Rapid CO2 changes cause oscillations in photosynthesis that implicate PSI acceptor-side limitations

McClain, Alan M.; Sharkey, Thomas D.; Lawson, ed., Tracy

doi:10.1093/jxb/erad084

Title: Rapid CO2 changes cause oscillations in photosynthesis that implicate PSI acceptor-side limitations

Journal Article · Wed Mar 08 00:00:00 UTC 2023 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/erad084 · OSTI ID:1974495

;

; Lawson, ed., Tracy

Abstract Oscillations in CO2 assimilation rate and associated fluorescence parameters have been observed alongside the triose phosphate utilization (TPU) limitation of photosynthesis for nearly 50 years. However, the mechanics of these oscillations are poorly understood. Here we utilize the recently developed dynamic assimilation techniques (DATs) for measuring the rate of CO2 assimilation to increase our understanding of what physiological condition is required to cause oscillations. We found that TPU-limiting conditions alone were insufficient, and that plants must enter TPU limitation quickly to cause oscillations. We found that ramps of CO2 caused oscillations proportional in strength to the speed of the ramp, and that ramps induce oscillations with worse outcomes than oscillations induced by step change of CO2 concentration. An initial overshoot is caused by a temporary excess of available phosphate. During the overshoot, the plant outperforms steady-state TPU and ribulose 1,5-bisphosphate regeneration limitations of photosynthesis, but cannot exceed the rubisco limitation. We performed additional optical measurements which support the role of PSI reduction and oscillations in availability of NADP+ and ATP in supporting oscillations.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: FG02-91ER20021

OSTI ID:: 1974495

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 10 Vol. 74; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (46)

Photosynthetic Measurements with the Idea Spec: an Integrated Diode Emitter Array Spectrophotometer/Fluorometer Hall, Christopher C.; Cruz, Jeffrey; Wood, Magnus Advanced Topics in Science and Technology in China https://doi.org/10.1007/978-3-642-32034-7_38	book	January 2013
Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle Laisk, Agu; Siebke, Katharina; Gerst, Ulvi Planta, Vol. 185, Issue 4 https://doi.org/10.1007/BF00202966	journal	November 1991
Regulation of photosynthetic electron-transport in Phaseolus vulgaris L., as determined by room-temperature chlorophyll a fluorescence Sharkey, Thomas D.; Berry, Joseph A.; Sage, Rowan F. Planta, Vol. 176, Issue 3 https://doi.org/10.1007/BF00395423	journal	December 1988
Limitation of photosynthesis by changes in temperature: Factors affecting the response of carbon-dioxide assimilation to temperature in barley leaves Labate, Carlos A.; Leegood, Richard C. Planta, Vol. 173, Issue 4 https://doi.org/10.1007/BF00958965	journal	January 1988
The in-vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic metabolites to elevated CO2 inPhaseolus vulgaris L. Sage, Rowan F.; Sharkey, Thomas D.; Seemann, Jeffrey R. Planta, Vol. 174, Issue 3 https://doi.org/10.1007/BF00959528	journal	June 1988
An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm Klughammer, Christof; Schreiber, Ulrich Planta, Vol. 192, Issue 2 https://doi.org/10.1007/BF01089043	journal	January 1994
Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations Sharkey, Thomas D. The Botanical Review, Vol. 51, Issue 1 https://doi.org/10.1007/BF02861058	journal	January 1985
Triose phosphate use limitation of photosynthesis: short-term and long-term effects Yang, Jennifer T.; Preiser, Alyssa L.; Li, Ziru Planta, Vol. 243, Issue 3 https://doi.org/10.1007/s00425-015-2436-8	journal	November 2015
Promoter strength and tissue specificity effects on growth of tomato plants transformed with maize sucrose-phosphate synthase Laporte, Marianne M.; Galagan, Julie A.; Prasch, Amy L. Planta, Vol. 212, Issue 5-6 https://doi.org/10.1007/s004250000433	journal	April 2001
Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase Farquhar, Graham D. Archives of Biochemistry and Biophysics, Vol. 193, Issue 2 https://doi.org/10.1016/0003-9861(79)90052-3	journal	April 1979
Simple oscillations in photosynthesis of higher plants Ogawa, Teruo Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 681, Issue 1 https://doi.org/10.1016/0005-2728(82)90283-3	journal	July 1982
The concerted reduction of the high- and low-potential chains of the bf complex by plastoquinol Kramer, David M.; Crofts, Antony R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 1 https://doi.org/10.1016/0005-2728(93)90006-2	journal	November 1993
Interactions between Sucrose Synthesis and CO2 Fixation IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation Stitt, Mark; Grosse, Heike Journal of Plant Physiology, Vol. 133, Issue 4 https://doi.org/10.1016/S0176-1617(88)80025-7	journal	November 1988
The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf Takizawa, Kenji; Cruz, Jeffrey A.; Kanazawa, Atsuko Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 10 https://doi.org/10.1016/j.bbabio.2007.07.006	journal	October 2007
Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase Kiirats, Olavi; Cruz, Jeffrey A.; Edwards, Gerald E. Functional Plant Biology, Vol. 36, Issue 11 https://doi.org/10.1071/FP09129	journal	January 2009
The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis Zhu, Xin‐Guang; Ort, Donald R.; Whitmarsh, John Journal of Experimental Botany, Vol. 55, Issue 400 https://doi.org/10.1093/jxb/erh141	journal	May 2004
Triose phosphate utilization and beyond: from photosynthesis to end product synthesis McClain, Alan M.; Sharkey, Thomas D. Journal of Experimental Botany, Vol. 70, Issue 6 https://doi.org/10.1093/jxb/erz058	journal	March 2019
Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity Taylor, Samuel H.; Long, Stephen P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730 https://doi.org/10.1098/rstb.2016.0543	journal	August 2017
Sucrose Phosphate Synthase and Sucrose Accumulation at Low Temperature Guy, Charles L.; Huber, Joan L. A.; Huber, Steven C. Plant Physiology, Vol. 100, Issue 1 https://doi.org/10.1104/pp.100.1.502	journal	September 1992
The Regulation of Rubisco Activity in Response to Variation in Temperature and Atmospheric CO 2 Partial Pressure in Sweet Potato Cen, Yan-Ping; Sage, Rowan F. Plant Physiology, Vol. 139, Issue 2 https://doi.org/10.1104/pp.105.066233	journal	September 2005
Effects of Mannose on Photosynthetic Gas Exchange in Spinach Leaf Discs Harris, Gary C.; Cheesbrough, John K.; Walker, David A. Plant Physiology, Vol. 71, Issue 1 https://doi.org/10.1104/pp.71.1.108	journal	January 1983
Simultaneous Measurement of Oscillations in Oxygen Evolution and Chlorophyll a Fluorescence in Leaf Pieces Walker, David A.; Sivak, Mirta N.; Prinsley, Roslyn T. Plant Physiology, Vol. 73, Issue 3 https://doi.org/10.1104/pp.73.3.542	journal	November 1983
Control of Photosynthetic Sucrose Synthesis by Fructose 2,6-Bisphosphate: II. Partitioning between Sucrose and Starch Stitt, Mark; Kürzel, Birgit; Heldt, Hans W. Plant Physiology, Vol. 75, Issue 3 https://doi.org/10.1104/pp.75.3.554	journal	July 1984
O ₂ -Insensitive Photosynthesis in C ₃ Plants : Its Occurrence and a Possible Explanation Sharkey, Thomas D. Plant Physiology, Vol. 78, Issue 1 https://doi.org/10.1104/pp.78.1.71	journal	May 1985
Regulation of Ribulose-1,5-Bisphosphate Carboxylase Activity in Response to Changing Partial Pressure of O 2 and Light in Phaseolus vulgaris Sharkey, Thomas D.; Seemann, Jeffrey R.; Berry, Joseph A. Plant Physiology, Vol. 81, Issue 3 https://doi.org/10.1104/pp.81.3.788	journal	July 1986
Limitation of Photosynthesis by Carbon Metabolism: I. Evidence for Excess Electron Transport Capacity in Leaves Carrying Out Photosynthesis in Saturating Light and CO Stitt, Mark Plant Physiology, Vol. 81, Issue 4 https://doi.org/10.1104/pp.81.4.1115	journal	August 1986
Limitation of Photosynthesis by Carbon Metabolism: II. O Sharkey, Thomas D.; Stitt, Mark; Heineke, Dieter Plant Physiology, Vol. 81, Issue 4 https://doi.org/10.1104/pp.81.4.1123	journal	August 1986
The Effect of Temperature on the Occurrence of O ₂ and CO ₂ Insensitive Photosynthesis in Field Grown Plants Sage, Rowan F.; Sharkey, Thomas D. Plant Physiology, Vol. 84, Issue 3 https://doi.org/10.1104/pp.84.3.658	journal	July 1987
Carbon Dioxide-Induced Oscillations in Fluorescence and Photosynthesis: Role of Thylakoid Membrane Energization in Regulation of Photosystem II Activity Peterson, Richard B.; Sivak, Mirta N.; Walker, David A. Plant Physiology, Vol. 88, Issue 4 https://doi.org/10.1104/pp.88.4.1125	journal	December 1988
Stromal Phosphate Concentration Is Low during Feedback Limited Photosynthesis Sharkey, Thomas D.; Vanderveer, Peter J. Plant Physiology, Vol. 91, Issue 2 https://doi.org/10.1104/pp.91.2.679	journal	October 1989
Changes in Activities of Enzymes of Carbon Metabolism in Leaves during Exposure of Plants to Low Temperature Holaday, A. Scott; Martindale, Wayne; Alred, Rhu Plant Physiology, Vol. 98, Issue 3 https://doi.org/10.1104/pp.98.3.1105	journal	March 1992
The temperature response of C ₃ and C ₄ photosynthesis Sage, Rowan F.; Kubien, David S. Plant, Cell & Environment, Vol. 30, Issue 9 https://doi.org/10.1111/j.1365-3040.2007.01682.x	journal	September 2007
Depletion of stromal Pi induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFO-CF1 ATP synthase: Depletion of Pi regulates the ATP synthase Takizawa, Kenji; Kanazawa, Atsuko; Kramer, David M. Plant, Cell & Environment, Vol. 31, Issue 2 https://doi.org/10.1111/j.1365-3040.2007.01753.x	journal	November 2007
Photosynthesis in vivo can be Limited by Phosphate Supply Sivak, Mirta N.; Walker, David A. New Phytologist, Vol. 102, Issue 4 https://doi.org/10.1111/j.1469-8137.1986.tb00826.x	journal	April 1986
Speedy stomata, photosynthesis and plant water use efficiency Lawson, Tracy; Vialet-Chabrand, Silvère New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15330	journal	July 2018
The rapid A/C _i response: a guide to best practices Stinziano, Joseph R.; McDermitt, Dayle K.; Lynch, Douglas J. New Phytologist, Vol. 221, Issue 2 https://doi.org/10.1111/nph.15383	journal	September 2018
Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species: Phosphorus recycling in photorespiration Ellsworth, David S.; Crous, Kristine Y.; Lambers, Hans Plant, Cell & Environment, Vol. 38, Issue 6 https://doi.org/10.1111/pce.12468	journal	January 2015
The rapid A-C _i response: photosynthesis in the phenomic era : Rapid Stinziano, Joseph R.; Morgan, Patrick B.; Lynch, Douglas J. Plant, Cell & Environment, Vol. 40, Issue 8 https://doi.org/10.1111/pce.12911	journal	March 2017
The triose phosphate utilization limitation of photosynthetic rate: Out of global models but important for leaf models Gregory, Luke M.; McClain, Alan M.; Kramer, David M. Plant, Cell & Environment, Vol. 44, Issue 10 https://doi.org/10.1111/pce.14153	journal	July 2021
Gas exchange measurements in the unsteady state Saathoff, Aaron J.; Welles, Jon Plant, Cell & Environment, Vol. 44, Issue 11 https://doi.org/10.1111/pce.14178	journal	September 2021
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aai8878	journal	November 2016
Role and Regulation of Sucrose-Phosphate Synthase in Higher Plants Huber, Steven C.; Huber, Joan L. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.arplant.47.1.431	journal	June 1996
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo Baker, Neil R. Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092759	journal	June 2008
Regulation of the Biosynthesis and Degradation of Starch Preiss, J. Annual Review of Plant Physiology, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.pp.33.060182.002243	journal	June 1982
Isoprene Suppression by CO2 Is Not Due to Triose Phosphate Utilization (TPU) Limitation Lantz, Alexandra T.; Solomon, Christine; Gog, Linus Frontiers in Forests and Global Change, Vol. 2 https://doi.org/10.3389/ffgc.2019.00008	journal	April 2019
Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection Kanazawa, Atsuko; Ostendorf, Elisabeth; Kohzuma, Kaori Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00719	journal	May 2017

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Title: Rapid CO2 changes cause oscillations in photosynthesis that implicate PSI acceptor-side limitations

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