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Evaluation De La Capacité Du Tomato Yellow Leaf Curl Virus À Maintenir

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Evaluation De La Capacité Du Tomato Yellow Leaf Curl Virus À Maintenir Délivré par le Centre international d’études supérieures en sciences agronomiques Montpellier Préparée au sein de l’école doctorale GAIA Et de l’unité de recherche UMR BGPI Spécialité : Biologie des Interactions Présentée par Déborah CONFLON Evaluation de la capacité du Tomato yellow leaf curl virus à maintenir des ADNs satellites Soutenue le 16 Décembre 2015 devant le jury composé de Mme Cécile Desbiez, Chercheur, INRA, Avignon Rapporteur M. Bruno Gronenborn, Directeur de Recherche, CNRS, Paris Rapporteur Mme Claire Neema, Professeur, SupAgro Montpellier Examinatrice M. Michel Peterschmitt, Chercheur, CIRAD, Montpellier Dir. de thèse Invité Pascal Gentit, Chercheur, ANSES, Angers Co-dir. de thèse Cica Urbino, Chercheur, CIRAD, Montpellier Co-dir. de thèse RESUME Les virus du genre Begomovirus (famille Geminiviridae) sont fréquemment détectés en association avec des ADN satellites appelées alphasatellite et betasatellite qui font la moitié de la taille du génome viral. L’alphasatellite est autonome pour sa réplication et dépend du virus pour son mouvement et son encapsidation tandis que le betasatellite est dépendant de ces fonctions virales. L’alphasatellite a rarement été montré comme ayant un impact sur le virus assistant, contrairement au betasatellite qui augmente la virulence de son virus assistant. En dehors des bégomovirus tels que le Cotton leaf curl virus (CLCuV) qui ont besoin d’un betasatellite pour initier une infection symptomatique dans leur hôte naturel, la plupart des bégomovirus peuvent causer des symptômes, même sans les satellites avec lesquels ils sont parfois détectés. Le Tomato yellow leaf curl virus (TYLCV), un des virus les plus dommageables dans le monde a rarement été détecté associé à des ADN satellites. Les souches méditerranéennes qui sont aussi les plus invasives, n’ont jamais été détectées avec des ADN satellites, bien qu’elles soient capables en conditions artificielles de les assister avec pour conséquence une considérable augmentation de la virulence en cas de co-inoculation avec un betasatellite. Le risque potentiel d’association de satellites avec le TYLCV-Mld a été évalué en testant divers facteurs potentiellement impliqués dans le maintien de l’association TYLCV-satellite: (i) l'accumulation relative intra-plante du TYLCV et des satellites, (ii) la fréquence de co-infection au niveau cellulaire du TYLCV et des satellites, et (iii) l'efficacité de transmission des satellites par le vecteur Bemisia tabaci. Trois satellites précédemment isolés sur coton au Burkina Faso ont été montrés comme pouvant être assistés par le TYLCV dans des plantes de tomate: Cotton leaf curl Gezira betasatellite (CLCuGB), Cotton leaf curl Gezira alphasatellite (CLCuGA) et Okra leaf curl Burkina Faso alphasatellite (OLCBFA). La quantification par PCR quantitative des ADN du TYLCV et des trois satellites entre 11 et 150 jours après inoculation (dpi) révèle qu’en général, les satellites ont une accumulation supérieure à celle du virus, et que, contrairement aux alphasatellites qui n’ont aucun impact, le betasatellite affecte l’accumulation du TYLCV-Mld. Bien que le rapport des quantités de virus/satellites varie au cours du temps, les satellites sont maintenus avec le TYLCV-Mld au temps tardif de 150 dpi et sont transmis par B. tabaci à 32 et 150 dpi. Le TYLCV-IL interagit différemment avec le CLCuGB car son accumulation n’est pas affectée dans les plantes coinfectées. L’estimation par la technique FISH à 18 et 32 dpi de la fréquence d’association des molécules au niveau cellulaire montre que plus de la moitié des cellules infectées sont coinfectées par le TYLCV et un satellite. Ce résultat est cohérent avec la fréquence observée d’ADN satellite dans les plantes. Cependant, on observe de manière inattendue un nombre important de cellules ne semblant contenir que le betasatellite, ce qui pose des questions sur le fonctionnement des associations virus/satellites. Comme la multiplicité d'infection (MOI) des bégomovirus et des satellites est attendue pour être un facteur déterminant de l’efficacité de la co-infection cellulaire, deux variants équi-competitifs de TYLCV ont été préparés afin de déterminer ce paramètre. Enfin, des amorces PCR permettant la détection générique de betasatellites ont été dessinées pour être utilisées dans le diagnostic par l'Agence française pour l'alimentation, l'environnement et la santé et sécurité au travail (ANSES). Outre les conséquences agronomiques d’un maintien possible des satellites avec le TYLCV, les résultats de cette étude donnent un aperçu novateur sur les interactions entre les bégomovirus et les satellites, au niveau de la plante, au niveau cellulaire et moléculaire. i ABSTRACT Begomoviruses (family Geminiviridae) are frequently detected with half genome sized defective virus DNAs, and for some of them with satellite DNAs of similar size, i.e. alphasatellite and betasatellite. Both molecules rely on the virus for maintenance in plant. The alphasatellite was rarely proved to have an impact on the helper virus but the betasatellite was often shown to increase its virulence. Except some begomoviruses, like Cotton leaf curl virus (CLCuV) which rely on a betasatellite for a full symptomatic infection in its natural host plant, most of the begomoviruses which were frequently detected with satellites do not rely on them for infectivity. Tomato yellow leaf curl virus (TYLCV) is one of the most damaging begomovirus worldwide. The Mediterranean IL and Mld strains, the most invasive ones, were never detected in association with satellites, although they were experimentally proved to readily assist them for replication and movement in plant. This was particularly true for betasatellites and resulted in a dramatic increase in the virulence of TYLCV. The potential of a TYLCV-satellite association was assessed by testing various factors involved in the maintenance of both molecules in tomato plants: (i) the relative intra-plant accumulation of TYLCV and satellites, (ii) the frequency of host cells co-infected with TYLCV and satellites, and (iii) the transmission efficiency of satellites by the natural whitefly vector of TYLCV, Bemisia tabaci. Three satellites previously isolated from okra in Burkina Faso, were shown here to be assisted by TYLCV in tomato plants: Cotton leaf curl Gezira betasatellite (CLCuGB), Cotton leaf curl Gezira alphasatellite (CLCuGA) and Okra leaf curl Burkina Faso alphasatellite (OLCBFA). The dynamic of TYLCV and satellite DNAs monitored between 11 and 150 days post- inoculation (dpi) by quantitative PCR revealed that satellites accumulated at a higher level than the virus, and that, in contrast with alphasatellites which have no impact, betasatellites affected TYLCV-Mld accumulation. Although the ratio of virus/satellite amounts varies over time, satellites were maintained in all test plants up to 150 dpi and were readily transmitted at 32 and 150 dpi. TYLCV-IL interacts differentially with CLCuGB as its accumulation was not affected in the coinfected plants. At 32 dpi, the TYLCV/satellite infection status of plant cells was determined by FISH and more than 50% of the monitored infected cells were co-infected with TYLCV and a satellite. The infection status was consistent with the frequency of satellite DNA in plants. Unexpectedly a substantial number of cells were positive only for betasatellite, suggesting that the coinfection with the virus could be dispensable for replication. This observation raises question on the functioning of virus/satellite association or multipartite viruses. As the multiplicity of infection (MOI) of begomoviruses and satellites is expected to be a determinant of the efficiency of virus/satellite cell coinfection, two equi-competitive TYLCV variants were prepared to determine this parameter for TYLCV. Finally, PCR primers designed for the generic detection of betasatellites were designed to be used as a diagnostic tool by the French Agency for Food, Environmental and Occupational Health & Safety (ANSES). Besides the agronomic concern of the possible maintenance of DNA satellites with TYLCV, the results of our study are expected to provide a new insight on the interactions between begomovirus and satellites, at the plant, cellular and molecular levels. ii Laboratoire d’accueil Cette thèse a été réalisée au sein de l’équipe : Interactions Virus Insecte Plante (VIP) Sous la Direction de : Dr Michel Peterschmitt, Directeur de Recherche CIRAD, Montpellier - Directeur de thèse Dr Pascal Gentit, Chercheur, ANSES, Angers – Co-Directeur de thèse Dr Cica Urbino, Chercheur, CIRAD, Montpellier – Co-Directeur de thèse UMR Biologie et Génétique des Interactions Plante-Parasite (BGPI) INRA-CIRAD-SupAgro Campus International de Baillarguet 34398 Montpellier cedex 5 France iii REMERCIEMENTS Je remercie, tout d’abord, les membres de mon jury pour le temps consacré à l’évaluation de mon travail : Mme Claire Neema, Mme Cécile Desbiez et M. Bruno Gronenborn. Je souhaite également remercier les membres de mon comité de thèse pour leurs conseils : Mme Eugénie Hebrard, Mme Véronique Ziegler-Graff, M. Sérafin Gutierrez, M. Stéphane Blanc et M. Pascal Gentit. Je remercie également Philippe Rott puis Claire Neema pour leur accueil au sein de l’UMR BGPI. Merci au CIRAD et à l’ANSES d’avoir accepté de financer ce projet. Merci à Stéphane Blanc de m’avoir accueillie au sein de l’équipe VIP, et de faire que cette équipe soit un super environnement de travail, que ce soit au niveau de la qualité de l’enseignement scientifique ou de l’ambiance de travail. Je tiens tout particulièrement à remercier mes encadrants, Michel Petershmitt et Cica Urbino, sans qui ce travail n’aurait pas été possible. C’est vrai que ça n’a pas toujours été facile, merci de m’avoir remotivée dans mes moments de doute et de m’avoir soutenue jusqu’à la fin. Tout au long de ces 3 années passées ensemble j’ai appris beaucoup de choses, tant au niveau professionnel que sur moi-même. Merci à Michel pour son enthousiasme à toutes épreuves, ses conseils et le partage de sa passion pour la recherche. Une grand merci à Cica pour son accompagnement, ses conseils et sa franchise.
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