Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection
Abstract
In photosynthetic thylakoid membranes the proton motive force (pmf) not only drives ATP synthesis, in addition it is central to controlling and regulating energy conversion. As a consequence, dynamic fine-tuning of the two pmf components, electrical (Δψ) and chemical (ΔpH), is an essential element for adjusting photosynthetic light reactions to changing environmental conditions. Good evidence exists that the Δψ/ΔpH partitioning is controlled by thylakoid potassium and chloride ion transporters and channels. However, a detailed mechanistic understanding of how these thylakoid ion transporter/channels control pmf partitioning is lacking. In this work, we combined functional measurements on potassium and chloride ion transporter and channel loss-of-function mutants with extended mathematical simulations of photosynthetic light reactions in thylakoid membranes to obtain detailed kinetic insights into the complex interrelationship between membrane energization and ion fluxes across thylakoid membranes. The data reveal that potassium and chloride fluxes in the thylakoid lumen determined by the K+/H+ antiporter KEA3 and the voltage-gated Cl– channel VCCN1/Best1 have distinct kinetic responses that lead to characteristic and light-intensity-dependent Δψ/ΔpH oscillations. These oscillations fine-tune photoprotective mechanisms and electron transport which are particularly important during the first minutes of illumination and under fluctuating light conditions. By employing the predictive power of the model,more »
- Authors:
-
- Washington State Univ., Pullman, WA (United States); Univ. of Washington, Seattle, WA (United States)
- Washington State Univ., Pullman, WA (United States)
- Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Washington State Univ., Pullman, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDA; National Science Foundation (NSF)
- OSTI Identifier:
- 1798328
- Grant/Contract Number:
- SC0017160; MCB-1616982; 1005351; 0119; IOS-1847382; IOS-1847193; SR- 2016049
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Plants
- Additional Journal Information:
- Journal Volume: 7; Journal ID: ISSN 2055-0278
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Li, Meng, Svoboda, Vaclav, Davis, Geoffry, Kramer, David, Kunz, Hans-Henning, and Kirchhoff, Helmut. Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection. United States: N. p., 2021.
Web. doi:10.1038/s41477-021-00947-5.
Li, Meng, Svoboda, Vaclav, Davis, Geoffry, Kramer, David, Kunz, Hans-Henning, & Kirchhoff, Helmut. Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection. United States. https://doi.org/10.1038/s41477-021-00947-5
Li, Meng, Svoboda, Vaclav, Davis, Geoffry, Kramer, David, Kunz, Hans-Henning, and Kirchhoff, Helmut. Thu .
"Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection". United States. https://doi.org/10.1038/s41477-021-00947-5. https://www.osti.gov/servlets/purl/1798328.
@article{osti_1798328,
title = {Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection},
author = {Li, Meng and Svoboda, Vaclav and Davis, Geoffry and Kramer, David and Kunz, Hans-Henning and Kirchhoff, Helmut},
abstractNote = {In photosynthetic thylakoid membranes the proton motive force (pmf) not only drives ATP synthesis, in addition it is central to controlling and regulating energy conversion. As a consequence, dynamic fine-tuning of the two pmf components, electrical (Δψ) and chemical (ΔpH), is an essential element for adjusting photosynthetic light reactions to changing environmental conditions. Good evidence exists that the Δψ/ΔpH partitioning is controlled by thylakoid potassium and chloride ion transporters and channels. However, a detailed mechanistic understanding of how these thylakoid ion transporter/channels control pmf partitioning is lacking. In this work, we combined functional measurements on potassium and chloride ion transporter and channel loss-of-function mutants with extended mathematical simulations of photosynthetic light reactions in thylakoid membranes to obtain detailed kinetic insights into the complex interrelationship between membrane energization and ion fluxes across thylakoid membranes. The data reveal that potassium and chloride fluxes in the thylakoid lumen determined by the K+/H+ antiporter KEA3 and the voltage-gated Cl– channel VCCN1/Best1 have distinct kinetic responses that lead to characteristic and light-intensity-dependent Δψ/ΔpH oscillations. These oscillations fine-tune photoprotective mechanisms and electron transport which are particularly important during the first minutes of illumination and under fluctuating light conditions. By employing the predictive power of the model, we unravelled the functional consequences of changes in KEA3 and VCCN1 abundance and regulatory/enzymatic parameters on membrane energization and photoprotection.},
doi = {10.1038/s41477-021-00947-5},
journal = {Nature Plants},
number = ,
volume = 7,
place = {United States},
year = {Thu Jun 17 00:00:00 EDT 2021},
month = {Thu Jun 17 00:00:00 EDT 2021}
}
Works referenced in this record:
A bestrophin-like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis : Involvement of AtBest in fine-tuning of photosynthesis
journal, April 2016
- Duan, Zhikun; Kong, Fanna; Zhang, Lin
- Journal of Integrative Plant Biology, Vol. 58, Issue 10
Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves
journal, January 1984
- Robinson, Simon P.; Downton, W. John S.
- Archives of Biochemistry and Biophysics, Vol. 228, Issue 1
The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II
journal, January 2012
- Jahns, Peter; Holzwarth, Alfred R.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
Possible functions of chains of catalysts II
journal, September 1962
- Williams, R. J. P.
- Journal of Theoretical Biology, Vol. 3, Issue 2
Compartmentalization of the protein repair machinery in photosynthetic membranes
journal, October 2014
- Puthiyaveetil, S.; Tsabari, O.; Lowry, T.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
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
Ion channels in the thylakoid membrane (a patch-clamp study)
journal, June 1993
- Enz, Christoph; Steinkamp, Thomas; Wagner, Richard
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1143, Issue 1
Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods
journal, March 1979
- Witt, H. T.
- Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 505, Issue 3-4
Determination of DeltapH in Chloroplasts. 2. Fluorescent Amines as a Probe for the Determination of DeltapH in Chloroplasts
journal, January 1972
- Schuldiner, Shimon; Rottenberg, Hagai; Avron, Mordhay
- European Journal of Biochemistry, Vol. 25, Issue 1
Ions channels/transporters and chloroplast regulation
journal, July 2015
- Finazzi, Giovanni; Petroutsos, Dimitris; Tomizioli, Martino
- Cell Calcium, Vol. 58, Issue 1
Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH
journal, August 2017
- Davis, Geoffry A.; Rutherford, A. William; Kramer, David M.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730
Global spectroscopic analysis to study the regulation of the photosynthetic proton motive force: A critical reappraisal
journal, September 2018
- Allorent, Guillaume; Byrdin, Martin; Carraretto, Luca
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 9
Molecular mechanisms involved in plant photoprotection
journal, April 2018
- Pinnola, Alberta; Bassi, Roberto
- Biochemical Society Transactions, Vol. 46, Issue 2
The structural and functional domains of plant thylakoid membranes
journal, November 2018
- Koochak, Haniyeh; Puthiyaveetil, Sujith; Mullendore, Daniel L.
- The Plant Journal, Vol. 97, 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
Balancing the central roles of the thylakoid proton gradient
journal, January 2003
- Kramer, David M.; Cruz, Jeffrey A.; Kanazawa, Atsuko
- Trends in Plant Science, Vol. 8, Issue 1
A voltage-dependent chloride channel fine-tunes photosynthesis in plants
journal, May 2016
- Herdean, Andrei; Teardo, Enrico; Nilsson, Anders K.
- Nature Communications, Vol. 7, Issue 1
An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis
journal, June 2017
- Spetea, Cornelia; Herdean, Andrei; Allorent, Guillaume
- Physiologia Plantarum, Vol. 161, Issue 1
Photosynthesis in Arabidopsis Is Unaffected by the Function of the Vacuolar K + Channel TPK3
journal, May 2019
- Höhner, Ricarda; Galvis, Viviana Correa; Strand, Deserah D.
- Plant Physiology, Vol. 180, Issue 3
Sensing and Responding to Excess Light
journal, June 2009
- Li, Zhirong; Wakao, Setsuko; Fischer, Beat B.
- Annual Review of Plant Biology, Vol. 60, Issue 1
Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes
journal, April 2015
- Tietz, Stefanie; Puthiyaveetil, Sujith; Enlow, Heather M.
- Journal of Biological Chemistry, Vol. 290, Issue 22
K+ and Cl− channels/transporters independently fine-tune photosynthesis in plants
journal, June 2019
- Dukic, Emilija; Herdean, Andrei; Cheregi, Otilia
- Scientific Reports, Vol. 9, Issue 1
Kinetics of Proton-Transport-Coupled ATP Synthesis in Chloroplasts. Activation of the ATPase by an Artificially Generated ΔpH and Δψ
journal, July 1984
- Gräber, Peter; Junesch, Ulrike; Schatz, Güther H.
- Berichte der Bunsengesellschaft für physikalische Chemie, Vol. 88, Issue 7
A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant
journal, December 1988
- Schönknecht, G.; Hedrich, R.; Junge, W.
- Nature, Vol. 336, Issue 6199
Electrochromism: a useful probe to study algal photosynthesis
journal, July 2010
- Bailleul, Benjamin; Cardol, Pierre; Breyton, Cécile
- Photosynthesis Research, Vol. 106, Issue 1-2
Voltage-dependent gating of SV channel TPC1 confers vacuole excitability
journal, June 2019
- Jaślan, Dawid; Dreyer, Ingo; Lu, Jinping
- Nature Communications, Vol. 10, Issue 1
Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity
journal, August 2011
- Johnson, Matthew P.; Zia, Ahmad; Ruban, Alexander V.
- Planta, Vol. 235, Issue 1
Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism
journal, July 1961
- Mitchell, Peter
- Nature, Vol. 191, Issue 4784
Light-triggered electrical events in the thylakoid membrane of plant chloroplasts
journal, March 1999
- Bulychev, Alexander A.; Vredenberg, Wim J.
- Physiologia Plantarum, Vol. 105, Issue 3
Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively
journal, July 2007
- Marmagne, A.; Vinauger-Douard, M.; Monachello, D.
- Journal of Experimental Botany, Vol. 58, Issue 12
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
Functional characterization of protonantiport regulation in the thylakoid membrane
journal, March 2021
- Uflewski, Michał; Mielke, Sarah; Correa Galvis, Viviana
- Plant Physiology
Light harvesting control in plants
journal, June 2018
- Ruban, Alexander V.
- FEBS Letters, Vol. 592, Issue 18
The Arabidopsis Thylakoid Chloride Channel AtCLCe Functions in Chloride Homeostasis and Regulation of Photosynthetic Electron Transport
journal, February 2016
- Herdean, Andrei; Nziengui, Hugues; Zsiros, Ottó
- Frontiers in Plant Science, Vol. 7
The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light
journal, June 2017
- Armbruster, Ute; Correa Galvis, Viviana; Kunz, Hans-Henning
- Current Opinion in Plant Biology, Vol. 37
KTN (RCK) Domains Regulate K+ Channels and Transporters by Controlling the Dimer-Hinge Conformation
journal, June 2009
- Roosild, Tarmo P.; Castronovo, Samantha; Miller, Samantha
- Structure, Vol. 17, Issue 6
Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM
journal, December 2019
- Schneider, Dominik; Lopez, Laura S.; Li, Meng
- Plant Methods, Vol. 15, 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
Fine‐tuned regulation of the K + /H + antiporter KEA 3 is required to optimize photosynthesis during induction
journal, February 2017
- Wang, Caijuan; Yamamoto, Hiroshi; Narumiya, Fumika
- The Plant Journal, Vol. 89, Issue 3
A Thylakoid-Located Two-Pore K + Channel Controls Photosynthetic Light Utilization in Plants
journal, September 2013
- Carraretto, Luca; Formentin, Elide; Teardo, Enrico
- Science, Vol. 342, Issue 6154
A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments
journal, March 2020
- Tang, Ren-Jie; Zhao, Fu-Geng; Yang, Yang
- Nature Plants, Vol. 6, Issue 4
Modification of Activity of the Thylakoid H + /K + Antiporter KEA3 Disturbs ∆pH-Dependent Regulation of Photosynthesis
journal, August 2019
- Wang, Caijuan; Shikanai, Toshiharu
- Plant Physiology, Vol. 181, Issue 2
Control of electron flow in intact chloroplasts by the intrathylakoid pH, not by the phosphorylation potential
journal, September 1979
- Kobayashi, Yoshichika; Inoue, Yorinao; Shibata, Kazuo
- Planta, Vol. 146, Issue 4
Possible functions of chains of catalysts
journal, January 1961
- Williams, R. J. P.
- Journal of Theoretical Biology, Vol. 1, Issue 1
H + Transport by K + EXCHANGE ANTIPORTER3 Promotes Photosynthesis and Growth in Chloroplast ATP Synthase Mutants
journal, February 2020
- Correa Galvis, Viviana; Strand, Deserah D.; Messer, Michaela
- Plant Physiology, Vol. 182, Issue 4
Continuous ECS-indicated recording of the proton-motive charge flux in leaves
journal, July 2013
- Klughammer, Christof; Siebke, Katharina; Schreiber, Ulrich
- Photosynthesis Research, Vol. 117, Issue 1-3
pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas
journal, April 2019
- Tian, Lijin; Nawrocki, Wojciech J.; Liu, Xin
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
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
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
Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis
journal, April 2010
- Nilkens, Manuela; Kress, Eugen; Lambrev, Petar
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 4
pH changes in the inner phase of the thylakoids during photosynthesis
journal, March 1969
- Rumberg, B.; Siggel, U.
- Die Naturwissenschaften, Vol. 56, Issue 3
Properties of the Isolated Intact Chloroplast at Cytoplasmic K + Concentrations : I. Light-Induced Cation Uptake into Intact Chloroplasts is Driven by an Electrical Potential Difference
journal, September 1983
- Demmig, Barbara; Gimmler, Hartmut
- Plant Physiology, Vol. 73, Issue 1