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

Niaz Bahar Chowdhury; Margaret Simons-Senftle; Berengere Decouard; Isabelle Quillere; Martine Rigault; Karuna Anna Sajeevan; Bibek Acharya; Ratul Chowdhury; Bertrand Hirel; Alia Dellagi; Costas Maranas; Rajib Saha

doi:10.1016/j.isci.2023.108400

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

iScience. 2023 Nov 7;26(12):108400. doi: 10.1016/j.isci.2023.108400. eCollection 2023 Dec 15.

Affiliations

¹ Chemical and Biomolecular Engineering, University of Nebraska-Lincoln, Lincoln, NE, USA.
² Chemical Engineering, The Pennsylvania State University, University Park, PA, USA.
³ Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000 Versailles, France.
⁴ Chemical and Biological Engineering, Iowa State University, Ames, IA, USA.
⁵ Centre de Versailles-Grignon, Institut National de Recherche pour l'Agriculture, Versailles, France.

Abstract

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.

Keywords: Environmental science; Microbial metabolism.