Probing Light-Dependent Regulation of the Calvin Cycle Using a Multi-Omics Approach

Yu King Hing, Nathaphon; Aryal, Uma K.; Morgan, John A.

doi:10.3389/fpls.2021.733122

Title: Probing Light-Dependent Regulation of the Calvin Cycle Using a Multi-Omics Approach

Journal Article · Mon Oct 04 00:00:00 EDT 2021 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2021.733122· OSTI ID:1981098

Yu King Hing, Nathaphon ^[1]; Aryal, Uma K. ^[1]; Morgan, John A. ^[1]

Purdue University, West Lafayette, IN (United States)

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 play a role under different light intensities remains unclear. In this work, we conducted non-targeted proteomics in tandem with isotopically non-stationary metabolic flux analysis (INST-MFA) at four different light intensities to determine the extent to which fluxes within the CBB cycle are controlled by enzymatic abundance. The correlation between specific enzyme abundances and their corresponding reaction fluxes is examined, revealing several enzymes with uncorrelated enzyme abundance and their corresponding flux, suggesting flux regulation by mechanisms other than enzyme abundance. Additionally, the kinetics of ¹³C labeling of CBB cycle intermediates and estimated inactive pool sizes varied significantly as a function of light intensity suggesting the presence of metabolite channeling, an additional method of flux regulation. These results highlight the importance of the diverse methods of regulation of CBB enzyme activity as a function of light intensity, and highlights the importance of considering these effects in future kinetic models.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Purdue Univ., West Lafayette, IN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0008628

OSTI ID:: 1981098

Journal Information:: Frontiers in Plant Science, Vol. 12; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (88)

Light Modulates the Biosynthesis and Organization of Cyanobacterial Carbon Fixation Machinery through Photosynthetic Electron Flow Sun, Yaqi; Casella, Selene; Fang, Yi Plant Physiology, Vol. 171, Issue 1 https://doi.org/10.1104/pp.16.00107	journal	March 2016
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
Systems-level analysis of mechanisms regulating yeast metabolic flux Hackett, S. R.; Zanotelli, V. R. T.; Xu, W. Science, Vol. 354, Issue 6311 https://doi.org/10.1126/science.aaf2786	journal	October 2016
Metabolic engineering tools in model cyanobacteria Carroll, Austin L.; Case, Anna E.; Zhang, Angela Metabolic Engineering, Vol. 50 https://doi.org/10.1016/J.YMBEN.2018.03.014	journal	November 2018
Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms Trost, P.; Fermani, S.; Marri, L. Photosynthesis Research, Vol. 89, Issue 2-3 https://doi.org/10.1007/s11120-006-9099-z	journal	September 2006
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
Chloroplast Alkaline Fructose 1,6-Bisphosphatase Exists in a Membrane-Bound Form Alscher-Herman, Ruth Plant Physiology, Vol. 70, Issue 3 https://doi.org/10.1104/PP.70.3.728	journal	September 1982
Transcriptional, Proteomic, and Metabolic Responses to Lithium in Galactose-grown Yeast Cells Bro, Christoffer; Regenberg, Birgitte; Lagniel, Gilles Journal of Biological Chemistry, Vol. 278, Issue 34 https://doi.org/10.1074/jbc.M304478200	journal	August 2003
Effect of alcohols on the association of photosynthetic fructose-1,6-bisphosphatase to thylakoid membranes Andres, A. Rodriguez; Lazaro, J. J.; Chueca, A. Physiologia Plantarum, Vol. 78, Issue 3 https://doi.org/10.1111/j.1399-3054.1990.tb09056.x	journal	March 1990
The biodiversity of carbon assimilation Kroth, Peter G. Journal of Plant Physiology, Vol. 172 https://doi.org/10.1016/j.jplph.2014.07.021	journal	January 2015
Cyanobacteria Maintain Constant Protein Concentration despite Genome Copy-Number Variation Zheng, Xiao-yu; O’Shea, Erin K. Cell Reports, Vol. 19, Issue 3 https://doi.org/10.1016/J.CELREP.2017.03.067	journal	April 2017
Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions Tcherkez, G.; Bligny, R.; Gout, E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 2 https://doi.org/10.1073/pnas.0708947105	journal	January 2008
Light-dependent Release of Carbon Metabolism Enzymes from Chloroplast Thylakoids Has No Relation to Light-activation of the Enzymes Tanaka, Kiyoshi; Ono, Chisato; Sugimoto, Toshio Agricultural and Biological Chemistry, Vol. 54, Issue 8 https://doi.org/10.1080/00021369.1990.10870258	journal	August 1990
Regulators of TNFα mediated insulin resistance elucidated by quantitative proteomics Mohallem, Rodrigo; Aryal, Uma K. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-77914-1	journal	November 2020
e -photosynthesis: a comprehensive dynamic mechanistic model of C3 photosynthesis: from light capture to sucrose synthesis : Dynamic systems model of C3 photosynthesis Zhu, Xin-Guang; Wang, Yu; Ort, Donald R. Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12025	journal	November 2012
Dynamic Inventory of Intermediate Metabolites of Cyanobacteria in a Diurnal Cycle Jaiswal, Damini; Wangikar, Pramod P. iScience, Vol. 23, Issue 11 https://doi.org/10.1016/j.isci.2020.101704	journal	November 2020
Sustained photosynthetic conversion of CO₂ to ethylene in recombinant cyanobacterium Synechocystis 6803 Ungerer, Justin; Tao, Ling; Davis, Mark Energy & Environmental Science, Vol. 5, Issue 10, p. 8998-9006 https://doi.org/10.1039/c2ee22555g	journal	January 2012
Isolation and characterization of a thylakoid membrane module showing partial light and dark reactions Dani, Diksha Narhar; Sainis, Jayashree Krishna Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1669, Issue 1 https://doi.org/10.1016/j.bbamem.2005.01.001	journal	May 2005
In vitro characterization of Arabidopsis CP12 isoforms reveals common biochemical and molecular properties Marri, Lucia; Pesaresi, Alessandro; Valerio, Concetta Journal of Plant Physiology, Vol. 167, Issue 12 https://doi.org/10.1016/j.jplph.2010.02.008	journal	August 2010
Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria Xiong, Wei; Lee, Tai-Chi; Rommelfanger, Sarah Nature Plants, Vol. 2, Issue 1, Article No. 15187 https://doi.org/10.1038/nplants.2015.187	journal	December 2015
Rerouting of carbon flux in a glycogen mutant of cyanobacteria assessed via isotopically non-stationary ¹³ C metabolic flux analysis : Rerouting of Carbon Flux in a Glycogen Mutant Hendry, John I.; Prasannan, Charulata; Ma, Fangfang Biotechnology and Bioengineering, Vol. 114, Issue 10 https://doi.org/10.1002/bit.26350	journal	June 2017
Regulation of CO2 Concentrating Mechanism in Cyanobacteria Burnap, Robert; Hagemann, Martin; Kaplan, Aaron Life, Vol. 5, Issue 1 https://doi.org/10.3390/life5010348	journal	January 2015
Photoinhibition of Cyanobacteria and its Application in Cultural Heritage Conservation Hsieh, Paul; Pedersen, Jens Z.; Bruno, Laura Photochemistry and Photobiology, Vol. 90, Issue 3 https://doi.org/10.1111/php.12208	journal	December 2013
Characterisation of CO2 and HCO3- Uptake during Steady-state Photosynthesis in the Cyanobacterium Synechococcus PCC7942 Steady-state Photosynthesis in the Cyanobacterium Synechococcus PCC7942 Yu, J.; Price, Gd; Badger, Mr Functional Plant Biology, Vol. 21, Issue 2 https://doi.org/10.1071/PP9940185	journal	January 1994
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
Quantitative insights into the cyanobacterial cell economy Zavřel, Tomáš; Faizi, Marjan; Loureiro, Cristina eLife, Vol. 8 https://doi.org/10.7554/elife.42508	journal	February 2019
Global coordination of metabolic pathways in Escherichia coli by active and passive regulation Kochanowski, Karl; Okano, Hiroyuki; Patsalo, Vadim Molecular Systems Biology, Vol. 17, Issue 4 https://doi.org/10.15252/msb.202010064	journal	April 2021
Photorespiration is complemented by cyclic electron flow and the alternative oxidase pathway to optimize photosynthesis and protect against abiotic stress Sunil, Bobba; Saini, Deepak; Bapatla, Ramesh B. Photosynthesis Research, Vol. 139, Issue 1-3 https://doi.org/10.1007/s11120-018-0577-x	journal	September 2018
Metabolic engineering of cyanobacteria for ethanol production Dexter, Jason; Fu, Pengcheng Energy & Environmental Science, Vol. 2, Issue 8 https://doi.org/10.1039/b811937f	journal	January 2009
Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability Howard, Thomas P.; Metodiev, Metodi; Lloyd, Julie C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10 https://doi.org/10.1073/pnas.0710518105	journal	March 2008
Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis Abernathy, Mary H.; Yu, Jingjie; Ma, Fangfang Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0958-y	journal	November 2017
Steady-state analysis of metabolic pathways: Comparing the double modulation method and the lin–log approach Link, Hannes; Weuster-Botz, Dirk Metabolic Engineering, Vol. 9, Issue 5-6 https://doi.org/10.1016/j.ymben.2007.07.002	journal	September 2007
Purification and Characterization of Class-I and Class-II Fructose-1,6-bisphosphate Aldolases from the Cyanobacterium Synechocystis sp. PCC 6803 Nakahara, Ken; Yamamoto, Hiroshi; Miyake, Chikahiro Plant and Cell Physiology, Vol. 44, Issue 3 https://doi.org/10.1093/pcp/pcg044	journal	March 2003
Cyanobacterial Carboxysomes: Microcompartments that Facilitate CO ₂ Fixation Rae, Benjamin D.; Long, Benedict M.; Whitehead, Lynne F. Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 4-5 https://doi.org/10.1159/000351342	journal	January 2013
A comprehensive time‐course metabolite profiling of the model cyanobacterium Synechocystis sp. PCC 6803 under diurnal light:dark cycles Werner, Allison; Broeckling, Corey D.; Prasad, Ashok The Plant Journal https://doi.org/10.1111/tpj.14320	journal	April 2019
Kinetic modeling of the Calvin cycle identifies flux control and stable metabolomes in Synechocystis carbon fixation Janasch, Markus; Asplund-Samuelsson, Johannes; Steuer, Ralf Journal of Experimental Botany https://doi.org/10.1093/jxb/ery382	journal	October 2018
The CP12 protein family: a thioredoxin-mediated metabolic switch? López-Calcagno, Patricia E.; Howard, Thomas P.; Raines, Christine A. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00009	journal	January 2014
Identification of the light-independent phosphoserine pathway as an additional source of serine in the cyanobacterium Synechocystis sp. PCC 6803 Volkmer, Thomas; Knoop, Henning; Beyer, Gabriele Microbiology, Vol. 161, Issue 5 https://doi.org/10.1099/mic.0.000055	journal	May 2015
Flux control coefficients determined by inhibitor titration: the design and analysis of experiments to minimize errors Small, J. R. Biochemical Journal, Vol. 296, Issue 2 https://doi.org/10.1042/bj2960423	journal	December 1993
Channeling in native microbial pathways: Implications and challenges for metabolic engineering Abernathy, Mary H.; He, Lian; Tang, Yinjie J. Biotechnology Advances, Vol. 35, Issue 6 https://doi.org/10.1016/j.biotechadv.2017.06.004	journal	November 2017
Growth of Cyanobacteria Is Constrained by the Abundance of Light and Carbon Assimilation Proteins Jahn, Michael; Vialas, Vital; Karlsen, Jan Cell Reports, Vol. 25, Issue 2 https://doi.org/10.1016/j.celrep.2018.09.040	journal	October 2018
Isotopically nonstationary 13C flux analysis of cyanobacterial isobutyraldehyde production Jazmin, Lara J.; Xu, Yao; Cheah, Yi Ern Metabolic Engineering, Vol. 42 https://doi.org/10.1016/j.ymben.2017.05.001	journal	July 2017
Reactive oxygen species generation and signaling in plants Tripathy, Baishnab Charan; Oelmüller, Ralf Plant Signaling & Behavior, Vol. 7, Issue 12 https://doi.org/10.4161/psb.22455	journal	December 2012
Engineering the fatty acid synthesis pathway in Synechococcus elongatus PCC 7942 improves omega-3 fatty acid production Santos-Merino, María; Garcillán-Barcia, M. Pilar; de la Cruz, Fernando Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1243-4	journal	September 2018
Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria Kusian, Bernhard; Bowien, Botho FEMS Microbiology Reviews, Vol. 21, Issue 2 https://doi.org/10.1111/j.1574-6976.1997.tb00348.x	journal	September 1997
Combining isotopically non-stationary metabolic flux analysis with proteomics to unravel the regulation of the Calvin-Benson-Bassham cycle in Synechocystis sp. PCC 6803 Yu King Hing, Nathaphon; Liang, Feiyan; Lindblad, Peter Metabolic Engineering, Vol. 56 https://doi.org/10.1016/j.ymben.2019.08.014	journal	December 2019
Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Suss, K. H.; Arkona, C.; Manteuffel, R. Proceedings of the National Academy of Sciences, Vol. 90, Issue 12 https://doi.org/10.1073/pnas.90.12.5514	journal	June 1993
Slow Protein Turnover Explains Limited Protein-Level Response to Diurnal Transcriptional Oscillations in Cyanobacteria Karlsen, Jan; Asplund-Samuelsson, Johannes; Jahn, Michael Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.657379	journal	April 2021
Synthetic metabolic channel by functional membrane microdomains for compartmentalized flux control Lv, Xueqin; Wu, Yaokang; Tian, Rongzhen Metabolic Engineering, Vol. 59 https://doi.org/10.1016/j.ymben.2020.02.003	journal	May 2020
Error associated with experimental flux control coefficient determinations in the Calvin cycle Pettersson, G. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1289, Issue 2 https://doi.org/10.1016/0304-4165(95)00078-X	journal	March 1996
Increasing the Photoautotrophic Growth Rate of Synechocystis sp. PCC 6803 by Identifying the Limitations of Its Cultivation van Alphen, Pascal; Abedini Najafabadi, Hamed; Branco dos Santos, Filipe Biotechnology Journal, Vol. 13, Issue 8 https://doi.org/10.1002/biot.201700764	journal	May 2018
Redox regulation of the Calvin–Benson cycle: something old, something new Michelet, Laure; Zaffagnini, Mirko; Morisse, Samuel Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00470	journal	January 2013
Effects of overexpressing photosynthetic carbon flux control enzymes in the cyanobacterium Synechocystis PCC 6803 Liang, Feiyan; Lindblad, Peter Metabolic Engineering, Vol. 38 https://doi.org/10.1016/j.ymben.2016.06.005	journal	November 2016
Modulation of the Major Paths of Carbon in Photorespiratory Mutants of Synechocystis Huege, Jan; Goetze, Jan; Schwarz, Doreen PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016278	journal	January 2011
Analysis of Protein Complexes in the Unicellular Cyanobacterium Cyanothece ATCC 51142 Aryal, Uma K.; Ding, Ziyun; Hedrick, Victoria Journal of Proteome Research, Vol. 17, Issue 11 https://doi.org/10.1021/acs.jproteome.8b00170	journal	September 2018
Metabolic flux of the oxidative pentose phosphate pathway under low light conditions in Synechocystis sp. PCC 6803 Ueda, Kentaro; Nakajima, Tsubasa; Yoshikawa, Katsunori Journal of Bioscience and Bioengineering, Vol. 126, Issue 1 https://doi.org/10.1016/j.jbiosc.2018.01.020	journal	July 2018
Diversity of regulatory mechanisms of photosynthetic carbon metabolism in plants and algae Tamoi, Masahiro; Shigeoka, Shigeru Bioscience, Biotechnology, and Biochemistry, Vol. 79, Issue 6 https://doi.org/10.1080/09168451.2015.1020754	journal	June 2015
Redox Control of the Activity of Phosphoglycerate Kinase in Synechocystis sp. PCC6803 Tsukamoto, Yu; Fukushima, Yuriko; Hara, Satoshi Plant and Cell Physiology, Vol. 54, Issue 4 https://doi.org/10.1093/pcp/pct002	journal	January 2013
Immunogold Localization of Photosynthetic Fructose-1,6-Bisphosphatase in Pea Leaf Tissue Hermoso, Rosario; de Felipe, María R.; Vivó, Amparo Plant Physiology, Vol. 89, Issue 1 https://doi.org/10.1104/pp.89.1.381	journal	January 1989
A new framework for the estimation of control parameters in metabolic pathways using lin-log kinetics: Control parameter estimation using lin-log kinetics Wu, Liang; Wang, Weiming; Van Winden, Wouter A. European Journal of Biochemistry, Vol. 271, Issue 16 https://doi.org/10.1111/j.0014-2956.2004.04269.x	journal	July 2004
Modeling the Calvin-Benson cycle Jablonsky, Jiri; Bauwe, Hermann; Wolkenhauer, Olaf BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-185	journal	January 2011
An improved method for extraction of polar and charged metabolites from cyanobacteria Prasannan, Charulata B.; Jaiswal, Damini; Davis, Rose PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0204273	journal	October 2018
Diurnal Regulation of Cellular Processes in the Cyanobacterium Synechocystis sp. Strain PCC 6803: Insights from Transcriptomic, Fluxomic, and Physiological Analyses Saha, Rajib; Liu, Deng; Hoynes-O’Connor, Allison mBio, Vol. 7, Issue 3 https://doi.org/10.1128/mBio.00464-16	journal	May 2016
The Path of Carbon in Photosynthesis. XXI. The Cyclic Regeneration of Carbon Dioxide Acceptor ¹ Bassham, J. A.; Benson, A. A.; Kay, Lorel D. Journal of the American Chemical Society, Vol. 76, Issue 7 https://doi.org/10.1021/ja01636a012	journal	April 1954
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
Integrating multiple 'omics' analysis for microbial biology: application and methodologies Zhang, W.; Li, F.; Nie, L. Microbiology, Vol. 156, Issue 2 https://doi.org/10.1099/mic.0.034793-0	journal	November 2009
Metabolic flux analysis of Synechocystis sp. PCC 6803 Δ nrtABCD mutant reveals a mechanism for metabolic adaptation to nitrogen-limited conditions Nakajima, Tsubasa; Yoshikawa, Katsunori; Toya, Yoshihiro Plant and Cell Physiology https://doi.org/10.1093/pcp/pcw233	journal	January 2017
Elucidation of photoautotrophic carbon flux topology in Synechocystis PCC 6803 using genome-scale carbon mapping models Gopalakrishnan, Saratram; Pakrasi, Himadri B.; Maranas, Costas D. Metabolic Engineering, Vol. 47 https://doi.org/10.1016/j.ymben.2018.03.008	journal	May 2018
Current knowledge and recent advances in understanding metabolism of the model cyanobacterium Synechocystis sp. PCC 6803 Mills, Lauren A.; McCormick, Alistair J.; Lea-Smith, David J. Bioscience Reports, Vol. 40, Issue 4 https://doi.org/10.1042/BSR20193325	journal	April 2020
Cyanobacterial carboxysome mutant analysis reveals the influence of enzyme compartmentalization on cellular metabolism and metabolic network rigidity Abernathy, Mary H.; Czajka, Jeffrey J.; Allen, Douglas K. Metabolic Engineering, Vol. 54 https://doi.org/10.1016/j.ymben.2019.04.010	journal	July 2019
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
Dynamic Changes in the Proteome of Synechocystis 6803 in Response to CO₂ Limitation Revealed by Quantitative Proteomics Battchikova, Natalia; Vainonen, Julia P.; Vorontsova, Natalia Journal of Proteome Research, Vol. 9, Issue 11 https://doi.org/10.1021/pr100651w	journal	September 2010
Isotopically nonstationary ¹³ C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation Ma, Fangfang; Jazmin, Lara J.; Young, Jamey D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 47 https://doi.org/10.1073/pnas.1319485111	journal	November 2014
A generalized computational framework to streamline thermodynamics and kinetics analysis of metabolic pathways Wu, Chao; Jiang, Huaiguang; Kalra, Isha Metabolic Engineering, Vol. 57 https://doi.org/10.1016/j.ymben.2019.08.006	journal	January 2020
Immunoelectron Microscopy for Locating Calvin Cycle Enzymes in the Thylakoids of Synechocystis 6803 Agarwal, Rachna; Ortleb, Stefan; Sainis, Jayashree Krishna Molecular Plant, Vol. 2, Issue 1 https://doi.org/10.1093/mp/ssn075	journal	January 2009
The effect of water motion on short-term rates of photosynthesis by marine phytoplankton MacIntyre, Hugh L.; Kana, Todd M.; Geider, Richard J. Trends in Plant Science, Vol. 5, Issue 1 https://doi.org/10.1016/S1360-1385(99)01504-6	journal	January 2000
Enzyme co-localization in pea leaf chloroplasts: glyceraldehyde-3-P dehydrogenase, triose-P isomerase, aldolase and sedoheptulose bisphosphatase Anderson, Louise E.; Gatla, Nandita; Carol, Andrew A. Photosynthesis Research, Vol. 83, Issue 3 https://doi.org/10.1007/s11120-005-0790-2	journal	March 2005
Light-Induced Release of Bound Glucose-6-phosphate Dehydrogenase to the Stroma in Pea Chloroplasts Ben-Bassat, David; Anderson, Louise E. Plant Physiology, Vol. 68, Issue 2 https://doi.org/10.1104/pp.68.2.279	journal	August 1981
Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis Nogales, J.; Gudmundsson, S.; Knight, E. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 7 https://doi.org/10.1073/pnas.1117907109	journal	January 2012
A quantitative comparison of Calvin–Benson cycle models Arnold, Anne; Nikoloski, Zoran Trends in Plant Science, Vol. 16, Issue 12 https://doi.org/10.1016/j.tplants.2011.09.004	journal	December 2011
Quantifying Reversible Oxidation of Protein Thiols in Photosynthetic Organisms Slade, William O.; Werth, Emily G.; McConnell, Evan W. Journal of the American Society for Mass Spectrometry, Vol. 26, Issue 4 https://doi.org/10.1007/s13361-014-1073-y	journal	February 2015
Fluxomics - connecting ‘omics analysis and phenotypes: Fluxomics - a systems biology tool Winter, Gal; Krömer, Jens O. Environmental Microbiology, Vol. 15, Issue 7 https://doi.org/10.1111/1462-2920.12064	journal	January 2013
Dynamics of photosynthesis in fluctuating light Rascher, Uwe; Nedbal, Ladislav Current Opinion in Plant Biology, Vol. 9, Issue 6 https://doi.org/10.1016/j.pbi.2006.09.012	journal	December 2006
Engineering cyanobacteria to generate high-value products Ducat, Daniel C.; Way, Jeffrey C.; Silver, Pamela A. Trends in Biotechnology, Vol. 29, Issue 2, p. 95-103 https://doi.org/10.1016/j.tibtech.2010.12.003	journal	February 2011
13C flux analysis of cyanobacterial metabolism Adebiyi, Adeola O.; Jazmin, Lara J.; Young, Jamey D. Photosynthesis Research, Vol. 126, Issue 1 https://doi.org/10.1007/s11120-014-0045-1	journal	October 2014
Metabolic control analysis of plant metabolism ap REES, T.; Hill, S. A. Plant, Cell and Environment, Vol. 17, Issue 5 https://doi.org/10.1111/j.1365-3040.1994.tb00151.x	journal	May 1994
Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts Long, Benedict M.; Hee, Wei Yih; Sharwood, Robert E. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06044-0	journal	September 2018
Tailoring cyanobacteria as a new platform for highly efficient synthesis of astaxanthin Diao, Jinjin; Song, Xinyu; Zhang, Li Metabolic Engineering, Vol. 61 https://doi.org/10.1016/j.ymben.2020.07.003	journal	September 2020

Similar Records

Engineering and Coordination of Regulatory Networks and Intracellular Complexes to Maximize Hydrogen Production by Phototrophic Microorganisms

Technical Report · Tue May 22 00:00:00 EDT 2012 · OSTI ID:1981098

Liao, James C.

Membrane-Inlet Mass Spectrometry Enables a Quantitative Understanding of Inorganic Carbon Uptake Flux and Carbon Concentrating Mechanisms in Metabolically Engineered Cyanobacteria

Journal Article · Tue Jun 25 00:00:00 EDT 2019 · Frontiers in Microbiology · OSTI ID:1981098

Douchi, Damien; Liang, Feiyan; Cano, Melissa; +5 more

A generalized computational framework to streamline thermodynamics and kinetics analysis of metabolic pathways

Journal Article · Thu Aug 08 00:00:00 EDT 2019 · Metabolic Engineering · OSTI ID:1981098

Wu, Chao; Jiang, Huaiguang; Kalra, Isha; +5 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
isotopically non-stationary metabolic flux analysis
metabolite channeling
photoautotrophic metabolism
carbon fixation
cyanobacteria
proteomics
metabolic flux analysis
MFA

Title: Probing Light-Dependent Regulation of the Calvin Cycle Using a Multi-Omics Approach

Citation Formats

References (88)

Similar Records

Related Subjects