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      Molecular characterization of the apical organ of the anthozoan Nematostella vectensis

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          Abstract

          Apical organs are sensory structures present in many marine invertebrate larvae where they are considered to be involved in their settlement, metamorphosis and locomotion. In bilaterians they are characterised by a tuft of long cilia and receptor cells and they are associated with groups of neurons, but their relatively low morphological complexity and dispersed phylogenetic distribution have left their evolutionary relationship unresolved. Moreover, since apical organs are not present in the standard model organisms, their development and function are not well understood. To provide a foundation for a better understanding of this structure we have characterised the molecular composition of the apical organ of the sea anemone Nematostella vectensis. In a microarray-based comparison of the gene expression profiles of planulae with either a wildtype or an experimentally expanded apical organ, we identified 78 evolutionarily conserved genes, which are predominantly or specifically expressed in the apical organ of Nematostella. This gene set comprises signalling molecules, transcription factors, structural and metabolic genes. The majority of these genes, including several conserved, but previously uncharacterized ones, are potentially involved in different aspects of the development or function of the long cilia of the apical organ. To demonstrate the utility of this gene set for comparative analyses, we further analysed the expression of a subset of previously uncharacterized putative orthologs in sea urchin larvae and detected expression for twelve out of eighteen of them in the apical domain. Our study provides a molecular characterization of the apical organ of Nematostella and represents an informative tool for future studies addressing the development, function and evolutionary history of apical organ cells.

          Highlights

          • Microarray-based characterization of the apical organ in Nematostella vectensis.

          • Apical organ expression of 78 conserved genes confirmed by in situ hybridization.

          • Putative orthologous genes in sea urchin are also expressed in its apical organ.

          • The data present a molecular signature for comparative studies of apical organs.

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          Most cited references105

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          Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

          Sea anemones are seemingly primitive animals that, along with corals, jellyfish, and hydras, constitute the oldest eumetazoan phylum, the Cnidaria. Here, we report a comparative analysis of the draft genome of an emerging cnidarian model, the starlet sea anemone Nematostella vectensis. The sea anemone genome is complex, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes, implying that the genome of the eumetazoan ancestor was similarly complex. Nearly one-fifth of the inferred genes of the ancestor are eumetazoan novelties, which are enriched for animal functions like cell signaling, adhesion, and synaptic transmission. Analysis of diverse pathways suggests that these gene "inventions" along the lineage leading to animals were likely already well integrated with preexisting eukaryotic genes in the eumetazoan progenitor.
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            Kinesin superfamily motor proteins and intracellular transport.

            Intracellular transport is fundamental for cellular function, survival and morphogenesis. Kinesin superfamily proteins (also known as KIFs) are important molecular motors that directionally transport various cargos, including membranous organelles, protein complexes and mRNAs. The mechanisms by which different kinesins recognize and bind to specific cargos, as well as how kinesins unload cargo and determine the direction of transport, have now been identified. Furthermore, recent molecular genetic experiments have uncovered important and unexpected roles for kinesins in the regulation of such physiological processes as higher brain function, tumour suppression and developmental patterning. These findings open exciting new areas of kinesin research.
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              Assessing the root of bilaterian animals with scalable phylogenomic methods.

              A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.
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                Author and article information

                Contributors
                Journal
                Dev Biol
                Dev. Biol
                Developmental Biology
                Elsevier
                0012-1606
                1095-564X
                01 February 2015
                01 February 2015
                : 398
                : 1
                : 120-133
                Affiliations
                [a ]Sars Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt 55, 5008 Bergen, Norway
                [b ]Department of Genetics, Evolution and Environment, University College London, Gower Street, London WC1E 6BT, UK
                Author notes
                [* ]Correspondence to: Sars International Centre for Marine Molecular Biology, Thormøhlensgt 55, N-5008 Bergen, Norway. fabian.rentzsch@ 123456sars.uib.no
                [1]

                Present address: Developmental Biology Unit, Observatoire Oceanologique, 06234 Villefranche-sur-mer, France.

                Article
                S0012-1606(14)00607-1
                10.1016/j.ydbio.2014.11.019
                4300403
                25478911
                8c4eaa62-6dc4-4293-9bf0-ba042721cad5
                © 2014 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

                History
                : 4 June 2014
                : 16 October 2014
                : 13 November 2014
                Categories
                Evolution of Developmental Control Mechanisms

                Developmental biology
                apical organ,nematostella,sea urchin,cilia,life cycle,fgf
                Developmental biology
                apical organ, nematostella, sea urchin, cilia, life cycle, fgf

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