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Comprendre l’implication des effecteurs fongiques dans l’infection d’une plante hôte : caractérisation fonctionnelle d’effecteurs de Leptosphaeria maculans, un champignon pathogène du colza

Abstract : During infection, plant pathogens secrete an arsenal of molecules collectively known as effectors that circumvent plant innate immunity and trigger infection. The phytopathogenic fungus Leptosphaeria maculans is the causal agent of stem canker of oilseed rape. More than 650 putative effector-encoding genes have been identified in its genome, 7 of them corresponding to avirulence genes. Fungal effectors mainly correspond to small secreted proteins (SSP) with no known homologs and no predicted functions. Their biological function is therefore difficult to predict, and very little is known about the mode of action of L. maculans effectors during infection.The objective of my thesis was to elucidate the role of L. maculans effectors during infection through their functional characterization which included: i) the determination of their subcellular localization in Nicotiana benthamiana et Arabidopsis thaliana; ii) a search for their plant targets; and iii) the determination of the cellular processes targeted by those effectors through their stable expression in A. thaliana and by testing their ability to suppress cell-death in N. benthamiana. We investigated four effectors in that study: AvrLm10-1, AvrLm10-2, AvrLm4-7 and AvrLm3.AvrLm10-1 and AvrLm10-2 are both necessary to trigger recognition by the Rlm10 resistance gene. We have identified orthologs for AvrLm10-1 and AvrLm10-2 in Dothideomycetes and Sordariomycetes phytopathogens, and several paralogs in L. maculans which are expressed specifically during oilseed rape infection. AvrLm10-1 and AvrLm10-2 both have a nucleo-cytoplasmic localization. AvrLm10-1 and AvrLm10-2 physically interact, and may also interact with a PR1 (Pathogenesis-related 1) protein and a secreted cysteine-protease. AvrLm4-7 is recognized by two resistance genes, Rlm4 and Rlm7, and suppresses recognition of AvrLm3 by Rlm3. AvrLm4-7 suppresses cell-death triggered by general inducers, PAMP-Triggered Immunity (PTI) and Effector-Triggered Immunity (ETI). AvrLm4-7 has a nucleo-cytoplasmic localization, whether expressed with or without its signal peptide, suggesting an intracellular mode of action. One of the potential plant targets for AvrLm4-7 is a ribosomal protein, just like a Blumeria graminis effector with structural analogy to AvrLm4-7. Transgenic lines of A. thaliana constitutively expressing AvrLm4-7 do not show any morphological phenotypes or any difference in their susceptibility to diverse fungal pathogens. AvrLm3 is an avirulence gene strongly conserved in L. maculans populations. Recognition of AvrLm3 by Rlm3 is suppressed by the presence of AvrLm4-7. AvrLm3 suppresses cell-death triggered by several inducers of PTI and ETI. AvrLm3 is localized in plant apoplasm when expressed with its signal peptide, suggesting an extracellular localization. AvrLm3 potentially interacts with a secreted myrosinase-associated protein implicated in the myrosinase-glucosinolate system, suggesting that AvrLm3 could disturb glucosinolate production, which is a novel mode of action never described for a plant pathogen effector.My thesis allowed us to improve our knowledge on fungal effector function during infection and to propose new strategies for plant diseases management
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Yohann Petit. Comprendre l’implication des effecteurs fongiques dans l’infection d’une plante hôte : caractérisation fonctionnelle d’effecteurs de Leptosphaeria maculans, un champignon pathogène du colza. Phytopathologie et phytopharmacie. Université Paris Saclay (COmUE), 2017. Français. ⟨NNT : 2017SACLS549⟩. ⟨tel-01709853⟩

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