Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection
Abstract
In wild type plants, decreasing CO2 lowers the activity of the chloroplast ATP synthase, slowing proton efflux from the thylakoid lumen resulting in buildup of thylakoid proton motive force (pmf). The resulting acidification of the lumen regulates both light harvesting, via the qE mechanism, and photosynthetic electron transfer through the cytochrome b6f complex. Here in this paper, we show that the cfq mutant of Arabidopsis, harboring single point mutation in its γ-subunit of the chloroplast ATP synthase, increases the specific activity of the ATP synthase and disables its down-regulation under low CO2. The increased thylakoid proton conductivity (gH+) in cfq results in decreased pmf and lumen acidification, preventing full activation of qE and more rapid electron transfer through the b6f complex, particularly under low CO2 and fluctuating light. These conditions favor the accumulation of electrons on the acceptor side of PSI, and result in severe loss of PSI activity. Comparing the current results with previous work on the pgr5 mutant suggests a general mechanism where increased PSI photodamage in both mutants is caused by loss of pmf, rather than inhibition of CEF per se. Overall, our results support a critical role for ATP synthase regulation in maintaining photosynthetic control ofmore »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemistry
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Cell and Molecular Biology
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. Biochemistry and Molecular Biology
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1368188
- Grant/Contract Number:
- FG02-91ER20021
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ATP synthase; proton motive force; pmf, photoprotection; PSI; PSII
Citation Formats
Kanazawa, Atsuko, Ostendorf, Elisabeth, Kohzuma, Kaori, Hoh, Donghee, Strand, Deserah D., Sato-Cruz, Mio, Savage, Linda, Cruz, Jeffrey A., Fisher, Nicholas, Froehlich, John E., and Kramer, David M. Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection. United States: N. p., 2017.
Web. doi:10.3389/fpls.2017.00719.
Kanazawa, Atsuko, Ostendorf, Elisabeth, Kohzuma, Kaori, Hoh, Donghee, Strand, Deserah D., Sato-Cruz, Mio, Savage, Linda, Cruz, Jeffrey A., Fisher, Nicholas, Froehlich, John E., & Kramer, David M. Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection. United States. https://doi.org/10.3389/fpls.2017.00719
Kanazawa, Atsuko, Ostendorf, Elisabeth, Kohzuma, Kaori, Hoh, Donghee, Strand, Deserah D., Sato-Cruz, Mio, Savage, Linda, Cruz, Jeffrey A., Fisher, Nicholas, Froehlich, John E., and Kramer, David M. Wed .
"Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection". United States. https://doi.org/10.3389/fpls.2017.00719. https://www.osti.gov/servlets/purl/1368188.
@article{osti_1368188,
title = {Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection},
author = {Kanazawa, Atsuko and Ostendorf, Elisabeth and Kohzuma, Kaori and Hoh, Donghee and Strand, Deserah D. and Sato-Cruz, Mio and Savage, Linda and Cruz, Jeffrey A. and Fisher, Nicholas and Froehlich, John E. and Kramer, David M.},
abstractNote = {In wild type plants, decreasing CO2 lowers the activity of the chloroplast ATP synthase, slowing proton efflux from the thylakoid lumen resulting in buildup of thylakoid proton motive force (pmf). The resulting acidification of the lumen regulates both light harvesting, via the qE mechanism, and photosynthetic electron transfer through the cytochrome b6f complex. Here in this paper, we show that the cfq mutant of Arabidopsis, harboring single point mutation in its γ-subunit of the chloroplast ATP synthase, increases the specific activity of the ATP synthase and disables its down-regulation under low CO2. The increased thylakoid proton conductivity (gH+) in cfq results in decreased pmf and lumen acidification, preventing full activation of qE and more rapid electron transfer through the b6f complex, particularly under low CO2 and fluctuating light. These conditions favor the accumulation of electrons on the acceptor side of PSI, and result in severe loss of PSI activity. Comparing the current results with previous work on the pgr5 mutant suggests a general mechanism where increased PSI photodamage in both mutants is caused by loss of pmf, rather than inhibition of CEF per se. Overall, our results support a critical role for ATP synthase regulation in maintaining photosynthetic control of electron transfer to prevent photodamage.},
doi = {10.3389/fpls.2017.00719},
journal = {Frontiers in Plant Science},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {5}
}
Web of Science
Works referenced in this record:
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
PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis
journal, August 2002
- Munekage, Yuri; Hojo, Masaya; Meurer, Jörg
- Cell, Vol. 110, Issue 3
Superoxide and Singlet Oxygen Produced within the Thylakoid Membranes Both Cause Photosystem I Photoinhibition
journal, March 2016
- Takagi, Daisuke; Takumi, Shigeo; Hashiguchi, Masaki
- Plant Physiology, Vol. 171, Issue 3
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
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
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
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes
journal, June 2016
- Cruz, Jeffrey A.; Savage, Linda J.; Zegarac, Robert
- Cell Systems, Vol. 2, Issue 6
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
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
Multi-level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance
journal, August 2016
- Carrillo, L. Ruby; Froehlich, John E.; Cruz, Jeffrey A.
- The Plant Journal, Vol. 87, Issue 6
PROTON GRADIENT REGULATION5 Is Essential for Proper Acclimation of Arabidopsis Photosystem I to Naturally and Artificially Fluctuating Light Conditions
journal, July 2012
- Suorsa, Marjaana; Järvi, Sari; Grieco, Michele
- The Plant Cell, Vol. 24, Issue 7
Non-Photochemical Quenching. A Response to Excess Light Energy
journal, April 2001
- Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K.
- Plant Physiology, Vol. 125, Issue 4
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
PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition
journal, November 2002
- Li, X. -P.; Muller-Moule, P.; Gilmore, A. M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
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
Mass Spectrometric Sequencing of Proteins from Silver-Stained Polyacrylamide Gels
journal, January 1996
- Shevchenko, Andrej; Wilm, Matthias; Vorm, Ole
- Analytical Chemistry, Vol. 68, Issue 5
In Situ Regulation of Chloroplast Coupling Factor Activity
journal, June 1992
- Ort, D. R.; Oxborough, K.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 43, Issue 1
The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged
journal, December 2000
- Sacksteder, C. A.; Kanazawa, A.; Jacoby, M. E.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 26
An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm
journal, January 1994
- Klughammer, Christof; Schreiber, Ulrich
- Planta, Vol. 192, Issue 2
Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants
journal, August 1989
- Kramer, David M.; Crofts, Antony R.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 976, 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
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
Light- and Metabolism-related Regulation of the Chloroplast ATP Synthase Has Distinct Mechanisms and Functions
journal, March 2013
- Kohzuma, Kaori; Dal Bosco, Cristina; Meurer, Jörg
- Journal of Biological Chemistry, Vol. 288, Issue 18
Regulation of coupling factor in field-grown sunflower: A Redox model relating coupling factor activity to the activities of other thioredoxin-dependent chloroplast enzymes
journal, December 1990
- Kramer, David M.; Wise, Robert R.; Frederick, James R.
- Photosynthesis Research, Vol. 26, Issue 3
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
The long-term responses of the photosynthetic proton circuit to drought
journal, March 2009
- Kohzuma, Kaori; Cruz, Jeffrey A.; Akashi, Kinya
- Plant, Cell & Environment, Vol. 32, Issue 3
Integrating the proton circuit into photosynthesis: progress and challenges
journal, January 2005
- Avenson, T. J.; Kanazawa, A.; Cruz, J. A.
- Plant, Cell and Environment, Vol. 28, Issue 1
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
Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control
journal, May 2014
- Schöttler, Mark A.; Tóth, Szilvia Z.
- Frontiers in Plant Science, Vol. 5
Photoprotection of photosystems in fluctuating light intensities
journal, December 2014
- Allahverdiyeva, Yagut; Suorsa, Marjaana; Tikkanen, Mikko
- Journal of Experimental Botany, Vol. 66, Issue 9
Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage
journal, January 2014
- Tikkanen, Mikko; Mekala, Nageswara Rao; Aro, Eva-Mari
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 1
Co-regulation of dark and light reactions in three biochemical subtypes of C4 species
journal, June 2010
- Kiirats, Olavi; Kramer, David M.; Edwards, Gerald E.
- Photosynthesis Research, Vol. 105, Issue 2
Moderate Photoinhibition of Photosystem II Protects Photosystem I from Photodamage at Chilling Stress in Tobacco Leaves
journal, February 2016
- Huang, Wei; Yang, Ying-Jie; Hu, Hong
- Frontiers in Plant Science, Vol. 7
An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm
journal, January 1994
- Klughammer, Christof; Schreiber, Ulrich
- Planta, Vol. 192, Issue 2
Co-incorporation of manure and inorganic fertilizer improves leaf physiological traits, rice production and soil functionality in a paddy field
journal, May 2021
- Iqbal, Anas; He, Liang; Ali, Izhar
- Scientific Reports, Vol. 11, Issue 1
Works referencing / citing this record:
Enhanced Photophosphorylation of a Chloroplast-Entrapping Long-Lived Photoacid
journal, September 2017
- Xu, Youqian; Fei, Jinbo; Li, Guangle
- Angewandte Chemie International Edition, Vol. 56, Issue 42
Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system
journal, November 2018
- Nikkanen, Lauri; Toivola, Jouni; Trotta, Andrea
- Plant Direct, Vol. 2, Issue 11
Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts
journal, October 2017
- Gómez, Rodrigo; Carrillo, Néstor; Morelli, María P.
- Photosynthesis Research, Vol. 136, Issue 2
In vivo regulation of thylakoid proton motive force in immature leaves
journal, July 2018
- Huang, Wei; Suorsa, Marjaana; Zhang, Shi-Bao
- Photosynthesis Research, Vol. 138, Issue 2
Genetic characterization of a flap1 null mutation in Arabidopsis npq4 and pgr5 plants suggests that the regulatory role of FLAP1 involves the control of proton homeostasis in chloroplasts
journal, November 2018
- Trinh, Mai Duy Luu; Sato, Ryoichi; Masuda, Shinji
- Photosynthesis Research, Vol. 139, Issue 1-3
Overexpression of the Rieske FeS protein of the Cytochrome b6f complex increases C4 photosynthesis in Setaria viridis
journal, August 2019
- Ermakova, Maria; Lopez-Calcagno, Patricia E.; Raines, Christine A.
- Communications Biology, Vol. 2, Issue 1
PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I
journal, July 2018
- Takagi, Daisuke; Miyake, Chikahiro
- Physiologia Plantarum, Vol. 164, Issue 3
Cyclic Electron Flow around Photosystem I Promotes ATP Synthesis Possibly Helping the Rapid Repair of Photodamaged Photosystem II at Low Light
journal, February 2018
- Huang, Wei; Yang, Ying-Jie; Zhang, Shi-Bao
- Frontiers in Plant Science, Vol. 9
Moderate Photoinhibition of Photosystem II Significantly Affects Linear Electron Flow in the Shade-Demanding Plant Panax notoginseng
journal, May 2018
- Huang, Wei; Zhang, Shi-Bao; Liu, Tao
- Frontiers in Plant Science, Vol. 9
Dehydration Stress Memory: Gene Networks Linked to Physiological Responses During Repeated Stresses of Zea mays
journal, July 2018
- Virlouvet, Laetitia; Avenson, Thomas J.; Du, Qian
- Frontiers in Plant Science, Vol. 9
Enhanced Photophosphorylation of a Chloroplast-Entrapping Long-Lived Photoacid
journal, September 2017
- Xu, Youqian; Fei, Jinbo; Li, Guangle
- Angewandte Chemie, Vol. 129, Issue 42