Entomopathogenic fungi are the only insect pathogens able to start the infection process by penetrating through the host cuticle. However, alternative routes have also been suggested for fungal infection. Among them, the possibility of spore ingestion was first mentioned 100 years ago, but it was little studied. This route is particularly interesting when applying entomopathogenic fungi for biocontrol of insects that avoid fungal infection by embedding their cuticle with antifungal compounds. This is the case of the red flour beetle Tribolium castaneum, which generates economical loss of great significance in stored product environments worldwide. In this study, we showed that T. castaneum was affected when exposed orally to spores of the entomopathogenic fungus Beauveria bassiana. Insect mortality started 2-4 days after conidia feeding, which is a shorter time than the 5-6 days B. bassiana typically takes to infect, colonize, and kill the host through the cuticle. Using the dual RNA-seq technique, we were able to reconstruct the gene expression pattern in both interacting organisms when few conidia are ingested by this recalcitrant insect. After mapping the total reads with the B. bassiana genome, 904 genes were identified during this process. The more expressed genes were related to carbon catabolite repression, cation binding, peptidase inhibition, redox processes, and stress response. Most T. castaneum genes were found to be up-regulated, and a very interesting expression dynamics of genes related to chitin modification was identified. Also, several immune-related genes from Toll, IMD, and JNK pathways were found to be differentially expressed in fungus-infected insects.
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