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Comparative Analyses of the Molecular Footprint of Domestication in Three Solanaceae Species : Eggplant, Pepper and Tomato Stéphanie Arnoux

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Comparative Analyses of the Molecular Footprint of Domestication in Three Solanaceae Species : Eggplant, Pepper and Tomato Stéphanie Arnoux Comparative analyses of the molecular footprint of domestication in three Solanaceae species : eggplant, pepper and tomato Stéphanie Arnoux To cite this version: Stéphanie Arnoux. Comparative analyses of the molecular footprint of domestication in three Solanaceae species : eggplant, pepper and tomato. Agricultural sciences. Université d’Avignon, 2019. English. NNT : 2019AVIG0351. tel-02185095v2 HAL Id: tel-02185095 https://tel.archives-ouvertes.fr/tel-02185095v2 Submitted on 17 Jul 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. Avignon Université INRA Centre de recherche PACA École Doctorale 536 Agrosciences et UR 1052, Génétique et Amélioration Sciences des Fruits et Légumes THÈSE Étude comparée des traces génétiques de la domestication chez trois Solanacées : l’aubergine, le piment et la tomate Présentée à Avignon Université pour obtenir le grade de Docteur en Sciences Spécialité : Biologie Soutenue le 21 février 2019 par Stéphanie Arnoux Encadrée par : Dr. Mathilde Causse (DR, HDR, INRA Avignon) Directeur de thèse Dr. Christopher Sauvage (CR, INRA Avignon) Co-encadrant Devant le jury composé de : Dr. Maud Tenaillon (DR, HDR, CNRS Gif/Yvette) Rapporteur Dr. Joëlle Ronfort (DR, HDR, INRA Montpellier) Rapporteur Dr. Concetta Burgarella (Chercheur, CIRAD Montpellier) Examinateur Dr. Jérémy Clotault (MC, Université d’Angers) Examinateur Résumé La domestication des plantes a débuté il y a quelques milliers d’années quand les hommes se sont sédentarisés. Ils ont sélectionné les plantes sauvages portant des caractères phénotypiques d’intérêt pour la consommation et production humaine. Ce processus évolutif a par conséquent modifié le patrimoine génétique des espèces domestiquées. Cette thèse se penche sur les traces génétiques induites par la domestication chez trois espèces de Solanacées : l’aubergine (Solanum melongena), le piment (Capsicum annuum) et la tomate (S. lycopersicum). En effet, si les caractères phénotypiques des plantes cultivées ont été sélectionnés depuis des milliers d’années, les conséquences moléculaires d’une telle sélection restent peu étudiées à l'échelle du génome. Cette étude est basée sur des données de diversité et d’expression de gènes (RNAseq). En utilisant des méthodes comparatives entre des variétés cultivées et leurs espèces sauvages apparentées, j’ai étudié, à l’échelle intra-spécifique, d’une part les histoires démographiques de chacune des espèces, et d’autre part les changements de diversité nucléotidique et d’expression des gènes dus à la domestication. La comparaison de ces trois événements indépendants de domestication, offre l’opportunité de décrypter les changements génétiques qui convergent chez ces trois espèces lors du processus de sélection humaine. Suite à une introduction qui pose le cadre de cette étude et présente l’état de l’art, le premier chapitre, s’inscrit dans un ouvrage portant sur la génomique des populations d’espèces modèles. Il propose une synthèse des connaissances accumulées en plus d’un siècle de recherche sur l’espèce modèle qu’est la tomate (S. lycopersicum). Ce chapitre permet également de compléter le contexte scientifique dans lequel cette thèse s’inscrit, notamment, en retraçant l’importance que les espèces sauvages apparentées ont eu dans l’amélioration de l’adaptabilité des variétés cultivées actuelles. L’hypothèse du deuxième chapitre révèle la convergence des changements démographiques entre les trois espèces malgré leurs événements indépendants de domestication. L’étude comparée d’inférences de scénarios démographiques a permis de reconstruire l’histoire démographique de chaque espèce cultivée. Ces inférences ont aussi facilité l’estimation des paramètres tels que les flux migratoires entre les espèces sauvages et cultivées, la force des goulots d’étranglement liés à l’intensité de la sélection humaine et la durée des événements de domestication. Ce chapitre permet de démontrer que les changements démographiques liés à la domestication dépendent de l’état de sympatrie ou d’allopatrie des variétés cultivées avec leurs sauvages apparentées. Les connaissances quant à la datation des événements de domestication de nos trois espèces restent très faibles, et les inférences ont permis d’établir des estimations de durée de domestication relativement précise. Ces nouvelles connaissances apportent une plus-value à cette étude pour nos trois espèces et nous invitent à s’interroger sur les différents compartiments du génome qui ont été sélectionnées et modifiées lors de la domestication. Le troisième chapitre teste l’hypothèse d’une convergence évolutive des changements moléculaires, notamment transcriptionnels, induits par la domestication et l’amélioration moderne. La comparaison des variétés cultivées à leurs espèces sauvages apparentées permet d’évaluer la convergence des mécanismes de régulation et d’adaptation liés à la domestication. C’est en testant la corrélation entre les traces génétiques (diversité nucléotidique) de sélection et les changements - 1 - d’expression des gènes observés chez les variétés cultivées que l’hypothèse de départ a été validée. Cette analyse montre que la domestication, au-delà même de changements nucléotidiques, a modifié l’expression des gènes chez les trois espèces. L’analyse des gènes orthologues des espèces a confirmé que la domestication a sélectionné des gènes liés aux phénotypes de développement des fruits et la croissance de la plante alors qu’elle avait, au contraire, contre-sélectionné des gènes liés à la défense des plantes et à leur capacité à tolérer des stress environnementaux. Enfin, en discussion, je réalise un bilan sur mon projet qui apporte de nombreuses preuves de convergence dues à la domestication et des connaissances utiles pour l’étude de l’histoire des Solanacées. De surcroit, des perspectives d’analyses complémentaires sur la liste de nombreux gènes candidats affectés par la domestication, offrent un potentiel de transversalité, pour l’amélioration des variétés cultivées et pour l’étude plus approfondie des conséquences biologiques et évolutives de la domestication. - 2 - Summary Domestication started thousand years ago when human shifted from hunter-gatherer to agrarian societies. They started selecting wild plants for phenotypes related to consumption and yield. This evolutionary process induced changes in the gene pool of domesticated plants. This thesis focuses on genetic footprints induced by domestication within a trio of Solanaceae species: the eggplant (Solanum melongena), the pepper (Capsicum annuum) and the tomato (S. lycopersicum). Crop plants have been selected for thousand years on phenotypic traits, but the molecular consequences of such selection remain unknown at the genome-wide scale. The study was performed on a RNAseq data set; using comparative methods between crops and their wild relatives, I studied, at the intra-specific scale, the demographic history, and, both the nucleotide diversity and the gene expression changes due to domestication. Comparing these three independent events of domestication, is a great opportunity to decipher the interspecific genetic changes, converging for the three species, during the human selection process. The first chapter is a book chapter about population genomics in model species. It details the state of art of hundred years of research on tomato as model species (S. lycopersicum). Tomato is a model species in genetics, as well as in population genomics thanks to the important collection of genomic data that have been accumulating over years. Tomato has the strongest economic importance within the trio of studied species. By highlighting the importance of crop wild relative species for adaptability improvement of modern cultivars, this chapter describes the scientific context of this thesis work. The two next chapters are following these researches and show the importance to both conserve and study the crop wild relative species. In the second chapter, I hypothesize that demographic changes within the three species experience a convergence, despite their independent domestication events. The comparative study of demographic inferences allows the reconstruction of each domesticated species demographic history. Theses inferences facilitate the parameter estimations such as the migration rate between crop and wild, the bottleneck strength paired with the human selection and the duration of the domestication events. This chapter reveals a common bottleneck phenomenon as well as migration rate dependent to the allopatric or sympatric state of the crops with their wild relatives. Knowledge concerning the domestication events dating, for each of the three species, remain poorly studied and this thesis work discloses relative domestication time durations. These new insights bring valuable knowledge to the three species and induce a questioning on the different genome parts that are selected and modified through domestication. The third chapter, test the hypothesis of a convergent evolution of molecular changes, especially transcriptional, induced by domestication
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