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Genetic and Epigenetic Control of Life Cycle Transitions in the Brown Alga Ectocarpus Sp

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Genetic and Epigenetic Control of Life Cycle Transitions in the Brown Alga Ectocarpus Sp Genetic and epigenetic control of life cycle transitions in the brown alga Ectocarpus sp. Simon Bourdareau To cite this version: Simon Bourdareau. Genetic and epigenetic control of life cycle transitions in the brown alga Ec- tocarpus sp.. Development Biology. Sorbonne Université, 2018. English. NNT : 2018SORUS028. tel-02111040 HAL Id: tel-02111040 https://tel.archives-ouvertes.fr/tel-02111040 Submitted on 25 Apr 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. Sorbonne Université Ecole Doctorale 515 Complexité du Vivant UMR 8227 CNRS – Sorbonne Université Laboratoire de Biologie Intégrative des Modèles Marins Equipe Génétique des Algues Contrôle génétique et épigénétique des transitions du cycle de vie chez l’algue brune Ectocarpus sp. Genetic and epigenetic control of life cycle transitions in the brown alga Ectocarpus sp. Par Simon Bourdareau Thèse de doctorat de Biologie du développement Dirigée par J. Mark Cock et Susana M. Coelho Présentée et soutenue publiquement le 27 Mars 2018 Devant un jury composé de : Dr Gareth Bloomfield, Rapporteur Medical Research Council, UK Dr Célia Baroux, Rapportrice University of Zurich, Switzerland Pr Christophe Destombe, Examinateur Sorbonne Université - CNRS Dr Akira F. Peters, Examinateur Chercheur Indépendant Dr Frédérique Peronnet, Invitée Sorbonne Université - CNRS Dr J. Mark Cock, Directeur de thèse Sorbonne Université – CNRS Dr Susana M. Coelho, Co-directrice de thèse Sorbonne Université – CNRS A ma famille i REMERCIEMENTS Je tiens à remercier toutes les personnes qui m’ont permis d’achever ce travail. En premier lieu, je remercie mes directeurs de thèse Mark Cock et Susana Coelho. Ils m’ont permis de m’épanouir dans le travail tout au long de la thèse. Je les remercie également pour la confiance qu’ils m’ont apportée. Je ne pouvais pas souhaiter mieux pour mes premiers pas dans le monde merveilleux de la recherche. Je les remercie également pour nous avoir toujours ramené des « spécialités culinaires » des pays d’où ils revenaient même si souvent c’était gustativement répugnant. Je remercie également les membres de mon comité de thèse, Angela Falciatore, Phillipe Potin et Leila Tirichine, d’avoir suivi le projet durant ces trois années et pour l’intérêt qu’ils y ont porté. Je veux remercier également Delphine Scornet, Laurent Pères et Josselin Guéno (mon petit Jojo) pour leur aide substantielle dans cette thèse. Sans eux, le projet n’aurait jamais abouti et ne serait pas ce qu’il est aujourd’hui. Je remercie spécialement Leila Tirichine (Ecole Normale Supérieure, Paris) pour les conseils qu’elle a apporté lors de la mise au point du protocole de ChIP-seq. Ainsi que Damarys Loew et Bérangère Lombard (Institut Curie, Paris) pour les analyses de spectrométrie de masse des histones. De plus, je remercie José Manuel Franco-Zorrilla (CSIC, Madrid) avec qui nous avons établi une collaboration fructueuse sur l’analyse des capacités de fixation à l’ADN des facteurs de transcription. Je remercie tous les membres de l’équipe présents et passés : la horde des post- doctorants, Olivier Godfroy, Fuli Liu, Martina Strittmatter, Komlan Avia, Svenja Heesch, Aga Lipinska, Marie-Mathilde Perrineau, Nick Toda et de contractuels Céline Caillard, Zofia Nehr, ainsi que la joyeuse tribu des doctorants (Alexandre Cormier, Josselin Guéno, Laure Mignerot, Rémi Luthringer et Yao Haiqin). Cela a été très enrichissant de rencontrer tant de personnes venues de quatre coins du monde avec tant de cultures différentes. ii Je remercie également l’ensemble des doctorants du LBI2M et notamment les voisins de bureau, Céline Conan, Léa Cabioch, Hetty Kleinjan, Jojo et Yao, pour les bonnes tranches de rigolades, de délires ou de soirées. Enfin, je remercie tous les membres du LBI2M pour leur gentillesse et pour tous les conseils échangés. iii CONTENTS Remerciements ii Contents iv Chapter 1 – General Introduction 1 SECTION I: Major evolutionary events during the emergence of the eukaryotes 3 The origins of photosynthetic eukaryotes 3 Eukaryotic life cycles 4 The origin of meiotic sex 5 Gamete fusion is broadly conserved across eukaryotes 6 The necessity for “self” recognition 6 Diversity of life-cycles and evolutionary considerations 7 SECTION II: Genetic mechanisms that regulate life-cycle progression: the role of 11 homeodomain transcription factors Genetic basis of life-cycle progression 11 Homeodomains, a brief history of their discovery 17 Diversity of Homeodomain TFs 18 The Homeodomain is a DNA-Binding domain 20 SECTION III: Epigenetic reprogramming and the specification of cell identity 23 Epigenetics: a brief history and a definition 23 DNA Methylation 24 Nucleosome positioning and DNA compaction 25 Core Histones and Variants 26 Post-translational Modifications of Histones 26 Writers, Erasers and Readers 28 SECTION IV: Using Ectocarpus to explore development and life cycle regulation 31 Ectocarpus, an emerging model for evolutionary developmental biology 31 Genetic dissection of life-cycle progression and related developmental processes in 34 Ectocarpus Objectives 36 iv Chapter 2 - Characterization of brown alga life cycle mutants indicates deep evolutionary origins of pathways controlling 39 deployment of the sporophyte program Manuscript (in preparation) : Characterization of brown alga life cycle mutants indicates deep 41 evolutionary origins of pathways controlling deployment of the sporophyte program Abstract 41 Introduction 42 Results 43 The OUROBOROS gene encodes a TALE HD TF 43 Characterisation of additional sporophyte-to-gametophyte conversion mutants 44 sam sporophyte-to-gametophyte conversion mutants exhibit a meiotic defect 45 The SAMSARA gene encodes a TALE HD TF 46 The expression patterns of the ORO and SAM genes are consistent with roles in determining 47 the sporophyte generation ORO and SAM regulate the expression of sporophyte generation genes 47 The ORO and SAM proteins interact in vitro 48 Evolutionary origins and domain structure of the ORO and SAM genes 49 Discussion 50 Methods and Materials 52 Biological material and mutagenesis 52 Microscopy 52 Photopolarisation 52 Treatment with the sporophyte-produced diffusible factor 53 Mapping of genetic loci 53 Reconstruction and sequence correction of the ORO and SAM loci 54 Quantitative reverse transcriptase polymerase chain reaction analysis of mRNA abundance 54 RNA-seq analysis 55 Detection of protein-protein interactions 56 Searches for HD proteins from other stramenopile species 56 Phylogenetic analysis and protein analysis and comparisons 56 References 57 Figures and tables 62 79 v Chapter 3 - Functional analysis of the Ectocarpus sp. life cycle regulators OUROBOROS and SAMSARA Introduction 81 Material and Methods 82 Plasmid Construction 82 Protein Binding Microarray, DAP-seq and epitope production 82 Yeast Two-hybrid bait constructs 83 Yeast Two-Hybrid cDNA library 83 Yeast Two-Hybrid Assay 84 Strain genotypes 84 Selection of bait and prey combinations in yeast 84 Mating and screening for prey-bait interactions 84 Extraction and cloning of prey plasmids 85 Small-scale interaction screening 85 Protein Binding Microarray 86 DAP-seq 86 Production of anti-ORO and anti-SAM antibodies 88 ChIP-nexus 88 Results 90 In vitro DNA-binding capacities of ORO and SAM 90 Genome-wide identification of ORO and SAM binding sites in vivo 98 Identification of ORO-interacting proteins 101 Discussion 104 The DNA binding sites of ORO and SAM are related to those of other TALE homeodomain TFs 104 but exhibit some novel features ORO and SAM interacting proteins suggest a role for TF complexes and chromatin 107 modification in the gametophyte-to-sporophyte transition vi Chapter 4 - An efficient chromatin immunoprecipitation 113 protocol for characterizing histone modifications in the brown alga Ectocarpus Manuscript (in preparation) : An efficient chromatin immunoprecipitation protocol for 115 characterizing histone modifications in the brown alga Ectocarpus Introduction 115 Procedure 117 Anticipated results 123 References 124 Figures 126 Chapter 5 - Epigenetic modifications associated with life cycle 129 transitions in the brown alga Ectocarpus Manuscript (in preparation) : Epigenetic modifications associated with life cycle transitions in the 131 brown alga Ectocarpus Introduction 131 Results 132 Ectocarpus histones and histone modifier enzymes 132 Identification of histone PTMs in Ectocarpus 133 Genome-wide distribution of selected histone PTMs 133 Epigenetic reprogramming during the Ectocarpus life cycle 135 Discussion 136 Material and Methods 138 Strains and growth conditions 138 Detection of histone PTMs using mass spectrometry 138 Detection of histone PTMs using western blots 138 Genome-wide detection of histone PTMs 138 Comparisons of sporophyte and gametophyte transcriptomes using RNA-seq 140 Searches for histone and histone modifying enzyme encoding genes in Ectocarpus 140 References 140 Figures and Tables 146 Supplementary material 157 vii Chapter 6 - General Conclusions and Perspectives 171 Regulation of life cycle progression by the ORO and SAM proteins
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