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      Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis

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          Abstract

          Animal evolution is closely linked to the emergence of the nervous system. At present it is unknown how the basic mechanisms of neural induction and formation of central nervous systems evolved. We addressed this question in Nematostella vectensis, a member of cnidarians, the ancient sister group of bilaterians. We found that β-catenin signalling is crucial for the early induction of the embryonic nervous system. β-Catenin activity at the blastopore induces specific neurogenic genes required for development of the oral nervous system. β-Catenin signalling induces also Bmp signalling, which, at later larval stages, becomes indispensible for the maintenance and asymmetric patterning of the oral nervous system along the primary and secondary (directive) axes. We hypothesize that the consecutive and functionally linked involvement of β-catenin and Bmp signalling in the formation of the cnidarian oral nervous system reflects an ancestral mechanism that evolved before the cnidarian/bilaterian split.

          Abstract

          The bilaterian central nervous system is thought to have evolved from a cnidarian-like ancestor, but the mechanisms of neural induction in cnidarians are largely unknown. Here the authors study the cnidarian Nematostella vectensis and show that β-catenin signalling is crucial for the early induction of its embryonic nervous system, suggesting evolutionary roots for this pathway.

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          Most cited references 64

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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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              The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution.

              An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. Toward this goal, we have sequenced, assembled, and annotated the genome of the ctenophore Mnemiopsis leidyi. Our phylogenomic analyses of both amino acid positions and gene content suggest that ctenophores rather than sponges are the sister lineage to all other animals. Mnemiopsis lacks many of the genes found in bilaterian mesodermal cell types, suggesting that these cell types evolved independently. The set of neural genes in Mnemiopsis is similar to that of sponges, indicating that sponges may have lost a nervous system. These results present a newly supported view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                23 December 2014
                : 5
                Affiliations
                [1 ]Department of Molecular Evolution and Genomics, Centre for Organismal Studies (COS), Heidelberg University , Im Neuenheimer Feld 329, 69120 Heidelberg, Germany
                [2 ]Department of Biophysics, Graduate School of Science, Kyoto University , Kitashirakawa-Oiwake, Sakyo-ku, Kyoto 606-8502, Japan
                [3 ]Center for the Promotion of Integrated Sciences, The Graduate University for Advanced Studies , Higashiyama 5-1, Myodaiji, Okazaki 444-8585, Japan
                Author notes
                Article
                ncomms6536
                10.1038/ncomms6536
                4284808
                25534229
                Copyright © 2014, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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