Associations between endophytic entomopathogenic fungi and Myzus persicae –tobacco–natural enemy interactions: links to volatile organic compound profiles and microbiome structure

BACKGROUND: Myzus persicae is a major tobacco pest that causes severe economic losses through rapid reproduction and virus transmission. Integrating endophytic entomopathogenic fungi with natural enemies offers a promising, sustainable management strategy. However, the mechanisms underlying four-trophic-level interactions (endophyte-plant-pest-natural enemy) are still poorly understood. RESULTS: Beauveria bassiana GL-5 and Cordyceps cateniannulata H8 both significantly inhibited aphid growth and reproduction. Strain-specific effects were observed: GL-5 enhanced parasitism by Aphidius gifuensis, whereas H8 reduced it. Fungal inoculation increased the female-to-male ratio in Aphidoletes aphidimyza but decreased it in Aphidius gifuensis. Furthermore, fungal inoculation reduced the emergence rates of both natural enemies and decreased the predation capacity of Aphidoletes aphidimyza. Fungal colonization also increased the diversity of tobacco volatile organic compounds (VOCs), and several tentatively identified VOCs may be linked to oviposition preference in Aphidoletes aphidimyza. Fungal treatments significantly reshaped microbial community composition and network complexity in aphid guts and tobacco leaves, altering dominant taxa (Buchnera, Acinetobacter, Pseudomonas, and Bradyrhizobium). Redundancy analysis suggested potential correlations among VOC profiles, microbial community shifts, aphid performance, and natural enemy behavior. CONCLUSION: Entomopathogenic fungi affect the M. persicae-tobacco-natural enemy system, potentially through simultaneous changes in VOCs and microbiomes; however, the underlying causal mechanisms remain unclear. GL-5 demonstrated superior aphid suppression and merits further evaluation for sustainable aphid management. This study advances our understanding of multitrophic regulation and lays the groundwork for integrating fungal endophytes into environmentally friendly pest control strategies. © 2026 Society of Chemical Industry.