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      Reiterative use of FGF signaling in mesoderm development during embryogenesis and metamorphosis in the hemichordate Ptychodera flava

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          Abstract

          Background

          Mesoderm is generally considered to be a germ layer that is unique to Bilateria, and it develops into diverse tissues, including muscle, and in the case of vertebrates, the skeleton and notochord. Studies on various deuterostome animals have demonstrated that fibroblast growth factor (FGF) signaling is required for the formation of many mesodermal structures, such as vertebrate somites, from which muscles are differentiated, and muscles in sea urchin embryos, suggesting an ancient role of FGF signaling in muscle development. However, the formation of trunk muscles in invertebrate chordates is FGF-independent, leading to ambiguity about this ancient role in deuterostomes. To further understand the role of FGF signaling during deuterostome evolution, we investigated the development of mesodermal structures during embryogenesis and metamorphosis in Ptychodera flava, an indirect-developing hemichordate that has larval morphology similar to echinoderms and adult body features that are similar to chordates.

          Results

          Here we show that genes encoding FGF ligands, FGF receptors and transcription factors that are known to be involved in mesoderm formation and myogenesis are expressed dynamically during embryogenesis and metamorphosis. FGF signaling at the early gastrula stage is required for the specification of the mesodermal cell fate in P. flava. The mesoderm cells are then differentiated stepwise into the hydroporic canal, the pharyngeal muscle and the muscle string; formation of the last two muscular structures are controlled by FGF signaling. Moreover, augmentation of FGF signaling during metamorphosis accelerated the process, facilitating the transformation from cilia-driven swimming larvae into muscle-driven worm-like juveniles.

          Conclusions

          Our data show that FGF signaling is required for mesoderm induction and myogenesis in the P. flava embryo, and it is reiteratively used for the morphological transition during metamorphosis. The dependence of muscle development on FGF signaling in both planktonic larvae and sand-burrowing worms supports its ancestral role in deuterostomes.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-018-1235-9) contains supplementary material, which is available to authorized users.

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          Most cited references60

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          Evolution of the Fgf and Fgfr gene families.

          Fibroblast growth factors (Fgfs) and Fgf receptors (Fgfrs) comprise a signaling system that is conserved throughout metazoan evolution. Twenty-two Fgfs and four Fgfrs have been identified in humans and mice. During evolution, the Fgf family appears to have expanded in two phases. In the first phase, during early metazoan evolution, Fgfs expanded from two or three to six genes by gene duplication. In the second phase, during the evolution of early vertebrates, the Fgf family expanded by two large-scale gen(om)e duplications. By contrast, the Fgfr family has expanded only in the second phase. However, the acquisition of alternative splicing by Fgfrs has increased their functional diversity. The mechanisms that regulate alternative splicing have been conserved since the divergences of echinoderms and vertebrates. The expansion of the Fgf and Fgfr gene families has enabled this signaling system to acquire functional diversity and, therefore, an almost ubiquitous involvement in developmental and physiological processes.
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            Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida.

            Deuterostomes comprise vertebrates, the related invertebrate chordates (tunicates and cephalochordates) and three other invertebrate taxa: hemichordates, echinoderms and Xenoturbella. The relationships between invertebrate and vertebrate deuterostomes are clearly important for understanding our own distant origins. Recent phylogenetic studies of chordate classes and a sea urchin have indicated that urochordates might be the closest invertebrate sister group of vertebrates, rather than cephalochordates, as traditionally believed. More remarkable is the suggestion that cephalochordates are closer to echinoderms than to vertebrates and urochordates, meaning that chordates are paraphyletic. To study the relationships among all deuterostome groups, we have assembled an alignment of more than 35,000 homologous amino acids, including new data from a hemichordate, starfish and Xenoturbella. We have also sequenced the mitochondrial genome of Xenoturbella. We support the clades Olfactores (urochordates and vertebrates) and Ambulacraria (hemichordates and echinoderms). Analyses using our new data, however, do not support a cephalochordate and echinoderm grouping and we conclude that chordates are monophyletic. Finally, nuclear and mitochondrial data place Xenoturbella as the sister group of the two ambulacrarian phyla. As such, Xenoturbella is shown to be an independent phylum, Xenoturbellida, bringing the number of living deuterostome phyla to four.
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              Animal Phylogeny and Its Evolutionary Implications*

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                Author and article information

                Contributors
                y3qo470@gmail.com
                HST9@pitt.edu
                jkyu@gate.sinica.edu.tw
                yhsu@gate.sinica.edu.tw
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                3 August 2018
                3 August 2018
                2018
                : 18
                Affiliations
                [1 ]ISNI 0000 0000 9360 4962, GRID grid.469086.5, Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, , National Chung Hsing University and Academia Sinica, ; Taipei, 11529 Taiwan
                [2 ]ISNI 0000 0001 2287 1366, GRID grid.28665.3f, Institute of Cellular and Organismic Biology, Academia Sinica, ; 128 Academia Rd., Sec. 2, Nankang, Taipei, 11529 Taiwan
                [3 ]ISNI 0000 0004 0532 3749, GRID grid.260542.7, Graduate Institute of Biotechnology, , National Chung Hsing University, ; Taichung, 40227 Taiwan
                [4 ]ISNI 0000 0004 0532 3749, GRID grid.260542.7, Biotechnology Center, , National Chung Hsing University, ; Taichung, 40227 Taiwan
                Article
                1235
                10.1186/s12862-018-1235-9
                6091094
                30075704
                b1e931c5-27ba-45b4-8d26-645fc6efb5a6
                © The Author(s). 2018

                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.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: MOST-103-2311-B-001-030-MY3
                Award ID: MOST-106-2321-B-001-039
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Evolutionary Biology
                fgf,mesoderm,ptychodera flava,hemichordate,metamorphosis
                Evolutionary Biology
                fgf, mesoderm, ptychodera flava, hemichordate, metamorphosis

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