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

## TL;DR

Winter-form pear psylla resist a fungus better than summer-form psylla due to stronger immune responses and energy adjustments.

## Contribution

The study reveals seasonal form-specific immune and metabolic responses in pear psylla to fungal infection, offering new biocontrol strategies.

## Key findings

- Summer-form psylla show immune suppression when infected with Beauveria bassiana.
- Winter-form psylla enhance immune responses and metabolic adjustments to resist the fungus.
- Shared and form-specific gene expression patterns were identified using RNA sequencing.

## Abstract

Pear psylla, a major pest in Chinese pear orchards, has two seasonal forms: summer and winter. We investigated why the entomopathogenic fungus Beauveria bassiana affects both forms differently. Transcription analysis revealed that when summer-form pear psylla were exposed to B. bassiana, their immune systems were suppressed. In contrast, winter-form pear psylla enhanced immune responses and made energy adjustments to resist B. bassiana effectively. This explains the winter form’s stronger resistance. These results advance our understanding of the immunological mechanisms underlying seasonal polyphenism and suggest that fungal biopesticides could be enhanced by developing immune-suppressing adjuvants (e.g., RNA interference-targeting immunity genes or biochemical inhibitors of key immune enzymes). Such precision strategies could synergize with fungal pathogens to achieve higher pest mortality rates, enabling substantially reduced chemical pesticide applications while maintaining effective control. This approach provides a targeted biological control framework that offers sustainable agricultural solutions by minimizing environmental contamination and delaying the evolution of pesticide resistance.

Pear psylla (Cacopsylla chinensis), 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 Beauveria bassiana conidial suspensions to the abdominal cuticle of C. chinensis, we demonstrated that the entomopathogenic fungus B. bassiana 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, B. bassiana 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 B. bassiana infection and supports efficient defense through metabolic reprogramming to fuel energy-demanding defenses. These findings advance our understanding of C. chinensis/B. bassiana interactions, providing a basis for elucidating immune regulation in seasonally polymorphic insects. The results also inform strategies to optimize B. bassiana-based biocontrol, contributing to sustainable pear psylla management.