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Aphanomyces Euteiches Laurent Camborde Fuctional characterization of different candidate effectors from the root rot oomycete Aphanomyces euteiches Laurent Camborde To cite this version: Laurent Camborde. Fuctional characterization of different candidate effectors from the root rot oomycete Aphanomyces euteiches. Vegetal Biology. Université Paul Sabatier - Toulouse III, 2020. English. NNT : 2020TOU30227. tel-03208760 HAL Id: tel-03208760 https://tel.archives-ouvertes.fr/tel-03208760 Submitted on 26 Apr 2021 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. Abstract Oomycetes are eukaryote pathogens able to infect plants and animals. During host interaction, oomycetes secrete various molecules, named effectors, to counteract plant defence and modulate plant immunity. Two different classes of cytoplasmic effectors have been described to date, Crinklers (CRNs) and RxLR proteins. The translocation process allowing the entrance into the host cells is still unclear, and while extended research gave insight into some molecular targets and role during infection, most of effectors have not been characterized. In the root rot pathogen of legumes Aphanomyces euteiches, only the CRNs are present. Based on a previous study reported by our research group, we published an opinion paper focused on the emergence of DNA damaging effectors and their role during infection. Previous experiments indicate that one of these Crinklers, AeCRN5, harbours a functional translocation domain and once the protein reaches host nuclei, dramatically disturbs root development. Here we reveal that AeCRN5 binds to RNA and interferes with biogenesis of various small RNAs, implicated in defence mechanisms or plant development. Furthermore, comparative genetic analyses revealed a new class of putative effectors specific to Aphanomyces euteiches, composed by a large repertoire of small-secreted protein coding genes (SSP), potentially involved during root infection. Preliminary results on these SSPs point out that AeSSP1256, which contains a functional nuclear localisation signal, enhances host susceptibility. Functional characterisation of AeSSP1256 evidenced that this effector binds to RNA, relocalizes a plant RNA helicase and interferes with its activity, causing stress on plant ribosome biogenesis. This work highlights that various effectors target nucleic acids and reveals that two effectors from distinct family are able to interact with plant RNA in order to interfere with RNA related defence mechanisms and plant development to promote pathogen infection. Keywords: Oomycetes, nucleus, DNA damage, RNA-binding proteins, CRN, SSP. Remerciements Alors par qui commencer… les membres de mon jury bien sûr, à commencer par Claire Veneault-Fourrey et Bruno Favery qui ont accepté d’évaluer mon travail. En ces temps de Covid et à l’heure où j’écris ces lignes, je ne sais pas encore si on se verra masqués, ou par écrans interposés, mais je vous remercie sincèrement pour le temps que vous m’accordez. Merci aussi à Christophe Roux pour avoir gentiment accepté de faire parti de mon jury. Un grand merci à Bernard Dumas, ancien chef de l’équipe lors de mon arrivée au laboratoire. Merci pour la confiance que tu m’as accordé et pour m’avoir un peu poussé à faire une thèse. Bon pour m’avoir beaucoup poussé à faire une thèse. Beaucoup. Mention spéciale à la plateforme d’imagerie, pour leur compétence, leur disponibilité et leur gentillesse en commençant par Alain Jauneau, avec qui j’ai passé des heures autour d’un laser, d’un microscope et d’un tableau Velleda, pour apprendre le FRET-FLIM. Il existe des gens qui rendent tout intéressant. Je n’oublie pas bien sûr Cécile Pouzet, avec qui j’ai beaucoup de plaisir à travailler, et qui en plus veut bien me prêter ses jouets à 500 000 euros. Merci aussi à Yves Martinez et Aurélie Le Ru, d’une patience rare, même si Aurélie me coûte plus cher en bières. Heureusement que vous êtes là. Merci à Jean Philippe Combier pour les discussions et les suggestions apportées. 5 min de discussion avec JP, c’est 5 mois de manips derrière. Faut pas y aller trop souvent non plus… Merci aux personnes avec qui j’ai travaillé sur ce sujet de thèse, notamment Annelyse, Amandine et Marie Alexane que j’ai eu en stage, Chiel Pel et Sarah Courbier qui ont initié le projet sur les SSP et avec qui j’ai passé de très bons moments. Diana Ramirez qui a effectué sa thèse sur les CRNs, ce qui nous a permis de découvrir le monde merveilleux des amphibiens, l’odeur de l’animal, les inséminations de grenouilles femelles, les injections d’ARN dans des centaines d’embryons. En fait on oublie, mais vraiment, travailler sur les plantes, c’est bien. Là c’est le paragraphe dédié aux gens qui m’ont rendu la vie plus facile. Par exemple David, qui réceptionne mes bons de commandes, donc mes erreurs hebdomadaires, dans une ambiance de zénitude et d’encens qui rappelle que rien n’est jamais grave avec David, c’est reposant. Catherine, notre gestionnaire, qui a su aussi être très patiente, mais sans la musique zen et l’encens. Son “CammmmmBBBOOORDEEEE” résonne encore dans ma tête. Merci aux membres de mon équipe, ancienne et actuelle, à ceux du LabCom, à Thomas et Olivier pour les discussions et conseils, c’est toujours agréable de parler avec vous. Merci à Charlène qui m’a soutenu, surveillé mes réinscriptions et ma phobie administrative, à Malo, à Andreï. Merci EMILIE, oui en majuscule, parce que tu m’as beaucoup aidé dans la gestion des affaires courantes comme on dit, en se partageant les tâches à merveille. En gros tu t’occupais de tout ce qui ne me plaisait pas! Enfin, un grand merci à ma directrice de thèse, Elodie Gaulin, qui a su me guider et me soutenir durant ce travail. Ta patience et la facilité avec laquelle tu évacues la pression m’ont beaucoup aidé. C’est un vrai plaisir de travailler avec toi! A ma famille, dont mes parents, éternelle source d’inspiration, à mes enfants, qui vont retrouver leur pôpa, et à ma femme, pour tout ce qu’elle est. List of abbreviations Ae Aphanomyces euteiches AEPs Apoplastic Effector Proteins AM Arbuscular Mycorrhiza Avr Avirulence Bd Batrachochytrium dendrobatidis BIC Biotrophic Interfacial Complex CSEPs Candidate Secreted Effector Proteins CBEL Cellulose Binding ELicitor CRN Crinkling and Necrosis CSEPs Candidate Secreted Effector Proteins CWDEs Cell Wall Degrading Enzymes ECM Ectomycorrhizal Fungi ER Endoplasmic Reticulum ESTs Expressed Sequence Tags ETI Effector-Triggered Immunity EVs Extracellular Vesicles FLIM Fluorescence Lifetime Imaging Microscopy FRET Fluorescence Resonance Energy Transfer GFP Green Fluorescent Protein GWAS Genome Wide Association Study HGT Horizontal Gene Transfer HIGS Host-Induced Gene Silencing HR Hypersensitive Response HRP HorseRadish Peroxidase HSP Heat Shock Protein JA Jasmonic Acid MAMP Microbe-Associated Molecular Pattern MAPKKK Mitogen Activated Protein (MAP) Kinase Kinase Kinase MAX Magnaporthe Avrs and ToX B-like effectors NES Nuclear Export Signal NLPs Necrosis and Ethylene inducing peptide 1 (Nep1)-like proteins NLRs Leucine-Rich Repeat proteins NLS Nuclear Localization Signal PAMP Pattern-Associated Molecular Pattern PTGS Post-Transcriptional Gene Silencing PTI PAMPs-Triggered Immunity PBS Phosphate-Buffered Saline PCW Plant Cell Wall PR Pathogenesis Related PTI PAMP-Triggered Immunity QTL Quantitative Trait Loci R Resistance RALPHs RnAse‐Like Proteins Associated with Haustoria REase Restriction Endonuclease (REase) superfamily RIP Repeat-Induced Point mutations RBPs RNA Binding Protein rDNA Ribosomal DNA ROS Reactive Oxygen Species SA Salicylic Acid SAR Systemic Acquired Resistance SAR Stramenopiles, Alveolates, and Rhizaria SDS Sodium Dodecyl Sulfate siRNA Small Interfering RNAs SSPs Small-Secreted Proteins SNPs Single Nucleotide Polymorphism TALE Transcription Activator-Like Effector TBS Tris-Buffered Saline TE Transposable Element TFs Transcription Factors Ubi Ubiquitin WGA Wheat Germ Agglutinin Y2H Yeast-2-Hybrid Table des matières Abstract ..................................................................................................................................................... List of abbreviations ................................................................................................................................. I – CHAPTER I: General Introduction ...................................................................................................... 1 I-1. Oomycetes and fungi, The World Is Not Enough .......................................................................... 1 I-1.1. The Phantom menace ................................................................................................................ 1 I-1.2. Defence and Resistance against pathogens ............................................................................... 2 I-2. Oomycetes, so close and yet so far from Fungi ............................................................................ 6 I-2.1. The false brothers ...................................................................................................................... 6
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