Volatile-mediated interactions between cereal aphids and Fusarium graminearum shape wheat susceptibility to pest and pathogen induced biotic stress

• Fusarium graminearum and cereal aphids co-occupy wheat and interact on shared hosts. • Alate aphids show species-specific responses to F. graminearum -infected wheat. • The pathogen attracts R. padi and repels S. avenae via altered host volatiles. • In distal pathogen interactions R. padi increases mycotoxins and disease severity. • F. graminearum and R. padi may co-evolve, amplifying risk under climate change. Cereal aphids ( Sitobion avenae F., Rhopalosiphum padi L.) and Fusarium graminearum , the causal agent of Fusarium head blight (FHB), are major biotic threats to wheat that interact via their shared host. Co-localised S. avenae -pathogen interactions have been shown to increase Fusarium mycotoxins, including deoxynivalenol (DON), reducing grain safety. However, interactions with R. padi had not been investigated. Here, we show that a DON-producing F. graminearum modifies wheat volatile emissions to differentially affect the behaviour, movement and fitness of R. padi and S. avenae . Using behavioural assays, volatile profiling, olfactometry and life history trait analyses, we demonstrate that pathogen-induced volatile organic compounds attract winged R. padi but repel S. avenae , revealing a novel mutualistic-antagonistic pest-pathogen interaction. Heneicosane, a key semiochemical, elevated in the FHB-susceptible cultivar Gallant, acted as a kairomone attracting R. padi and as an allomone repelling S. avenae , altering aphid host selection and fecundity. In direct co-localisation, F. graminearum reduced the fitness of both aphids, but increased mycotoxin production in response to S. avenae , consistent with competitive exclusion. In contrast, distal interactions showed that R. padi benefited from enhanced reproduction while increasing pathogen virulence, fungal biomass, and accumulation of DON, 15-acetyl-DON, and nivalenol. These synergistic effects compromised FHB-resistance in Sumai3, suggesting aphid-induced systemic suppression of defence. Our findings highlight volatile-mediated co-evolution between pathogens and pests revealing a mutualism between R. padi and F. graminearum with significant implications for integrated pest and disease management and for forecasting disease risk under climate change scenarios favouring increased aphid and Fusarium incidence.