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Title: 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 Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.13226· OSTI ID:1437167
 [1];  [1];  [2];  [2];  [1]
  1. Michigan State Univ., East Lansing, MI (United States). Biochemistry & Molecular Biology; Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.

Summary The chloroplast ATP synthase is known to be regulated by redox modulation of a disulfide bridge on the γ‐subunit through the ferredoxin–thioredoxin regulatory system. We show that a second enzyme, the recently identified chloroplast NADPH thioredoxin reductase C ( NTRC ), plays a role specifically at low irradiance. Arabidopsis mutants lacking NTRC ( ntrc ) displayed a striking photosynthetic phenotype in which feedback regulation of the light reactions was strongly activated at low light, but returned to wild‐type levels as irradiance was increased. This effect was caused by an altered redox state of the γ‐subunit under low, but not high, light. The low light‐specific decrease in ATP synthase activity in ntrc resulted in a buildup of the thylakoid proton motive force with subsequent activation of non‐photochemical quenching and downregulation of linear electron flow. We conclude that NTRC provides redox modulation at low light using the relatively oxidizing substrate NADPH , whereas the canonical ferredoxin–thioredoxin system can take over at higher light, when reduced ferredoxin can accumulate. Based on these results, we reassess previous models for ATP synthase regulation and propose that NTRC is most likely regulated by light. We also find that ntrc is highly sensitive to rapidly changing light intensities that probably do not involve the chloroplast ATP synthase, implicating this system in multiple photosynthetic processes, particularly under fluctuating environmental conditions.

Research Organization:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1437167
Alternate ID(s):
OSTI ID: 1400765
Journal Information:
The Plant Journal, Vol. 87, Issue 6; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 64 works
Citation information provided by
Web of Science

References (56)

In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase journal August 2002
New results about structure, function and regulation of the chloroplast ATP synthase (CF0CF1) journal May 1999
Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions journal February 2012
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana journal August 2003
Control of the Quantum Efficiencies of Photosystems I and II, Electron Flow, and Enzyme Activation following Dark-to-Light Transitions in Pea Leaves: Relationship between NADP/NADPH Ratios and NADP-Malate Dehydrogenase Activation State journal July 1992
ACHT4-driven oxidation of APS1 attenuates starch synthesis under low light intensity in Arabidopsis plants journal September 2015
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
Fourteen Protomers Compose the Oligomer III of the Proton-rotor in Spinach Chloroplast ATP Synthase journal October 2003
The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged journal December 2000
Gamma–epsilon Interactions Regulate the Chloroplast ATP Synthase journal January 2004
Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis: Thioredoxin networks in chloroplasts journal April 2016
Simultaneous Measurement of ΔpH and Electron Transport in Chloroplast Thylakoids by 9-Aminoacridine Fluorescence journal September 2000
Thioredoxin Reductase Type C (NTRC) Orchestrates Enhanced Thermotolerance to Arabidopsis by Its Redox-Dependent Holdase Chaperone Function journal March 2013
Thiol modulation of chloroplast CF 0 -CF 1 in isolated barley protoplasts and its significance to regulation of carbon dioxide fixation journal September 1986
Overexpression of chloroplast NADPH-dependent thioredoxin reductase in Arabidopsis enhances leaf growth and elucidates in vivo function of reductase and thioredoxin domains journal January 2013
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction journal June 2004
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
Mutants of Chloroplast Coupling Factor Reduction in Arabidopsis journal February 1994
Effects of changes in the capacity for photosynthetic electron transfer and photophosphorylation on the kinetics of fluorescence induction in isolated chloroplasts journal September 1983
The Transiently Generated Nonphotochemical Quenching of Excitation Energy in Arabidopsis Leaves Is Modulated by Zeaxanthin journal February 2007
Adenine Nucleotide Levels, the Redox State of the NADP System, and Assimilatory Force in Nonaqueously Purified Mesophyll Chloroplasts from Maize Leaves under Different Light Intensities journal December 1988
N ONPHOTOSYNTHETIC M ETABOLISM IN P LASTIDS journal June 2000
Distinct Redox Behaviors of Chloroplast Thiol Enzymes and their Relationships with Photosynthetic Electron Transport in Arabidopsis thaliana journal May 2014
Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase journal January 2009
Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods journal July 2013
Rice NTRC Is a High-Efficiency Redox System for Chloroplast Protection against Oxidative Damage journal August 2006
The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling journal July 2012
NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts journal May 2009
A Point Mutation in atpC1 Raises the Redox Potential of the Arabidopsis Chloroplast ATP Synthase γ-Subunit Regulatory Disulfide above the Range of Thioredoxin Modulation journal October 2007
Role of Light in the Regulation of Chloroplast Enzymes journal June 1980
Adenine Nucleotide Levels in the Cytosol, Chloroplasts, and Mitochondria of Wheat Leaf Protoplasts journal October 1982
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
Thioredoxin targets in plants: The first 30 years journal April 2009
Significance of the ε subunit in the thiol modulation of chloroplast ATP synthase journal May 2004
Photosynthetic regulatory protein found in animal and bacterial cells journal December 1976
The Arabidopsis Plastidial Thioredoxins : NEW FUNCTIONS AND NEW INSIGHTS INTO SPECIFICITY journal April 2003
Redox Transfer across the Inner Chloroplast Envelope Membrane journal April 1991
Chloroplast NADPH-Thioredoxin Reductase Interacts with Photoperiodic Development in Arabidopsis journal January 2009
A Novel NADPH Thioredoxin Reductase, Localized in the Chloroplast, Which Deficiency Causes Hypersensitivity to Abiotic Stress in Arabidopsis thaliana journal July 2004
In Situ Regulation of Chloroplast Coupling Factor Activity journal June 1992
Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants journal August 1989
Important subunit interactions in the chloroplast ATP synthase journal May 2000
NTRC new ways of using NADPH in the chloroplast journal July 2008
Comprehensive survey of proteins targeted by chloroplast thioredoxin journal September 2001
Correlation between the activity of membrane-bound ATPase and the decay rate of flash-induced 515-nm absorbance change in chloroplasts in intact leaves, assayed by means of rapid isolation of chloroplasts journal January 1982
Influence of the redox state and the activation of the chloroplast ATP synthase on proton-transport-coupled ATP synthesis/hydrolysis journal September 1987
Molecular devices of chloroplast F1-ATP synthase for the regulation journal September 2002
Light- and Metabolism-related Regulation of the Chloroplast ATP Synthase Has Distinct Mechanisms and Functions journal March 2013
Assimilatory power as a driving force in photosynthesis journal November 1986
Correlation between photosynthesis and the transthylakoid proton gradient journal April 1981
The long-term responses of the photosynthetic proton circuit to drought journal March 2009
The rate of ATP-synthesis as a function of ΔpH and Δψ catalyzed by the active, reduced H + -ATPase from chloroplasts journal December 1991
Plant Thioredoxin Systems Revisited journal June 2000
The chloroplast NADPH thioredoxin reductase C, NTRC, controls non-photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis : NTRC controls photosynthetic electron transport journal January 2016
The effects of chloroplast coupling factor reduction on the energetics of activation and on the energetics and efficiency of ATP formation. journal October 1987
Role of the gamma subunit of chloroplast coupling factor 1 in the light-dependent activation of photophosphorylation and ATPase activity by dithiothreitol. journal June 1984

Cited By (5)

Efficient photosynthesis in dynamic light environments: a chloroplast's perspective journal October 2019
Photosynthetic activity of cotyledons is critical during post-germinative growth and seedling establishment journal September 2017
High-value biomass from microalgae production platforms: strategies and progress based on carbon metabolism and energy conversion journal August 2018
Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection journal May 2017
Physiological and Transcriptome Analyses of Early Leaf Senescence for ospls1 Mutant Rice (Oryza sativa L.) during the Grain-Filling Stage journal March 2019

Figures / Tables (5)


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