De Luca, Maria Giovanna (2025) Role of endophytic microorganisms in the control of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) in tomato: Study of functional mechanisms in multitrophic interactions for sustainable agriculture. [Tesi di dottorato]

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Abstract

The intimate mutualism established between plants and endophytic microorganisms often promotes plant growth and defense, conferring protection against several biotic stress agents, including pest populations. The use of these microorganisms in agriculture offers a valid alternative to synthetic agrochemicals, allowing their gradual reduction, with positive impacts on food safety and the environment. In this study, the well-known antagonist fungus of plant pathogens Trichoderma afroharzianum strain T22, the entomopathogenic fungus Beauveria bassiana, and the entomopathogenic bacterium Bacillus thuringiensis were selected to obtain colonized tomato plants (respectively named T22, Bb, and Bt plants) and evaluate whether and how these microorganisms influence the biology of the pest Spodoptera littoralis (Lepidoptera: Noctuidae) through either direct or indirect effects mediated by the plant. Larvae fed with leaves from Bt plants showed a significant reduction in survival during the first two larval instars, reduced pupal survival, and decreased adult longevity and fertility. The observed effects were mainly attributed to the ingestion of the bacterium present in the leaves and its direct impact on the intestinal epithelium of the larvae. Differently, T22 exerts its control by modulating plant responses and inducing gut dysbiosis in the larvae, resulting in insufficient nutritional intake for insect development. In fact, the survival and weight of larvae fed with T22-plants leaves showed a significant reduction compared to controls starting from the fourth instar, with delayed development observed in later stages. Endophytic colonization by B. bassiana, on the other hand, induces metabolic alterations that do not induce mortality in the feeding larvae, which are also larger. However, their reduced nutritional profile, associated with a higher water content, interferes with the neuroendocrine control network underlying development regulation, manifesting as a high pupal mortality rate. Furthermore, ingestion of leaves from plants treated with the three endophytes induces reduced immunocompetence by impairing the cellular immune response of the larvae. This makes them more susceptible to sublethal doses of a B. thuringiensis-based bioinsecticide, while larvae fed on Bb-plant are also more susceptible to topical treatment with a B. bassiana-based bioformulation. These findings contribute to the understanding of the functional mechanisms underlying multitrophic interactions among beneficial endophytic microorganisms, plants, and insects, which will allow the development of new biological strategies for crop protection.

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