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

Journal Article · Mon Nov 03 00:00:00 EST 2014 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1319485111· OSTI ID:1348223

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)

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.

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

Sponsoring Organization:: USDOE; USDA; National Science Foundation (NSF)

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

OSTI ID:: 1348223

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, Issue 47; ISSN 0027-8424

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

Country of Publication:: United States

Language:: English

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Cited by: 148 works

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References (52)

Increasing Photosynthetic Carbon Assimilation in C ₃ Plants to Improve Crop Yield: Current and Future Strategies Raines, Christine A. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.168559	journal	November 2010
The Dynamics of Photosynthesis Eberhard, Stephan; Finazzi, Giovanni; Wollman, Francis-André Annual Review of Genetics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.genet.42.110807.091452	journal	December 2008
Sink regulation of photosynthesis Paul, Matthew J.; Foyer, Christine H. Journal of Experimental Botany, Vol. 52, Issue 360 https://doi.org/10.1093/jexbot/52.360.1383	journal	July 2001
Metabolic profiling reveals metabolic shifts in Arabidopsis plants grown under different light conditions: Metabolic profiling under different light regime JÄNkÄNpÄÄ, Hanna Johansson; Mishra, Yogesh; SchrÖDer, Wolfgang P. Plant, Cell & Environment, Vol. 35, Issue 10 https://doi.org/10.1111/j.1365-3040.2012.02519.x	journal	May 2012
Plants, CO2 and photosynthesis in the 21st century Griffin, Kevin L.; Seemann, Jeffrey R. Chemistry & Biology, Vol. 3, Issue 4 https://doi.org/10.1016/S1074-5521(96)90104-0	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 Sage, Rowan F. Journal of Experimental Botany, Vol. 53, Issue 369 https://doi.org/10.1093/jexbot/53.369.609	journal	April 2002
Overexpression of C4‐cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3‐photosynthesis Häusler, Rainer E.; Hirsch, Heinz‐Josef; Kreuzaler, Fritz Journal of Experimental Botany, Vol. 53, Issue 369 https://doi.org/10.1093/jexbot/53.369.591	journal	April 2002
Photorespiration: current status and approaches for metabolic engineering Maurino, Veronica G.; Peterhansel, Christoph Current Opinion in Plant Biology, Vol. 13, Issue 3 https://doi.org/10.1016/j.pbi.2010.01.006	journal	June 2010
Rubisco activity and regulation as targets for crop improvement Parry, M. A. J.; Andralojc, P. J.; Scales, J. C. Journal of Experimental Botany, Vol. 64, Issue 3 https://doi.org/10.1093/jxb/ers336	journal	November 2012
Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth Miyagawa, Yoshiko; Tamoi, Masahiro; Shigeoka, Shigeru Nature Biotechnology, Vol. 19, Issue 10 https://doi.org/10.1038/nbt1001-965	journal	October 2001
A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism Henkes, Stefan; Sonnewald, Uwe; Badur, Ralf The Plant Cell, Vol. 13, Issue 3 https://doi.org/10.1105/tpc.13.3.535	journal	March 2001
Photorespiratory bypasses: how can they work? Peterhansel, Christoph; Blume, Christian; Offermann, Sascha Journal of Experimental Botany, Vol. 64, Issue 3 https://doi.org/10.1093/jxb/ers247	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 Zhu, Xin-Guang; de Sturler, Eric; Long, Stephen P. Plant Physiology, Vol. 145, Issue 2 https://doi.org/10.1104/pp.107.103713	journal	August 2007
Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii Boyle, Nanette R.; Morgan, John A. BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-4	journal	January 2009
Responses to Light Intensity in a Genome-Scale Model of Rice Metabolism Poolman, Mark G.; Kundu, Sudip; Shaw, Rahul Plant Physiology, Vol. 162, Issue 2 https://doi.org/10.1104/pp.113.216762	journal	May 2013
Multiscale Metabolic Modeling: Dynamic Flux Balance Analysis on a Whole-Plant Scale Grafahrend-Belau, E.; Junker, A.; Eschenroder, A. PLANT PHYSIOLOGY, Vol. 163, Issue 2 https://doi.org/10.1104/pp.113.224006	journal	August 2013
Seed Architecture Shapes Embryo Metabolism in Oilseed Rape Borisjuk, Ljudmilla; Neuberger, Thomas; Schwender, Jörg The Plant Cell, Vol. 25, Issue 5 https://doi.org/10.1105/tpc.113.111740	journal	May 2013
Analysis of Metabolic Flux Phenotypes for Two Arabidopsis Mutants with Severe Impairment in Seed Storage Lipid Synthesis Lonien, Joachim; Schwender, Jörg Plant Physiology, Vol. 151, Issue 3 https://doi.org/10.1104/pp.109.144121	journal	September 2009
Carbon and Nitrogen Provisions Alter the Metabolic Flux in Developing Soybean Embryos Allen, Doug K.; Young, Jamey D. Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.203299	journal	January 2013
Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering Alonso, Ana P.; Val, Dale L.; Shachar-Hill, Yair Metabolic Engineering, Vol. 13, Issue 1 https://doi.org/10.1016/j.ymben.2010.10.002	journal	January 2011
Metabolic flux analysis using ¹³ C peptide label measurements Mandy, Dominic E.; Goldford, Joshua E.; Yang, Hong The Plant Journal, Vol. 77, Issue 3 https://doi.org/10.1111/tpj.12390	journal	January 2014
The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a complex response to changes in nitrogen supply Masakapalli, Shyam K.; Kruger, Nicholas J.; Ratcliffe, R. George The Plant Journal, Vol. 74, Issue 4 https://doi.org/10.1111/tpj.12142	journal	February 2013
Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by 13C labeling and comprehensive bondomer balancing Sriram, Ganesh; Fulton, D. Bruce; Shanks, Jacqueline V. Phytochemistry, Vol. 68, Issue 16-18 https://doi.org/10.1016/j.phytochem.2007.04.009	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 Arrivault, Stéphanie; Guenther, Manuela; Ivakov, Alexander The Plant Journal, Vol. 59, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.03902.x	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 Hasunuma, Tomohisa; Harada, Kazuo; Miyazawa, Shin-Ichi Journal of Experimental Botany, Vol. 61, Issue 4 https://doi.org/10.1093/jxb/erp374	journal	December 2009
A transient isotopic labeling methodology for 13C metabolic flux analysis of photoautotrophic microorganisms Shastri, Avantika A.; Morgan, John A. Phytochemistry, Vol. 68, Issue 16-18 https://doi.org/10.1016/j.phytochem.2007.03.042	journal	August 2007
Metabolic Fluxes in an Illuminated Arabidopsis Rosette Szecowka, Marek; Heise, Robert; Tohge, Takayuki The Plant Cell, Vol. 25, Issue 2 https://doi.org/10.1105/tpc.112.106989	journal	February 2013
Kinetic flux profiling for quantitation of cellular metabolic fluxes Yuan, Jie; Bennett, Bryson D.; Rabinowitz, Joshua D. Nature Protocols, Vol. 3, Issue 8 https://doi.org/10.1038/nprot.2008.131	journal	July 2008
Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis Young, Jamey D.; Shastri, Avantika A.; Stephanopoulos, Gregory Metabolic Engineering, Vol. 13, Issue 6 https://doi.org/10.1016/j.ymben.2011.08.002	journal	November 2011
The diurnal metabolism of leaf starch Zeeman, Samuel C.; Smith, Steven M.; Smith, Alison M. Biochemical Journal, Vol. 401, Issue 1 https://doi.org/10.1042/BJ20061393	journal	December 2006
Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake Stitt, Mark; Lunn, John; Usadel, Björn The Plant Journal, Vol. 61, Issue 6 https://doi.org/10.1111/j.1365-313X.2010.04142.x	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 Tcherkez, Guillaume; Mahé, Aline; Gauthier, Paul Plant Physiology, Vol. 151, Issue 2 https://doi.org/10.1104/pp.109.142976	journal	August 2009
Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1. Ainsworth, Elizabeth A.; Bush, Daniel R. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.167684	journal	October 2010
Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading Amiard, V.; Mueh, K. E.; Demmig-Adams, B. Proceedings of the National Academy of Sciences, Vol. 102, Issue 36 https://doi.org/10.1073/pnas.0503784102	journal	August 2005
Quantification of Peptide m / z Distributions from ¹³ C-Labeled Cultures with High-Resolution Mass Spectrometry Allen, Doug K.; Goldford, Joshua; Gierse, James K. Analytical Chemistry, Vol. 86, Issue 3 https://doi.org/10.1021/ac403985w	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 Allen, Doug K.; Laclair, Russell W.; Ohlrogge, John B. Plant, Cell & Environment, Vol. 35, Issue 7 https://doi.org/10.1111/j.1365-3040.2012.02485.x	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 Huege, Jan; Sulpice, Ronan; Gibon, Yves Phytochemistry, Vol. 68, Issue 16-18 https://doi.org/10.1016/j.phytochem.2007.03.026	journal	August 2007
Estimating the rate of photorespiration in leaves Sharkey, Thomas D. Physiologia Plantarum, Vol. 73, Issue 1 https://doi.org/10.1111/j.1399-3054.1988.tb09205.x	journal	May 1988
Current methods for estimating the rate of photorespiration in leaves Busch, F. A. Plant Biology, Vol. 15, Issue 4 https://doi.org/10.1111/j.1438-8677.2012.00694.x	journal	November 2012
A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis Timm, Stefan; Nunes-Nesi, Adriano; Pärnik, Tiit The Plant Cell, Vol. 20, Issue 10 https://doi.org/10.1105/tpc.108.062265	journal	October 2008
Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration Collakova, Eva; Goyer, Aymeric; Naponelli, Valeria The Plant Cell, Vol. 20, Issue 7 https://doi.org/10.1105/tpc.108.058701	journal	July 2008
NMR determination of photorespiration in intact leaves using in vivo 13CO2 labeling Cegelski, Lynette; Schaefer, Jacob Journal of Magnetic Resonance, Vol. 178, Issue 1 https://doi.org/10.1016/j.jmr.2005.10.010	journal	January 2006
Photorespiratory and respiratory decarboxylations in leaves of C ₃ plants under different CO ₂ concentrations and irradiances PÄRnik, T.; Ivanova, H.; Keerberg, O. Plant, Cell & Environment, Vol. 30, Issue 12 https://doi.org/10.1111/j.1365-3040.2007.01725.x	journal	December 2007
Leaf anatomy enables more equal access to light and CO2 between chloroplasts Evans, John R. New Phytologist, Vol. 143, Issue 1 https://doi.org/10.1046/j.1469-8137.1999.00440.x	journal	July 1999
Leaf Functional Anatomy in Relation to Photosynthesis Terashima, Ichiro; Hanba, Yuko T.; Tholen, Danny Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.165472	journal	November 2010
The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand Hanba, Y. T.; Kogami, H.; Terashima, I. Plant, Cell and Environment, Vol. 25, Issue 8 https://doi.org/10.1046/j.1365-3040.2002.00881.x	journal	August 2002
Photorespiratory Metabolism: Genes, Mutants, Energetics, and Redox Signaling Foyer, Christine H.; Bloom, Arnold J.; Queval, Guillaume Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.091948	journal	June 2009
Insights into plant metabolic networks from steady-state metabolic flux analysis Kruger, Nicholas J.; Ratcliffe, R. George Biochimie, Vol. 91, Issue 6 https://doi.org/10.1016/j.biochi.2009.01.004	journal	June 2009
Enzymes, metabolites and fluxes Fell, D. A. Journal of Experimental Botany, Vol. 56, Issue 410 https://doi.org/10.1093/jxb/eri011	journal	December 2004
INCA: a computational platform for isotopically non-stationary metabolic flux analysis Young, J. D. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu015	journal	January 2014
An elementary metabolite unit (EMU) based method of isotopically nonstationary flux analysis Young, Jamey D.; Walther, Jason L.; Antoniewicz, Maciek R. Biotechnology and Bioengineering, Vol. 99, Issue 3 https://doi.org/10.1002/bit.21632	journal	February 2008
Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements Antoniewicz, Maciek R.; Kelleher, Joanne K.; Stephanopoulos, Gregory Metabolic Engineering, Vol. 8, Issue 4 https://doi.org/10.1016/j.ymben.2006.01.004	journal	July 2006

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

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