Mécanismes épigénétiques impliqués dans la réponse d’Arabidopsis thaliana à l’infection par Plasmodiophora brassicae sous différentes conditions abiotiques

Plasmodiophora brassicae, the obligatory biotrophic pathogen causal of clubroot disease, provokes gall formation on roots and induces major cellular and physiological reprogramming in host plants such as Arabidopsis thaliana. Genetic and epigenetic factors are involved in the response of A. thaliana to infection, the effect of which can be modulated by environmental conditions. The aims of this thesis are to determine whether water availability and temperature constraints, alone or combined, modify the epigenetic architecture controlling the clubroot response in Arabidopsis and the involvement of miRNAs in this response. A quantitative epigenetic strategy using an epiRIL population epigenotyped with markers based on DNA methylation variations identified 36 epigenetic QTL (QTLepi), including QTLepi common to several abiotic conditions and QTLepi specific to one condition. Illumina sequencing of mRNAs and miRNAs differentially expressed in susceptible and partially resistant genotypes has enabled the identification of 14 miRNA families targeting 332 genes notably involved in energy production, cell wall degradation and pathogen recognition. Two miRNA families were described for the firsttime. This thesis work provides new insights into the epigenetic mechanisms underlying clubroot resistance and into the epigenetic variability that could potentially be used to construct diseaseresistant varieties in constrained environments.Plasmodiophora brassicae, agent pathogène biotrophe obligatoire causal de la hernie des crucifères, provoque la formation de galles sur les racines et induit des bouleversements cellulaires et physiologiques importants chez les plantes hôtes dont Arabidopsis thaliana. La réponse d’A. thaliana à l’infection implique des facteurs génétiques et épigénétiques dont l’effet peut être modulé par les conditions environnementales. Les objectifs de cette thèse sont de déterminer si des contraintes hydrique et thermique, seules ou combinées, modifient l’architecture épigénétique contrôlant la réponse d’Arabidopsis à la hernie et l’implication des miARN dans cette réponse. Une stratégie d'épigénétique quantitative, utilisant une population epiRIL, épigénotypée avec des marqueurs basés sur des variations de méthylation de l’ADN, a permis d’identifier 36 QTL épigénétiques (QTLepi)dont des QTLepi communs à plusieurs conditions abiotiques et des QTLepi spécifiques d’une condition. Le séquençage Illumina des ARNm et miARN différentiellement exprimés chez des génotypes sensible et partiellement résistant a permis l’identification de 14 familles de miARN ciblant 332 gènes impliqués notamment dans la production d’énergie, la dégradation des parois cellulaires et la reconnaissance des agents pathogènes. Deux familles de miARN ont été décrites pour la première fois. Ce travail de thèse apporte de nouveaux éléments sur les mécanismes épigénétiques sous-tendant la résistance à la hernie et sur la variabilité épigénétique potentiellement utilisable pour la construction de variétés résistantes aux maladies dans des environnements contraints

Environmental conditions modulate the effect of epigenetic factors controlling the response of Arabidopsis thaliana to Plasmodiophora brassicae

International audienceThe resistance of Arabidopsis thaliana to clubroot, a major disease of Brassicaceae caused by the obligate protist Plasmodiophora brassicae, is controlled in part by epigenetic factors. The detection of some of these epigenetic quantitative trait loci (QTLepi) has been shown to depend on experimental conditions. The aim of the present study was to assess whether and how temperature and/or soil water availability influenced both the detection and the extent of the effect of response QTLepi. The epigenetic recombinant inbred line (epiRIL) population, derived from the cross between ddm1-2 and Col-0 (partially resistant and susceptible to clubroot, respectively), was phenotyped for response to P. brassicae under four abiotic conditions including standard conditions, a 5°C temperature increase, drought, and flooding. The abiotic constraints tested had a significant impact on both the leaf growth of the epiRIL population and the outcome of the epiRIL–pathogen interaction. Linkage analysis led to the detection of a total of 31 QTLepi, 18 of which were specific to one abiotic condition and 13 common to at least two environments. EpiRIL showed significant plasticity under epigenetic control, which appeared to be specific to the traits evaluated and to the abiotic conditions. These results highlight that the environment can affect the epigenetic architecture of plant growth and immune responses and advance our understanding of the epigenetic factors underlying plasticity in response to climate change