Clavé, Corentin (2025) The role of symbiotic microorganisms in the modulation of insect-plant interactions - Toward the development of new tools and strategies for pest control. [Tesi di dottorato]

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Abstract

Reducing the use of synthetic pesticides for crop protection is essential to improve the ecological and economic sustainability of agriculture and to reduce their impact on human health. Entomopathogenic fungi (EEF) have been proposed as an environmentally friendly alternative to chemical control; however, their effectiveness continues to be limited by their susceptibility to extreme environmental conditions. Nevertheless, entomopathogenic fungi, thanks to their adaptability, can evolve in the environment through different lifestyles, particularly as plant endophytes. They can thus establish mutualistic symbiotic associations with their plant host, favouring growth and defences against various abiotic and biotic stress agents, particularly insects. As endophytes, EEF could overcome the traditional obstacles of fungal entomopathogens and provide a novel alternative for management of insect pests. However, the mechanisms associated with this complex network of interactions between EEF, plant, insect pest and natural antagonist of insects are still poorly understood. Consequently, the aim of this PhD is to study the functional and molecular basis of multitrophic interactions involving the EEF Beauveria bassiana colonising tomato plants, and the lepidopteran pest Spodoptera littoralis, responsible for significant damage to tomato plants each year. In the first chapter of this study, feeding bioassays demonstrated the promising endophytic role B. bassiana in reducing the immunocompetence of S. littoralis larvae, making them more susceptible to other biocontrol agents. The second chapter provided a better understanding of the mechanisms underlying this interaction. A metabolomic approach showed the effect of B. bassiana colonisation on activation of the plant's systemic responses. In addition, metagenomic and metatranscriptomic analysis revealed the contribution of the insect microbiota on the endophytic effect of B. bassiana on S. littoralis performance. Finally, the risk to which beneficial organisms can be exposed using insect feeding on plant conditioned by endophytic colonisation has been determined. Thus, the bottom-up effect of the endophytic colonisation of B. bassiana on the endoparasitoid M. pulchricornis was studied and showed a probable compatibility of the fungus in its role as endophyte with the other bio control agent. Taken together, these results represent a new contribution in the understanding of interaction in a multitrophic complex. The exploitation of such knowledge paves the way for the development of a new sustainable biocontrol strategies for the benefits of agriculture.

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