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Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection

Journal Article · · Nature Plants (Online)
 [1];  [2];  [3];  [3];  [2];  [2]
  1. Washington State Univ., Pullman, WA (United States); Univ. of Washington, Seattle, WA (United States); Washington State University
  2. Washington State Univ., Pullman, WA (United States)
  3. Michigan State Univ., East Lansing, MI (United States)
+ Show Author Affiliations
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.
Research Organization:
Washington State Univ., Pullman, WA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDA; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0017160
OSTI ID:
1798328
Journal Information:
Nature Plants (Online), Journal Name: Nature Plants (Online) Vol. 7; ISSN 2055-0278
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (53)

Light harvesting control in plants journal June 2018
Kinetics of Proton-Transport-Coupled ATP Synthesis in Chloroplasts. Activation of the ATPase by an Artificially Generated ΔpH and Δψ journal July 1984
Control of electron flow in intact chloroplasts by the intrathylakoid pH, not by the phosphorylation potential journal September 1979
pH changes in the inner phase of the thylakoids during photosynthesis journal March 1969
Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity journal August 2011
Electrochromism: a useful probe to study algal photosynthesis journal July 2010
Continuous ECS-indicated recording of the proton-motive charge flux in leaves journal July 2013
Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves journal January 1984
Ion channels in the thylakoid membrane (a patch-clamp study) journal June 1993
Possible functions of chains of catalysts journal January 1961
Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods journal March 1979
Possible functions of chains of catalysts II journal September 1962
Balancing the central roles of the thylakoid proton gradient journal January 2003
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
The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II journal January 2012
Global spectroscopic analysis to study the regulation of the photosynthetic proton motive force: A critical reappraisal journal September 2018
Ions channels/transporters and chloroplast regulation journal July 2015
The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light journal June 2017
KTN (RCK) Domains Regulate K+ Channels and Transporters by Controlling the Dimer-Hinge Conformation journal June 2009
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
New Fluorescence Parameters for the Determination of Q A Redox State and Excitation Energy Fluxes journal January 2004
Light-triggered electrical events in the thylakoid membrane of plant chloroplasts journal March 1999
Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism journal July 1961
A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant journal December 1988
A voltage-dependent chloride channel fine-tunes photosynthesis in plants journal May 2016
Ion antiport accelerates photosynthetic acclimation in fluctuating light environments journal November 2014
Voltage-dependent gating of SV channel TPC1 confers vacuole excitability journal June 2019
A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments journal March 2020
K+ and Cl− channels/transporters independently fine-tune photosynthesis in plants journal June 2019
Molecular mechanisms involved in plant photoprotection journal April 2018
Modulation of energy-dependent quenching of excitons in antennae of higher plants journal April 2004
Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis journal May 2014
Compartmentalization of the protein repair machinery in photosynthetic membranes journal October 2014
pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas journal April 2019
Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes journal April 2015
Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively journal July 2007
Functional characterization of protonantiport regulation in the thylakoid membrane journal March 2021
Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH
  • Davis, Geoffry A.; Rutherford, A. William; Kramer, David M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730 https://doi.org/10.1098/rstb.2016.0381
journal August 2017
Photosynthesis in Arabidopsis Is Unaffected by the Function of the Vacuolar K + Channel TPK3 journal May 2019
Modification of Activity of the Thylakoid H + /K + Antiporter KEA3 Disturbs ∆pH-Dependent Regulation of Photosynthesis journal August 2019
H + Transport by K + EXCHANGE ANTIPORTER3 Promotes Photosynthesis and Growth in Chloroplast ATP Synthase Mutants journal February 2020
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
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
Determination of DeltapH in Chloroplasts. 2. Fluorescent Amines as a Probe for the Determination of DeltapH in Chloroplasts journal January 1972
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
An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis journal June 2017
Fine‐tuned regulation of the K + /H + antiporter KEA 3 is required to optimize photosynthesis during induction journal February 2017
The structural and functional domains of plant thylakoid membranes journal November 2018
A Thylakoid-Located Two-Pore K + Channel Controls Photosynthetic Light Utilization in Plants journal September 2013
Sensing and Responding to Excess Light journal June 2009
Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM journal December 2019
The Arabidopsis Thylakoid Chloride Channel AtCLCe Functions in Chloride Homeostasis and Regulation of Photosynthetic Electron Transport journal February 2016
Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM collection January 2019

Cited By (13)

Additional file 10 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 12 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 13 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 14 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 1 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 2 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 3 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 4 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 5 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 6 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 7 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 8 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022
Additional file 9 of Overdominant expression of related genes of ion homeostasis improves K+ content advantage in hybrid tobacco leaves dataset January 2022

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59 BASIC BIOLOGICAL SCIENCES