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4D Exploration of Genetic Data for an Extended Range of Tunicates

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4D Exploration of Genetic Data for an Extended Range of Tunicates ANISEED 2019: 4D exploration of genetic data for an extended range of tunicates Justine Dardaillon, Delphine Dauga, Paul Simion, Emmanuel Faure, Takeshi Onuma, Melissa Debiasse, Alexandra Louis, Kazuhiro Nitta, Magali Naville, Lydia Besnardeau, et al. To cite this version: Justine Dardaillon, Delphine Dauga, Paul Simion, Emmanuel Faure, Takeshi Onuma, et al.. ANISEED 2019: 4D exploration of genetic data for an extended range of tunicates. Nucleic Acids Research, Oxford University Press, 2019, 10.1093/nar/gkz955. hal-02415680 HAL Id: hal-02415680 https://hal.archives-ouvertes.fr/hal-02415680 Submitted on 18 Dec 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Nucleic Acids Research, 2019 1 doi: 10.1093/nar/gkz955 ANISEED 2019: 4D exploration of genetic data for an extended range of tunicates Justine Dardaillon1, Delphine Dauga 2, Paul Simion 3, Emmanuel Faure 4, Takeshi Downloaded from https://academic.oup.com/nar/advance-article-abstract/doi/10.1093/nar/gkz955/5611675 by LIRMM user on 18 December 2019 A. Onuma 5, Melissa B. DeBiasse 6,7, Alexandra Louis 8, Kazuhiro R. Nitta 9, Magali Naville 10, Lydia Besnardeau11, Wendy Reeves12, Kai Wang13, Marie Fagotto14, Marion Gueroult-Bellone´ 2, Shigeki Fujiwara 15,Remi´ Dumollard 11, Michael Veeman 12, Jean-Nicolas Volff 10, Hugues Roest Crollius 8, Emmanuel Douzery 3, Joseph F. Ryan 6,7, Bradley Davidson16, Hiroki Nishida 5, Christelle Dantec 1,*,† and Patrick Lemaire 1,*,† 1CRBM, Universite´ de Montpellier, CNRS, Montpellier, France, 2Bioself Communication; 28 rue de la Bibliotheque,` F-13001 Marseille, France, 3ISEM, Universite´ de Montpellier, CNRS, IRD, EPHE, Montpellier, France, 4Laboratoire d’Informatique de Robotique et de Microelectronique´ de Montpellier (LIRMM), Universite´ de Montpellier, CNRS, Montpellier, France, 5Department of Biological Sciences, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka, Osaka 560-0043, Japan, 6Whitney Laboratory for Marine Bioscience, 9505 Ocean Shore Boulevard, St. Augustine, FL 32080, USA, 7Department of Biology, University of Florida, 220 Bartram Hall, Gainesville, FL 32611, USA, 8DYOGEN, IBENS, Departement´ de Biologie, Ecole Normale Superieure,´ CNRS, Inserm, PSL Research University, F-75005 Paris, France, 9IBDM, Universite´ Aix-Marseille, CNRS, Marseille, France, 10Institut de Genomique´ Fonctionnelle de Lyon, Universite´ de Lyon, Ecole Normale Superieure´ de Lyon, Universite´ Claude Bernard Lyon 1, CNRS; 46 allee´ d’Italie, F-69364 Lyon, France, 11Laboratoire de Biologie du Developpement´ de Villefranche-sur-mer (LBDV), Sorbonne Universites,´ Universite´ Pierre-et-Marie-Curie, CNRS; Quai de la Darse, F-06234 Villefranche-sur-Mer Cedex, France., 12Division of Biology, Kansas State University, Manhattan, KS 66506, USA, 13State Key Laboratory of Cell Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yueyang Road, Shanghai 200031, China, 14Universitede´ Montpellier, Montpellier, France, 15Department of Chemistry and Biotechnology, Faculty of Science and Technology, Kochi University, Kochi-shi, Kochi, Japan and 16Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA Received September 16, 2019; Revised October 08, 2019; Editorial Decision October 09, 2019; Accepted October 11, 2019 ABSTRACT other genetic elements, including repeated elements and cis-regulatory modules. Gene expression pro- ANISEED (https://www.aniseed.cnrs.fr)isthemain files for several thousand genes are formalized in model organism database for the worldwide com- both wild-type and experimentally-manipulated con- munity of scientists working on tunicates, the ver- ditions, using formal anatomical ontologies. These tebrate sister-group. Information provided for each data can be explored through three complementary species includes functionally-annotated gene and types of browsers, each offering a different view- transcript models with orthology relationships within point. A developmental browser summarizes the in- tunicates, and with echinoderms, cephalochordates formation in a gene- or territory-centric manner. and vertebrates. Beyond genes the system describes Advanced genomic browsers integrate the genetic *To whom correspondence should be addressed. Tel: +33 4 34 35 94 00; Email: [email protected] Correspondence may also be addressed to Christelle Dantec. Tel: +33 4 34 35 94 00; Email: [email protected] †The authors wish it to be known that, in their opinion, the last two authors should be regarded as Joint Last Authors. Present addresses: Paul Simion, Laboratory of Evolutionary Genetics and Ecology, URBE, NAXYS, University of Namur, Namur, Belgium. Kazuhiro R. Nitta, Juntendo University, Graduate School of Medicine, Diagnostics and Therapeutics of Intractable Diseases Intractable Disease Research Center, Tokyo, Japan. C The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. 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. 2 Nucleic Acids Research, 2019 features surrounding genes or gene sets within a phylogenies as a comparative framework to study the devel- species. A Genomicus synteny browser explores the opmental programs of different species; (iii) a multispecies conservation of local gene order across deuteros- genomic browser to visualize the position of genetic features tome. This new release covers an extended taxo- along chromosomes; (iv) a Genomicus synteny browser (25) nomic range of 14 species, including for the first time to analyse the evolution of gene order across tunicate and other chordate genomes. Care was taken during the devel- a non-ascidian species, the appendicularian Oiko- Downloaded from https://academic.oup.com/nar/advance-article-abstract/doi/10.1093/nar/gkz955/5611675 by LIRMM user on 18 December 2019 opment of ANISEED that the tool remains generic and pleura dioica. Functional annotations, provided for adaptable with minimal effort to any developmental model each species, were enhanced through a combination organism. of manual curation of gene models and the develop- During the preparation of ANISEED 2019, we added ment of an improved orthology detection pipeline. Fi- three additional solitary or colonial ascidian species with nally, gene expression profiles and anatomical terri- recently sequenced genome: Molgula occulta, Corella in- tories can be explored in 4D online through the newly flata and Botryllus leachii and extended for the first time developed Morphonet morphogenetic browser. the system to a non-ascidian species, the appendicularian Oikopleura dioica. We significantly improved the functional annotation of genes, through the manual curation of gene INTRODUCTION model sets in some species and the refinement of our orthol- Tunicates are marine invertebrates with a key phylogenetic ogy assignment procedure, which now detects vertebrate or- position as the sister group of the vertebrates (1,2). Three thologs for a majority of genes from all ascidians species, major groups of tunicates have been classically described. including the main ascidian model species, Ciona robusta The sessile ascidians form the largest group with several (formerly referred to as Ciona intestinalis type A). We en- thousand species listed. Two additional groups of tuni- riched the genomics datasets related to the control of gene cates have a pelagic life-style and rapid molecular evolu- expression in existing and new species. Finally, we inter- tion rates, the thaliaceans and the appendicularians. Their faced the developmental browser of ANISEED 2019 to the phylogenetic position with respect to ascidians has long re- MORPHONET morphogenetic browser, allowing 4D ex- mained debated. Molecular phylogenies suggest that the ploration of gene expression profiles. fast-evolving appendicularians are the sister group of all other tunicates, and that thaliaceans form a monophyletic Extension of the taxonomic range covered group nested within ascidians (3,4) Tunicates studies have led to important discoveries in a In addition to the ten ANISEED 2017 species, three new variety of scientific fields. They illuminated the origin of ascidian species, for which genome and gene models were vertebrate features, including the neural crest (5) or the sec- recently made available, were added to the portal. The soli- ondary heart field (6,7). The simplicity of ascidian embryos tary stolidobranch Molgula occulta is so closely related to makes them ideal to decipher the regulatory networks con- M. oculata that hybrids between these two species can be trolling embryonic development (8–10) and their evolution
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