Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation

Ma, Fangfang; Jazmin, Lara J.; Young, Jamey D.; Allen, Doug K.

doi:10.1073/pnas.1319485111

Title: Isotopically nonstationary ¹³C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation

Abstract

Improving plant productivity is an important aim for metabolic engineering. There are few comprehensive methods that quantitatively describe leaf metabolism, although such information would be valuable for increasing photosynthetic capacity, enhancing biomass production, and rerouting carbon flux toward desirable end products. Isotopically nonstationary metabolic flux analysis (INST-MFA) has been previously applied to map carbon fluxes in photoautotrophic bacteria, which involves model-based regression of transient ¹³C-labeling patterns of intracellular metabolites. However, experimental and computational difficulties have hindered its application to terrestrial plant systems. Here, we performed in vivo isotopic labeling of Arabidopsis thaliana rosettes with ¹³CO₂ and estimated fluxes throughout leaf photosynthetic metabolism by INST-MFA. Plants grown at 200 µmol m^$$-$$2s^$$-$$1 light were compared with plants acclimated for 9 d at an irradiance of 500 µmol∙m^$$-$$2∙s^$$-$$1. Approximately 1,400 independent mass isotopomer measurements obtained from analysis of 37 metabolite fragment ions were regressed to estimate 136 total fluxes (54 free fluxes) under each condition. The results provide a comprehensive description of changes in carbon partitioning and overall photosynthetic flux after long-term developmental acclimation of leaves to high light. Despite a doubling in the carboxylation rate, the photorespiratory flux increased from 17 to 28% of net CO₂ assimilation with high-light acclimation (Vc/Vo: 3.5:1 vs. 2.3:1, respectively). In conclusion, this study highlights the potential of ¹³C INST-MFA to describe emergent flux phenotypes that respond to environmental conditions or plant physiology and cannot be obtained by other complementary approaches.

Authors:

Ma, Fangfang ^[1]; Jazmin, Lara J. ^[2]; Young, Jamey D. ^[2]; Allen, Doug K. ^[1]

U.S. Dept. of Agriculture, St. Louis, MO (United States)
Vanderbilt Univ., Nashville, TN (United States)

Publication Date:: Mon Nov 03 00:00:00 EST 2014

Research Org.:: Vanderbilt Univ., Nashville, TN (United States)

Sponsoring Org.:: USDOE; USDA; National Science Foundation (NSF)

OSTI Identifier:: 1348223

Grant/Contract Number:: AC05-06OR23100; EF-1105249; P200A090323

Resource Type:: Accepted Manuscript

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Volume: 111; Journal Issue: 47; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; isotopomer modeling; metabolic flux analysis; photosynthesis; 13C-labeling; primary metabolism

Citation Formats


                    Ma, Fangfang, Jazmin, Lara J., Young, Jamey D., and Allen, Doug K. Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation.  United States: N. p., 2014. 
Web.  doi:10.1073/pnas.1319485111.

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                    Ma, Fangfang, Jazmin, Lara J., Young, Jamey D., & Allen, Doug K. Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation.  United States.  https://doi.org/10.1073/pnas.1319485111

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                    Ma, Fangfang, Jazmin, Lara J., Young, Jamey D., and Allen, Doug K. Mon .  
"Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation".  United States.  https://doi.org/10.1073/pnas.1319485111.  https://www.osti.gov/servlets/purl/1348223.

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@article{osti_1348223,

  title        = {Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation},

  author       = {Ma, Fangfang and Jazmin, Lara J. and Young, Jamey D. and Allen, Doug K.},

  abstractNote = {Improving plant productivity is an important aim for metabolic engineering. There are few comprehensive methods that quantitatively describe leaf metabolism, although such information would be valuable for increasing photosynthetic capacity, enhancing biomass production, and rerouting carbon flux toward desirable end products. Isotopically nonstationary metabolic flux analysis (INST-MFA) has been previously applied to map carbon fluxes in photoautotrophic bacteria, which involves model-based regression of transient 13C-labeling patterns of intracellular metabolites. However, experimental and computational difficulties have hindered its application to terrestrial plant systems. Here, we performed in vivo isotopic labeling of Arabidopsis thaliana rosettes with 13CO2 and estimated fluxes throughout leaf photosynthetic metabolism by INST-MFA. Plants grown at 200 µmol m$-$2s$-$1 light were compared with plants acclimated for 9 d at an irradiance of 500 µmol∙m$-$2∙s$-$1. Approximately 1,400 independent mass isotopomer measurements obtained from analysis of 37 metabolite fragment ions were regressed to estimate 136 total fluxes (54 free fluxes) under each condition. The results provide a comprehensive description of changes in carbon partitioning and overall photosynthetic flux after long-term developmental acclimation of leaves to high light. Despite a doubling in the carboxylation rate, the photorespiratory flux increased from 17 to 28% of net CO2 assimilation with high-light acclimation (Vc/Vo: 3.5:1 vs. 2.3:1, respectively). In conclusion, this study highlights the potential of 13C INST-MFA to describe emergent flux phenotypes that respond to environmental conditions or plant physiology and cannot be obtained by other complementary approaches.},

  doi          = {10.1073/pnas.1319485111},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 47,

  volume       = 111,

  place        = {United States},

  year         = {Mon Nov 03 00:00:00 EST 2014},

  month        = {Mon Nov 03 00:00:00 EST 2014}

}

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DOI: 10.1093/jxb/erz051

Sterile spikelets assimilate carbon in sorghum and related grasses
journal, January 2019

AuBuchon-Elder, Taylor; Coneva, Viktoriya; Goad, David M.
The Plant Cell
DOI: 10.1101/396473

Arabidopsis PPC2 is crucial for growth at low CO₂ by involvement in photorespiratory metabolism and integration of ABI5
posted_content, September 2019

You, Lei; Zhang, Jumei; Li, Long
BioRxiv
DOI: 10.1101/764589

In silico metabolic network analysis of Arabidopsis leaves
journal, October 2016

Beckers, Veronique; Dersch, Lisa Maria; Lotz, Katrin
BMC Systems Biology, Vol. 10, Issue 1
DOI: 10.1186/s12918-016-0347-3

Mass Isotopologue Distribution of dimer ion adducts of intracellular metabolites for potential applications in 13C Metabolic Flux Analysis
journal, August 2019

Prasannan, Charulata B.; Mishra, Vivek; Jaiswal, Damini
PLOS ONE, Vol. 14, Issue 8
DOI: 10.1371/journal.pone.0220412

13C-Metabolic Flux Analysis: An Accurate Approach to Demystify Microbial Metabolism for Biochemical Production
journal, December 2015

Guo, Weihua; Sheng, Jiayuan; Feng, Xueyang
Bioengineering, Vol. 3, Issue 1
DOI: 10.3390/bioengineering3010003

Strategies for Extending Metabolomics Studies with Stable Isotope Labelling and Fluxomics
journal, October 2016

Srivastava, Anubhav; Kowalski, Greg; Callahan, Damien
Metabolites, Vol. 6, Issue 4
DOI: 10.3390/metabo6040032

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Photoautotrophic microorganisms are increasingly explored for the conversion of atmospheric carbon dioxide into biomass and valuable products. The Calvin-Benson-Bassham (CBB) cycle is the primary metabolic pathway for net CO₂ fixation within oxygenic photosynthetic organisms. The cyanobacteria, Synechocystissp. PCC 6803, is a model organism for the study of photosynthesis and a platform for many metabolic engineering efforts. The CBB cycle is regulated by complex mechanisms including enzymatic abundance, intracellular metabolite concentrations, energetic cofactors and post-translational enzymatic modifications that depend on the external conditions such as the intensity and quality of light. However, the extent to which each of these mechanisms playmore »« less
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Title: Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation

Abstract

Citation Formats

Increasing Photosynthetic Carbon Assimilation in C 3 Plants to Improve Crop Yield: Current and Future Strategies journal, November 2010

The Dynamics of Photosynthesis journal, December 2008

Sink regulation of photosynthesis journal, July 2001

Metabolic profiling reveals metabolic shifts in Arabidopsis plants grown under different light conditions: Metabolic profiling under different light regime journal, May 2012

Plants, CO2 and photosynthesis in the 21st century journal, April 1996

Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature journal, April 2002

Overexpression of C4‐cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3‐photosynthesis journal, April 2002

Photorespiration: current status and approaches for metabolic engineering journal, June 2010

Rubisco activity and regulation as targets for crop improvement journal, November 2012

Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth journal, October 2001

A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism journal, March 2001

Photorespiratory bypasses: how can they work? journal, September 2012

Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm journal, August 2007

Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii journal, January 2009

Responses to Light Intensity in a Genome-Scale Model of Rice Metabolism journal, May 2013

Multiscale Metabolic Modeling: Dynamic Flux Balance Analysis on a Whole-Plant Scale journal, August 2013

Seed Architecture Shapes Embryo Metabolism in Oilseed Rape journal, May 2013

Analysis of Metabolic Flux Phenotypes for Two Arabidopsis Mutants with Severe Impairment in Seed Storage Lipid Synthesis journal, September 2009

Carbon and Nitrogen Provisions Alter the Metabolic Flux in Developing Soybean Embryos journal, January 2013

Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering journal, January 2011

Metabolic flux analysis using 13 C peptide label measurements journal, January 2014

The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a complex response to changes in nitrogen supply journal, February 2013

Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by 13C labeling and comprehensive bondomer balancing journal, August 2007

Use of reverse-phase liquid chromatography, linked to tandem mass spectrometry, to profile the Calvin cycle and other metabolic intermediates in Arabidopsis rosettes at different carbon dioxide concentrations journal, September 2009

Metabolic turnover analysis by a combination of in vivo13C-labelling from 13CO2 and metabolic profiling with CE-MS/MS reveals rate-limiting steps of the C3 photosynthetic pathway in Nicotiana tabacum leaves journal, December 2009

A transient isotopic labeling methodology for 13C metabolic flux analysis of photoautotrophic microorganisms journal, August 2007

Metabolic Fluxes in an Illuminated Arabidopsis Rosette journal, February 2013

Kinetic flux profiling for quantitation of cellular metabolic fluxes journal, July 2008

Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis journal, November 2011

The diurnal metabolism of leaf starch journal, December 2006

Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake journal, March 2010

In Folio Respiratory Fluxomics Revealed by 13 C Isotopic Labeling and H/D Isotope Effects Highlight the Noncyclic Nature of the Tricarboxylic Acid “Cycle” in Illuminated Leaves journal, August 2009

Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1. journal, October 2010

Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading journal, August 2005

Quantification of Peptide m / z Distributions from 13 C-Labeled Cultures with High-Resolution Mass Spectrometry journal, January 2014

Isotope labelling of Rubisco subunits provides in vivo information on subcellular biosynthesis and exchange of amino acids between compartments: Probing subcellular metabolism in seeds journal, February 2012

GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after 13CO2 labelling journal, August 2007

Estimating the rate of photorespiration in leaves journal, May 1988

Current methods for estimating the rate of photorespiration in leaves journal, November 2012

A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis journal, October 2008

Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration journal, July 2008

NMR determination of photorespiration in intact leaves using in vivo 13CO2 labeling journal, January 2006

Photorespiratory and respiratory decarboxylations in leaves of C 3 plants under different CO 2 concentrations and irradiances journal, December 2007

Leaf anatomy enables more equal access to light and CO2 between chloroplasts journal, July 1999

Leaf Functional Anatomy in Relation to Photosynthesis journal, November 2010

The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand journal, August 2002

Photorespiratory Metabolism: Genes, Mutants, Energetics, and Redox Signaling journal, June 2009

Insights into plant metabolic networks from steady-state metabolic flux analysis journal, June 2009

Enzymes, metabolites and fluxes journal, December 2004

INCA: a computational platform for isotopically non-stationary metabolic flux analysis journal, January 2014

An elementary metabolite unit (EMU) based method of isotopically nonstationary flux analysis journal, February 2008

Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements journal, July 2006

Comparative studies of glycolytic pathways and channeling under in vitro and in vivo modes journal, September 2018

Light Stress Responses and Prospects for Engineering Light Stress Tolerance in Crop Plants journal, March 2019

Methods and advances in metabolic flux analysis: a mini-review journal, January 2015

The challenge and potential of photosynthesis: unique considerations for metabolic flux measurements in photosynthetic microorganisms journal, November 2018

Dissecting metabolic flux in C4 plants: experimental and theoretical approaches journal, June 2018

Insights into the spatial and temporal organisation of plant metabolism from network flux analysis journal, December 2018

Computational analysis of the productivity potential of CAM journal, February 2018

Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H journal, November 2018

Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by 13 C labelling journal, February 2016

Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network journal, April 2016

Synthetic biology approaches for improving photosynthesis journal, January 2019

Metabolite profiles reveal interspecific variation in operation of the Calvin–Benson cycle in both C4 and C3 plants journal, February 2019

Triose phosphate utilization and beyond: from photosynthesis to end product synthesis journal, March 2019

Relationship between irradiance and levels of Calvin–Benson cycle and other intermediates in the model eudicot Arabidopsis and the model monocot rice journal, July 2019

Arabidopsis PPC2 is crucial for growth at low CO2 by involvement in photorespiratory metabolism and integration of ABI5 posted_content, September 2019

Engineering central metabolism - a grand challenge for plant biologists journal, March 2017

Integrated omics analysis of specialized metabolism in medicinal plants journal, March 2017

Concurrent isotope-assisted metabolic flux analysis and transcriptome profiling reveal responses of poplar cells to altered nitrogen and carbon supply journal, January 2018

In silico metabolic network analysis of Arabidopsis leaves journal, October 2016

Shoot tip culture: a step towards 13C metabolite flux analysis of sink leaf metabolism journal, May 2019

A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa journal, October 2015

Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis journal, November 2017

Parallel isotope differential modeling for instationary 13C fluxomics at the genome scale journal, June 2020

Pool size measurements facilitate the determination of fluxes at branching points in non-stationary metabolic flux analysis: the case of Arabidopsis thaliana journal, June 2015

Decoding Biosynthetic Pathways in Plants by Pulse-Chase Strategies Using 13CO2 as a Universal Tracer journal, July 2016

Title: Isotopically nonstationary ¹³C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation

Increasing Photosynthetic Carbon Assimilation in C ₃ Plants to Improve Crop Yield: Current and Future Strategies
journal, November 2010

The Dynamics of Photosynthesis
journal, December 2008

Sink regulation of photosynthesis
journal, July 2001

Metabolic profiling reveals metabolic shifts in Arabidopsis plants grown under different light conditions: Metabolic profiling under different light regime
journal, May 2012

Plants, CO2 and photosynthesis in the 21st century
journal, April 1996

Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature
journal, April 2002

Overexpression of C4‐cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3‐photosynthesis
journal, April 2002

Photorespiration: current status and approaches for metabolic engineering
journal, June 2010

Rubisco activity and regulation as targets for crop improvement
journal, November 2012

Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth
journal, October 2001

A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism
journal, March 2001

Photorespiratory bypasses: how can they work?
journal, September 2012

Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm
journal, August 2007

Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii
journal, January 2009

Responses to Light Intensity in a Genome-Scale Model of Rice Metabolism
journal, May 2013

Multiscale Metabolic Modeling: Dynamic Flux Balance Analysis on a Whole-Plant Scale
journal, August 2013

Seed Architecture Shapes Embryo Metabolism in Oilseed Rape
journal, May 2013

Analysis of Metabolic Flux Phenotypes for Two Arabidopsis Mutants with Severe Impairment in Seed Storage Lipid Synthesis
journal, September 2009

Carbon and Nitrogen Provisions Alter the Metabolic Flux in Developing Soybean Embryos
journal, January 2013

Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering
journal, January 2011

Metabolic flux analysis using ¹³ C peptide label measurements
journal, January 2014

The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a complex response to changes in nitrogen supply
journal, February 2013

Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by 13C labeling and comprehensive bondomer balancing
journal, August 2007

Use of reverse-phase liquid chromatography, linked to tandem mass spectrometry, to profile the Calvin cycle and other metabolic intermediates in Arabidopsis rosettes at different carbon dioxide concentrations
journal, September 2009

Metabolic turnover analysis by a combination of in vivo13C-labelling from 13CO2 and metabolic profiling with CE-MS/MS reveals rate-limiting steps of the C3 photosynthetic pathway in Nicotiana tabacum leaves
journal, December 2009

A transient isotopic labeling methodology for 13C metabolic flux analysis of photoautotrophic microorganisms
journal, August 2007

Metabolic Fluxes in an Illuminated Arabidopsis Rosette
journal, February 2013

Kinetic flux profiling for quantitation of cellular metabolic fluxes
journal, July 2008

Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis
journal, November 2011

The diurnal metabolism of leaf starch
journal, December 2006

Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake
journal, March 2010

In Folio Respiratory Fluxomics Revealed by ¹³ C Isotopic Labeling and H/D Isotope Effects Highlight the Noncyclic Nature of the Tricarboxylic Acid “Cycle” in Illuminated Leaves
journal, August 2009

Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1.
journal, October 2010

Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading
journal, August 2005

Quantification of Peptide m / z Distributions from ¹³ C-Labeled Cultures with High-Resolution Mass Spectrometry
journal, January 2014

Isotope labelling of Rubisco subunits provides in vivo information on subcellular biosynthesis and exchange of amino acids between compartments: Probing subcellular metabolism in seeds
journal, February 2012

GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after 13CO2 labelling
journal, August 2007

Estimating the rate of photorespiration in leaves
journal, May 1988

Current methods for estimating the rate of photorespiration in leaves
journal, November 2012

A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis
journal, October 2008

Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration
journal, July 2008

NMR determination of photorespiration in intact leaves using in vivo 13CO2 labeling
journal, January 2006

Photorespiratory and respiratory decarboxylations in leaves of C ₃ plants under different CO ₂ concentrations and irradiances
journal, December 2007

Leaf anatomy enables more equal access to light and CO2 between chloroplasts
journal, July 1999

Leaf Functional Anatomy in Relation to Photosynthesis
journal, November 2010

The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand
journal, August 2002

Photorespiratory Metabolism: Genes, Mutants, Energetics, and Redox Signaling
journal, June 2009

Insights into plant metabolic networks from steady-state metabolic flux analysis
journal, June 2009

Enzymes, metabolites and fluxes
journal, December 2004

INCA: a computational platform for isotopically non-stationary metabolic flux analysis
journal, January 2014

An elementary metabolite unit (EMU) based method of isotopically nonstationary flux analysis
journal, February 2008

Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements
journal, July 2006

Comparative studies of glycolytic pathways and channeling under in vitro and in vivo modes
journal, September 2018

Light Stress Responses and Prospects for Engineering Light Stress Tolerance in Crop Plants
journal, March 2019

Methods and advances in metabolic flux analysis: a mini-review
journal, January 2015

The challenge and potential of photosynthesis: unique considerations for metabolic flux measurements in photosynthetic microorganisms
journal, November 2018

Dissecting metabolic flux in C4 plants: experimental and theoretical approaches
journal, June 2018

Insights into the spatial and temporal organisation of plant metabolism from network flux analysis
journal, December 2018

Computational analysis of the productivity potential of CAM
journal, February 2018

Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H
journal, November 2018

Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by ¹³ C labelling
journal, February 2016

Perspectives for a better understanding of the metabolic integration of photorespiration within a complex plant primary metabolism network
journal, April 2016

Synthetic biology approaches for improving photosynthesis
journal, January 2019

Metabolite profiles reveal interspecific variation in operation of the Calvin–Benson cycle in both C4 and C3 plants
journal, February 2019

Triose phosphate utilization and beyond: from photosynthesis to end product synthesis
journal, March 2019

Relationship between irradiance and levels of Calvin–Benson cycle and other intermediates in the model eudicot Arabidopsis and the model monocot rice
journal, July 2019

Arabidopsis PPC2 is crucial for growth at low CO₂ by involvement in photorespiratory metabolism and integration of ABI5
posted_content, September 2019

Engineering central metabolism - a grand challenge for plant biologists
journal, March 2017

Integrated omics analysis of specialized metabolism in medicinal plants
journal, March 2017

Concurrent isotope-assisted metabolic flux analysis and transcriptome profiling reveal responses of poplar cells to altered nitrogen and carbon supply
journal, January 2018

In silico metabolic network analysis of Arabidopsis leaves
journal, October 2016

Shoot tip culture: a step towards 13C metabolite flux analysis of sink leaf metabolism
journal, May 2019

A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa
journal, October 2015

Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis
journal, November 2017

Parallel isotope differential modeling for instationary 13C fluxomics at the genome scale
journal, June 2020

Pool size measurements facilitate the determination of fluxes at branching points in non-stationary metabolic flux analysis: the case of Arabidopsis thaliana
journal, June 2015

Decoding Biosynthetic Pathways in Plants by Pulse-Chase Strategies Using 13CO2 as a Universal Tracer
journal, July 2016

Limitations of Deuterium-Labelled Substrates for Quantifying NADPH Metabolism in Heterotrophic Arabidopsis Cell Cultures
journal, September 2019

The challenge and potential of photosynthesis: unique considerations for metabolic flux measurements in photosynthetic microorganisms
journal, November 2018