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Analyse moléculaire de la réponse immunitaire du lépidoptère Spodoptera frugiperda au complexe nématobactérien entomopathogène Steinernema carpocapsae-Xenorhabdus nematophila

Abstract : Entomopathogenic nematobacterial complexes (NBCs) are natural symbiotic associations between nematodes and bacteria that are pathogenic for insects. In these associations, the bacterial partner uses the nematode as a vector, which transports it in the soil and releases it inside the insect’s body. The bacterium then increases the NBC’s virulence and is used as a food supply by the nematode partner in the insect’s dead body. Due to the originality of these dual pathogens and to their potential for biological control of insect crop pests, studies have been conducted on diverse aspects of their interactions with insects. These works have shown the ability of an NBC to infect and kill an insect depends on a combination of ecological and behavioral factors, as well as on the dialogue between the two partners of the NBC and the insect’s immune system. Insects possess an elaborate immune system which is able the respond by adapted ways to a huge diversity of infectious agents. This system relies on three main components: epithelial barriers, local cellular and humoral responses and systemic humoral responses. A large number of strategies and factors used by NBCs to counteract these three components have already been identified in several NBC-insect interaction models. However, the study of the dialogue between each NBC partner and the hosts’ immune systems is currently suffering from a lack of knowledge of the signaling and molecular aspects of the insects’ immune responses to these dual infections.The first goal of this thesis was to increase this knowledge through a detailed and structured transcriptional analysis of the immune responses of a lepidopteran model, Spodoptera frugiperda, to one of the most studied NBCs, the S. carpocapsae-X. nematophila association. In the current scientific context, this work was mainly characterized by two methodologic novelties: the use of a topologic approach for the transcriptomic analysis of the induced immune responses to the infection by the NBC, and the use of an infection by injection method for the discrimination between the nematode- and the bacterium-induced immune responses. This work allowed the observation of a structured and highly resolutive picture of the induced immune responses, which will be used as a working base for (i) the functional characterization of the interactions of identified immune genes with each partner of the NBC, and (ii) for the detailed analysis of the molecular dialogue between the immune system of S. frugiperda and the NBC. Finally, this work also allowed the identification of two potential new clusters of immune genes, the GBHs and the UNKs, which are among the most overexpressed genes during the tripartite interaction. Our preliminary bioinformatics analyses and activity tests suggest the GBHs could have been acquired by horizontal gene transfer from bacteria and the UNKs could result from a coevolution between noctuids and some Steinernema-Xenorhabdus NBCs. This hypothesis opens new research trails for the understanding of the NBC-sensitivity variations within insect diversity.
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Louise Huot. Analyse moléculaire de la réponse immunitaire du lépidoptère Spodoptera frugiperda au complexe nématobactérien entomopathogène Steinernema carpocapsae-Xenorhabdus nematophila. Sciences agricoles. Université Montpellier, 2019. Français. ⟨NNT : 2019MONTG084⟩. ⟨tel-02861890⟩

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