Metarhizium anisopliae affects brown planthopper survival by disrupting microbial symbiosis and mediating plant defense

Metarhizium anisopliae is an entomopathogenic fungus known for its dual role as an insect pathogen and beneficial plant endophyte. While its direct insecticidal activity is well documented, its indirect contribution to crop resistance through modulation of plant–insect–microbe interactions remain underexplored. The brown planthopper (BPH) ( Nilaparvata lugens ), a major rice pest, depends on yeast-like symbionts (YLS) for nutrition and development. Understanding how M. anisopliae -colonized rice affects BPH physiology and symbiosis is essential for advancing sustainable pest management. Rice plants were endophytically colonized with M. anisopliae and exposed to BPH infestation. Survival was compared between treated and control plants. LC–MS/MS metabolomics, DGGE, and RT-qPCR quantified fungal-induced metabolic shifts and YLS dynamics ( Ascomycetes , Candida , Pichia ) in male, female, and gravid female BPH, supported by pathway analysis. BPH feeding on M. anisopliae colonized rice showed a marked reduction in survival, reducing survival 53.3% compared with controls. Metabolomic profiling revealed substantial reprogramming of rice defense metabolism, particularly within fatty acid–derived pathways, including jasmonic acid, linoleic, arachidonic, and α-linolenic acid metabolism, alongside alterations in tryptophan metabolism and ABC transporters. These plant defense shifts corresponded with a significant decline in essential BPH yeast-like symbionts. DGGE and RT-qPCR showed a strong temporal reduction in Ascomycetes , Candida , and Pichia , most pronounced in gravid females. Overall, these results demonstrate a dual mode of action involving both direct fungal pathogenicity and potential plant-mediated effect on symbionts dynamics. M. anisopliae effectively suppresses brown planthopper populations through dual action, combining direct pathogenicity with plant-mediated disruption of essential symbionts. By enhancing rice defense metabolism and impairing BPH physiology, it offers a promising, sustainable strategy for integrated rice pest management.