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      Conservation and divergence of bHLH genes in the calcisponge Sycon ciliatum

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          Abstract

          Background

          Basic Helix-Loop-Helix (bHLH) genes encode a large family of eukaryotic transcription factors, categorized into six high-order groups: pan-eukaryotic group B involved in regulation of cell cycle, metabolism, and development; holozoan-specific groups C and F involved in development and maintenance of homeostasis; and metazoan-specific groups A, D and E including well-studied genes, such as Atonal, Twist and Hairy, with diverse developmental roles including control of morphogenesis and specification of neurons. Current scenarios of bHLH evolution in animals are mainly based on the bHLH gene set found in the genome of demosponge Amphimedon queenslandica. In this species, the majority of the 21 identified bHLH genes belong to group B, and the single group A gene is orthologous to several neurogenic bilaterian subfamilies, including atonal and neurogenin.

          Results

          Given recently discovered differences in developmental toolkit components between siliceous and calcareous sponges, we have carried out genome-wide analysis of bHLH genes in Sycon ciliatum, an emerging calcisponge model. We identified 30 bHLH genes in this species, representing 12 individual families, including four group A families not found in Amphimedon, and two larger family groupings. Notably, the families represented in Sycon are only partially overlapping with those represented in Amphimedon. Developmental expression analysis of a subset of the identified genes revealed patterns consistent with deeply conserved roles, such as specification of sensory cells by Atona- related and stem cells by Myc genes.

          Conclusions

          Our results demonstrate independent gene loss events in demosponges and calcisponges, implying a complex bHLH toolkit in the last common metazoan ancestor.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13227-016-0060-8) contains supplementary material, which is available to authorized users.

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          Most cited references42

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          PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference

          PHYML Online is a web interface to PHYML, a software that implements a fast and accurate heuristic for estimating maximum likelihood phylogenies from DNA and protein sequences. This tool provides the user with a number of options, e.g. nonparametric bootstrap and estimation of various evolutionary parameters, in order to perform comprehensive phylogenetic analyses on large datasets in reasonable computing time. The server and its documentation are available at .
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            The Amphimedon queenslandica genome and the evolution of animal complexity.

            Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
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              The Ctenophore Genome and the Evolutionary Origins of Neural Systems

              The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores, or comb jellies, have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here, we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well-recognized in ctenophores, many bilaterian neuron-specific genes and genes of “classical” neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.
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                Author and article information

                Contributors
                sofia.valerofortunato@jcu.edu.au
                +33 1 57 27 80 02 , michel.vervoort@ijm.fr
                marcin.adamski@anu.edu.au
                +61 2 6125 1631 , maja.adamska@anu.edu.au
                Journal
                EvoDevo
                Evodevo
                EvoDevo
                BioMed Central (London )
                2041-9139
                14 October 2016
                14 October 2016
                2016
                : 7
                : 23
                Affiliations
                [1 ]Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
                [2 ]Institut Jacques Monod – CNRS, Université Paris Diderot, 75005 Paris Cedex 13, France
                [3 ]ARC Centre for Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811 Australia
                [4 ]Research School of Biology, Australian National University, Canberra, Australia
                Author information
                http://orcid.org/0000-0002-4223-8450
                Article
                60
                10.1186/s13227-016-0060-8
                5064789
                27757221
                05412cf9-3b4b-40ad-8a4f-24b68c517aec
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 19 July 2016
                : 27 September 2016
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Developmental biology
                bhlh,transcription factors,developmental regulatory genes,sycon ciliatum,sponges,evolution

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