Temperature response of Rubisco kinetics in Arabidopsis thaliana: thermal breakpoints and implications for reaction mechanisms

Boyd, Ryan A.; Cavanagh, Amanda P.; Kubien, David S.; Cousins, Asaph B.

doi:10.1093/jxb/ery355

Title: Temperature response of Rubisco kinetics in Arabidopsis thaliana: thermal breakpoints and implications for reaction mechanisms

Journal Article · 07 November 2018 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/ery355 · OSTI ID:1610565

Boyd, Ryan A. ^[1]; Cavanagh, Amanda P. ^[2]; Kubien, David S. ^[3]; Cousins, Asaph B. ^[4]

Washington State Univ., Pullman, WA (United States); Univ. of Illinois at Urbana-Champaign, IL (United States). Carl R. Woese Institute for Genomic Biology; DOE/OSTI
Univ. of New Brunswick, Fredericton NB (Canada); Univ. of Illinois at Urbana-Champaign, IL (United States). Carl R. Woese Institute for Genomic Biology
Univ. of New Brunswick, Fredericton NB (Canada)
Washington State Univ., Pullman, WA (United States)

Enhancement of Rubisco kinetics could improve photosynthetic efficiency, ultimately resulting in increased crop yield. However, imprecise knowledge of the reaction mechanism and the individual rate constants limits our ability to optimize the enzyme. Membrane inlet mass spectrometry (MIMS) may offer benefits over traditional methods for determining individual rate constants of the Rubisco reaction mechanism, as it can directly monitor concentration changes in CO₂, O₂, and their isotopologs during assays. However, a direct comparison of MIMS with the traditional radiolabel method of determining Rubisco kinetic parameters has not been made. Here, the temperature responses of Rubisco kinetic parameters from Arabidopsis thaliana were measured using radiolabel and MIMS methods. The two methods provided comparable parameters above 25 °C, but temperature responses deviated at low temperature as MIMS-derived catalytic rates of carboxylation, oxygenation, and CO₂/O₂ specificity showed thermal breakpoints. Here, we discuss the variability and uncertainty surrounding breakpoints in the Rubisco temperature response and the relevance of individual rate constants of the reaction mechanisms to potential breakpoints.

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Research Organization:: Washington State University, Pullman, WA (United States)

Sponsoring Organization:: National Science Foundation (NSF); National Science and Engineering Research Council of Canada (NSERC); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: SC0001685

OSTI ID:: 1610565

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 1 Vol. 70; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters: Rubisco kinetics Tcherkez, Guillaume Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12066	journal	February 2013
Estimating regression models with unknown break-points Muggeo, Vito M. R. Statistics in Medicine, Vol. 22, Issue 19 https://doi.org/10.1002/sim.1545	journal	January 2003
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How various factors influence the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase Chen, Zhixiang; Spreitzer, Robert J. Photosynthesis Research, Vol. 31, Issue 2 https://doi.org/10.1007/BF00028792	journal	February 1992
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Temperature dependence of in vitro Rubisco kinetics in species of Flaveria with different photosynthetic mechanisms Perdomo, Juan Alejandro; Cavanagh, Amanda P.; Kubien, David S. Photosynthesis Research, Vol. 124, Issue 1 https://doi.org/10.1007/s11120-015-0092-2	journal	February 2015
The arc mutants of Arabidopsis with fewer large chloroplasts have a lower mesophyll conductance Weise, Sean E.; Carr, David J.; Bourke, Ashley M. Photosynthesis Research, Vol. 124, Issue 1 https://doi.org/10.1007/s11120-015-0110-4	journal	March 2015
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D ₂ O Solvent Isotope Effects Suggest Uniform Energy Barriers in Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Catalysis Tcherkez, Guillaume G. B.; Bathellier, Camille; Stuart-Williams, Hilary Biochemistry, Vol. 52, Issue 5 https://doi.org/10.1021/bi300933u	journal	January 2013
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Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized Tcherkez, G. G. B.; Farquhar, G. D.; Andrews, T. J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 19 https://doi.org/10.1073/pnas.0600605103	journal	April 2006
Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2 Crafts-Brandner, S. J.; Salvucci, M. E. Proceedings of the National Academy of Sciences, Vol. 97, Issue 24 https://doi.org/10.1073/pnas.230451497	journal	November 2000
Differences in Carbon Isotope Discrimination of Three Variants of D-Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Reflect Differences in Their Catalytic Mechanisms McNevin, Dennis B.; Badger, Murray R.; Whitney, Spencer M. Journal of Biological Chemistry, Vol. 282, Issue 49 https://doi.org/10.1074/jbc.M706274200	journal	October 2007
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A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling Galmés, Jeroni; Hermida-Carrera, Carmen; Laanisto, Lauri Journal of Experimental Botany, Vol. 67, Issue 17 https://doi.org/10.1093/jxb/erw267	journal	July 2016
C ₄ Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco Kubien, David S.; von Caemmerer, Susanne; Furbank, Robert T. Plant Physiology, Vol. 132, Issue 3 https://doi.org/10.1104/pp.103.021246	journal	June 2003
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Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters: Rubisco kinetics Tcherkez, Guillaume Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12066	journal	February 2013
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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Arabidopsis
Rubisco
kinetic breakpoints
membrane inlet mass spectrometery
plant sciences
reaction mechanisms
temperature

Title: Temperature response of Rubisco kinetics in Arabidopsis thaliana: thermal breakpoints and implications for reaction mechanisms

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References (65)

Cited By (1)

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