10):759 - 768. · 4.95 Impact Factor
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ABSTRACT: The genus Axinella is difficult to define on the basis of morphological characters and includes a heterogeneous assemblage of species. Several previous authors have suspected the polyphyly of both this genus and the family Axinellidae. To clarify the phylogeny of Axinellidae and Axinella, we propose a new hypothesis based on two molecular markers. In our analyses, Axinellidae and Axinella are polyphyletic assemblages. The 15 species of Axinellidae in our dataset belong to five clades and the nine species of Axinella to three clades. One Axinella clade, named Axinella(p), contains the type-species of the genus: A. polypoides (plus A. aruensis, A. dissimilis, A. infundibuliformis and A. vaceleti). A new clade, Cymbaxinella(p), is proposed, following the PhyloCode, it includes C. damicornis, C. verrucosa, C. corrugata and C. cantharella. The species Axinella cannabina is reallocated to a clade named Acanthella(p). The clades Agelas(p) and Cymbaxinella(p) constitute a new clade: Agelasida(p). Few morphological, biochemical and secondary structures characters support these groupings, highlighting the need for new characters for such problematic sponge groups. This work is an attempt to build a framework for the phylogeny of taxa allocated to Axinella and Axinellidae in the traditional classification.
Molecular Phylogenetics and Evolution 10/2010; 57(1):35-47. · 3.61 Impact Factor
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ABSTRACT: Homoscleromorpha is the fourth major sponge lineage, recently recognized to be distinct from the Demospongiae. It contains <100 described species of exclusively marine sponges that have been traditionally subdivided into 7 genera based on morphological characters. Because some of the morphological features of the homoscleromorphs are shared with eumetazoans and are absent in other sponges, the phylogenetic position of the group has been investigated in several recent studies. However, the phylogenetic relationships within the group remain unexplored by modern methods.
Here we describe the first molecular phylogeny of Homoscleromorpha based on nuclear (18S and 28S rDNA) and complete mitochondrial DNA sequence data that focuses on inter-generic relationships. Our results revealed two robust clades within this group, one containing the spiculate species (genera Plakina, Plakortis, Plakinastrella and Corticium) and the other containing aspiculate species (genera Oscarella and Pseudocorticium), thus rejecting a close relationship between Pseudocorticium and Corticium. Among the spiculate species, we found affinities between the Plakortis and Plakinastrella genera, and between the Plakina and Corticium. The validity of these clades is furthermore supported by specific morphological characters, notably the type of spicules. Furthermore, the monophyly of the Corticium genus is supported while the monophyly of Plakina is not.
As the result of our study we propose to restore the pre-1995 subdivision of Homoscleromorpha into two families: Plakinidae Schulze, 1880 for spiculate species and Oscarellidae Lendenfeld, 1887 for aspiculate species that had been rejected after the description of the genus Pseudocorticium. We also note that the two families of homoscleromorphs exhibit evolutionary stable, but have drastically distinct mitochondrial genome organizations that differ in gene content and gene order.
PLoS ONE 01/2010; 5(12):e14290. · 4.09 Impact Factor
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ABSTRACT: Of the 20 or so signal transduction pathways that orchestrate cell-cell interactions in metazoans, seven are involved during development. One of these is the Notch signalling pathway which regulates cellular identity, proliferation, differentiation and apoptosis via the developmental processes of lateral inhibition and boundary induction. In light of this essential role played in metazoan development, we surveyed a wide range of eukaryotic genomes to determine the origin and evolution of the components and auxiliary factors that compose and modulate this pathway.
We searched for 22 components of the Notch pathway in 35 different species that represent 8 major clades of eukaryotes, performed phylogenetic analyses and compared the domain compositions of the two fundamental molecules: the receptor Notch and its ligands Delta/Jagged. We confirm that a Notch pathway, with true receptors and ligands is specific to the Metazoa. This study also sheds light on the deep ancestry of a number of genes involved in this pathway, while other members are revealed to have a more recent origin. The origin of several components can be accounted for by the shuffling of pre-existing protein domains, or via lateral gene transfer. In addition, certain domains have appeared de novo more recently, and can be considered metazoan synapomorphies.
The Notch signalling pathway emerged in Metazoa via a diversity of molecular mechanisms, incorporating both novel and ancient protein domains during eukaryote evolution. Thus, a functional Notch signalling pathway was probably present in Urmetazoa.
BMC Evolutionary Biology 10/2009; 9:249. · 3.52 Impact Factor
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ABSTRACT: The capacity of all cells to respond to stimuli implies the conduction of information at least over short distances. In multicellular organisms, more complex systems of integration and coordination of activities are necessary. In most animals, the processing of information is performed by a nervous system. Among the most basal taxa, sponges are nerveless so that it is traditionally assumed that the integrated neuro-sensory system originated only once in Eumetazoa, a hypothesis not in agreement with some recent phylogenomic studies. The aim of this review is to show that recent data on sponges might provide clues for understanding the origin of this complex system. First, sponges are able to react to external stimuli, and some of them display spontaneous movement activities. These coordinated behaviors involve nervous system-like mechanisms, such as action potentials and/or neurotransmitters. Second, genomic analyses show that sponges possess genes orthologous to those involved in the patterning or functioning of the neuro-sensory system in Eumetazoa. Finally, some of these genes are expressed in specific cells (flask cells, choanocytes). Together with ultrastructural data, this gives rise to challenging hypotheses concerning cell types that might play neuro-sensory-like roles in sponges.
Integrative Zoology 09/2009; 4(3):294-308. · 1.21 Impact Factor
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Hervé Philippe,
Romain Derelle,
Philippe Lopez,
Kerstin Pick, Carole Borchiellini,
Nicole Boury-Esnault,
Jean Vacelet,
Emmanuelle Renard,
Evelyn Houliston,
Eric Quéinnec,
Corinne Da Silva,
Patrick Wincker,
Hervé Le Guyader,
Sally Leys,
Daniel J Jackson,
Fabian Schreiber,
Dirk Erpenbeck,
Burkhard Morgenstern,
Gert Wörheide,
Michaël Manuel
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ABSTRACT: The origin of many of the defining features of animal body plans, such as symmetry, nervous system, and the mesoderm, remains shrouded in mystery because of major uncertainty regarding the emergence order of the early branching taxa: the sponge groups, ctenophores, placozoans, cnidarians, and bilaterians. The "phylogenomic" approach [1] has recently provided a robust picture for intrabilaterian relationships [2, 3] but not yet for more early branching metazoan clades. We have assembled a comprehensive 128 gene data set including newly generated sequence data from ctenophores, cnidarians, and all four main sponge groups. The resulting phylogeny yields two significant conclusions reviving old views that have been challenged in the molecular era: (1) that the sponges (Porifera) are monophyletic and not paraphyletic as repeatedly proposed [4-9], thus undermining the idea that ancestral metazoans had a sponge-like body plan; (2) that the most likely position for the ctenophores is together with the cnidarians in a "coelenterate" clade. The Porifera and the Placozoa branch basally with respect to a moderately supported "eumetazoan" clade containing the three taxa with nervous system and muscle cells (Cnidaria, Ctenophora, and Bilateria). This new phylogeny provides a stimulating framework for exploring the important changes that shaped the body plans of the early diverging phyla.
Current biology: CB 05/2009; 19(8):706-12. · 10.99 Impact Factor
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ABSTRACT: Sponges branch basally in the metazoan phylogenetic tree and are believed to be composed of four distinct lineages with still uncertain relationships. Indeed, some molecular studies propose that Homoscleromorpha may be a fourth Sponge lineage, distinct from Demospongiae in which they were traditionally classified. They harbour many features that distinguish them from other sponges and are more evocative of those of the eumetazoans. They are notably the only sponges to possess a basement membrane with collagen IV and specialized cell-junctions, thus possessing true epithelia. Among Homoscleromorphs, we have chosen Oscarella lobularis as a model species. This common and easily accessible sponge is characterized by relatively simple histology and cell composition, absence of skeleton, and strongly pronounced epithelial structure. In this review, we explore the specific features that make O. lobularis a promising homoscleromorph sponge model for evolutionary and developmental researches.
BioEssays 02/2009; 31(1):89-97. · 4.95 Impact Factor
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ABSTRACT: Sponges branch basally in the metazoan phylogenetic tree and are thus well positioned to provide insights into the evolution of mechanisms controlling animal development, likely to remain active in adult sponges. Of the four sponge clades, the Homoscleromorpha are of particular interest as they alone show the "true" epithelial organization seen in other metazoan phyla (the Eumetazoa). We have examined the deployment in sponges of Wnt signalling pathway components, since this pathway is an important regulator of many developmental patterning processes. We identified a reduced repertoire of three divergent Wnt ligand genes in the recently-sequenced Amphimedon queenslandica (demosponge) genome and two Wnts from our EST collection from the homoscleromorph Oscarella lobularis, along with well-conserved genes for intracellular pathway components (beta-catenin, GSK3beta). Remarkably, the two O. lobularis Wnt genes showed complementary expression patterns in relation to the evenly spaced ostia (canal openings) of the exopinacoderm (ectoderm), highly reminiscent of Wnt expression during skin appendage formation in vertebrates. Furthermore, experimental activation of the Wnt/beta-catenin pathway using GSK3beta inhibitors provoked formation of ectopic ostia, as has been shown for epithelial appendages in Eumetazoa. We thus suggest that deployment of Wnt signalling is a common and perhaps ancient feature of metazoan epithelial patterning and morphogenesis.
PLoS ONE 02/2009; 4(6):e5823. · 4.09 Impact Factor
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ABSTRACT: Sponges branch basally in the metazoan phylogenetic tree and are believed to be composed of four distinct lineages with still uncertain relationships. Indeed, some molecular studies propose that Homoscleromorpha may be a fourth Sponge lineage, distinct from Demospongiae in which they were traditionally classified. They harbour many features that distinguish them from other sponges and are more evocative of those of the eumetazoans. They are notably the only sponges to possess a basement membrane with collagen IV and specialized cell-junctions, thus possessing true epithelia. Among Homoscleromorphs, we have chosen Oscarella lobularis as a model species. This common and easily accessible sponge is characterized by relatively simple histology and cell composition, absence of skeleton, and strongly pronounced epithelial structure. In this review, we explore the specific features that make O. lobularis a promising homoscleromorph sponge model for evolutionary and developmental researches.
BioEssays 01/2009; 31(1):89 - 97. · 4.95 Impact Factor
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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.
Archiv für Entwickelungsmechanik der Organismen 10/2008; 218(9):479-89. · 1.77 Impact Factor
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ABSTRACT: A survey across the most basal animal phylum, the Porifera, for the presence of homeobox-containing genes led to the isolation of 24 partial or complete homeobox sequences from 21 sponge species distributed in 15 families and 6 orders of Demospongiae. All the new sequences shared a high identity/similarity with EmH-3 (Ephydatia muelleri), a non-Hox gene from the Antp class. The Demox sequences, EmH-3, and related homeodomains formed a well-supported clade with no true affinity with any known bilaterian family, including the Tlx/Hox11 family, suggesting that the EmH-3 family of genes, comprising 31 members, represents a novel family of non-Hox genes, called the Demox family, widespread among Demospongiae. The presence of the Tlx/Hox11 specific signature in the Demox family and common regulatory elements suggested that the Demox and Tlx/Hox11 families are closely related. In the phylogenetic analyses, freshwater Haplosclerida appeared as monophyletic, and Haplosclerida and Halichondrida as polyphyletic, with a clade comprising Agelas species and Axinella corrugata. As for their expression, high levels of Demox transcripts were found in adult tissues. Our data add to the number of published poriferan homeobox sequences and provide independent confirmation of the current Demospongiae phylogenies.
Journal of Molecular Evolution 09/2006; 63(2):222-30. · 2.27 Impact Factor
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ABSTRACT: The Brachyury family of T-domain containing transcription factor has been recently the subject of a number of Evo-Devo studies, with expression data obtained from a wide sampling of eumetazans, pointing to a possible conserved role in the formation of the blastopore and the extremities of the digestive tract. Here we present a comparative analysis of Brachyury sequences at the metazoan scale, using published data and two new sponge Brachyury sequences. Alignment features, gene phylogeny, and the evolution of variable positions within the T-domain are discussed in the light of available data about functional constraints on the residues. Interestingly, the high sequence divergence observed in Brachyury T-domains from sponges appears to be mostly the consequence of autapomorphic changes within the sponge lineages, rather than the retention of primitive character states.
Gene 11/2004; 340(2):291-301. · 2.34 Impact Factor
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ABSTRACT: An analysis of the phylogenetic relationships of the 13 orders of Demospongiae, based on 18S and C1, D1 and C2 domains of 28S rRNA (for, respectively, 26 and 32 taxa) has been performed. The class Demospongiae as traditionally defined is not found to be monophyletic. Instead, a clade comprising all demosponges except Homoscleromorpha is well-supported, and we define phylogenetically the name Demospongiae in this more restricted sense to preclude the possibility of drastic alterations of the meaning of Demospongiae in the future, depending on the position of Homoscleromorpha. Within this clade Demospongiae s.s., ceractinomorphs and tetractinomorphs are polyphyletic, implying homoplastic evolution of characters such as reproductive strategies (viviparity vs. oviparity) and skeleton architecture (reticulate vs. radiate). The topology derived from our molecular data provides a basis for proposing a new classification of Demospongiae s.s., and suggests a reverse polarity of some characters, with respect to traditional conceptions: viviparity, presence of monaxon spicules and of spongin appear to be ancestral, whereas oviparity, and presence of tetraxon spicules appear as derived characters.
Molecular Phylogenetics and Evolution 10/2004; 32(3):823-37. · 3.61 Impact Factor
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ABSTRACT: Because calcareous sponges are triggering renewed interest with respect to basal metazoan evolution, a phylogenetic framework of their internal relationships is needed to clarify the evolutionary history of key morphological characters. Morphological variation was scored at the suprageneric level within Calcispongia, but little phylogenetic information could be retrieved from morphological characters. For the main subdivision of Calcispongia, the analysis of morphological data weakly supports a classification based upon cytological and embryological characters (Calcinea/Calcaronea) rather than the older classification scheme based upon the aquiferous system (Homocoela/Heterocoela). The 18S ribosomal RNA data were then analyzed, both alone and in combination with morphological characters. The monophyly of Calcispongia is highly supported, but the position of this group with respect to other sponge lineages and to eumetazoan taxa is not resolved. The monophyly of both Calcinea and Calcaronea is retrieved, and the data strongly rejected the competing Homocoela/Heterocoela hypothesis. The phylogeny implies that characters of the skeleton architecture are highly homoplastic, as are characters of the aquiferous system. However, axial symmetry seems to be primitive for all Calcispongia, a conclusion that has potentially far-reaching implications for hypotheses of early body plan evolution in Metazoa.
Systematic Biology 07/2003; 52(3):311-33. · 10.23 Impact Factor
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ABSTRACT: Type IV collagen forms a network that provides the major structural support for basement membranes. Basement membranes are specialized forms of extracellular matrix with important functions in development. One collagen gene (Dcg1) was characterized in Drosophila melanogaster and shown to encode a collagen chain related to vertebrate basement membrane type IV collagen chains. Therefore, to access the functional importance of type IV collagen during Drosophila myogenesis, we adopted two different approaches to decrease the Dcg1 gene expression in Drosophila embryos. We describe, here, that the decrease in Dcg1 gene expression causes, in particular, defective muscle attachments. These mutant phenotypes suggest that type IV collagen acts to stabilize cell-matrix interactions.
Mechanisms of Development.
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