PreprintCited by 25Microbial Metabolic Engineering and BioproductionBioinformatics and Genomic NetworksPlant nutrient uptake and metabolism

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Multi-organ Metabolic Model of Zea mays Connects Temperature Stress with Thermodynamics-Reducing Power-Energy Generation Axis

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Preprint — published as 10.1016/j.isci.2023.108400 · Paper page

Abstract

Global climate change has severely impacted maize productivity. A holistic understanding of metabolic crosstalk among its organs is essential to address this issue. Thus, we reconstructed the first multi-organ maize genome-scale metabolic model, i ZMA6517, and contextualized it with heat and cold stress-related transcriptomics data using the novel EX pression dis T ributed REA ction flux M easurement (EXTREAM) algorithm. Furthermore, implementing metabolic bottleneck analysis on contextualized models revealed fundamental differences between these stresses. While both stresses had reducing power bottlenecks, heat stress had additional energy generation bottlenecks. To tie these signatures, we performed thermodynamic driving force analysis, revealing thermodynamics-reducing power-energy generation axis dictating the nature of temperature stress responses. Thus, for global food security, 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 potential to alleviate temperature stress. In summary, this study will guide the engineering effort of temperature stress-tolerant maize ideotypes.

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Metadata

Authors
Chowdhury, N. B., Decouard, B., Quillere, I., Rigault, M., Sajeevan, K. A., Acharya, B., Chowdhury, R., Hirel, B., Dellagi, A., Maranas, C., & Saha, R.
Affiliations
  • University of Nebraska–Lincoln (US)
  • AgroParisTech (FR)
  • Iowa State University (US)
  • Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
  • Pennsylvania State University (US)
Corresponding author
Saha, Rajib
Venue
iScience
Publisher
openRxiv
Published
2023-07-10
Volume
26
Issue
12
Pages
108400-108400
ISSN
2589-0042 (ISSN-L)
OpenAlex
W4388461873
Cited by
25
References
1
Citations by year
2026: 10 · 2025: 11 · 2024: 3 · 2023: 1
FWCI
2.23
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • iScience (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by-nc-nd)
  • Lincoln (University of Nebraska) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • National Science Foundation (1943310)
  • U.S. Department of Energy
  • Iowa State University (2242763, RII Track-1)
  • Agence Nationale de la Recherche (ANR-11-IDEX-0003)
  • Institut National de la Recherche Agronomique (IB BAP 2021 MYCORN)
  • Institut National de Recherche en Sciences et Technologies pour l'Environnement et l'Agriculture (IB BAP 2021 MYCORN)
  • Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
  • Office of Science
  • Biological and Environmental Research
  • Center for Bioenergy Innovation
  • Vermont Agency of Natural Resources (18-CARN-024-01 \u2013 2018, 18-CARN-024-01 – 2018)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
Keywords
maize, temperature stress, heat stress, cold stress, reducing power, energy production, metabolic crosstalk, transcriptomics, Glomus intraradices, mycorrhizal fungi, climate change

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