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THÈSE Présentée Et Soutenue Publiquement Le 16 Juin 2014 UNIVERSITÉ EVRY VAL D’ESSONNE Ecole Doctorale - Des Génomes Aux Organismes (GAO) Laboratoire : UNITE DE RECHERCHE EN GENOMIQUE VEGETALE Equipe de recherche : Organisation et évolution des génomes de plantes (OEGP) THÈSE Présentée et soutenue publiquement le 16 juin 2014 Pour l’obtention du grade de Docteur de l’Université d’Evry Val d’Essonne Discipline ou Spécialité: Bioinformatique et Génomique Par : Harry Belcram Organisation, évolution et fonctionnement des gènes majeurs de domestication (Q/q) chez les blés polyploïdes COMPOSITION DU JURY Malika AINOUCHE Professeur, Université Rennes Rapporteur Marie-Angèle GRANDBASTIEN Directeur de Recherche, INRA Versailles Rapporteur Sarah SAMADI Professeur, Muséum National d’Histoire Naturelle Examinateur Pierre ROUMET Directeur de Recherche, INRA Montpellier Examinateur Jérôme SALSE Directeur de Recherche, INRA Clermont-Ferrand Examinateur Boulos CHALHOUB Directeur de Recherche, INRA Versailles Directeur de thèse Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 2 « Viva la re-evolution » Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 3 Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 4 Remerciements Voila ! La fin du début ou le début de la fin…est proche Quand on arrive aux remerciements c’est que l’on à passé les principales turbulences dans la ré- daction et que l’on devrait voir une courte période d’accalmie profiler à l’horizon. Mais la réalité vous rappelle que ce n’est pas fini et qu’il y a encore du pain sur la planche. Alors je profite de cette accalmie pour remercier ceux qui m’ont soutenu, si ce n’est supporté… Je commencerai par remercier les menbres de mon jury de thèse (Marie-Angèle Grandbastien, Malika Ainouche, Sarah Samadi, Pierre Roumet et Jérôme Salse) qui ont accepté de juger mon travail. Mon directeur de thèse, Boulos Chalhoub alias Boubou d’avoir accepté le dur labeur de me diriger dans ma thèse. Après 15 années de travail en commun, je suis content de voir que nos débats res- tent toujours aussi animés. Mes remerciements vont également à mes amours, Katia, Ambre et Mayleen, qui commençaient à sérieusement perdre patience. A mes amis, pour lesquels, Je commence à comprendre les «Tu fait une thèse ? C’est Super ! » Avec un sourire « qui en dit long». C’est ça les amis, ils ne disent rien sur l’instant, mais sont tou- jours présents, y compris aux bons «moments». Vivement les soirées entre poteaux avec le Jej, Agnés, Hélène, Soph et Sof, Pitchoune, Ben, MissTiti et tous les petits bouts. A mes neveux et nièce, Jean-Yves, François-Joseph, José-Luc, Joé, et mes filleuls Adeline et Chris- tophe qui ont supporté leur oncle comme des supporters d’une équipe de Basket. Ma mère qui ne pourra pas être présente, et le reste de ma famille qui est trop loin. Je remercie les thésards et les PostDoc qui sont travaillés dans notre équipe, ou à l’URGV (Mat- Dieu (Mathieu Charles), JJ (Jérémie Just), Mimi (Imen ex Mestiri), Bella « Reine du logiciel End- Note » (Smahane Chalabi), Vivi (Vin Ha Din Thi), Dominique Arnaud, Houda Chelaïfa, Cléclé (Cléa Rouel), et monsieur Soleil (Cyril Zahabi). Tout mes collègues et amis de l’URGV qui on su me soutenir dans les moments de solitudes à la paillasse ou devant l’écran. (Steph & Steph, Lulu, Alex, Sansan, Phiphi, Juju, Véro, Cécile, Isa, Aurélie, Jess, Christelle, Marion, Jean-Luc, Jean-Philippe, Laure, Seb, Marie-Laure, Arnaud Charpentier pour mes inscriptions à l’université. Les personnes du CNS et du CNG qui me supportent depuis le début. Une spéciale dédicace pour Audrey Didier du centre de ressources de Clermont-Ferrand qui à su trouver les lignées de blés manquantes pour mes analyses. « Que la génomique soit avec vous ! » Harry Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 5 Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 6 Résumé En 2006, après un siècle d‘investigations, le gène majeur de domestication 5AQ, conférant de nom- breux caractères comme la non-déhiscence et un battage facile des épillets des blés polyploïdes, a été identifié comme un facteur de transcription homologue au gène Apetala2 d‘Arabidopsis. Bien que ceci représente une avancée importante, le rôle des autres homéologues de ce gène, présents dans le blé tétraploïde (Triticum turgidum) et le blé hexaploïde (T. aestivum), reste à élucider. Dans ce con- texte mon sujet de recherche porte sur l‘appréciation de l‘organisation, l’évolution et le fonction- nement du gène majeur de domestication (Q) et de ses homéologues chez les blés polyploïdes. J‘ai tout d‘abord séquencé et analysé 11 régions génomiques (clones BAC) portant les copies du gène Q/q dans différents génomes de blés polyploïdes et diploïdes; constituant ainsi la plus grande analyse comparative réalisée aujourd‘hui chez le blé. Les comparaisons entre les différents génomes et diffé- rents niveaux de ploïdie montrent que le gène Q/q est la seule séquence conservée, en commun dans les régions génomiques comparées, et que l‘homéologue 5Bq est pseudogénéisé dans les blés hexa- ploïdes. Les comparaisons montrent que le reste des séquences génomiques sont constituées d‘environ 80% d‘éléments transposables (TEs) qui sont entièrement différents quand on compare les génomes A, B, D et S entre eux. A l‘inverse, les TEs sont relativement mieux conservés entre haplotypes du même génome et continuent leurs dynamiques d‘insertions et de délétions différentielles, conduisant à 19 événements de rupture de synténie. Parmi ces événements, j‘ai pu identifier le premier Hélitron actif du blé, inséré dans le pseudogène 5Bq du cultivar Renan. La recherche de son origine par compa- raison de séquences et l‘étude de la variabilité haplotypique m‘ont permis de confirmer l‘insertion récente et l‘origine commune de cet élément au blé sauvage Aegilops ventricosa. Cette espèce a été introgressée dans certaines variétés de blés hexaploïdes. L‘analyse fonctionnelle comparant les caractères de domestication ainsi que l‘expression et les inte- ractions entre les différents homéologues du gène Q/q dans le blé hexaploïde a été rendue possible par la caractérisation des « lignées de délétion », où une ou plusieurs copies homéologues ont été perdues ou substituées. J‘ai pu ainsi caractériser l‘hyper-fonctionalisation de l‘homéologue 5AQ, et la sous- fonctionalisation des homéologues 5Dq et plus étonnamment 5Bq, pseudogénéisé ; les trois homéo- logues contribuent aux caractères de domestication et se régulent entre eux. Les comparaisons pré- cises des séquences des allèles 5AQ et 5Aq pour plusieurs génotypes domestiqués et sauvages m‘ont permis d‘identifier une mutation SNP associée, dans le site d‘adressage d‘un micro RNA (miR172). L‘utilisation d‘une technique RACE-PCR semi-quantitative montre que la mutation dans l‘allèle 5AQ conduit à moins d‘ARNm clivés par les miR172 et donc à sa plus forte expression ; comparée à celle de l‘allèle 5Aq. Ceci suggère un rôle des miR172 dans la régulation des différents homéologues du gène Q/q Mots-Clés : domestication, gène Q, blé, polyploïdie, élément transposable, Hélitron Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 7 Les gènes majeurs de domestication (Q/q) chez les blés polyploïdes Harry Belcram 8 Abstract In 2006, and after a century of investigations, the major domestication gene in polyploid wheat (5AQ), involved in non free threshing and spike easy beating, among many other traits, has been identified as a homolog of Apetala2 gene of Arabidopsis. While this represents an important breakthrough, nothing was yet known about the role of other homoeologs of the Q/q gene present in tetraploid (Triticum turgidum) and hexaploid (T. aestivum) wheat. In this context, my PhD thesis consists in characterizing organization, evolution and function of the major wheat domestication (Q/q) gene and its ho- moeologs in polyploid wheat. I realized first comparative sequencing and analysis of 11 genomic regions (BAC clones) spanning the Q/q gene homolog‘s in different hexaploid, tetraploid and diploid wheat; constituting the most important comparative analysis done for this group of species. Comparisons show that only Q/q gene homologs are conserved in different genomes and across different ploidy levels and that the 5Bq ho- moeolog is pseudogenized in hexaploid wheat. The remaining genomic sequences, constituted of ~80% of transposable elements (TEs) are completely different when comparing A, B, D and S ge- nomes between each others. On the contrary, TEs are more conserved between different haplotypes of a same genome and continue their active insertion and deletion dynamic, leading to 19 identified syn- teny breaks. Among these, I identified the first active Hélitron in wheat inserted into the 5Bq pseudo- gene of a hexaploid wheat cv. Renan. The Hélitron insertion was subsequently retraced as recently occurring whereas it could have been originated from the wild wheat Aegilops ventricosa which has been introgressed into hexaploid wheat. Functional analysis comparing phenotype, domestication traits, expression and interaction between different Q/q homoeologs was rendered possible using series of ―deletion lines‖, where one or several homoeologs were deleted. This allows determining the hyper-functionalization of 5AQ and the sub- functionalization of 5Dq and more interestingly the subfunctionalization of the pseudogene 5Bq. All three homoeologs were shown to contribute to the domestication traits and regulate each others. Precise sequence comparison of 5AQ and 5Aq alleles from different domesticated and wild genotypes allow identification of a SNP mutation, associated with domestication, in the target site of a micro RNA (miR172). Using an adapted semi-quantitative RACE-PCR, I showed that the mutation leads to less cleaved mRNA of the 5AQ gene by the miR172 and consequently its higher expression than the 5Aq allele.
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