A multi-organ maize metabolic model connects temperature stress with energy production and reducing power generation
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Abstract
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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Dissecting metabolic landscape of alveolar macrophage
Malla, S., Sajeevan, K. A., Acharya, B., Chowdhury, R., & Saha, R. (2024) · Scientific Reports · doi:10.1038/s41598-024-81253-w · Cited by 13 · see citing works
Self-citationA Guide to Metabolic Network Modeling for Plant Biology
Rao, X., & Liu, W. (2025) · Plants · doi:10.3390/plants14030484 · Cited by 13 · see citing works
AraRoot—a comprehensive genome-scale metabolic model for the Arabidopsis root system
Esterhuizen, L., Ampimah, N., Yandeau‐Nelson, M. D., Nikolau, B. J., Sparks, E. E., & Saha, R. (2025) · in silico Plants · doi:10.1093/insilicoplants/diaf003 · Cited by 8 · see citing works
Self-citationMulti-omics integration in genome-scale metabolic models: a review of constraint-based approaches
Shahreen, N., Osinuga, A., Malla, S., Razmpour, T., Tabibian, M., & Saha, R. (2026) · Molecular Omics · doi:10.1093/molecular-omics/aaiag005 · Cited by 8 · see citing works
Self-citationKumar, S. P., & Bhatt, N. (2025) · iScience · doi:10.1016/j.isci.2025.113005 · Cited by 7 · see citing works
Metabolic modelling: Insights into the machine room of plant metabolism
Machado, T. M., Töpfer, N., & Soltani, F. (2025) · Journal of Plant Physiology · doi:10.1016/j.jplph.2025.154584 · Cited by 7 · see citing works
Genome-scale metabolic models in plant stress physiology: implications for future climate resilience
Mangaravite, É., Vinson, C. C., de Almeida, E. L. M., & Williams, T. C. R. (2025) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiaf406 · Cited by 7 · see citing works
Walker, B. J., & Schroeder, W. L. (2026) · Planta · doi:10.1007/s00425-026-04961-9 · Cited by 7 · see citing works
GAN-enhanced machine learning and metabolic modeling identify reprogramming in pancreatic cancer
Razmpour, T., Tabibian, M., Roohi, A., & Saha, R. (2026) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013862 · Cited by 6 · see citing works
Self-citationChowdhury, N. B., Chandran, A. K. N., Walia, H., & Saha, R. (2025) · Scientific Reports · doi:10.1038/s41598-025-00504-6 · Cited by 4 · see citing works
Self-citationChowdhury, N. B., Pokorzynski, N., Rucks, E. A., Ouellette, S. P., Carabeo, R. A., & Saha, R. (2024) · mSystems · doi:10.1128/msystems.00717-24 · Cited by 3 · see citing works
Self-citationDecouard, B., Chowdhury, N. B., Saou, A., Rigault, M., Quilleré, I., Sapir, T., Marmagne, A., Roux, C. P. L., Launay‐Avon, A., Guérard, F., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.13.562190 · Cited by 2 · see citing works
Self-citationChowdhury, R., Schroeder, W. L., Sarkar, D., Chowdhury, N. B., Dey, S., & Saha, R. (2025) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiaf103 · Cited by 1 · see citing works
Self-citationAryee, R., Zargar, M. R., Vaishnavey, S. R., Arunraj, B., Mohammed, N. S., Dey, S., Sajeevan, K. A., Frazier, A., Koziel, J. A., Beck, M. R., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.25.708075 · Cited by 1 · see citing works
Self-citationKaste, J. A. M., Ji, R., Sydow, P. W., Sawers, R. J. H., & Matthews, M. L. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.28.635303
Wu, Y., Li, X., Wang, Y. Q., Lu, S., Li, Y., Liang, Z., Jia, X., Zhang, Y., & Liu, Y. (2026) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2026.119766
Malla, S., & Saha, R. (2026) · Immunometabolism · doi:10.1097/in9.0000000000000077
Self-citationSrinivasan, S., Raman, K., & Srivastava, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-40259-2
Solute Carrier Transporter Family Modulates Neutrophil Metabolism During Health and DiseasePreprint
Malla, S., & Saha, R. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.20.726273
Self-citationKaste, J. A. M., Ji, R., Sydow, P. W., Sawers, R. J. H., & Matthews, M. L. (2026) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiag327
Zargar, M. R., Malla, S., Saha, R., & Chowdhury, R. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.25.734531
Self-citation
- Authors
- Chowdhury, N. B., Simons-Senftle, M., 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
- ORCID
- Venue
- iScience
- Publisher
- Elsevier BV
- Published
- 2023-12
- Volume
- 26
- Issue
- 12
- Pages
- 108400
- ISSN
- 2589-0042 (ISSN-L)
- PMC
- PMC10709110
- OpenAlex
- W4388461873
- Cited by
- 25
- References
- 92
- Citations by year
- 2026: 10 · 2025: 11 · 2024: 3 · 2023: 1
- FWCI
- 2.23
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- 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)
- Iowa State University (RII Track-1, 2242763)
- Vermont Agency of Natural Resources (18-CARN-024-01 \u2013 2018)
- Office of Science
- Biological and Environmental Research
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
- Center for Bioenergy Innovation
- Agence Nationale de la Recherche
- Department of Energy
- French National Institute for Agricultural Research (IB BAP 2021 MYCORN)
- 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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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