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Sugarcane multitrophic interactions: integrating microbiota composition and function with herbivorous insects

Abstract

Over the past few decades, functional studies have led to remarkable advances in characterizing the interactions between plants and their associated organisms, whether harmful or beneficial. The necessary simplification of study models (typically, a plant interacting with a single pathogen/insect pest or symbiotic agent) made it possible to identify the main signaling pathways (pathogenic defensive genes, deregulated signaling cascades, etc.). However, studies on plant responses to multiple infections are relatively rare, although interactions between defense pathways are known to exist. Furthermore, studies on plant interactions with biotic stressors such as herbivorous insects have shown that plant adaptation to these stressors is highly influenced by the composition of the microbiota. Taken together, these observations show that studies with highly simplified models do not take into account the biological complexity of in natural interactions (Figure 1) and compromise a future global understanding of plant responses in their environment.In the last 20 years, our laboratory has made significant contributions to the understanding of the plant-insect-pathogen interactions. These studies range from the elucidation of mechanisms of plant responses to herbivorous insects and pathogens, as well as the characterization of the adaptive mechanisms of insects against plant defenses. Our research group has become a reference on the subject both at home and abroad. More recently, we made a very important contribution, which rewrites the complex mechanisms involving the sugarcane borer (D. saccharalis) and the rot caused by the fungi F. verticillioides and C. falcatum. Contrary to the current understanding that opportunistic fungi penetrated sugarcane plants from the holes left by the caterpillars at the time of the infestation of the plants, we showed that, in fact, the caterpillar is their vector. Furthermore, we showed that the fungus F. verticillioides controls both the plant and the insect (caterpillar and adult female) in order to ensure its dispersion via the production of specific volatiles. No less important was the discovery that the fungus is transmitted vertically to the next generation, perpetuating itself in order to maximize its infestation in the fields. Cane plants infected by the fungus emit volatiles that attract healthy females to oviposition, while females of D. saccaharalis infected by the fungus are attracted to uninfected plants. Thus, a pioneering study of the manipulation of plants and insects by the fungus was described.This project will capitalize on the assets of the partners to move forward on the front of integrative biology of plant health. It will combine the study of complex experimental situations directly inspired by real agronomic conditions with multidisciplinary approaches supported by skills, tools and cutting-edge equipments (confocal microscopy, molecular biology, facilities for transgenic plants, chemical identification of VOCs, insects and fungal cultures, insect bioassays, RNAseq, microbiome sequencing, etc). This project will be carried out on insect pests responsible for considerable economic losses, such as D. saccharalis and fungi and on economically important crop plants Saccharum spp. (sugarcane) and Zea mays (maize). (AU)

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