A multi-organ maize metabolic model connects temperature stress with energy production and reducing power generation

Climate change has adversely affected maize productivity. Thereby, a holistic understanding of metabolic crosstalk among its organs is important to address this issue. Thus, we reconstructed the first multi-organ maize metabolic model, iZMA6517, and contextualized it with heat and cold stress transcriptomics data using expression distributed reaction flux measurement (EXTREAM) algorithm. Furthermore, implementing metabolic bottleneck analysis on contextualized models revealed differences between these stresses. While both stresses had reducing power bottlenecks, heat stress had additional energy generation bottlenecks. We also performed thermodynamic driving force analysis, revealing thermodynamics-reducing power-energy generation axis dictating the nature of temperature stress responses. Thus, a temperature-tolerant maize ideotype can be engineered by leveraging the proposed thermodynamics-reducing power-energy generation axis. We experimentally inoculated maize root with a beneficial mycorrhizal fungus, Rhizophagus irregularis, and as a proof-of-concept demonstrated its efficacy in alleviating temperature stress. Overall, this study will guide the engineering effort of temperature stress-tolerant maize ideotypes. [Display omitted] •We reconstructed the largest maize B73 multi-organ plant metabolic model, iZMA6517•The proposed transcriptomics data integration algorithm, EXTREAM, successfully predicted the starch distribution pattern in the maize leaf•Metabolic Bottleneck Analysis (MBA) pinpointed plant-wide metabolic bottlenecks for heat and cold stresses•We demonstrated that Rhizophagus irregularis can effectively reduces temperature stress in maize Environmental science; Microbial metabolism