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Title: 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 » electron transfer to prevent photodamage.« less

Authors:
 [1];  [2];  [2];  [3];  [2];  [2];  [2];  [4];  [2];  [4];  [4]
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  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemistry
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  3. 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
  4. 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.
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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
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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.
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@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}
}
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https://doi.org/10.3389/fpls.2017.00719
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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
  • DOI: 10.1073/pnas.182427499

PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis
journal, August 2002

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
  • DOI: 10.1104/pp.16.00246

New Fluorescence Parameters for the Determination of Q A Redox State and Excitation Energy Fluxes
journal, January 2004

COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949

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
  • DOI: 10.1105/tpc.109.071084

Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes
journal, June 2016

Determining the limitations and regulation of photosynthetic energy transduction in leaves
journal, September 2007

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
  • DOI: 10.1104/pp.125.4.1558

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
  • DOI: 10.1016/j.bbabio.2007.07.006

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
  • DOI: 10.1074/jbc.M308435200

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
  • DOI: 10.1073/pnas.232447699

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

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
  • DOI: 10.1021/ac950914h

In Situ Regulation of Chloroplast Coupling Factor Activity
journal, June 1992

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
  • DOI: 10.1073/pnas.97.26.14283

Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants
journal, August 1989

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
  • DOI: 10.1073/pnas.0503952102

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

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
  • DOI: 10.1074/jbc.M113.453225

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
  • DOI: 10.1007/BF00033134

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
  • DOI: 10.1073/pnas.0401269101

The long-term responses of the photosynthetic proton circuit to drought
journal, March 2009

Integrating the proton circuit into photosynthesis: progress and challenges
journal, January 2005

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

Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control
journal, May 2014

Photoprotection of photosystems in fluctuating light intensities
journal, December 2014

  • Allahverdiyeva, Yagut; Suorsa, Marjaana; Tikkanen, Mikko
  • Journal of Experimental Botany, Vol. 66, Issue 9
  • DOI: 10.1093/jxb/eru463

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
  • DOI: 10.1016/j.bbabio.2013.10.001

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
  • DOI: 10.1007/s11120-010-9561-9

Moderate Photoinhibition of Photosystem II Protects Photosystem I from Photodamage at Chilling Stress in Tobacco Leaves
journal, February 2016

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    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
    • DOI: 10.1002/anie.201706368

    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
    • DOI: 10.1002/pld3.93

    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
    • DOI: 10.1007/s11120-017-0449-9

    In vivo regulation of thylakoid proton motive force in immature leaves
    journal, July 2018

    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
    • DOI: 10.1038/s42003-019-0561-9

    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
    • DOI: 10.1111/ppl.12723

    Cyclic Electron Flow around Photosystem I Promotes ATP Synthesis Possibly Helping the Rapid Repair of Photodamaged Photosystem II at Low Light
    journal, February 2018

    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
    • DOI: 10.3389/fpls.2018.01058

    Enhanced Photophosphorylation of a Chloroplast-Entrapping Long-Lived Photoacid
    journal, September 2017

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