Morphotype-Specific Antifungal Defense in Cacopsylla chinensis Arises from Metabolic and Immune Network Restructuring

Pear psylla (<i>Cacopsylla chinensis</i>), a major pear tree pest widely distributed in China, is increasingly affecting the productivity of orchards. This species exhibits seasonal polyphenism with two distinct forms, namely, a summer form and a winter form. Through topically applying <i>Beauveria bassiana</i> conidial suspensions to the abdominal cuticle of <i>C. chinensis</i>, we demonstrated that the entomopathogenic fungus <i>B. bassiana</i> exhibits significant yet phenotypically divergent virulence against these two forms. Using PacBio SMRT sequencing and Illumina RNA-seq, we analyzed transcriptomic changes post-infection, revealing form-specific immune responses, with 18,232 and 5027 differentially expressed genes identified in summer- and winter-form pear psylla, respectively, and a total of 3715 DEGs shared between the two seasonal phenotypes. In summer-form individuals, <i>B. bassiana</i> infection disrupted oxidative phosphorylation and downregulated immune recognition genes, cellular immune-related genes, and signaling genes, along with the upregulation of the immune inhibitor serpin, indicating immunosuppression. Conversely, in winter-form individuals, immune-related genes and glycolytic rate-limiting enzymes were upregulated after infection, suggesting that the winter-form immune system normally responds to <i>B. bassiana</i> infection and supports efficient defense through metabolic reprogramming to fuel energy-demanding defenses. These findings advance our understanding of <i>C. chinensis</i>/<i>B. bassiana</i> interactions, providing a basis for elucidating immune regulation in seasonally polymorphic insects. The results also inform strategies to optimize <i>B. bassiana</i>-based biocontrol, contributing to sustainable pear psylla management.