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Title: Elucidation of Triacylglycerol Overproduction in the C4 Bioenergy Crop Sorghum bicolor by Constraint-Based Analysis

Journal Article · · Frontiers in Plant Science

Upregulation of triacylglycerols (TAGs) in vegetative plant tissues such as leaves has the potential to drastically increase the energy density and biomass yield of bioenergy crops. In this context, constraint-based analysis has the promise to improve metabolic engineering strategies. Here we present a core metabolism model for the C4 biomass crop Sorghum bicolor (iTJC1414) along with a minimal model for photosynthetic CO2 assimilation, sucrose and TAG biosynthesis in C3 plants. Extending iTJC1414 to a four-cell diel model we simulate C4 photosynthesis in mature leaves with the principal photo-assimilatory product being replaced by TAG produced at different levels. Independent of specific pathways and per unit carbon assimilated, energy content and biosynthetic demands in reducing equivalents are about 1.3 to 1.4 times higher for TAG than for sucrose. For plant generic pathways, ATP- and NADPH-demands per CO2 assimilated are higher by 1.3- and 1.5-fold, respectively. If the photosynthetic supply in ATP and NADPH in iTJC1414 is adjusted to be balanced for sucrose as the sole photo-assimilatory product, overproduction of TAG is predicted to cause a substantial surplus in photosynthetic ATP. This means that if TAG synthesis was the sole photo-assimilatory process, there could be an energy imbalance that might impede the process. Adjusting iTJC1414 to a photo-assimilatory rate that approximates field conditions, we predict possible daily rates of TAG accumulation, dependent on varying ratios of carbon partitioning between exported assimilates and accumulated oil droplets (TAG, oleosin) and in dependence of activation of futile cycles of TAG synthesis and degradation. We find that, based on the capacity of leaves for photosynthetic synthesis of exported assimilates, mature leaves should be able to reach a 20% level of TAG per dry weight within one month if only 5% of the photosynthetic net assimilation can be allocated into oil droplets. From this we conclude that high TAG levels should be achievable if TAG synthesis is induced only during a final phase of the plant life cycle.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States); Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
SC0018420; SC0012704
OSTI ID:
1845559
Alternate ID(s):
OSTI ID: 1863088; OSTI ID: 1996359
Report Number(s):
BNL-222913-2022-JAAM; 787265
Journal Information:
Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 13; ISSN 1664-462X
Publisher:
Frontiers Media SACopyright Statement
Country of Publication:
Switzerland
Language:
English

References (89)

Comparative Analysis of Miscanthus and Saccharum Reveals a Shared Whole-Genome Duplication but Different Evolutionary Fates journal June 2014
Increasing growth and yield by altering carbon metabolism in a transgenic leaf oil crop journal March 2020
A multi-tissue genome-scale metabolic modeling framework for the analysis of whole plant systems journal January 2015
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
Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor journal July 2018
Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis journal February 2014
Modelling metabolic CO 2 evolution - a fresh perspective on respiration : Modelling metabolic CO journal May 2013
Leaf Gas Exchange and Oxidative Stress in Sorghum Plants Supplied with Silicon and Infected by Colletotrichum sublineolum journal September 2012
Reorganization of Acyl Flux through the Lipid Metabolic Network in Oil-Accumulating Tobacco Leaves journal December 2019
A Dynamic Multi-Tissue Flux Balance Model Captures Carbon and Nitrogen Metabolism and Optimal Resource Partitioning During Arabidopsis Growth journal June 2018
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Dorsoventral regulation of photosynthetic functions related to morphological and anatomical structures in field-grown sorghum journal May 2019
Syntenic gene analysis between Brassica rapa and other Brassicaceae species journal January 2012
Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis journal March 2014
Induction, purification and characterization of NADH-specific enoyl acyl carrier protein reductase from developing seeds of oil seed rape (Brassica napus) journal June 1986
Step changes in leaf oil accumulation via iterative metabolic engineering journal January 2017
The potential of C4 grasses for cellulosic biofuel production journal January 2013
Crystallization of the NADH-specific Enoyl Acyl Carrier Protein Reductase from Brassica napus journal March 1994
Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue journal April 2000
On the Tetraploid Origin of the Maize Genome journal January 2004
In Vivo Packaging of Triacylglycerols Enhances Arabidopsis Leaf Biomass and Energy Density journal April 2013
A Diel Flux Balance Model Captures Interactions between Light and Dark Metabolism during Day-Night Cycles in C 3 and Crassulacean Acid Metabolism Leaves journal March 2014
Seed Storage Oil Mobilization journal June 2008
Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism journal April 2010
Bioenergy sorghum maintains photosynthetic capacity in elevated ozone concentrations journal January 2021
Integration of a constraint-based metabolic model of Brassica napus developing seeds with 13C-metabolic flux analysis journal December 2014
Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum journal May 2005
Phloem Transport of Amino Acids in Relation to their Cytosolic Levels in Barley Leaves journal July 1992
Carbohydrate Dynamics in Maize Leaves and Developing Ears in Response to Nitrogen Application journal December 2018
Flexibility in the Energy Balancing Network of Photosynthesis Enables Safe Operation under Changing Environmental Conditions journal March 2020
More Productive Than Maize in the Midwest: How Does Miscanthus Do It? journal June 2009
Modeling dry Matter Accumulation and Yield of Grain Sorghum journal July 1979
Mechanism of C 4 Photosynthesis: A Model Describing the Inorganic Carbon Pool in Bundle Sheath Cells journal December 1989
Assessing the Metabolic Impact of Nitrogen Availability Using a Compartmentalized Maize Leaf Genome-Scale Model journal September 2014
Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain journal January 2003
Metabolite pools and carbon flow during C 4 photosynthesis in maize: 13 CO 2 labeling kinetics and cell type fractionation journal November 2016
Biochemical and cytological relationships in C4 plants journal January 1974
Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues journal April 2016
Sunflower (Helianthus annuus) fatty acid synthase complex: enoyl-[acyl carrier protein]-reductase genes journal September 2014
The B73 Maize Genome: Complexity, Diversity, and Dynamics journal November 2009
Biotechnology and synthetic biology approaches for metabolic engineering of bioenergy crops journal June 2016
Variation in Quantum Yield for CO 2 Uptake among C 3 and C 4 Plants journal November 1983
Storing carbon in leaf lipid sinks enhances perennial ryegrass carbon capture especially under high N and elevated CO2 journal November 2019
Senescence-inducible LEC2 enhances triacylglycerol accumulation in leaves without negatively affecting plant growth journal March 2015
Seasonal and diurnal patterns of non-structural carbohydrates in source and sink tissues in field maize journal November 2019
Production of Seed-Like Storage Lipids and Increase in Oil Bodies in Corn (Maize; Zea mays L.) Vegetative Biomass journal December 2017
Evidence That Isolated Chloroplasts Contain an Integrated Lipid-Synthesizing Assembly That Channels Acetate into Long-Chain Fatty Acids journal April 1996
Phosphoenolpyruvate Carboxykinase in C4 Plants: Its Role and Regulation journal January 1997
Transcriptional regulation of fatty acid production in higher plants: Molecular bases and biotechnological outcomes: The WRINKLED transcription factors journal August 2014
Does greater leaf-level photosynthesis explain the larger solar energy conversion efficiency of Miscanthus relative to switchgrass? journal November 2009
Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: Past, present and future journal April 2015
Metabolic engineering for enhanced oil in biomass journal April 2019
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization journal December 2017
The Importance of Energy Balance in Improving Photosynthetic Productivity journal November 2010
Oleosin genes in maize kernels having diverse oil contents are constitutively expressed independent of oil contents: Size and shape of intracellular oil bodies are determined by the oleosins/oils ratio journal May 1996
Advances in the use of genetically modified plant biomass for biodiesel generation journal May 2017
Genome Evolution in the Genus Sorghum (Poaceae) journal January 2005
The energy budget in C 4 photosynthesis: insights from a cell-type-specific electron transport model journal March 2018
Metabolic flux analysis of the non-transitory starch tradeoff for lipid production in mature tobacco leaves journal January 2022
Lipid turnover during senescence journal May 2013
Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0 journal February 2019
Predictive Modeling of Biomass Component Tradeoffs in Brassica napus Developing Oilseeds Based on in Silico Manipulation of Storage Metabolism journal September 2012
Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. journal January 1994
Localisation of sucrose-phosphate synthase and starch in leaves of C 4 plants journal April 1997
Gene Family of Oleosin Isoforms and Their Structural Stabilization in Sesame Seed Oil Bodies journal January 2002
Commentary: Why don’t plant leaves get fat? journal June 2013
Leaf photosynthetic rate is correlated with biomass and grain production in grain sorghum lines journal April 1991
C4GEM, a Genome-Scale Metabolic Model to Study C 4 Plant Metabolism journal October 2010
Vegetable oil production in vegetative plant tissues journal October 2017
Lipid biosynthesis from [ 14 C] bicarbonate, [2- 14 C] pyruvate and [1- 14 C] acetate during photosynthesis by isolated spinach chloroplasts journal May 1977
Maize and sorghum: genetic resources for bioenergy grasses journal August 2008
Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae: Phloem amino acids and A. fabae journal February 2003
An ethanol inducible gene switch for plants used to manipulate carbon metabolism journal February 1998
Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C 4 grass Sorghum bicolor journal March 2016
From reconstruction to C4 metabolic engineering: A case study for overproduction of polyhydroxybutyrate in bioenergy grasses journal August 2018
Diurnal Changes in Maize Leaf Photosynthesis: I. Carbon Exchange Rate, Assimilate Export Rate, and Enzyme Activities journal February 1987
Multiscale Metabolic Modeling of C4 Plants: Connecting Nonlinear Genome-Scale Models to Leaf-Scale Metabolism in Developing Maize Leaves journal March 2016
Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves journal October 2013
Towards oilcane: Engineering hyperaccumulation of triacylglycerol into sugarcane stems journal May 2020
A general definition of metabolic pathways useful for systematic organization and analysis of complex metabolic networks journal March 2000
Photorespiration journal January 2010
The glucose 6-phosphate shunt around the Calvin–Benson cycle journal November 2015
Multiscale Metabolic Modeling: Dynamic Flux Balance Analysis on a Whole-Plant Scale journal August 2013
Why Combustions Are Always Exothermic, Yielding About 418 kJ per Mole of O 2 journal September 2015
Metabolic network reconstruction and flux variability analysis of storage synthesis in developing oilseed rape (Brassica napus L.) embryos: Flux variability analysis of storage synthesis journal May 2011
Changes in Leaf-Level Nitrogen Partitioning and Mesophyll Conductance Deliver Increased Photosynthesis for Lolium perenne Leaves Engineered to Accumulate Lipid Carbon Sinks journal March 2021
Technoeconomic Analysis of Biodiesel and Ethanol Production from Lipid-Producing Sugarcane and Sweet Sorghum journal December 2016
The Calvin cycle revisited journal January 2003
A Synergistic Genetic Engineering Strategy Induced Triacylglycerol Accumulation in Potato (Solanum tuberosum) Leaf journal March 2020