Infection with the Entomopathogenic Fungus Metarhizium robertsii Suppresses Cellular Immunity and Activates Humoral Antibacterial Responses in Spodoptera frugiperda

The fall armyworm, Spodoptera frugiperda, is a globally distributed agricultural pest. Metarhizium robertsii is an entomopathogenic fungus (EPF) with great application potential for the biological control of S. frugiperda. Nevertheless, to date, there have been no reports describing the interactions between M. robertsii and the immune system of S. frugiperda. In the present study, we investigated the pathogenicity of M. robertsii against S. frugiperda and demonstrated that this fungus exhibits high virulence toward the pest. M. robertsii infection induces apoptosis and necrosis in hemocytes of S. frugiperda, which, in turn, reduces circulating hemocyte abundance. Fungal infection also impairs the spreading capacity of plasmatocytes. These adverse effects on hemocytes collectively lead to a marked suppression of host cellular immune responses, including phagocytosis, nodulation, and encapsulation. Meanwhile, M. robertsii infection upregulates the expression of prophenoloxidase genes in hemocytes, resulting in significantly elevated phenoloxidase activity in host hemolymph. Transcription of antimicrobial peptide genes is also increased in the fat body following fungal challenge. Upregulation of these humoral antibacterial response-related genes enhances the antibacterial activity of hemolymph. This study reveals the mechanistic basis underlying immune interactions between M. robertsii and S. frugiperda and deepens our understanding of the pathogenic mechanisms employed by EPF.