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Characterization of the Hox Patterning Genes in Acoel Flatworms

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Characterization of the Hox Patterning Genes in Acoel Flatworms Characterization of the Hox patterning genes in acoel flatworms Eduardo Moreno González ADVERTIMENT. La consulta d’aquesta tesi queda condicionada a l’acceptació de les següents condicions d'ús: La difusió d’aquesta tesi per mitjà del servei TDX (www.tesisenxarxa.net) ha estat autoritzada pels titulars dels drets de propietat intel·lectual únicament per a usos privats emmarcats en activitats d’investigació i docència. No s’autoritza la seva reproducció amb finalitats de lucre ni la seva difusió i posada a disposició des d’un lloc aliè al servei TDX. No s’autoritza la presentació del seu contingut en una finestra o marc aliè a TDX (framing). Aquesta reserva de drets afecta tant al resum de presentació de la tesi com als seus continguts. En la utilització o cita de parts de la tesi és obligat indicar el nom de la persona autora. ADVERTENCIA. 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On having consulted this thesis you’re accepting the following use conditions: Spreading this thesis by the TDX (www.tesisenxarxa.net) service has been authorized by the titular of the intellectual property rights only for private uses placed in investigation and teaching activities. Reproduction with lucrative aims is not authorized neither its spreading and availability from a site foreign to the TDX service. Introducing its content in a window or frame foreign to the TDX service is not authorized (framing). This rights affect to the presentation summary of the thesis as well as to its contents. In the using or citation of parts of the thesis it’s obliged to indicate the name of the author. UNIVERSITY OF BARCELONA SCHOOL OF BIOLOGY DEPARTMENT OF GENETICS CHARACTERIZATION OF THE HOX PATTERNING GENES IN ACOEL FLATWORMS PhD THESIS Eduardo Moreno González THESIS DIRECTOR: THESIS CO-DIRECTOR: Dr. Pedro Martínez Serra Dr. Jaume Baguñà i Monjo ICREA Researcher Cathedratic Professor Department of Genetics Department of Genetics School of Biology School of Biology University of Barcelona University of Barcelona Barcelona, Spain Barcelona, Spain Memoria presentada por Eduardo Moreno González para acceder al título de Doctor por la Universidad de Barcelona, bajo la dirección de los Doctores Pedro Martínez Serra y Jaume Baguñà Monjo. Barcelona, a 10 de Marzo del 2010 Preface Preface This thesis is the result of a four-year PhD project carried out from January 2006 to December 2009. Most of my work has been carried out in the “Evolutionary Developmental Biology” Research Group of the Genetics Department, University of Barcelona, Spain. The Director of this thesis has been the ICREA Researcher Pedro Martinez and the Co-Director has been the Professor of Genetics Jaume Baguñà. The thesis has been possible thanks to the financial support of the Spanish Ministry of Education, which has provided me with a F.P.U. PhD scholarship. This thesis contains six sections. In the first place, I start with a general introduction to the topics relevant to my research project. Second, I describe the list of major aims of this work. In the third place I include a general discussion of the results obtained and emphasize its scientific relevance. Next, I list the major conclusions from this project. This section is followed by a complete list of references. At the end I include some appendices with the publications derived from this thesis plus supplementary information. Eduardo Moreno González Barcelona, March 2010 i Acknoledgments Acknowledgments To my family; for the support, affection, understanding, patience, advice and encouragement. To my friends; to everybody who has accompanied me along this way, to the ones who arrived and stayed, to the ones who arrived and went but left me with their imprint, to the ones that will come. To mi advisor Pedro Martínez; for his attention, interest, energy and support, and for having done so rewarding this stage of my life and training. To my co-advisor Jaume Baguñà; for his contribution to the birth and maturation on this thesis. To the people who have collaborated with me and made this thesis possible; to Marga, Katrien, Andi and Peter, for their help, enthusiasm and encouragement. To my lab mates; for having always been ready to help me, and for having created a really enriching multicultural environment. To Barcelona. iii Table of Contents Table of Contents Preface i Acknowledgments iii Table of Contents v List of Figures and Tables viii List of Abbreviations xi Informe del Director sobre los Artículos Publicados xv General Introduction 1 1. On the origins of Bilateria 3 1.1. Radiata and Bilateria 3 1.1.1. The Bilateria 3 1.1.2. The Radiata 4 1.2. Radial or bilateral ancestor? Hypothesis on the type of symmetry borne by the last common ancestor of cnidarians and bilaterians 6 1.2.1. The Radial-Bilateral Transition hypothesis 6 1.2.2. The Turbellarian theory 7 1.3. How did the Urbilateria look like? Hypotheses on the nature and evolution of the last common bilaterian ancestor 8 1.3.1. The Planuloid-Acoeloid hypothesis 9 1.3.2. The Archicoelomate hypothesis 11 2. The approach from the Evolutionary Developmental Biology to the origin of the bilateral animals 13 2.1. Hox and ParaHox genes 15 2.1.1. Hox and ParaHox genes in bilaterians 16 2.1.2. Hox and ParaHox genes in non-bilaterians 20 v Table of Contents 3. The phylogenetic position of the acoelomorph flatworms within the Platyhelminthes and within the Bilateria as seen from morphological/embryological data and phylogenetic analyses 23 3.1. Morphological and developmental features that separate Acoelomorpha from the rest of the Platyhelminthes 25 3.2. The advent of molecular phylogenies. Are the Platyhelminthes basal bilaterians and monophyletic? 27 3.3. Phylogenetic, genomic and phylogenomic data support the polyphyly of the Platyhelminthes and the basal position of Acoelomorpha within the Bilateria 28 3.4. A cautionary note from phylogenomics and other molecular data 30 4. The acoel species Symsagittifera roscoffensis and Isodiametra pulchra, new animal models in Evolution and Development 31 4.1. Symsagittifera roscoffensis Kostenko and Mamkaev, 1990 (Graff, 1891) 32 4.2. Isodiametra pulchra Hooge and Tyler, 2005 (Smith and Bush, 1991) 35 Aims of This Study 37 General Discussion 41 1. The Hox-ParaHox complement in acoel flatworms, and its genomic arrangement and structure in the acoel Symsagittifera roscoffensis 43 1.1. The Hox-ParaHox complement in acoels 43 1.2. The arrangement of the genomic Hox gene containing regions in S. roscoffensis 45 1.3. The structure of the genomic regions containing Hox genes in S. roscoffensis 46 2. Hox gene expression patterns in juvenile specimens of Symsagittifera roscoffensis 54 3. Nucleotide sequence and expression pattern of the Cdx ParaHox gene in Symsagittifera roscoffensis 56 vi Table of Contents 4. Number, types, arrangement, and expression of Hox and ParaHox gene complements in Cnidaria 59 5. Scenarios for HOX and ParaHox cluster origin and evolution within the Metazoa 67 6. Functional analysis of the IpHoxPost gene in the acoel Isodiametra pulchra and the ancestral function of the posterior Hox gene in the LCBA 72 7. Axial body pattern mechanism before the advent of Hox genes: the Wnt genes and the co-option of Hox genes 77 8. On the LCBA and the Cambrian “explosion”. A speculative scenario 79 9. Perspectives 84 Conclusions 85 References 89 Appendices 113 Appendix A. Publications 115 Appendix B. Primers used for RACE 117 Appendix C. Sequences 119 Appendix D. Papers not included in this thesis 129 vii List of Figures and Tables List of Figures and Tables FIGURES Cover General anatomy of an acoel (dorsal view). Scheme extracted from http://devbio.umesci.maine.edu/styler/globalworming General Introduction 1. Representation of a bilaterally symmetrical animal. 4 2. Representation of a radially symmetrical animal. 5 3. Hypotheses on the origin of bilateral symmetry in metazoans. 8 4. Diagrammatic representation of the Planuloid–Acoeloid hypothesis. 9 5. Two possible models for the origin of the Bilateria according to the Planuloid-Acoeloid hypothesis. 10 6. Diagrammatic representation of the Archicoelomate hypothesis. 11 7. Origin of the Bilateria from a cnidarian polyp ancestor according to the Archicoelomate hypotheses. 12 8. Hox homeodomain consensus sequence represented as a sequence logo. 16 9. Three dimensional structure of the homeodomain with the three alpha helices binding to the major groove of the DNA chain. 16 10. Diagrammatic representation of HOX clusters and their corresponding expression patterns in deuterostomes and protostomes plotted onto a consensus phylogeny of the represented taxa. 18 11. Morphology of the Acoela. 26 12. Phylogenetic position of the phylum Acoelomorpha as a sister group to the Nephrozoa (protostomes + deuterostomes) bilaterians. 30 13. Dorsal view of an adult specimen of Symsagittifera roscoffensis. 33 14. Dorsal view of an adult specimen of Isodiametra pulchra. 35 viii List of Figures and Tables General Discussion 1. Structure of the coding regions of SrHox5 and SrHoxPost genes. 48 2. Sequence alignment of anterior Hox orthologues. 50 3. Sequence alignment of central Hox orthologues.
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