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      New Non-Bilaterian Transcriptomes Provide Novel Insights into the Evolution of Coral Skeletomes

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          Abstract

          A general trend observed in animal skeletomes—the proteins occluded in animal skeletons—is the copresence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend. However, distributions and phylogenetic analyses of biomineralization-related genes are often based on only a few species, with other anthozoan calcifiers such as octocorals (soft corals), not being fully considered. We de novo assembled the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published nonbilaterian transcriptome resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. Cnidaria shared no skeletome proteins with Placozoa or Ctenophora, but did share some skeletome proteins with Porifera, such as galaxin-related proteins. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes such as secreted acidic proteins, scleritin, and carbonic anhydrases, and propose an early, single biomineralization-recruitment event for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia–Scleractinia transition, but appears to be associated with protein secretion into the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e., aragonite/calcite) with no differences in the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins such as galaxins and SCRiP-3a could represent instances of commonality.

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          Most cited references61

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            The Cambrian conundrum: early divergence and later ecological success in the early history of animals.

            Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.
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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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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                November 2019
                13 September 2019
                13 September 2019
                : 11
                : 11
                : 3068-3081
                Affiliations
                [1 ] Department of Earth and Environmental Sciences , Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Munich, Germany
                [2 ] GeoBio-Center LMU, Ludwig-Maximilians-Universität München , Munich, Germany
                [3 ] SNSB—Bayerische Staatssammlung für Paläontologie und Geologie, Munich, Germany
                Author notes
                Corresponding author: E-mail: sergio.vargas@ 123456lmu.de .
                Author information
                http://orcid.org/0000-0002-6380-7421
                http://orcid.org/0000-0001-8704-1339
                Article
                evz199
                10.1093/gbe/evz199
                6824150
                31518412
                3a426b32-57f3-4dbd-ab25-efda55bfb5c4
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 9 September 2019
                Page count
                Pages: 14
                Funding
                Funded by: German Research Foundation (DFG)
                Award ID: Va1146-2/1
                Funded by: LMU Munich’s Institutional Strategy
                Award ID: Wo896/18-1
                Funded by: Marie Skłodowska-Curie
                Award ID: 764840
                Categories
                Research Article

                Genetics
                coral calcification,biomineralization,octocorallia,galaxin,molecular evolution,scleractinia
                Genetics
                coral calcification, biomineralization, octocorallia, galaxin, molecular evolution, scleractinia

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