Chen Jia, Amr Mohamed, Rasha Al-Akeel, Weiyujie Tian, Xiang Li, Yulu Lou, Ioannis Eleftherianos, Nemat O Keyhani, Wei Zhang
Entomopathogenic fungi can manipulate host behavior to promote infection success, but the molecular effectors remain largely unknown. Here we show that Metarhizium anisopliae suppresses feeding in the migratory locust Locusta migratoria by downregulating an antenna-enriched odorant-binding protein gene, LmOBP2. Metabolomic profiling of infected hemolymph identified infection-associated increases in indole, taurine, DL-serine and dimethylglycine; injection or exposure to these metabolites reduced antennal LmOBP2 transcript abundance. Recombinant LmOBP2 bound key corn volatiles (e.g., leaf alcohol, linalool, 1-nonanol) and several infection-associated metabolites with micromolar affinities, and these interactions were further supported by molecular docking analyses. RNAi knockdown of LmOBP2 (≈90% reduction) decreased antennal electrophysiological (EAG) responses and significantly suppressed host-plant feeding behavior, resulting in a ≈ 30% decline in corn-leaf consumption relative to controls. Dual-choice assays further showed that LmOBP2 silencing abolished preference for leaf alcohol and linalool, while preference for ethyl 2-hydroxyacetate remained largely unchanged. Together, the data support a model in which infection-associated metabolites interfere with olfactory ligand binding and suppress LmOBP2 expression, disrupting food-odor recognition and reducing feeding. These findings reveal a metabolite-mediated route for fungal manipulation of insect olfaction and suggest new avenues for olfaction-targeted biocontrol.