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1. Eph and Ephrin function in dispersal and epithelial insertion of pigmented immunocytes in sea urchin embryos

Author

Oliver A Krupke, Ivona Zysk, Dan O Mellott, and Robert D Burke

Subjects
purple sea urchin, Strongylocentrouts, purpuratus, deuterostome, Medicine, Science, Biology (General), QH301-705.5
Abstract

The mechanisms that underlie directional cell migration are incompletely understood. Eph receptors usually guide migrations of cells by exclusion from regions expressing Ephrin. In sea urchin embryos, pigmented immunocytes are specified in vegetal epithelium, transition to mesenchyme, migrate, and re-enter ectoderm, distributing in dorsal ectoderm and ciliary band, but not ventral ectoderm. Immunocytes express Sp-Eph and Sp-Efn is expressed throughout dorsal and ciliary band ectoderm. Interfering with expression or function of Sp-Eph results in rounded immunocytes entering ectoderm but not adopting a dendritic form. Expressing Sp-Efn throughout embryos permits immunocyte insertion in ventral ectoderm. In mosaic embryos, immunocytes insert preferentially in ectoderm expressing Sp-Efn. We conclude that Sp-Eph signaling is necessary and sufficient for epithelial insertion. As well, we propose that immunocytes disperse when Sp-Eph enhances adhesion, causing haptotactic movement to regions of higher ligand abundance. This is a distinctive example of Eph/Ephrin signaling acting positively to pattern migrating cells.

Published
2016
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2. Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

Author

Jonathan E. Valencia, Roberto Feuda, Dan O. Mellott, Robert D. Burke, and Isabelle S. Peter

Subjects
Cell type evolution, Photoreceptors, Regulatory state, GRN evolution, Echinoderms, Biology (General), QH301-705.5
Abstract

Abstract Background The evolutionary history of cell types provides insights into how morphological and functional complexity arose during animal evolution. Photoreceptor cell types are particularly broadly distributed throughout Bilateria; however, their evolutionary relationship is so far unresolved. Previous studies indicate that ciliary photoreceptors are homologous at least within chordates, and here, we present evidence that a related form of this cell type is also present in echinoderm larvae. Results Larvae of the purple sea urchin Strongylocentrotus purpuratus have photoreceptors that are positioned bilaterally in the oral/anterior apical neurogenic ectoderm. Here, we show that these photoreceptors express the transcription factor Rx, which is commonly expressed in ciliary photoreceptors, together with an atypical opsin of the GO family, opsin3.2, which localizes in particular to the cilia on the cell surface of photoreceptors. We show that these ciliary photoreceptors express the neuronal marker synaptotagmin and are located in proximity to pigment cells. Furthermore, we systematically identified additional transcription factors expressed in these larval photoreceptors and found that a majority are orthologous to transcription factors expressed in vertebrate ciliary photoreceptors, including Otx, Six3, Tbx2/3, and Rx. Based on the developmental expression of rx, these photoreceptors derive from the anterior apical neurogenic ectoderm. However, genes typically involved in eye development in bilateria, including pax6, six1/2, eya, and dac, are not expressed in sea urchin larval photoreceptors but are instead co-expressed in the hydropore canal. Conclusions Based on transcription factor expression, location, and developmental origin, we conclude that the sea urchin larval photoreceptors constitute a cell type that is likely homologous to the ciliary photoreceptors present in chordates.

Published
2021
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3. Notch signaling patterns neurogenic ectoderm and regulates the asymmetric division of neural progenitors in sea urchin embryos

Author

Robert D. Burke, Jordan Thisdelle, and Dan O Mellott

Subjects
0301 basic medicine, Embryo, Nonmammalian, Morpholino, Neurogenesis, Green Fluorescent Proteins, Notch signaling pathway, Mitosis, Ectoderm, Apoptosis, Biology, Models, Biological, 03 medical and health sciences, Neural Stem Cells, Live cell imaging, medicine, Animals, Progenitor cell, Molecular Biology, SOX Transcription Factors, Body Patterning, Genetics, Neurons, Receptors, Notch, Asymmetric Cell Division, Cell biology, Gastrulation, 030104 developmental biology, medicine.anatomical_structure, Hes3 signaling axis, Sea Urchins, Developmental Biology, Signal Transduction
Abstract

We have examined regulation of neurogenesis by Delta/Notch signaling in sea urchin embryos. At gastrulation neural progenitors enter S-phase coincident with expression of Sp-SoxC. We used a BAC (bacterial artificial chromosome) containing GFP knocked into the Sp-SoxC locus to label neural progenitors. Live imaging and immunolocalizations indicate that Sp-SoxC-expressing cells divide producing pairs of adjacent cells expressing GFP. Over an interval of about 6 h, one cell fragments, undergoes apoptosis, and expresses high levels of activated Caspase3. A Notch reporter indicates that Notch signaling is activated in cells adjacent to cells expressing Sp-SoxC. Inhibition of γ-secretase, injection of Sp-Delta morpholinos, or CRISPR/Cas9-induced mutation of Sp-Delta results in supernumerary neural progenitors and neurons. Interfering with Notch signaling increases neural progenitor recruitment and pairs of neural progenitors. Thus, Notch signaling restricts the number of neural progenitors recruited and regulates the fate of progeny of the asymmetric division. We propose a model in which localized signaling converts ectodermal and ciliary band cells to neural progenitors that divide asymmetrically to produce a neural precursor and an apoptotic cell.

Published
2017

5. Eph and Ephrin function in dispersal and epithelial insertion of pigmented immunocytes in sea urchin embryos

Author

Ivona Zysk, Dan O Mellott, Oliver A. Krupke, and Robert D. Burke

Subjects
0301 basic medicine, animal structures, QH301-705.5, Science, Mesenchyme, purpuratus, Ectoderm, Biology, General Biochemistry, Genetics and Molecular Biology, Epithelium, 03 medical and health sciences, Cell Movement, medicine, Ephrin, Animals, Biology (General), deuterostome, purple sea urchin, Deuterostome, General Immunology and Microbiology, Receptor, EphA1, General Neuroscience, Erythropoietin-producing hepatocellular (Eph) receptor, Cell migration, Embryo, General Medicine, Anatomy, biology.organism_classification, biological factors, Cell biology, 030104 developmental biology, medicine.anatomical_structure, Sea Urchins, embryonic structures, Medicine, Other, biological phenomena, cell phenomena, and immunity, Ephrins, Strongylocentrouts, Research Article
Abstract

The mechanisms that underlie directional cell migration are incompletely understood. Eph receptors usually guide migrations of cells by exclusion from regions expressing Ephrin. In sea urchin embryos, pigmented immunocytes are specified in vegetal epithelium, transition to mesenchyme, migrate, and re-enter ectoderm, distributing in dorsal ectoderm and ciliary band, but not ventral ectoderm. Immunocytes express Sp-Eph and Sp-Efn is expressed throughout dorsal and ciliary band ectoderm. Interfering with expression or function of Sp-Eph results in rounded immunocytes entering ectoderm but not adopting a dendritic form. Expressing Sp-Efn throughout embryos permits immunocyte insertion in ventral ectoderm. In mosaic embryos, immunocytes insert preferentially in ectoderm expressing Sp-Efn. We conclude that Sp-Eph signaling is necessary and sufficient for epithelial insertion. As well, we propose that immunocytes disperse when Sp-Eph enhances adhesion, causing haptotactic movement to regions of higher ligand abundance. This is a distinctive example of Eph/Ephrin signaling acting positively to pattern migrating cells. DOI: http://dx.doi.org/10.7554/eLife.16000.001, eLife digest During animal development, numerous cells move around the embryo to form and shape the growing tissues. As these cells move, they are guided to their destination by molecular cues. The embryo’s tissues produce these cues and the cues can either repel or attract migrating cells. Ephrins are a large and well-studied family of proteins that serve as guidance cues and are found on the surface of certain types of cells. Some migrating cells have receptors for Ephrin and are repelled from tissues that contain Ephrin proteins. In these cases, the repulsive interaction between Ephrins and cells with receptors ensures that migrating cells avoid certain locations and reach the correct final destination. The sea urchin is an important model organism for studying how animals develop and in particular how genes control animal development. This is in part because these animals can be easily manipulated in the laboratory and are more closely related to animals with backbones than many other model organisms. Sea urchins also have a relatively simple set of genes; many of which are similar to the human form of the gene. In sea urchin embryos, pigmented cells called immunocytes are known to migrate from one region of the embryo to another where they form part of its immune system. However it was not clear what guides this migration. Sea urchins produce one type of Ephrin protein and its associated receptor, and now Krupke et al. show that immunocytes carry the receptor for Ephrin and migrate to embryonic tissues that produce high levels of this Ephrin. This finding suggested that the Ephrin is actually attracting the immunocytes to their final destination rather than repelling them. Further experiments supported this idea and revealed that immunocytes that lack the Ephrin receptor fail to enter the right tissue. Similarly, altering the pattern of Ephrin in the embryo’s tissues altered immunocyte migration in a predictable way. These findings of Krupke et al. suggest that Ephrin and its receptor have changed their biological functions during evolution of animals. This raises a number of questions for future research including whether the molecular mechanisms used by Ephrin and its receptor to attract immunocytes in sea urchins is the same as that used to repel cells in other species. DOI: http://dx.doi.org/10.7554/eLife.16000.002

Published
2016

6. A genomic view of the sea urchin nervous system

Author

Allison M. Churcher, Dan O Mellott, G. Murray, Matthew L. Rowe, Finn Hallböök, Diana Wang, Michael C. Thorndyke, Robert D. Burke, Nansheng Chen, Shuguang Liang, Lynne M. Angerer, Bruce P. Brandhorst, Cavit Agca, Glen Humphrey, Shunsuke Yaguchi, John S. Taylor, Karen Wilson, Xiuqian Mu, Takae Kiyama, William Klein, Robert Piotr Olinski, and Maurice R. Elphick

Subjects
Evolution, Gene regulatory network, Nerve Tissue Proteins, Deuterostome, Nervous System, Article, Connexins, 03 medical and health sciences, 0302 clinical medicine, Neurobiology, biology.animal, Animals, Humans, 14. Life underwater, Molecular Biology, Sea urchin, Transcription factor, Phylogeny, 030304 developmental biology, Mammals, Neurons, Genetics, 0303 health sciences, Genome, Echinoderm, biology, Genomics, Cell Biology, biology.organism_classification, Strongylocentrotus purpuratus, Axons, Electrophysiology, Neural development, Larva, Sea Urchins, Synapses, PAX6, Tube feet, 030217 neurology & neurosurgery, Transcription Factors, Developmental Biology
Abstract

The sequencing of the Strongylocentrotus purpuratus genome provides a unique opportunity to investigate the function and evolution of neural genes. The neurobiology of sea urchins is of particular interest because they have a close phylogenetic relationship with chordates, yet a distinctive pentaradiate body plan and unusual neural organization. Orthologues of transcription factors that regulate neurogenesis in other animals have been identified and several are expressed in neurogenic domains before gastrulation indicating that they may operate near the top of a conserved neural gene regulatory network. A family of genes encoding voltage-gated ion channels is present but, surprisingly, genes encoding gap junction proteins (connexins and pannexins) appear to be absent. Genes required for synapse formation and function have been identified and genes for synthesis and transport of neurotransmitters are present. There is a large family of G-protein-coupled receptors, including 874 rhodopsin-type receptors, 28 metabotropic glutamate-like receptors and a remarkably expanded group of 161 secretin receptor-like proteins. Absence of cannabinoid, lysophospholipid and melanocortin receptors indicates that this group may be unique to chordates. There are at least 37 putative G-protein-coupled peptide receptors and precursors for several neuropeptides and peptide hormones have been identified, including SALMFamides, NGFFFamide, a vasotocin-like peptide, glycoprotein hormones and insulin/insulin-like growth factors. Identification of a neurotrophin-like gene and Trk receptor in sea urchin indicates that this neural signaling system is not unique to chordates. Several hundred chemoreceptor genes have been predicted using several approaches, a number similar to that for other animals. Intriguingly, genes encoding homologues of rhodopsin, Pax6 and several other key mammalian retinal transcription factors are expressed in tube feet, suggesting tube feet function as photosensory organs. Analysis of the sea urchin genome presents a unique perspective on the evolutionary history of deuterostome nervous systems and reveals new approaches to investigate the development and neurobiology of sea urchins.

Published
2006
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7. The molecular phylogeny of eph receptors and ephrin ligands

Author

Dan O Mellott and Robert D. Burke

Subjects
animal structures, Cell Communication, Biology, Ligands, EPH receptor B2, Evolution, Molecular, 03 medical and health sciences, 0302 clinical medicine, EPH receptor A3, Animals, Humans, Ephrin, Urochordata, lcsh:QH573-671, Binding site, Receptor, Phylogeny, Receptors, Eph Family, 030304 developmental biology, Likelihood Functions, 0303 health sciences, Binding Sites, lcsh:Cytology, Erythropoietin-producing hepatocellular (Eph) receptor, Receptor Cross-Talk, Cell Biology, Protein-Tyrosine Kinases, EPH receptor A2, biological factors, Cell biology, Neural Crest, Vertebrates, embryonic structures, sense organs, biological phenomena, cell phenomena, and immunity, Ephrins, Sequence Alignment, Sequence Analysis, 030217 neurology & neurosurgery, Research Article
Abstract

Background The tissue distributions and functions of Eph receptors and their ephrin ligands have been well studied, however less is known about their evolutionary history. We have undertaken a phylogenetic analysis of Eph receptors and ephrins from a number of invertebrate and vertebrate species. Results Our findings indicate that Eph receptors form three major clades: one comprised of non-chordate and cephalochordate Eph receptors, a second comprised of urochordate Eph receptors, and a third comprised of vertebrate Eph receptors. Ephrins, on the other hand, fall into either a clade made up of the non-chordate and cephalochordate ephrins plus the urochordate and vertebrate ephrin-Bs or a clade made up of the urochordate and vertebrate ephrin-As. Conclusion We have concluded that Eph receptors and ephrins diverged into A and B-types at different points in their evolutionary history, such that primitive chordates likely possessed an ancestral ephrin-A and an ancestral ephrin-B, but only a single Eph receptor. Furthermore, ephrin-As appear to have arisen in the common ancestor of urochordates and vertebrates, whereas ephrin-Bs have a more ancient bilaterian origin. Ancestral ephrin-B-like ligands had transmembrane domains; as GPI anchors appear to have arisen or been lost at least 3 times.

Published
2008
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8. The Genome of the Sea Urchin Strongylocentrotus purpuratus

Author

Amro Hamdoun, Virginia Brockton, Huyen Dinh, Qiang Tu, Richard O. Hynes, Maria Ina Arnone, Wratko Hlavina, L. Courtney Smith, Mariano A. Loza, David R. Burgess, Matthew P. Hoffman, Florian Raible, Qiu Autumn Yuan, Geoffrey Okwuonu, Mark Y. Tong, Jennifer Hume, Donna Maglott, Manisha Goel, Olivier Fedrigo, Manuel L. Gonzalez-Garay, Celina E. Juliano, Judith Hernandez, Gary M. Wessel, William F. Marzluff, Audrey J. Majeske, Christian Gache, Louise Duloquin, Xingzhi Song, François Lapraz, Fowler J, Alexandre Souvorov, Jared V. Goldstone, Georgia Panopoulou, Sandra Hines, Kyle M. Judkins, Clay Davis, Christine G. Elsik, Paul Kitts, Mariano Loza-Coll, Greg Wray, Taku Hibino, Eric Röttinger, Allison M. Churcher, Annamaria Locascio, Arcady Mushegian, Masashi Kinukawa, Anna Reade, Katherine M. Buckley, I. R. Gibbons, Bert Gold, Aleksandar Milosavljevic, David Epel, Victor D. Vacquier, Ling Ling Pu, Vincenzo Cavalieri, Erin L. Allgood, Lan Zhang, Lynne V. Nazareth, Constantin N. Flytzanis, Ian Bosdet, Yi-Hsien Su, Zeev Pancer, Matthew L. Rowe, Robert C. Angerer, David R. McClay, William H. Klein, Rachel F. Gray, Julian L. Wong, Shunsuke Yaguchi, Robert Bellé, Aaron J. Mackey, Herath Jayantha Gunaratne, Karl Frederik Bergeron, Bruce P. Brandhorst, Greg Murray, Avis H. Cohen, Stephanie Bell, Kristin Tessmar-Raible, Ian K. Townley, Bertrand Cosson, Thomas D. Glenn, Jongmin Nam, Cynthia A. Bradham, Michael Dean, Joseph Chacko, Anthony J. Robertson, Margherita Branno, Valeria Matranga, K. James Durbin, Esther Miranda, Lili Chen, Eran Elhaik, Robert D. Burke, Rita A. Wright, Paola Oliveri, Sandra L. Lee, Gary W. Moy, Alexander E Primus, Shawn S. McCafferty, Cristina Calestani, David A. Garfield, Erica Sodergren, Karen Wilson, Joel Smith, Marco A. Marra, Cynthia Messier, Julia Morales, Kim D. Pruitt, Rachel Thorn, Rachel Gill, John S. Taylor, Mark E. Hahn, Victor Sapojnikov, Meredith Howard-Ashby, Lynne M. Angerer, Maurice R. Elphick, Kathy R. Foltz, Anne Marie Genevière, Justin T. Reese, Blanca E. Galindo, Kim C. Worley, Andrew Leone, Glen Humphrey, Kevin Berney, Olga Ermolaeva, George Miner, David P. Terwilliger, Elly Suk Hen Chow, Lora Lewis, Dan Graur, C. Titus Brown, Gerard Manning, Kevin J. Peterson, Angela Jolivet, Michele K. Anderson, Francesca Rizzo, Ekaterina Voronina, Thierry Lepage, Giorgio Matassi, Antonio Fernandez-Guerra, Mamoru Nomura, Charles A. Whittaker, James R.R. Whittle, James A. Coffman, George M. Weinstock, Mohammed M. Idris, Ashlan M. Musante, Sebastian D. Fugmann, Katherine D. Walton, Sorin Istrail, Shu-Yu Wu, Cerrissa Hamilton, Jonah Cool, Jacqueline E. Schein, Stacey M. Curry, Athula Wikramanayke, Seth Carbonneau, Blair J. Rossetti, Christopher E. Killian, Melissa J. Landrum, Amanda P. Rawson, Jenifer C. Croce, Ryan C. Range, Rahul Satija, John J. Stegeman, Yufeng Shen, Cavit Agca, Terry Gaasterland, Rocky Cheung, Takae Kiyama, Nikki Adams, Jonathan P. Rast, Robert Piotr Olinski, Andrew Cree, Mark Scally, Shuguang Liang, David A. Parker, Rebecca Thomason, Gretchen E. Hofmann, Michelle M. Roux, Ronghui Xu, Robert A. Obar, Enrique Arboleda, Odile Mulner-Lorillon, Shannon Dugan-Rocha, David J. Bottjer, Gabriele Amore, Manoj P. Samanta, Waraporn Tongprasit, Véronique Duboc, La Ronda Jackson, Fred H. Wilt, Viktor Stolc, Anna T. Neill, Michael Raisch, Pei Yun Lee, Jia L. Song, Margaret Morgan, Brian T. Livingston, Sofia Hussain, Zheng Wei, Bryan J. Cole, Tonya F. Severson, Victor V. Solovyev, Finn Hallböök, Donna M. Muzny, Christine A. Byrum, Albert J. Poustka, Xiuqian Mu, Andrew R. Jackson, Shin Heesun, Euan R. Brown, Nansheng Chen, Patrick Cormier, Ralph Haygood, Pedro Martinez, R. Andrew Cameron, D. Wang, Wendy S. Beane, Eric H. Davidson, Christie Kovar, Hemant Kelkar, Charles A. Ettensohn, Sham V. Nair, Robert L. Morris, Stefan C. Materna, Michael C. Thorndyke, Richard A. Gibbs, Dan O Mellott, Department of Physiology and Biophysics, Stony Brook University [The State University of New York] ( SBU ), Astronomy Unit ( AU ), Queen Mary University of London ( QMUL ), Urban and Industrial Air Quality Group, CSIRO Energy Technology, Commonwealth Scientific and Industrial Research Organisation Energy Technology ( CSIRO Energy Technology ), Commonwealth Scientific and Industrial Research Organisation, Center for Polymer Studies ( CPS ), Boston University [Boston] ( BU ), Physics Department [Boston] ( BU-Physics ), Max Planck Institute for Psycholinguistics, Max-Planck-Institut, Department of Biology [Norton], Wheaton College [Norton], Mathematical Institute [Oxford] ( MI ), University of Oxford [Oxford], Centre for the Analysis of Time Series ( CATS ), London School of Economics and Political Science ( LSE ), Thomas Jefferson National Accelerator Facility ( Jefferson Lab ), Thomas Jefferson National Accelerator Facility, Laboratoire d'Energétique et de Mécanique Théorique Appliquée ( LEMTA ), Université de Lorraine ( UL ) -Centre National de la Recherche Scientifique ( CNRS ), Laboratoire Evolution, Génomes et Spéciation ( LEGS ), Centre National de la Recherche Scientifique ( CNRS ), Department of Geology, University of Illinois at Urbana-Champaign [Urbana], Department of Electrical and Computer Engineering [Portland] ( ECE ), Portland State University [Portland] ( PSU ), Saint-Gobain Crystals [USA], SAINT-GOBAIN, Institute for Animal Health ( IAH ), Biotechnology and Biological Sciences Research Council, Center for Agricultural Resources Research, Chinese Academy of Sciences [Changchun Branch] ( CAS ), Ipsen Inc. [Milford] ( Ipsen ), IPSEN, Department of Physics [Berkeley], University of California [Berkeley], Institute for Climate and Atmospheric Science [Leeds] ( ICAS ), University of Leeds, Chung-Ang University ( CAU ), Chung-Ang University [Seoul], Antarctic Climate and Ecosystems Cooperative Research Center ( ACE-CRC ), Institute of Aerodynamics and Fluid Mechanics ( AER ), Technische Universität München [München] ( TUM ), Mer et santé ( MS ), Université Pierre et Marie Curie - Paris 6 ( UPMC ) -Centre National de la Recherche Scientifique ( CNRS ), Imperial College London, Radio and Atmospheric Sciences Division, National Physical Laboratory [Teddington] ( NPL ), International Research Institute for Climate and Society ( IRI ), Earth Institute at Columbia University, Columbia University [New York]-Columbia University [New York], Soils Group, The Macaulay Institute, Department of Haematology, University of Cambridge [UK] ( CAM ), School of Biology and Biochemistry, Queen's University, Leslie Hill Institute for Plant Conservation ( PCU ), University of Cape Town, Institute for Microelectronics and Microsystems/ Istituto per la Microelettronica e Microsistemi ( IMM ), Consiglio Nazionale delle Ricerche ( CNR ), Laboratoire d'acoustique de l'université du Mans ( LAUM ), Le Mans Université ( UM ) -Centre National de la Recherche Scientifique ( CNRS ), Interactive Systems Labs ( ISL ), Carnegie Mellon University [Pittsburgh] ( CMU ), Dalian Institute of Chemical Physics ( DICP ), Architectures, Languages and Compilers to Harness the End of Moore Years ( ALCHEMY ), Laboratoire de Recherche en Informatique ( LRI ), Université Paris-Sud - Paris 11 ( UP11 ) -Institut National de Recherche en Informatique et en Automatique ( Inria ) -CentraleSupélec-Centre National de la Recherche Scientifique ( CNRS ) -Université Paris-Sud - Paris 11 ( UP11 ) -Institut National de Recherche en Informatique et en Automatique ( Inria ) -CentraleSupélec-Centre National de la Recherche Scientifique ( CNRS ) -Inria Saclay - Ile de France, Institut National de Recherche en Informatique et en Automatique ( Inria ), Clean Air Task Force ( CATF ), Clean Air Task Force, Space Physics Laboratory, Indian Space Research Organisation ( ISRO ), Centre d'études et de recherches appliquées à la gestion ( CERAG ), Université Pierre Mendès France - Grenoble 2 ( UPMF ) -Centre National de la Recherche Scientifique ( CNRS ), Department of Microbiology and Immunology, College of Medicine and Health Sciences-Sultan Qaboos University, European Molecular Biology Laboratory [Heidelberg] ( EMBL ), Department of Biostatistics, University of Michigan [Ann Arbor], Department of Radiation Oncology [Michigan] ( Radonc ), Department of Physics and Astronomy [Leicester], University of Leicester, Informatique, Biologie Intégrative et Systèmes Complexes ( IBISC ), Université d'Évry-Val-d'Essonne ( UEVE ) -Centre National de la Recherche Scientifique ( CNRS ), Institut für Meteorologie und Klimaforschung ( IMK ), Karlsruher Institut für Technologie ( KIT ), Physics Department [UNB], University of New Brunswick ( UNB ), Laboratoire Parole et Langage ( LPL ), Centre National de la Recherche Scientifique ( CNRS ) -Aix Marseille Université ( AMU ), Institut des Sciences Chimiques de Rennes ( ISCR ), Université de Rennes 1 ( UR1 ), Université de Rennes ( UNIV-RENNES ) -Université de Rennes ( UNIV-RENNES ) -Ecole Nationale Supérieure de Chimie de Rennes-Institut National des Sciences Appliquées ( INSA ) -Centre National de la Recherche Scientifique ( CNRS ), Biogéosciences [Dijon] ( BGS ), Université de Bourgogne ( UB ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique ( CNRS ), Bioprojet, Laboratoire de Matériaux à Porosité Contrôlée ( LMPC ), Université de Haute-Alsace (UHA) Mulhouse - Colmar ( Université de Haute-Alsace (UHA) ) -Ecole Nationale Supérieure de Chimie de Mulhouse-Centre National de la Recherche Scientifique ( CNRS ), School of Information Engineering [USTB] ( SIE ), University of Science and Technology Beijing [Beijing] ( USTB ), Laboratory for Atmospheric and Space Physics [Boulder] ( LASP ), University of Colorado Boulder [Boulder], Department of Applied Mathematics [Sheffield], University of Sheffield [Sheffield], School of Mathematics and Statistics [Sheffield] ( SoMaS ), Laboratoire de Mécanique de Lille - FRE 3723 ( LML ), Université de Lille, Sciences et Technologies-Ecole Centrale de Lille-Centre National de la Recherche Scientifique ( CNRS ), Computer Science Department [UCLA] ( CSD ), University of California at Los Angeles [Los Angeles] ( UCLA ), Développement et évolution ( DE ), Université Paris-Sud - Paris 11 ( UP11 ) -Centre National de la Recherche Scientifique ( CNRS ), Laboratoire de Biologie du Développement de Villefranche sur mer ( LBDV ), Laboratoire Pierre Aigrain ( LPA ), Fédération de recherche du Département de physique de l'Ecole Normale Supérieure - ENS Paris ( FRDPENS ), Centre National de la Recherche Scientifique ( CNRS ) -École normale supérieure - Paris ( ENS Paris ) -Centre National de la Recherche Scientifique ( CNRS ) -École normale supérieure - Paris ( ENS Paris ) -Université Pierre et Marie Curie - Paris 6 ( UPMC ) -Université Paris Diderot - Paris 7 ( UPD7 ) -Centre National de la Recherche Scientifique ( CNRS ), Department of Mathematics and Statistics [Mac Gill], McGill University, Departamento de Botánica [Comahue], Universidad nacional del Comahue, Bioénergétique Cellulaire et Pathologique ( BECP ), Université Joseph Fourier - Grenoble 1 ( UJF ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ), Environnements et Paléoenvironnements OCéaniques ( EPOC ), Observatoire aquitain des sciences de l'univers ( OASU ), Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers ( INSU - CNRS ) -Centre National de la Recherche Scientifique ( CNRS ) -Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers ( INSU - CNRS ) -Centre National de la Recherche Scientifique ( CNRS ) -École pratique des hautes études ( EPHE ) -Centre National de la Recherche Scientifique ( CNRS ), Institut Jacques Monod ( IJM ), Université Paris Diderot - Paris 7 ( UPD7 ) -Centre National de la Recherche Scientifique ( CNRS ), Laboratori Nazionali del Sud ( LNS ), National Institute for Nuclear Physics ( INFN ), Departament de Matemàtiques [Barcelona], Universitat Autònoma de Barcelona [Barcelona] ( UAB ), Max-Planck-Institut für Kohlenforschung (coal research), Institute of Oceanology [CAS] ( IOCAS ), National Chiao Tung University ( NCTU ), Department of Hydrology and Water Resources ( HWR ), University of Arizona, Centre for Educational Technology, Environment Department [York], University of York [York, UK], State Key Laboratory of Nuclear Physics and Technology ( SKL-NPT ), Peking University [Beijing], Department of Physics and Astronomy [Iowa City], University of Iowa [Iowa], NASA Ames Research Center ( ARC ), Department of Materials, Digital Language & Knowledge Contents Research Association ( DICORA ), Hankuk University of Foreign Studies, Department of Physics [Coventry], University of Warwick [Coventry], Space Science and Technology Department [Didcot] ( RAL Space ), STFC Rutherford Appleton Laboratory ( RAL ), Science and Technology Facilities Council ( STFC ) -Science and Technology Facilities Council ( STFC ), Institut de biologie et chimie des protéines [Lyon] ( IBCP ), Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique ( CNRS ), H M Nautical Almanac Office [RAL] ( HMNAO ), Rutherford Appleton Laboratory, United Kingdom Met Office [Exeter], University College of London [London] ( UCL ), Department of Pathology and Laboratory Medicine [UCLA], University of California at Los Angeles [Los Angeles] ( UCLA ) -School of Medicine, School of Earth and Environmental Sciences [Seoul] ( SEES ), Seoul National University [Seoul], Department of Chemistry, Seoul Women's University, MicroMachines Centre ( MMC ), Nanyang Technological University [Singapour], Regroupement Québécois sur les Matériaux de Pointe ( RQMP ), École Polytechnique de Montréal ( EPM ) -Université de Sherbrooke [Sherbrooke]-McGill University-Université de Montréal-Fonds Québécois de Recherche sur la Nature et les Technologies ( FQRNT ), Département de Physique [Montréal], Université de Montréal, School of Earth and Environment [Leeds] ( SEE ), Centre for Ecology and Hydrology ( CEH ), Natural Environment Research Council ( NERC ), Norwegian Institute for Water Research ( NIVA ), Norwegian Institute for Water Research, Stony Brook University [SUNY] (SBU), State University of New York (SUNY)-State University of New York (SUNY), Astronomy Unit [London] (AU), Queen Mary University of London (QMUL), Commonwealth Scientific and Industrial Research Organisation Energy Technology (CSIRO Energy Technology), Commonwealth Scientific and Industrial Research Organisation [Canberra] (CSIRO), Department of Biochemistry and Molecular Biology [Houston], The University of Texas Medical School at Houston, Mathematical Institute [Oxford] (MI), University of Oxford, Centre for the Analysis of Time Series (CATS), London School of Economics and Political Science (LSE), Thomas Jefferson National Accelerator Facility (Jefferson Lab), Laboratoire Énergies et Mécanique Théorique et Appliquée (LEMTA ), Université de Lorraine (UL)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Evolution, Génomes et Spéciation (LEGS), Centre National de la Recherche Scientifique (CNRS), University of Illinois System-University of Illinois System, Department of Electrical and Computer Engineering [Portland] (ECE), Portland State University [Portland] (PSU), Saint-Gobain, Institute for Animal Health (IAH), Biotechnology and Biological Sciences Research Council (BBSRC), Chinese Academy of Sciences [Changchun Branch] (CAS), Ipsen Inc. [Milford] (Ipsen), University of California [Berkeley] (UC Berkeley), University of California (UC)-University of California (UC), Institute for Climate and Atmospheric Science [Leeds] (ICAS), School of Earth and Environment [Leeds] (SEE), University of Leeds-University of Leeds, Chung-Ang University (CAU), Antarctic Climate and Ecosystems Cooperative Research Centre (ACE-CRC), Institute of Aerodynamics and Fluid Mechanics (AER), Technische Universität Munchen - Université Technique de Munich [Munich, Allemagne] (TUM), Mer et santé (MS), Station biologique de Roscoff [Roscoff] (SBR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), National Physical Laboratory [Teddington] (NPL), International Research Institute for Climate and Society (IRI), Macaulay Institute, University of Cambridge [UK] (CAM), Queen's University [Kingston, Canada], Leslie Hill Institute for Plant Conservation (PCU), Istituto per la Microelettronica e Microsistemi [Catania] (IMM), National Research Council of Italy | Consiglio Nazionale delle Ricerche (CNR), Laboratoire d'Acoustique de l'Université du Mans (LAUM), Le Mans Université (UM)-Centre National de la Recherche Scientifique (CNRS), Interactive Systems Labs (ISL), Carnegie Mellon University [Pittsburgh] (CMU), Dalian Institute of Chemical Physics (DICP), Architectures, Languages and Compilers to Harness the End of Moore Years (ALCHEMY), Laboratoire de Recherche en Informatique (LRI), Université Paris-Sud - Paris 11 (UP11)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Inria Saclay - Ile de France, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria), Clean Air Task Force (CATF), Indian Space Research Organisation (ISRO), Centre d'études et de recherches appliquées à la gestion (CERAG), Université Pierre Mendès France - Grenoble 2 (UPMF)-Centre National de la Recherche Scientifique (CNRS), Sultan Qaboos University (SQU)-College of Medicine and Health Sciences [Baylor], Baylor University-Baylor University, European Molecular Biology Laboratory [Heidelberg] (EMBL), University of Michigan System-University of Michigan System, Department of Radiation Oncology [Michigan] (Radonc), Informatique, Biologie Intégrative et Systèmes Complexes (IBISC), Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Institute for Meteorology and Climate Research (IMK), Karlsruhe Institute of Technology (KIT), University of New Brunswick (UNB), Laboratoire Parole et Langage (LPL), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut des Sciences Chimiques de Rennes (ISCR), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Supérieure de Chimie de Rennes (ENSCR)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), Biogéosciences [UMR 6282] (BGS), Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Matériaux à Porosité Contrôlée (LMPC), Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Centre National de la Recherche Scientifique (CNRS), School of Information Engineering [USTB] (SIE), University of Science and Technology Beijing [Beijing] (USTB), Laboratory for Atmospheric and Space Physics [Boulder] (LASP), University of Colorado [Boulder], School of Mathematics and Statistics [Sheffield] (SoMaS), Laboratoire de Mécanique de Lille - FRE 3723 (LML), Université de Lille, Sciences et Technologies-Centrale Lille-Centre National de la Recherche Scientifique (CNRS), Computer Science Department [UCLA] (CSD), University of California [Los Angeles] (UCLA), Développement et évolution (DE), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Biologie du Développement de Villefranche sur mer (LBDV), Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Pierre Aigrain (LPA), Fédération de recherche du Département de physique de l'Ecole Normale Supérieure - ENS Paris (FRDPENS), École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Department of Mathematics and Statistics [Montréal], McGill University = Université McGill [Montréal, Canada], Departamento de Botánica [Bariloche], Centro Regional Universitario Bariloche [Bariloche] (CRUB), Universidad Nacional del Comahue [Neuquén] (UNCOMA)-Universidad Nacional del Comahue [Neuquén] (UNCOMA), Bioénergétique Cellulaire et Pathologique (BECP), Université Joseph Fourier - Grenoble 1 (UJF)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Environnements et Paléoenvironnements OCéaniques (EPOC), Observatoire aquitain des sciences de l'univers (OASU), Université Sciences et Technologies - Bordeaux 1 (UB)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Sciences et Technologies - Bordeaux 1 (UB)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS), Institut Jacques Monod (IJM (UMR_7592)), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Laboratori Nazionali del Sud (LNS), Istituto Nazionale di Fisica Nucleare (INFN), Departament de Matemàtiques [Barcelona] (UAB), Universitat Autònoma de Barcelona (UAB), Max-Planck-Institut für Kohlenforschung (Coal Research), Max-Planck-Gesellschaft, CAS Institute of Oceanology (IOCAS), Chinese Academy of Sciences [Beijing] (CAS), National Chiao Tung University (NCTU), Department of Hydrology and Water Resources (HWR), State Key Laboratory of Nuclear Physics and Technology (SKL-NPT), University of Iowa [Iowa City], NASA Ames Research Center (ARC), Digital Language & Knowledge Contents Research Association (DICORA), Space Science and Technology Department [Didcot] (RAL Space), STFC Rutherford Appleton Laboratory (RAL), Science and Technology Facilities Council (STFC)-Science and Technology Facilities Council (STFC), Institut de biologie et chimie des protéines [Lyon] (IBCP), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), H M Nautical Almanac Office [RAL] (HMNAO), University College of London [London] (UCL), University of California (UC)-University of California (UC)-School of Medicine, School of Earth and Environmental Sciences [Seoul] (SEES), Seoul National University [Seoul] (SNU), MicroMachines Centre (MMC), Regroupement Québécois sur les Matériaux de Pointe (RQMP), École Polytechnique de Montréal (EPM)-Université de Sherbrooke (UdeS)-McGill University = Université McGill [Montréal, Canada]-Université de Montréal (UdeM)-Fonds Québécois de Recherche sur la Nature et les Technologies (FQRNT), Université de Montréal (UdeM), Centre for Ecology and Hydrology (CEH), Natural Environment Research Council (NERC), Norwegian Institute for Water Research (NIVA), SEA URCHIN GENOME SEQUENCING CONSORTIUM, SODERGREN E, WEINSTOCK GM, DAVIDSON EH, CAMERON RA, GIBBS RA, ANGERER RC, ANGERER LM, ARNONE MI, BURGESS DR, BURKE RD, COFFMAN JA, DEAN M, ELPHICK MR, ETTENSOHN CA, FOLTZ KR, HAMDOUN A, HYNES RO, KLEIN WH, MARZLUFF W, MCCLAY DR, MORRIS RL, MUSHEGIAN A, RAST JP, SMITH LC, THORNDYKE MC, VACQUIER VD, WESSEL GM, WRAY G, ZHANG L, ELSIK CG, ERMOLAEVA O, HLAVINA W, HOFMANN G, KITTS P, LANDRUM MJ, MACKEY AJ, MAGLOTT D, PANOPOULOU G, POUSTKA AJ, PRUITT K, SAPOJNIKOV V, SONG X, SOUVOROV A, SOLOVYEV V, WEI Z, WHITTAKER CA, WORLEY K, DURBIN KJ, SHEN Y, FEDRIGO O, GARFIELD D, HAYGOOD R, PRIMUS A, SATIJA R, SEVERSON T, GONZALEZ-GARAY ML, JACKSON AR, MILOSAVLJEVIC A, TONG M, KILLIAN CE, LIVINGSTON BT, WILT FH, ADAMS N, BELLE R, CARBONNEAU S, CHEUNG R, CORMIER P, COSSON B, CROCE J, FERNANDEZ-GUERRA A, GENEVIERE AM, GOEL M, KELKAR H, MORALES J, MULNER-LORILLON O, ROBERTSON AJ, GOLDSTONE JV, COLE B, EPEL D, GOLD B, HAHN ME, HOWARD-ASHBY M, SCALLY M, STEGEMAN JJ, ALLGOOD EL, COOL J, JUDKINS KM, MCCAFFERTY SS, MUSANTE AM, OBAR RA, RAWSON AP, ROSSETTI BJ, GIBBONS IR, HOFFMAN MP, LEONE A, ISTRAIL S, MATERNA SC, SAMANTA MP, STOLC V, TONGPRASIT W, TU Q, BERGERON KF, BRANDHORST BP, WHITTLE J, BERNEY K, BOTTJER DJ, CALESTANI C, PETERSON K, CHOW E, YUAN QA, ELHAIK E, GRAUR D, REESE JT, BOSDET I, HEESUN S, MARRA MA, SCHEIN J, ANDERSON MK, BROCKTON V, BUCKLEY KM, COHEN AH, FUGMANN SD, HIBINO T, LOZA-COLL M, MAJESKE AJ, MESSIER C, NAIR SV, PANCER Z, TERWILLIGER DP, AGCA C, ARBOLEDA E, CHEN N, CHURCHER AM, HALLBOOK F, HUMPHREY GW, IDRIS MM, KIYAMA T, LIANG S, MELLOTT D, MU X, MURRAY G, OLINSKI RP, RAIBLE F, ROWE M, TAYLOR JS, TESSMAR-RAIBLE K, WANG D, WILSON KH, YAGUCHI S, GAASTERLAND T, GALINDO BE, GUNARATNE HJ, JULIANO C, KINUKAWA M, MOY GW, NEILL AT, NOMURA M, RAISCH M, READE A, ROUX MM, SONG JL, SU YH, TOWNLEY IK, VORONINA E, WONG JL, AMORE G, BRANNO M, BROWN ER, CAVALIERI, V, DUBOC V, DULOQUIN L, FLYTZANIS C, GACHE C, LAPRAZ F, LEPAGE T, LOCASCIO A, MART, University of California-University of California, Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC), Consiglio Nazionale delle Ricerche (CNR), Centre National de la Recherche Scientifique (CNRS)-Le Mans Université (UM), Centre National de la Recherche Scientifique (CNRS)-Université Pierre Mendès France - Grenoble 2 (UPMF), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Supérieure de Chimie de Rennes (ENSCR)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), Biogéosciences [UMR 6282] [Dijon] (BGS), Centre National de la Recherche Scientifique (CNRS)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Ecole Nationale Supérieure de Chimie de Mulhouse-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Diderot - Paris 7 (UPD7)-Fédération de recherche du Département de physique de l'Ecole Normale Supérieure - ENS Paris (FRDPENS), Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-École pratique des hautes études (EPHE), University of California-University of California-School of Medicine, Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Ecole Nationale Supérieure de Chimie de Rennes (ENSCR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA), Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique (CNRS), Université de Lille, Sciences et Technologies-Centre National de la Recherche Scientifique (CNRS)-Centrale Lille, Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Joseph Fourier - Grenoble 1 (UJF), University of Manchester Institute of Science and Technology (UMIST), Condensed Matter Physics and Materials Science Department, Brookhaven National Laboratory, Brookhaven National Laboratory [Upton, NY] (BNL), UT-Battelle, LLC-Stony Brook University [SUNY] (SBU), State University of New York (SUNY)-State University of New York (SUNY)-U.S. Department of Energy [Washington] (DOE)-UT-Battelle, LLC-Stony Brook University [SUNY] (SBU), State University of New York (SUNY)-State University of New York (SUNY)-U.S. Department of Energy [Washington] (DOE), Baylor College of Medicine (BCM), Baylor University, Laboratoire de Traitement de l'Information Medicale (LaTIM), Université européenne de Bretagne - European University of Brittany (UEB)-Université de Brest (UBO)-Télécom Bretagne-Institut Mines-Télécom [Paris] (IMT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre Hospitalier Régional Universitaire de Brest (CHRU Brest), Laboratoire de Modélisation et Simulation Multi Echelle (MSME), Université Paris-Est Marne-la-Vallée (UPEM)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS), Duke University [Durham], Instituto Andaluz de Geofísica y Prevención de Desastres Sísmicos [Granada] (IAGPDS), Universidad de Granada (UGR), Laboratoire d'Ingénierie des Matériaux de Bretagne (LIMATB), Université de Bretagne Sud (UBS)-Université de Brest (UBO)-Institut Brestois du Numérique et des Mathématiques (IBNM), Université de Brest (UBO)-Université de Brest (UBO), University of New South Wales [Sydney] (UNSW), Celera Genomics (CRA), Celera Genomics, Paléobiodiversité et paléoenvironnements, Muséum national d'Histoire naturelle (MNHN)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Università degli Studi di Roma Tor Vergata [Roma], Unité de recherches forestières (BORDX PIERR UR ), Institut National de la Recherche Agronomique (INRA), Deptartment of Neuroscience, Uppsala University, State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology (NIGPAS-CAS), Chinese Academy of Sciences [Nanjing Branch]-Chinese Academy of Sciences [Nanjing Branch], Institut Méditerranéen d'Ecologie et de Paléoécologie (IMEP), Université Paul Cézanne - Aix-Marseille 3-Université de Provence - Aix-Marseille 1-Avignon Université (AU)-Centre National de la Recherche Scientifique (CNRS), Key Laboratory of Ocean Circulation and Waves, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China, Université Paris Diderot - Paris 7 (UPD7), Department of Physical and Environmental Sciences [Toronto], University of Toronto at Scarborough, inconnu temporaire UPEMLV, Inconnu, Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Department of Atmospheric Sciences [Seattle], University of Washington [Seattle], National Institute of Advanced Industrial Science and Technology (AIST), Department of Pharmacy, Università degli studi di Genova = University of Genoa (UniGe), Interdisciplinary Arts and Sciences Department, St. Vincent's Hospital, Sydney, Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Department of Electrical Engineering (DEE-POSTECH), Pohang University of Science and Technology (POSTECH), Centre Suisse d'Electronique et de Microtechnique SA [Neuchatel] (CSEM), Centre Suisse d'Electronique et Microtechnique SA (CSEM), Human Genome Sequencing Center [Houston] (HGSC), Brookhaven National Laboratory, Meteorological Service of Canada, 4905 Dufferin Street, Université européenne de Bretagne - European University of Brittany (UEB)-Télécom Bretagne-Centre Hospitalier Régional Universitaire de Brest (CHRU Brest)-Université de Brest (UBO)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Mines-Télécom [Paris] (IMT), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Université Paris-Est Marne-la-Vallée (UPEM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Unité de Recherches Forestières, Department of Physical and Environmental Sciences, University of Toronto [Scarborough, Canada], National Institute for Nuclear Physics (INFN), University of Genoa (UNIGE), Institut de Recherche pour le Développement (IRD)-Institut Universitaire Européen de la Mer (IUEM), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Université de Brest (UBO)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS), Universidad de Granada = University of Granada (UGR), Laboratoire d'Energétique et de Mécanique Théorique Appliquée (LEMTA ), Technische Universität München [München] (TUM), Queen's University [Kingston], Centre National de la Recherche Scientifique (CNRS)-Université Pierre Mendès France - Grenoble 2 (UPMF)-Université Grenoble Alpes (UGA), Institut für Meteorologie und Klimaforschung (IMK), Karlsruher Institut für Technologie (KIT), Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU), Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Supérieure de Chimie de Rennes-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES), Centre National de la Recherche Scientifique (CNRS)-Université de Lille, Sciences et Technologies-Ecole Centrale de Lille-Université de Lille, Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Sciences et Technologies - Bordeaux 1-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-École pratique des hautes études (EPHE)-Centre National de la Recherche Scientifique (CNRS), Universitat Autònoma de Barcelona [Barcelona] (UAB), École Polytechnique de Montréal (EPM)-Université de Sherbrooke [Sherbrooke]-Université de Montréal [Montréal]-McGill University-Fonds Québécois de Recherche sur la Nature et les Technologies (FQRNT), Université de Montréal [Montréal], U.S. Department of Energy [Washington] (DOE)-UT-Battelle, LLC-Stony Brook University [SUNY] (SBU), Université de Bretagne Sud (UBS)-Institut Brestois du Numérique et des Mathématiques (IBNM), Université de Brest (UBO)-Université de Brest (UBO)-Université de Brest (UBO), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC), Université Paul Cézanne - Aix-Marseille 3-Centre National de la Recherche Scientifique (CNRS)-Avignon Université (AU)-Université de Provence - Aix-Marseille 1, Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Brest (UBO), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université de Lille, Sciences et Technologies-Ecole Centrale de Lille-Université de Lille-Centre National de la Recherche Scientifique (CNRS), École normale supérieure - Paris (ENS Paris), and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, MESH: Signal Transduction, MESH: Sequence Analysis, DNA, MESH : Transcription Factors, MESH : Calcification, Physiologic, Genome, MESH : Proteins, 0302 clinical medicine, MESH : Embryonic Development, MESH: Gene Expression Regulation, Developmental, Innate, MESH: Embryonic Development, Developmental, Nervous System Physiological Phenomena, MESH: Animals, MESH: Proteins, [SDV.BDD]Life Sciences [q-bio]/Development Biology, Complement Activation, ComputingMilieux_MISCELLANEOUS, MESH: Evolution, Molecular, MESH : Strongylocentrotus purpuratus, Genetics, 0303 health sciences, MESH: Nervous System Physiological Phenomena, Multidisciplinary, biology, Medicine (all), MESH: Immunologic Factors, Gene Expression Regulation, Developmental, Genome project, MESH: Transcription Factors, MESH : Immunity, Innate, MESH : Complement Activation, MESH: Genes, Bacterial artificial chromosome (BAC)DeuterostomesStrongylocentrotus purpuratusVertebrate innovations, Echinoderm, MESH : Nervous System Physiological Phenomena, embryonic structures, MESH: Cell Adhesion Molecules, MESH : Genes, MESH: Immunity, Innate, Sequence Analysis, Signal Transduction, MESH: Computational Biology, Genome evolution, MESH: Complement Activation, Sequence analysis, Evolution, MESH: Strongylocentrotus purpuratus, MESH : Male, Embryonic Development, MESH : Immunologic Factors, Article, MESH: Calcification, Physiologic, Calcification, MESH : Cell Adhesion Molecules, Evolution, Molecular, 03 medical and health sciences, Calcification, Physiologic, Animals, Immunologic Factors, MESH: Genome, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, MESH : Evolution, Molecular, Physiologic, Gene, Strongylocentrotus purpuratus, [ SDV.BBM ] Life Sciences [q-bio]/Biochemistry, Molecular Biology, 030304 developmental biology, MESH : Signal Transduction, Bacterial artificial chromosome, Immunity, Molecular, Computational Biology, Proteins, Cell Adhesion Molecules, Genes, Immunity, Innate, Transcription Factors, Sequence Analysis, DNA, DNA, biology.organism_classification, MESH: Male, Gene Expression Regulation, MESH : Animals, MESH : Gene Expression Regulation, Developmental, MESH : Genome, 030217 neurology & neurosurgery, MESH : Computational Biology, MESH : Sequence Analysis, DNA
Abstract

We report the sequence and analysis of the 814-megabase genome of the sea urchin Strongylocentrotus purpuratus , a model for developmental and systems biology. The sequencing strategy combined whole-genome shotgun and bacterial artificial chromosome (BAC) sequences. This use of BAC clones, aided by a pooling strategy, overcame difficulties associated with high heterozygosity of the genome. The genome encodes about 23,300 genes, including many previously thought to be vertebrate innovations or known only outside the deuterostomes. This echinoderm genome provides an evolutionary outgroup for the chordates and yields insights into the evolution of deuterostomes.

Published
2006
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9. Divergent roles for Eph and Ephrin in Avian Cranial Neural Crest

Author

Robert D. Burke and Dan O Mellott

Subjects
animal structures, Receptor, EphB2, EPHA7, Ectoderm, Ephrin-B2, Chick Embryo, Ephrin-B1, Biology, 03 medical and health sciences, Mice, 0302 clinical medicine, Cranial neural crest, EPHB3, medicine, Ephrin, Animals, lcsh:QH301-705.5, Cells, Cultured, In Situ Hybridization, 030304 developmental biology, Body Patterning, 0303 health sciences, Erythropoietin-producing hepatocellular (Eph) receptor, Neural crest, Gene Expression Regulation, Developmental, Anatomy, biological factors, Cell biology, Rhombencephalon, medicine.anatomical_structure, lcsh:Biology (General), Neural Crest, embryonic structures, Crest, sense organs, 030217 neurology & neurosurgery, Developmental Biology, Research Article, Plasmids
Abstract

Background As in other vertebrates, avian hindbrain neural crest migrates in streams to specific branchial arches. Signalling from Eph receptors and ephrins has been proposed to provide a molecular mechanism that guides the cells restricting them to streams. In mice and frogs, cranial neural crest express a combination of Eph receptors and ephrins that appear to exclude cells from adjacent tissues by forward and reverse signalling. The objective of this study was to provide comparative data on the distribution and function of Eph receptors and ephrins in avian embryos. Results To distinguish neural crest from bordering ectoderm and head mesenchyme, we have co-labelled embryos for Eph or ephrin RNA and a neural crest marker protein. Throughout their migration avian cranial neural crest cells express EphA3, EphA4, EphA7, EphB1, and EphB3 and move along pathways bordered by non-neural crest cells expressing ephrin-B1. In addition, avian cranial neural crest cells express ephrin-B2 and migrate along pathways bordered by non-neural crest cells expressing EphB2. Thus, the distribution of avian Eph receptors and ephrins differs from those reported in other vertebrates. In stripe assays when explanted cranial neural crest were given the choice between FN or FN plus clustered ephrin-B1 or EphB2 fusion protein, the cells strongly localize to lanes containing only FN. This preference is mitigated in the presence of soluble ephrin-B1 or EphB2 fusion protein. Conclusion These findings show that avian cranial neural crest use Eph and ephrin receptors as other vertebrates in guiding migration. However, the Eph receptors are expressed in different combinations by neural crest destined for each branchial arch and ephrin-B1 and ephrin-B2 appear to have opposite roles to those reported to guide cranial neural crest migration in mice. Unlike many of the signalling, specification, and effector pathways of neural crest, the roles of Eph receptors and ephrins have not been rigorously conserved. This suggests diversification of receptor and ligand expression is less constrained, possibly by promiscuous binding and use of common downstream pathways.

Published
2008

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