Limitations to photosynthesis by proton motive force-induced photosystem II photodamage
Abstract
The thylakoid proton motive force (pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.
- Authors:
-
- Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Graduate Program of Cell and Molecular Biology, Michigan State University, East Lansing, United States
- Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Department of Chemistry, Michigan State University, East Lansing, United States
- Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam-Golm, Germany
- Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
- Department of Life Sciences, Imperial College London, London, United Kingdom
- Department of Horticulture, Washington State University, Pullman, United States
- Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); Biotechnology and Biological Sciences Research Council (BBSRC); Royal Society
- OSTI Identifier:
- 1328499
- Alternate Identifier(s):
- OSTI ID: 1328500; OSTI ID: 1602544
- Grant/Contract Number:
- FG02-91ER20021; BB/K002627/1
- Resource Type:
- Published Article
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Name: eLife Journal Volume: 5; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, and Kramer, David M. Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. United States: N. p., 2016.
Web. doi:10.7554/eLife.16921.
Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, & Kramer, David M. Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. United States. https://doi.org/10.7554/eLife.16921
Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, and Kramer, David M. Tue .
"Limitations to photosynthesis by proton motive force-induced photosystem II photodamage". United States. https://doi.org/10.7554/eLife.16921.
@article{osti_1328499,
title = {Limitations to photosynthesis by proton motive force-induced photosystem II photodamage},
author = {Davis, Geoffry A. and Kanazawa, Atsuko and Schöttler, Mark Aurel and Kohzuma, Kaori and Froehlich, John E. and Rutherford, A. William and Satoh-Cruz, Mio and Minhas, Deepika and Tietz, Stefanie and Dhingra, Amit and Kramer, David M.},
abstractNote = {The thylakoid proton motive force (pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.},
doi = {10.7554/eLife.16921},
journal = {eLife},
number = ,
volume = 5,
place = {United States},
year = {Tue Oct 04 00:00:00 EDT 2016},
month = {Tue Oct 04 00:00:00 EDT 2016}
}
https://doi.org/10.7554/eLife.16921
Web of Science
Works referenced in this record:
Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow
journal, February 1997
- Keren, N.; Berg, A.; van Kan, P. J. M.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 4
In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase
journal, August 2002
- Kanazawa, A.; Kramer, D. M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 20
A New Electrochemical Gradient Generator in Thylakoid Membranes of Green Algae
journal, February 1999
- Rappaport, Fabrice; Finazzi, Giovanni; Pierre, Yves
- Biochemistry, Vol. 38, Issue 7
An exploration of how the thermodynamic efficiency of bioenergetic membrane systems varies with c-subunit stoichiometry of F1F0 ATP synthases
journal, April 2014
- Silverstein, Todd P.
- Journal of Bioenergetics and Biomembranes, Vol. 46, Issue 3
Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions
journal, February 2012
- Kohzuma, K.; Dal Bosco, C.; Kanazawa, A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 9
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes
journal, June 2016
- Cruz, Jeffrey A.; Savage, Linda J.; Zegarac, Robert
- Cell Systems, Vol. 2, Issue 6
Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions
journal, July 2004
- Kramer, David M.; Avenson, Thomas J.; Edwards, Gerald E.
- Trends in Plant Science, Vol. 9, Issue 7
ATP Synthase Repression in Tobacco Restricts Photosynthetic Electron Transport, CO 2 Assimilation, and Plant Growth by Overacidification of the Thylakoid Lumen
journal, January 2011
- Rott, Markus; Martins, Nádia F.; Thiele, Wolfram
- The Plant Cell, Vol. 23, Issue 1
Singlet oxygen photosensitisation by the fluorescent probe Singlet Oxygen Sensor Green®
journal, January 2009
- Ragàs, Xavier; Jiménez-Banzo, Ana; Sánchez-García, David
- Chemical Communications, Issue 20
The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf
journal, October 2007
- Takizawa, Kenji; Cruz, Jeffrey A.; Kanazawa, Atsuko
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 10
Inactivation of the Chloroplast ATP Synthase γ Subunit Results in High Non-photochemical Fluorescence Quenching and Altered Nuclear Gene Expression in Arabidopsis thaliana
journal, October 2003
- Bosco, Cristina Dal; Lezhneva, Lina; Biehl, Alexander
- Journal of Biological Chemistry, Vol. 279, Issue 2
Contribution of Electric Field (Δψ) to Steady-State Transthylakoid Proton Motive Force ( pmf ) in Vitro and in Vivo. Control of pmf Parsing into Δψ and ΔpH by Ionic Strength †
journal, February 2001
- Cruz, Jeffrey A.; Sacksteder, Colette A.; Kanazawa, Atsuko
- Biochemistry, Vol. 40, Issue 5
The Importance of Energy Balance in Improving Photosynthetic Productivity
journal, November 2010
- Kramer, David M.; Evans, John R.
- Plant Physiology, Vol. 155, Issue 1
Zeaxanthin Protects Plant Photosynthesis by Modulating Chlorophyll Triplet Yield in Specific Light-harvesting Antenna Subunits
journal, October 2012
- Dall'Osto, Luca; Holt, Nancy E.; Kaligotla, Shanti
- Journal of Biological Chemistry, Vol. 287, Issue 50
Regulation of Photosynthetic Light Harvesting Involves Intrathylakoid Lumen pH Sensing by the PsbS Protein
journal, March 2004
- Li, Xiao-Ping; Gilmore, Adam M.; Caffarri, Stefano
- Journal of Biological Chemistry, Vol. 279, Issue 22
Effects of pH on the kinetics of redox reactions in and around the cytochromebf complex in an isolated system
journal, November 1994
- Hope, A. B.; Valente, P.; Matthews, D. B.
- Photosynthesis Research, Vol. 42, Issue 2
Singlet Oxygen-Induced Cell Death in Arabidopsis under High-Light Stress Is Controlled by OXI1 Kinase
journal, January 2016
- Shumbe, Leonard; Chevalier, Anne; Legeret, Bertrand
- Plant Physiology, Vol. 170, Issue 3
Ions channels/transporters and chloroplast regulation
journal, July 2015
- Finazzi, Giovanni; Petroutsos, Dimitris; Tomizioli, Martino
- Cell Calcium, Vol. 58, Issue 1
Regulating the proton budget of higher plant photosynthesis
journal, June 2005
- Avenson, T. J.; Cruz, J. A.; Kanazawa, A.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 27
Kinetics of the oxidation-reduction reactions of the photosystem II quinone acceptor complex, and the pathway for deactivation
journal, March 1983
- Robinson, Howard H.; Crofts, Antony R.
- FEBS Letters, Vol. 153, Issue 1
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011
- Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
- Nature, Vol. 473, Issue 7345
Flash-induced 519 nm absorption change in green algae
journal, August 1974
- Joliot, Pierre; Delosme, Rene
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 357, Issue 2
Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium
journal, February 2015
- Behrendt, Lars; Brejnrod, Asker; Schliep, Martin
- The ISME Journal, Vol. 9, Issue 9
Simple and versatile selection of Arabidopsis transformants
journal, August 2002
- M., Hadi; E., Kemper; E., Wendeler
- Plant Cell Reports, Vol. 21, Issue 2
How acidic is the lumen?
journal, May 1999
- Kramer, David M.; Sacksteder, Colette A.; Cruz, Jeffrey A.
- Photosynthesis Research, Vol. 60, Issue 2/3, p. 151-163
Photosynthetic Constraints on Fuel from Microbes
journal, March 2015
- Cotton, Charles A. R.; Douglass, Jeffrey S.; De Causmaecker, Sven
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Chlorophyll d as a major pigment
journal, October 1996
- Miyashita, Hideaki; Ikemoto, Hisato; Kurano, Norihide
- Nature, Vol. 383, Issue 6599
Rapid Regulation of Light Harvesting and Plant Fitness in the Field
journal, July 2002
- Kulheim, C.
- Science, Vol. 297, Issue 5578
Excess Copper Predisposes Photosystem II to Photoinhibition in Vivo by Outcompeting Iron and Causing Decrease in Leaf Chlorophyll
journal, June 2002
- Pätsikkä, Eija; Kairavuo, Marja; Šeršen, Frantisek
- Plant Physiology, Vol. 129, Issue 3
Singlet oxygen detection in biological systems: Uses and limitations
journal, May 2016
- Koh, Eugene; Fluhr, Robert
- Plant Signaling & Behavior, Vol. 11, Issue 7
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy
journal, August 1989
- Porra, R. J.; Thompson, W. A.; Kriedemann, P. E.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3
Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis
journal, May 2014
- Kunz, H. -H.; Gierth, M.; Herdean, A.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
A niche for cyanobacteria containing chlorophyll d
journal, February 2005
- Kühl, Michael; Chen, Min; Ralph, Peter J.
- Nature, Vol. 433, Issue 7028
Photoprotection and Other Responses of Plants to High Light Stress
journal, June 1992
- Demmig-Adams, B.; Adams, W. W.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 43, Issue 1
Cost and color of photosynthesis
journal, January 2010
- Marosvölgyi, Marcell A.; van Gorkom, Hans J.
- Photosynthesis Research, Vol. 103, Issue 2
Photoprotection of photosystems in fluctuating light intensities
journal, December 2014
- Allahverdiyeva, Yagut; Suorsa, Marjaana; Tikkanen, Mikko
- Journal of Experimental Botany, Vol. 66, Issue 9
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement
journal, May 2011
- Blankenship, R. E.; Tiede, D. M.; Barber, J.
- Science, Vol. 332, Issue 6031, p. 805-809
External electric field effects on prompt and delayed fluorescence in chloroplasts
journal, May 1981
- De Grooth, B. G.; Van Gorkom, H. J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 635, Issue 3
Energy thresholds for ATP synthesis in chloroplasts
journal, September 1982
- Hangarter, Roger P.; Good, Norman E.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 681, Issue 3
Effect of the transmembrane electric field on the photochemical and quenching properties of Photosystem II in vivo
journal, March 1976
- Diner, Bruce; Joliot, Pierre
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 423, Issue 3
Purification of Intact Chloroplasts from Arabidopsis and Spinach Leaves by Isopycnic Centrifugation
journal, September 2008
- Seigneurin-Berny, Daphné; Salvi, Daniel; Joyard, Jacques
- Current Protocols in Cell Biology, Vol. 40, Issue 1
Electrochromism: a useful probe to study algal photosynthesis
journal, July 2010
- Bailleul, Benjamin; Cardol, Pierre; Breyton, Cécile
- Photosynthesis Research, Vol. 106, Issue 1-2
Engineered and Artificial Photosynthesis: Human Ingenuity Enters the Game
journal, April 2008
- Gust, Devens; Kramer, David; Moore, Ana
- MRS Bulletin, Vol. 33, Issue 4
New Fluorescence Parameters for the Determination of Q A Redox State and Excitation Energy Fluxes
journal, January 2004
- Kramer, David M.; Johnson, Giles; Kiirats, Olavi
- Photosynthesis Research, Vol. 79, Issue 2
Plasticity in light reactions of photosynthesis for energy production and photoprotection
journal, November 2004
- Cruz, J. A.
- Journal of Experimental Botany, Vol. 56, Issue 411
The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity.
journal, March 1996
- Tyystjarvi, E.; Aro, E. M.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 5
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex
journal, January 2010
- Livingston, Aaron K.; Cruz, Jeffrey A.; Kohzuma, Kaori
- The Plant Cell, Vol. 22, Issue 1
Dissipation of the Proton Electrochemical Potential in Intact Chloroplasts (II. The pH Gradient Monitored by Cytochrome f Reduction Kinetics)
journal, January 1993
- Nishio, J. N.; Whitmarsh, J.
- Plant Physiology, Vol. 101, Issue 1
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light
journal, August 2014
- Gan, F.; Zhang, S.; Rockwell, N. C.
- Science, Vol. 345, Issue 6202
515nm absorption changes in Chlorella at short times (4–100 μs) after a flash
journal, January 1977
- Joliot, Pierre; Delosme, René; Joliot, Anne
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 459, Issue 1
Determining the limitations and regulation of photosynthetic energy transduction in leaves
journal, September 2007
- Baker, Neil R.; Harbinson, Jeremy; Kramer, David M.
- Plant, Cell & Environment, Vol. 30, Issue 9
Two genes, atpC1 and atpC2, for the γ subunit of Arabidopsis thaliana chloroplast ATP synthase
journal, April 1991
- Inohara, N.; Iwamoto, A.; Moriyama, Y.
- Journal of Biological Chemistry, Vol. 266, Issue 12
Singlet oxygen-mediated and EXECUTER-dependent signalling and acclimation of Arabidopsis thaliana exposed to light stress
journal, April 2014
- Zhang, Shengrui; Apel, Klaus; Kim, Chanhong
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1640
The cost of photoinhibition
journal, March 2011
- Raven, John A.
- Physiologia Plantarum, Vol. 142, Issue 1
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
journal, November 2007
- Takizawa, Kenji; Kanazawa, Atsuko; Kramer, David M.
- Plant, Cell & Environment, Vol. 31, Issue 2
Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis
journal, October 2013
- Cazzaniga, Stefano; Dall' Osto, Luca; Kong, Sam-Geun
- The Plant Journal, Vol. 76, Issue 4
Singlet oxygen production in photosystem II and related protection mechanism
journal, September 2008
- Krieger-Liszkay, Anja; Fufezan, Christian; Trebst, Achim
- Photosynthesis Research, Vol. 98, Issue 1-3
Photoinhibition: molecular mechanisms and physiological significance
journal, March 2011
- Keren, Nir; Krieger-Liszkay, Anja
- Physiologia Plantarum, Vol. 142, Issue 1
Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery
journal, August 2014
- Nishiyama, Yoshitaka; Murata, Norio
- Applied Microbiology and Biotechnology, Vol. 98, Issue 21
Light-Induced Acclimation of the Arabidopsis chlorina1 Mutant to Singlet Oxygen
journal, April 2013
- Ramel, Fanny; Ksas, Brigitte; Akkari, Elsy
- The Plant Cell, Vol. 25, Issue 4
Proton-powered turbine of a plant motor
journal, May 2000
- Seelert, Holger; Poetsch, Ansgar; Dencher, Norbert A.
- Nature, Vol. 405, Issue 6785
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
Impairment of the Photorespiratory Pathway Accelerates Photoinhibition of Photosystem II by Suppression of Repair But Not Acceleration of Damage Processes in Arabidopsis
journal, March 2007
- Takahashi, Shunichi; Bauwe, Hermann; Badger, Murray
- Plant Physiology, Vol. 144, Issue 1
What governs the reaction center excitation wavelength of photosystems I and II?
journal, July 2009
- Milo, Ron
- Photosynthesis Research, Vol. 101, Issue 1
Detailed Balance Limit of Efficiency of p‐n Junction Solar Cells
journal, March 1961
- Shockley, William; Queisser, Hans J.
- Journal of Applied Physics, Vol. 32, Issue 3, p. 510-519
Modulation of energy-dependent quenching of excitons in antennae of higher plants
journal, April 2004
- Avenson, T. J.; Cruz, J. A.; Kramer, D. M.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 15
Singlet Oxygen Production by PSII Under Light Stress: Mechanism, Detection and the Protective role of β-Carotene
journal, March 2014
- Telfer, Alison
- Plant and Cell Physiology, Vol. 55, Issue 7
Ion antiport accelerates photosynthetic acclimation in fluctuating light environments
journal, November 2014
- Armbruster, Ute; Carrillo, L. Ruby; Venema, Kees
- Nature Communications, Vol. 5, Issue 1
A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution
journal, April 1995
- Johnson, Giles N.; Rutherford, A. William; Krieger, Anja
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1229, Issue 2
Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O 2
journal, January 2012
- Rutherford, A. William; Osyczka, Artur; Rappaport, Fabrice
- FEBS Letters, Vol. 586, Issue 5
The role of calcium in the pH-dependent control of Photosystem II
journal, August 1993
- Krieger, Anja; Weis, Engelbert
- Photosynthesis Research, Vol. 37, Issue 2
Electroluminescence
journal, May 1996
- van Gorkom, Hans J.
- Photosynthesis Research, Vol. 48, Issue 1-2
Regulation of cyclic electron flow in C3 plants: differential effects of limiting photosynthesis at ribulose-1,5-bisphosphate carboxylase/oxygenase and glyceraldehyde-3-phosphate dehydrogenase: Regulation of cyclic electron flow
journal, June 2010
- Livingston, Aaron K.; Kanazawa, Atsuko; Cruz, Jeffrey A.
- Plant, Cell & Environment, Vol. 33, Issue 11
Influence of Herbicide Binding on the Redox Potential of the Quinone Acceptor in Photosystem II: Relevance to Photodamage and Phytotoxicity †
journal, December 1998
- Krieger-Liszkay, Anja; Rutherford, A. William
- Biochemistry, Vol. 37, Issue 50
An electroluminescence study of stabilization reactions in the oxygen-evolving complex of Photosystem II
journal, January 1991
- Vos, Marten H.; van Gorkom, Hans J.; van Leeuwen, Peter J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1056, Issue 1