Endophytic entomopathogenic fungi remodel phyllosphere microbiome and metabolome to suppress Spodoptera frugiperda and enhance parasitoid biocontrol

Spodoptera frugiperda severely damages maize and causes massive agricultural economic losses. Combining endophytic entomopathogenic fungi with natural enemies is a sustainable pest management approach. However, how these fungi modify plant physiology to affect S. frugiperda and regulate parasitoid performance remains unclear. Two endophytic entomopathogenic fungal strains (GL-5 and H8) were used. We detected fungal colonization effects on maize growth, leaf antioxidant enzyme activity, phyllosphere microbiota, and metabolome. We further investigated fungal-mediated changes in the development, reproduction, and detoxification metabolism of S. frugiperda and analyzed the tritrophic interaction with the parasitoid Microplitis manilae . Both strains significantly promoted maize seedling growth and disrupted S. frugiperda pupal development, prolonging development and suppressing pest population growth. GL-5 increased the parasitism rate and cocoon weight of M. manilae . Fungal colonization inhibited maize superoxide dismutase (SOD) and peroxidase (POD) activities. GL-5 activated larval glutathione S-transferase (GST), carboxylesterase (CarE), and cytochrome P450 (CYP450) detoxification pathways, while H8 enhanced acetylcholinesterase (AChE) activity and suppressed core detoxification systems. GL-5 enriched Enterobacter and induced flavonoid and phenolic acid accumulation; H8 recruited Chryseobacterium and regulated carbohydrate metabolism and alkaloid biosynthesis. Endophytic entomopathogenic fungi remodel maize phyllosphere microecology and metabolome, impairing pest detoxification and development and synergizing with natural enemies to suppress S. frugiperda . This study provides mechanistic support for eco-friendly fall armyworm management.