Metabolic modeling reveals synergistic growth benefits of engineering maize symbiosis with rhizobia and arbuscular mycorrhizal fungi

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Abstract

Engineering N 2 -fixing rhizobia symbiosis in cereals and enhancing association with arbuscular mycorrhizal fungi (AMF) are two strategies being pursued to improve agricultural sustainability. However, the metabolic fluxes and consequent costs and benefits of these strategies in a cereal crop have not been examined. We developed a metabolic model describing how the relative growth rate of Zea mays is impacted by hypothetical association with the rhizobium Bradyrhizobium diazoefficiens and the AMF Rhizophagus irregularis . We found that the lower N content of cereal crops makes the relative growth rate cost associated with acquiring nitrogen from N 2 -fixing rhizobia smaller than in legumes. Our model also predicts positive synergies between rhizobia and AMF under nutrient-limited conditions but negative synergies under nutrient, particularly phosphorus, replete conditions. These findings indicate that these bioengineering strategies could improve cereal crop yields and may achieve greater gains in tandem, but soil nutrient status of target sites should be considered.

Significance Statement

Fertilizer application is responsible for substantial environmental impacts and represents a significant cost to farmers, both barriers to sustainable agricultural development. Engineering cereal crops to associate with N 2 -fixing rhizobia and enhancing existing associations between crops and arbuscular mycorrhizal fungi (AMF) are two strategies that could address these challenges. However, quantitative predictions of their potential effectiveness have not been determined. We use metabolic modeling to demonstrate that engineering maize to associate with N 2 -fixing rhizobia could be a highly metabolic and cost-effective strategy for sustainably supplying nitrogen to cereal crops. We also develop and experimentally validate a model of plant-AMF carbon and nutrient exchanges and demonstrate that AMF and rhizobia symbioses can act synergistically under nitrogen– and phosphorus-deprivation to improve crop growth.

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