Below‐ and aboveground plant fungal symbionts from crop–pasture systems interactively influence grass and legume wellness

Abstract

Agricultural practices that promote or introduce plant symbionts, such as arbuscular mycorrhizal fungi (AMF) and foliar fungal endophytes of grasses, may offer a sustainable alternative to traditional agricultural models, reducing environmental costs while preserving agroecosystem functions and productivity. However, their interactive effects within long-term agricultural systems remain underexplored. Here, we investigate how promoted AMF and introduced foliar fungal endophytes influence grass and legume wellness.We tested whether the mycorrhizal community promoted through crop–pasture rotation favours plant growth by improving the associational protection against insects and pathogens provided by a foliar endophyte introduced through the seeding of its host. We conducted an outdoor mesocosm experiment using soil from the Pampa region of Argentina, with an intensive agricultural history. Half of the mesocosms were inoculated with spores extracted from an adjacent system where agricultural activities ceased 5 years ago, and a grass–legume pasture was established to start a crop–pasture rotation. Additionally, we set up a factorial design by sowing half of the mesocosms with Lolium multiflorum plants with high and low association with the endophyte Epichloë occultans. A mixture of grasses and legumes was sown in all mesocosms.The presence of E. occultans-associated L. multiflorum conferred associational protection to non-host neighbouring plants against pests and diseases. In powdery mildew and aphid incidence, this endophyte protection was further enhanced when the AMF community was enriched with spores from the 5-year grass–legume pasture, while in barley yellow dwarf virus (BYDV) and chewing insects in T. pratense, the addition of these AMF spores increased susceptibility. Nevertheless, AMF promoted by crop–pasture rotations favoured legume biomass over grasses and can either improve plant wellness by enhancing the associational protection provided by E. occultans or directly increase plant susceptibility.Synthesis and applications. Our results demonstrate that the interaction between promoted AMF and introduced endophytes can enhance plant resilience by mitigating biotic threats, thereby enhancing plant health and productivity. This underscores the importance of symbiotic microorganisms in agroecosystem sustainability and highlights the need to foster more diverse microbial communities by adopting agronomic practices, such as crop–pasture rotations with perennial forage species.