DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Dissecting the metabolic reprogramming of maize root under nitrogen-deficient stress conditions

Journal Article · · Journal of Experimental Botany
 [1];  [1];  [2];  [3];  [3];  [3];  [2]; ORCiD logo [4];  [5]
  1. Department of Chemical and Biomolecular Engineering, University of Nebraska-Lincoln, Lincoln, NE, USA
  2. Department of Chemical Engineering, The Pennsylvania State University, University Park, PA, USA
  3. Institut National de Recherche pour l’Agriculure, l’Alimentation et l’Envionnement (INRAE), Centre de Versailles-Grignon, Versailles cedex, France
  4. Department of Chemical and Biomolecular Engineering, University of Nebraska-Lincoln, Lincoln, NE, USA, Center for Root and Rhizobiome Innovation, University of Nebraska-Lincoln, Lincoln, NE, USA
  5. INRAE, France

Abstract The growth and development of maize (Zea mays L.) largely depends on its nutrient uptake through the root. Hence, studying its growth, response, and associated metabolic reprogramming to stress conditions is becoming an important research direction. A genome-scale metabolic model (GSM) for the maize root was developed to study its metabolic reprogramming under nitrogen stress conditions. The model was reconstructed based on the available information from KEGG, UniProt, and MaizeCyc. Transcriptomics data derived from the roots of hydroponically grown maize plants were used to incorporate regulatory constraints in the model and simulate nitrogen-non-limiting (N+) and nitrogen-deficient (N−) condition. Model-predicted flux-sum variability analysis achieved 70% accuracy compared with the experimental change of metabolite levels. In addition to predicting important metabolic reprogramming in central carbon, fatty acid, amino acid, and other secondary metabolism, maize root GSM predicted several metabolites (l-methionine, l-asparagine, l-lysine, cholesterol, and l-pipecolate) playing a regulatory role in the root biomass growth. Furthermore, this study revealed eight phosphatidylcholine and phosphatidylglycerol metabolites which, even though not coupled with biomass production, played a key role in the increased biomass production under N-deficient conditions. Overall, the omics-integrated GSM provides a promising tool to facilitate stress condition analysis for maize root and engineer better stress-tolerant maize genotypes.

Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI ID:
1827759
Journal Information:
Journal of Experimental Botany, Journal Name: Journal of Experimental Botany; ISSN 0022-0957
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (86)

Metabolic Reprogramming is a Hallmark of Metabolism Itself journal September 2020
An in silico compartmentalized metabolic model of Brassica napus enables the systemic study of regulatory aspects of plant central metabolism journal March 2011
Exogenous succinate increases resistance of maize plants to copper stress journal April 2006
Multi-tissue to whole plant metabolic modelling journal November 2019
Plant growth promotion by Pseudomonas putida KT2440 under saline stress: role of eptA journal March 2020
Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana journal July 2017
Current understanding of the factors regulating methionine content in vegetative tissues of higher plants journal February 2010
Involvement of polyamines in plant response to abiotic stress journal September 2006
Effect of alkaline pH and nitrogen starvation on the triacylglycerol (TAG) content, growth, biochemical composition, and fatty acid profile of Auxenochlorella protothecoides KP7 journal November 2020
Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response journal August 2018
Drought-induced proline synthesis depends on root-to-shoot communication mediated by light perception journal December 2017
Transcriptome response to nitrogen starvation in rice journal August 2012
Relationships between the rate of synthesis of ATP and the concentrations of reactants and products of ATP hydrolysis in maize root tips, determined by 31P nuclear magnetic resonance journal August 1985
Amino acid and glycine betaine accumulation in cold-stressed wheat seedlings journal January 1991
Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation journal February 2011
Flavin Monooxygenase-Generated N-Hydroxypipecolic Acid Is a Critical Element of Plant Systemic Immunity journal April 2018
Emerging Roles of Sphingolipid Signaling in Plant Response to Biotic and Abiotic Stresses journal November 2018
Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants journal October 2009
Genetic variability of the phloem sap metabolite content of maize (Zea mays L.) during the kernel-filling period journal November 2016
Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics journal June 2017
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models journal October 2003
Hydroxamic Acids Derived from 2-Hydroxy-2 H -1,4-Benzoxazin-3(4 H )-one: Key Defense Chemicals of Cereals journal January 2009
Integrated Quantitative Analysis of Nitrogen Stress Response in Chlamydomonas reinhardtii Using Metabolite and Protein Profiling journal February 2014
Omic data from evolved E. coli are consistent with computed optimal growth from genome‐scale models journal January 2010
Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability journal January 2006
What is flux balance analysis? journal March 2010
Sphingosine-1-phosphate: an enigmatic signalling lipid journal May 2003
Metabolic regulation of the maize rhizobiome by benzoxazinoids journal February 2019
Kicking off sphingolipid biosynthesis: structures of the serine palmitoyltransferase complex journal February 2021
Probabilistic integrative modeling of genome-scale metabolic and regulatory networks in Escherichia coli and Mycobacterium tuberculosis journal September 2010
N -hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis journal May 2018
The Response of the Root Proteome to the Synthetic Strigolactone GR24 in Arabidopsis journal August 2016
The role of strigolactones in root development journal January 2016
Maize���A potential source of human nutrition and health: A review journal April 2016
MAnGO: an interactive R-based tool for two-colour microarray analysis journal June 2007
iMAT: an integrative metabolic analysis tool journal November 2010
Functional integration of a metabolic network model and expression data without arbitrary thresholding journal December 2010
Standardizing biomass reactions and ensuring complete mass balance in genome-scale metabolic models journal July 2017
Amino acid accumulation in sink and source tissues of Coleus blumei Benth. during salinity stress journal January 1998
The multifaceted role of aspartate-family amino acids in plant metabolism journal April 2012
The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize journal August 2012
New Insights into the Shikimate and Aromatic Amino Acids Biosynthesis Pathways in Plants journal November 2010
Regulation of Shoot and Root Development through Mutual Signaling journal September 2012
Data, information, knowledge and principle: back to metabolism in KEGG journal November 2013
UniProt: a worldwide hub of protein knowledge November 2018
Flux Balance Analysis of Barley Seeds: A Computational Approach to Study Systemic Properties of Central Metabolism journal November 2008
A Genome-Scale Metabolic Model of Arabidopsis and Some of Its Properties journal September 2009
AraGEM, a Genome-Scale Reconstruction of the Primary Metabolic Network in Arabidopsis journal December 2009
Arabidopsis Roots and Shoots Show Distinct Temporal Adaptation Patterns toward Nitrogen Starvation   journal September 2011
The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants journal November 2011
Maize Source Leaf Adaptation to Nitrogen Deficiency Affects Not Only Nitrogen and Carbon Metabolism But Also Control of Phosphate Homeostasis     journal September 2012
Diverse Roles of Strigolactone Signaling in Maize Architecture and the Uncoupling of a Branching-Specific Subnetwork       journal September 2012
A Developmental Transcriptional Network for Maize Defines Coexpression Modules       journal February 2013
Responses to Light Intensity in a Genome-Scale Model of Rice Metabolism journal May 2013
Bottom-up Metabolic Reconstruction of Arabidopsis and Its Application to Determining the Metabolic Costs of Enzyme Production journal May 2014
Assessing the Metabolic Impact of Nitrogen Availability Using a Compartmentalized Maize Leaf Genome-Scale Model journal September 2014
Proline Accumulation Is Regulated by Transcription Factors Associated with Phosphate Starvation journal August 2017
Boosting Crop Yields with Plant Steroids journal March 2012
New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum) plants grown under different nitrogen regimes journal February 2004
Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis journal March 2009
Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters: Lipid changes during nitrogen deficiency journal January 2007
Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte: Metabolomics of Thellungiella under osmotic stress journal October 2010
Computational analysis of storage synthesis in developing Brassica napus L. (oilseed rape) embryos: flux variability analysis in relation to 13C metabolic flux analysis: Quantitative analysis of storage synthesis in oilseed rape journal May 2011
Physiology of maize I: A comprehensive and integrated view of nitrogen metabolism in a C4 plant journal June 2005
Nitrogen–phosphorus interplay: old story with molecular tale journal September 2019
The role of amino acid metabolism during abiotic stress release journal January 2019
A method for accounting for maintenance costs in flux balance analysis improves the prediction of plant cell metabolic phenotypes under stress conditions journal August 2013
A plant’s diet, surviving in a variable nutrient environment journal April 2020
De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes journal August 2021
The Emergence of 2-Oxoglutarate as a Master Regulator Metabolite journal September 2015
Optimization based automated curation of metabolic reconstructions journal January 2007
Flux-sum analysis: a metabolite-centric approach for understanding the metabolic network journal December 2009
A mass and charge balanced metabolic model of Setaria viridis revealed mechanisms of proton balancing in C4 plants journal June 2019
Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed journal June 2017
Stress, nutrients and genotype: understanding and managing asparagine accumulation in wheat grain journal July 2020
Context-Specific Metabolic Networks Are Consistent with Experiments journal May 2008
Interpreting Expression Data with Metabolic Flux Models: Predicting Mycobacterium tuberculosis Mycolic Acid Production journal August 2009
Zea mays iRS1563: A Comprehensive Genome-Scale Metabolic Reconstruction of Maize Metabolism journal July 2011
Benzoxazinoids in Root Exudates of Maize Attract Pseudomonas putida to the Rhizosphere journal April 2012
Inferring Carbon Sources from Gene Expression Profiles Using Metabolic Flux Models journal May 2012
Carbon, Nitrogen and Phosphorus Accumulation and Partitioning, and C:N:P Stoichiometry in Late-Season Rice under Different Water and Nitrogen Managements journal July 2014
Co‐catabolism of arginine and succinate drives symbiotic nitrogen fixation journal June 2020
Improved evidence-based genome-scale metabolic models for maize leaf, embryo, and endosperm journal March 2015
Reconstruction of Oryza sativa indica Genome Scale Metabolic Model and Its Responses to Varying RuBisCO Activity, Light Intensity, and Enzymatic Cost Conditions journal November 2017
Massive Loss of DNA Methylation in Nitrogen-, but Not in Phosphorus-Deficient Zea mays Roots Is Poorly Correlated With Gene Expression Differences journal April 2018
Maize Metabolic Network Construction and Transcriptome Analysis journal January 2013