Mycorrhizal status impacts the genetic architecture of mineral accumulation in field grown maize (Zea mays ssp. mays L.)

Arbuscular mycorrhizal fungi (AMF) establish symbioses with major crop species, providing their hosts with greater access to mineral nutrients and promoting tolerance to heavy metal toxicity. There is considerable interest in AMF as biofertilizers and for their potential in breeding for greater nutrient efficiency and stress tolerance. However, it remains a challenge to estimate the nutritional benefits of AMF in the field, in part due to a lack of suitable AMF-free controls. Here we evaluated the impact of AMF on the concentration of 20 elements in the leaves and grain of field grown maize using a custom genetic mapping population in which half of the families carry the AMF-incompatibility mutation castor. By comparing AMF-compatible and AMF-incompatible families, we confirmed the benefits of AMF in increasing the concentration of essential mineral nutrients (e.g., P, Zn, and Cu) and reducing the concentration of toxic elements (e.g., Cd and As) in a medium-input subtropical field. We characterised the genetic architecture of element concentration using quantitative trait mapping and identified loci that were specific to AMF-compatible or AMF-incompatible families, consistent with their respective involvement in mycorrhizal or direct nutrient uptake. Patterns of element covariance changed depending on AMF status and could be used to predict variation in mycorrhizal colonisation. We comment on the potential of AMF to drive genotype-specific differences in the host ionome across fields and to impact the alignment of biofortification breeding targets. Our results highlight the benefits of AMF in improving plant access to micronutrients while protecting from heavy metals, and indicate the potential benefits of considering AMF in biofortification programs.