Mycorrhizal fungi compromise production of endophytic alkaloids, increasing plant susceptibility to an aphid herbivore

Abstract Symbiosis plays a critical role in plant biology. Temperate grasses often associate with several symbiotic fungi simultaneously, including Epichloë endophytes and arbuscular mycorrhizal (AM) fungi, in shoots and roots, respectively. These symbionts often modulate plant–herbivore interactions by influencing nutritional traits (i.e. AM fungi‐mediated nutrient uptake) and/or the secondary chemistry (i.e. endophytic alkaloids) of their host plant. Moreover, such grasses also accumulate large amounts of silicon (Si) from the soil, which can be deposited in tissues to act as a physical anti‐herbivore defence. Recent evidence suggests that both endophytes and AM fungi independently facilitate Si uptake. However, the consequences of their interactions with piercing‐sucking insects (i.e. aphids), or whether Si supply, endophytes, and AM fungi interact in this regard, are currently unknown. While Si deposition may be less effective against aphids than other herbivores (i.e. chewing caterpillars), Si supply can also alter plant secondary metabolite defences, which could affect sucking insects. In a factorial greenhouse experiment, we evaluated whether these components, acting alone or in combination, altered (1) foliar primary chemistry, (2) Si and symbiont‐chemical (endophytic alkaloids) defences, as well as (3) performance of the bird cherry‐oat aphid ( Rhopalosiphum padi ) feeding on tall fescue ( Festuca arundinacea ). Endophytes decreased all aphid performance parameters, including population growth and reproduction by 40%, but their impact was reversed by the presence of AM fungi, leading to a 52% increase in aphid performance compared with plants solely hosting endophytes. This improvement in performance was associated with reduced loline alkaloid levels and higher shoot nitrogen in AM‐endophytic plants. Endophytes and AM fungi exhibited antagonism, with endophytes reducing AM colonization by 34% and AM presence decreasing endophyte loline alkaloids by 44%. While both fungi jointly increased Si accumulation by 39% under Si‐supplied conditions, Si had no noticeable effects on aphids. Moreover, although Si supply had no identifiable effects on AM colonization, it reduced endophyte peramine alkaloids by 24%. Synthesis . Our findings indicate that symbiotic fungal partnerships and silicon provision may benefit plants but could weaken anti‐herbivore defences when combined. Revealing the complex interactions among diverse fungal symbionts and showcasing their effects on different anti‐herbivore defences (chemical and physical) and herbivore performance for the first time.