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      Development of the aboral domain in Nematostella requires β -catenin and the opposing activities of S ix3/6 and F rizzled5/8

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          ABSTRACT

          The development of the oral pole in cnidarians and the posterior pole in bilaterians is regulated by canonical Wnt signaling, whereas a set of transcription factors, including Six3/6 and FoxQ2, controls aboral development in cnidarians and anterior identity in bilaterians. However, it is poorly understood how these two patterning systems are initially set up in order to generate correct patterning along the primary body axis. Investigating the early steps of aboral pole formation in the sea anemone Nematostella vectensis, we found that, at blastula stage, oral genes are expressed before aboral genes and that Nvβ-catenin regulates both oral and aboral development. In the oral hemisphere, Nvβ-catenin specifies all subdomains except the oral-most, NvSnailA-expressing domain, which is expanded upon Nv β-catenin knockdown. In addition, Nvβ-catenin establishes the aboral patterning system by promoting the expression of NvSix3/6 at the aboral pole and suppressing the Wnt receptor NvFrizzled5/8 at the oral pole. NvFrizzled5/8 expression thereby gets restricted to the aboral domain. At gastrula stage, NvSix3/6 and NvFrizzled5/8 are both expressed in the aboral domain, but they have opposing activities, with NvSix3/6 maintaining and NvFrizzled5/8 restricting the size of the aboral domain. At planula stage, NvFrizzled5/8 is required for patterning within the aboral domain and for regulating the size of the apical organ by modulation of a previously characterized FGF feedback loop. Our findings suggest conserved roles for S ix3/6 and F rizzled5/8 in aboral/anterior development and reveal key functions for Nv β-catenin in the patterning of the entire oral-aboral axis of Nematostella.

          Abstract

          Summary: Wnt signalling and the Six3/6 transcription factors play conserved functions in primary axis patterning in bilateria, controlling aboral/anterior identity in Nematostella.

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          Most cited references58

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          Unexpected complexity of the Wnt gene family in a sea anemone.

          The Wnt gene family encodes secreted signalling molecules that control cell fate in animal development and human diseases. Despite its significance, the evolution of this metazoan-specific protein family is unclear. In vertebrates, twelve Wnt subfamilies were defined, of which only six have counterparts in Ecdysozoa (for example, Drosophila and Caenorhabditis). Here, we report the isolation of twelve Wnt genes from the sea anemone Nematostella vectensis, a species representing the basal group within cnidarians. Cnidarians are diploblastic animals and the sister-group to bilaterian metazoans. Phylogenetic analyses of N. vectensis Wnt genes reveal a thus far unpredicted ancestral diversity within the Wnt family. Cnidarians and bilaterians have at least eleven of the twelve known Wnt gene subfamilies in common; five subfamilies appear to be lost in the protostome lineage. Expression patterns of Wnt genes during N. vectensis embryogenesis indicate distinct roles of Wnts in gastrulation, resulting in serial overlapping expression domains along the primary axis of the planula larva. This unexpectedly complex inventory of Wnt family signalling factors evolved in early multi-cellular animals about 650 million years (Myr) ago, predating the Cambrian explosion by at least 100 Myr (refs 5, 8). It emphasizes the crucial function of Wnt genes in the diversification of eumetazoan body plans.
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            Animal Phylogeny and Its Evolutionary Implications*

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              Anteroposterior patterning in hemichordates and the origins of the chordate nervous system.

              The chordate central nervous system has been hypothesized to originate from either a dorsal centralized, or a ventral centralized, or a noncentralized nervous system of a deuterostome ancestor. In an effort to resolve these issues, we examined the hemichordate Saccoglossus kowalevskii and studied the expression of orthologs of genes that are involved in patterning the chordate central nervous system. All 22 orthologs studied are expressed in the ectoderm in an anteroposterior arrangement nearly identical to that found in chordates. Domain topography is conserved between hemichordates and chordates despite the fact that hemichordates have a diffuse nerve net, whereas chordates have a centralized system. We propose that the deuterostome ancestor may have had a diffuse nervous system, which was later centralized during the evolution of the chordate lineage.
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                Author and article information

                Journal
                Development
                Development
                DEV
                develop
                Development (Cambridge, England)
                The Company of Biologists Ltd
                0950-1991
                1477-9129
                15 May 2016
                15 May 2016
                : 143
                : 10
                : 1766-1777
                Affiliations
                [1 ]Sars Centre for Marine Molecular Biology, University of Bergen , Thormøhlensgt 55, Bergen 5008, Norway
                [2 ]Sorbonne Universités, UPMC Univ Paris 06, CNRS , Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), 181 chemin du Lazaret, Villefranche-sur-mer 06230, France
                Author notes
                [*]

                Present address: Institute of Biology Valrose, CNRS UMR7277 - INSERM U1091, Université Nice Sophia Antipolis, Nice 06108, France.

                Article
                DEV120931
                10.1242/dev.120931
                4874479
                26989171
                73f10272-7e9e-48b0-8c79-21f999b59e2c
                © 2016. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 10 December 2014
                : 8 March 2016
                Funding
                Funded by: Universitetet i Bergen, http://dx.doi.org/10.13039/501100005036;
                Categories
                Research Article

                Developmental biology
                anterior posterior axis,apical organ,axis formation,cnidaria,wnt signaling
                Developmental biology
                anterior posterior axis, apical organ, axis formation, cnidaria, wnt signaling

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