Entomopathogenic fungi are the only insect pathogens able to infect their host by adhesion to the surface and penetration through the cuticle. Although the possibility of fungal infection per os was described almost a century ago, there is an information gap of several decades regarding this topic, which was poorly explored due to the continuous elucidation of cuticular infection processes that lead to insect death by mycosis. Recently, with the advent of next-generation sequencing technologies, the genomes of the main entomopathogenic fungi became available, and many fungal genes potentially useful for oral infection were described. Among the entomopathogenic Hypocreales that have been sequenced, Beauveria bassiana (Balsamo-Crivelli) Vuillemin (Cordycipitaceae) is the main candidate to explore this pathway since it has a major number of shared genes with other non-fungal pathogens that infect orally, such as Bacillus thuringiensis Berliner (Bacillales: Bacillaceae). This finding gives B. bassiana a potential advantage over other entomopathogenic fungi: the possibility to infect through both routes, oral and cuticular. In this review, we explore all known entry gates for entomopathogenic fungi, with emphasis on the infection per os. We also set out the fungal infection process in a more integral approach, as a need to exploit its full potential for insect control, considering all of its virulence factors and the conditions needed to improve its virulence against insect that might offer some resistance to the common infection through the cuticle.

Entomopathogenic fungi such as Beauveria bassiana are extensively used for the control of insect pests worldwide. They infect mostly by adhesion to the insect surface and penetration through the cuticle. However, some insects, such as the red flour beetle Tribolium castaneum (Herbst), have evolved resistance by embedding their cuticle with antifungal compounds. Thus, they avoid fungal germination on the cuticle, which result in low susceptibility to entomopathogenic fungi. In adult T. castaneum, these antifungals are the well-known defensive compounds methyl-1,4- and ethyl-1,4-benzoquinone. In this study, we added B. bassiana conidia on the diet of adult beetles to study the effect of the entomopathogen on the secretion and detection of the beetle volatile blend containing both benzoquinones. The compounds were analyzed by solid phase microextraction coupled to gas chromatography–flame ionization detection, and were detected by electroantennography. In addition, we measured the expression level of four genes encoding for two odorant-binding proteins (OBP), one chemosensory protein (CSP), and one odorant receptor (OR) in both healthy and fungus-treated insects. Significant alterations in the secretion of both benzoquinones, as well as in the perception of methyl-1,4-benzoquinone, were found in fungus-treated insects. TcOBP7D, TcOBP0A and TcCSP3A genes were down-regulated in insects fed conidia for 12 and 48 h, and the latter gene was up-regulated in 72 h samples. TcOR1 expression was not altered at the feeding times studied. We conclude that fungus-treated insects alter both secretion and perception of benzoquinones, but additional functional and genetic studies are needed to fully understand the effects of fungal infection on the insect chemical ecology.