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THESE Le Grade De Docteur SAUVION Nicolas N° d’ordre 95 ISAL0042 Année 1995 THESE présentée devant l’Institut National des Sciences Appliquées de Lyon pour obtenir le grade de Docteur Formation Doctorale : Analyse et Modélisation des Systèmes Biologiques par SAUVION Nicolas DEA Analyse et Modélisation des Systèmes Biologiques Effets et modes d'action de deux lectines à mannose sur le puceron du pois, Acyrthosiphon pisum (Harris). Potentiel d'utilisation des lectines végétales dans une stratégie de création de plantes transgéniques résistantes aux pucerons. Soutenue le 20 juin 1995 devant la commission d’examen : NARDON Paul Prof. INSA de Lyon Directeur thèse LEGAY Jean-Marie Prof. UCB Lyon 1 Président GATEHOUSE Angharad Res. Fellow - Univ. Durham (GB) Rapporteur BOURNOVILLE René DR INRA Rapporteur ROUGE Pierre Prof. UPS Toulouse Rapporteur RAHBE Yvan CR INRA RIBA Guy DR INRA Résumé Nous avons recherché des protéines toxiques pour les pucerons (Homoptères, insectes piqueurs-suceurs phloémophages) et étudié le mode d'action de certaines d’entre elles. Ce travail constitue une première étape d'un programme de création de plantes résistantes aux pucerons par génie génétique. Les caractéristiques toxicologiques de nombreuses protéines sont évaluées par des tests d’ingestion sur milieux artificiels définis. Des lectines d’origine végétale se liant au mannose présentent des propriétés toxiques intéressantes. Notre étude porte sur la Concanavaline A (lectine de Canavalia ensiformis [L.] DC, ConA) qui est une lectine modèle très étudiée du point de vue biochimique, et la lectine du perce-neige (Galanthus nivalis L., GNA) dont les caractéristiques en font un bon candidat à l'application envisagée. Nous mettons en évidence une variabilité de la toxicité des lectines à mannose chez six espèces de pucerons. La ConA est moins active sur les espèces polyphages. Elle n’est pas phagorépulsive pour notre puceron modèle, Acyrthosiphon pisum (Harris) et agit en quelques heures aux doses moyennes, notamment en inhibant l’ingestion. Une adaptation comportementale à moyen terme (24 h-48 h) est également mise en évidence. Des techniques de marquage révèlent que la cible physiologique primaire de la ConA est la portion antérieure du mésentéron. Elle s’y fixe en très grande quantité. Après liaison aux cellules épithéliales, la lectine induit une hypertrophie de ces cellules et un détachement de leur membrane apicale. Des expériences de compétition lectines/mannosides indiquent que la liaison toxine- épithélium ne semble pas dépendre uniquement d’une interaction sucre-lectine. Nous observons également une forte perturbation du métabolisme des acides aminés des pucerons. Le mode d’action de la ConA et de la GNA diffèrent sensiblement sur ce point. Les premiers tests biologiques effectués sur des pommes de terre transgéniques exprimant de manière constitutive le gène de la GNA sont variables mais prometteurs. Abstract The aim of this study is to identify proteins that are deleterious to aphids (Homoptera; Aphididae), and to determine the mechanisms of action of some of them. This work is a first step in a defence strategy against aphids based upon the use of transgenic plants expressing such toxic plant proteins. Amongst the molecules tested, two mannose-binding lectins, ConA and GNA, from jackbean (Canavalia ensiformis) and snowdrop (Galanthus nivalis) respectively, induced significant mortality and growth inhibitory effects on aphid nymphal development; these were thus chosen for subsequent investigations. Dose-response curves of mannose binding lectins were shown to differ substantially between the six aphid species tested. At sub-lethal doses GNA and ConA adversely affected total fecundity and the dynamics of reproduction of both pea aphid, Acyrthosiphon pisum (Harris), and peach-potato aphid, Myzus persicae Sulzer. ConA acted as an antifeedant, but not as a feeding deterrent. On the model aphid A. pisum, high levels of ConA significantly altered ingestion rates, but at moderate levels, insects appeared to exhibit a time-dependent tolerance of the antifeedant. The stomach and anterior part of the midgut were shown to be the primary physiological targets of ConA. As a result of its binding to epithelial cells, the lectin was shown to induce hypertrophic growth of these cells and subsequent shedding of the membrane surface. Competitive experiments with different mannosides suggested that this interaction appeared not to be simply a consequence of binding of the lectin to mannose residues. Both ConA and GNA caused distinct disturbances in the steady-state levels of free amino acids in the aphid, but the effects of the two lectins differed significantly from each other. Effects of lectins are discussed in relation to the use of transgenic plants expressing such toxic proteins for potential control of aphid populations. 2 Avant-propos Mes premiers remerciements s'adresseront au Professeur Paul Nardon, directeur du laboratoire de Biologie Appliquée (INRA-INSA) de Lyon, qui m'a accueilli dans son laboratoire. Je tiens à souligner les efforts qu'il met en oeuvre pour assurer aux étudiants un soutien scientifique et matériel leur permettant de se former à la recherche et de réaliser leur travail dans de bonnes conditions. Je remercie le Ministère de la Recherche et de l'Enseignement Supérieur pour la bourse qu'il m'a octroyée. Sans cette aide, je n'aurais pu conduire ce travail de thèse et il est fort probable que mes espoirs de faire carrière dans la recherche auraient été remis en cause. Toute ma reconnaissance va à l'"équipe puceron" du laboratoire : Yvan Rahbé, Gérard Febvay et Guy Bonnot. Non seulement ils m'ont fait bénéficier de la complémentarité de leur compétences, mais surtout ils ont su me transmettre toute leur rigueur scientifique. Yvan m'a encadré tout au long des années du DEA et de la thèse avec le dynamisme et l'enthousiasme qui le caractérise. J'ai beaucoup apprécié ses qualités tant scientifiques qu'humaines. Gérard et Guy m'ont apporté principalement leur aide dans les analyses statistiques des données et dans les étapes de rédaction d'articles ou de la thèse. Une partie de ce travail a été réalisée au Laboratoire de Biologie Moléculaire de l'Université de Durham (GB). Je remercie John Gatehouse de m'y avoir accueilli. Je suis très reconnaissant à Angharad Gatehouse pour la qualité de son encadrement et pour l'intérêt qu'elle a porté à mon travail. Je suis très honoré qu'elle ait accepté de le juger en tant que rapporteur. Je remercie vivement Monsieur René Bournoville, directeur du laboratoire de Zoologie de l'INRA de Lusignan (86). Il a guidé mes premiers pas dans le domaine de la recherche et m’a vivement encouragé à la fin de mon année de Maîtrise à poursuivre mes études pour effectuer une thèse. C’est avec beaucoup de plaisir que je l’ai vu accepter d’être rapporteur. Mes remerciements s’adressent également au Professeur Pierre Rougé, directeur du laboratoire de Pharmacologie et de Toxicologie Fondamentale au CNRS de Toulouse, pour avoir accepté de juger ce travail en tant que rapporteur, alors même que le monde complexe des pucerons lui était peu connu. J’adresse mes sincères remerciements au Professeur Jean-Marie Legay, ex-Directeur de la Formation Doctorale, pour les conseils qu’il m’a prodigués et pour avoir accepté d’être membre du jury. Merci également à Monsieur Guy Riba, directeur du département de Zoologie de l’INRA pour sa présence en tant que membre du jury. J’ai vraiment beaucoup de plaisir à associer à ce travail tous les membres du laboratoire chercheurs ou techniciens. Je voudrais en particulier remercier Christiane, la partie consacrée à l’histologie n’aurait pas été réalisable sans son aide, et Josette qui a effectué les dosages d’acides aminés libres. Je ne voudrais pas non plus oublier Gabrielle pour son aide (préparations des solutions de milieu, tests de toxicité, etc) et Alain (plantations), ni Bernard, Simon et Hubert pour leurs conseils pertinents et avisés, ni bien-sûr Annie pour ses talents de relectrice ! Je tiens également à remercier chaleureusement le personnel du Centre de Microscopie Electronique Appliquée à la Biologie et à la Géologie de l’Université Claude Bernard. Leur patience et leur persévérance ont permis de surmonter les nombreuses difficultés rencontrées pour l’observation de l’ultrastructure de l’intestin des pucerons. J’ai été aidé dans la frappe de ce manuscript par Christelle. Je la remercie d’avoir sacrifié certains de ses samedis et de ses dimanches pour qu’il soit rédigé dans les temps... Et puis, je m’en voudrais de ne pas associer mes parents à ce travail. Merci Denis, Bérengère, Frédérique, Anne et Papy pour vos encouragements. Mention spéciale quand même à Guillaume pour ses superbes dessins. Ce travail te doit aussi beaucoup Joël et pas seulement pour les quelques heures de relecture que je t’ai imposée... Enfin, Anne, je ne saurais trop louer ta patience et te remercier pour le soutien que tu m’as toujours apporté, en particulier pendant ces derniers mois... 3 Liste des abréviations ACA : lectine de l'amaranthe, Amaranthus caudatus L. ACP : Analyses en Composantes Principales ADN : acide désoxyribonucléique AFC : Analyse Factorielle des Correspondances ARN : acide ribonucléique ASA : lectine de l'ail, Allium sativum L. BCH : chitinase du haricot BDA : lectine de la bryone dioïque, Bryonia dioica Jacq. BPA : lectine de Bauhinia purpurea L. BSII : lectine de Griffonia simplicifolia (Welw.) Baill ConA : lectine de la canavalia, Canavalia ensiformis [L.] DC CPA : lectine du pois-chiche, Cicer arietinum L. CpTI : serpine inhibiteur de protéase du niébé, Vigna unguiculata Walp CSA : lectine du genêt-à-balais, Cytisus scoparius Link. DDT : dichloro-diphényl trichloroéthane (insecticide) DIMBOA : 2.4-dihydroxy-7-, méthoxy-1.4-benzoxine-3-one = acide hydroxamique DSA : lectine de la Datura stramonium L. ECA : lectine du flamboyant, Erythrina cristagalli L. ECL : Enhanced ChimioLuminescence EHL : lectine d'Eranthis hyemalis [L.]Salisb. ELISA : Enzyme Linked ImmunoSorbent Assay FAO : Food and Agriculture Organisation GalNAc : N-acétyl-galactosamine GlcNAc : N-acétyl-glucosamine GNA : lectine du perce-neige, Galanthus nivalis L.
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