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Title: Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids

Journal Article · · Biochimica et Biophysica Acta - Bioenergetics

The chloroplast must regulate supply of reducing equivalents and ATP to meet rapid changes in downstream metabolic demands. Cyclic electron flow around photosystem I (CEF) is proposed to balance the ATP/NADPH budget by using reducing equivalents to drive plastoquinone reduction, leading to the generation of proton motive force and subsequent ATP synthesis. While high rates of CEF have been observed in vivo, isolated thylakoids show only very slow rates, suggesting that the activity of a key complex is lost or down-regulated upon isolation. In this paper, we show that isolation of thylakoids while in the continuous presence of reduced thiol reductant dithiothreitol (DTT), but not oxidized DTT, maintains high CEF activity through an antimycin A sensitive ferredoxin:quinone reductase (FQR). Maintaining low concentrations (~ 2 mM) of reduced DTT while modulating the concentration of oxidized DTT leads to reversible activation/inactivation of CEF with an apparent midpoint potential of - 306 mV (±10 mV) and n = 2, consistent with redox modulation of a thiol/disulfide couple and thioredoxin-mediated regulation of the plastoquinone reductase involved in the antimycin A-sensitive pathway, possibly at the level of the PGRL1 protein. Finally, based on proposed differences in regulatory modes, we propose that the FQR and NADPH:plastoquinone oxidoreductase (NDH) pathways for CEF are activated under different conditions and fulfill different roles in chloroplast energy balance.

Research Organization:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-04ER15559
OSTI ID:
1390669
Alternate ID(s):
OSTI ID: 1437111
Journal Information:
Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1857 Journal Issue: 1; ISSN 0005-2728
Publisher:
ElsevierCopyright Statement
Country of Publication:
Netherlands
Language:
English
Citation Metrics:
Cited by: 49 works
Citation information provided by
Web of Science

References (58)

Thioredoxin m4 Controls Photosynthetic Alternative Electron Pathways in Arabidopsis journal November 2012
PGRL1 Is the Elusive Ferredoxin-Plastoquinone Reductase in Photosynthetic Cyclic Electron Flow journal February 2013
Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii journal February 2002
Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas journal December 2011
Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability journal October 2013
A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas journal December 2008
Activation of cyclic electron flow by hydrogen peroxide in vivo journal April 2015
Characterization of Nda2, a Plastoquinone-reducing Type II NAD(P)H Dehydrogenase in Chlamydomonas Chloroplasts journal December 2008
Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of Δ ATPase pgr5 and Δ rbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii journal March 2014
The protonmotive Q cycle: A general formulation journal November 1975
The Importance of Energy Balance in Improving Photosynthetic Productivity journal November 2010
The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged journal December 2000
Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex journal October 2012
Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase journal December 2011
The plastid ndh genes code for an NADH-specific dehydrogenase: Isolation of a complex I analogue from pea thylakoid membranes journal February 1998
The Standard Redox Potential of Cysteine-Cystine from the Thiol-Disulphide Exchange Reaction with Glutathione and Lipoic Acid journal October 1967
Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b 6 f complex journal February 2013
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
REDOX REGULATION: A Broadening Horizon journal June 2005
Cyclic photophosphorylation and electron transport journal April 1995
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy journal August 1989
The Dynamics of Photosynthesis journal December 2008
Integrating the proton circuit into photosynthesis: progress and challenges journal January 2005
Redox Potentials of Glutaredoxins and Other Thiol-Disulfide Oxidoreductases of the Thioredoxin Superfamily Determined by Direct Protein-Protein Redox Equilibria journal December 1997
Hydrogen Peroxide Mediates the Induction of Chloroplastic Ndh Complex under Photooxidative Stress in Barley journal March 2001
Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions: Figure 1. journal June 2006
Malate valves to balance cellular energy supply journal January 2004
Purification of Intact Chloroplasts from Arabidopsis and Spinach Leaves by Isopycnic Centrifugation journal September 2008
Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii journal June 2014
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
PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis journal August 2002
Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes journal February 1998
Plasticity in light reactions of photosynthesis for energy production and photoprotection journal November 2004
Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves journal June 2004
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
The Ferredoxin/Thioredoxin System of Oxygenic Photosynthesis journal July 2008
An Src Homology 3 Domain-Like Fold Protein Forms a Ferredoxin Binding Site for the Chloroplast NADH Dehydrogenase-Like Complex in Arabidopsis journal April 2011
Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant journal December 2012
Photosynthesis of ATP—Electrons, Proton Pumps, Rotors, and Poise journal August 2002
Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis journal April 2010
Irreversible cross-linking of heme to the distal tryptophan of stromal ascorbate peroxidase in response to rapid inactivation by H2O2: H2O2-mediated inactivation of stromal APX journal May 2007
How Does Cyclic Electron Flow Alleviate Photoinhibition in Arabidopsis? journal December 2008
Photosystem I cyclic electron transport: Measurement of ferredoxin-plastoquinone reductase activity journal December 1992
Towards Characterization of the Chloroplast NAD(P)H Dehydrogenase Complex journal November 2009
Redox Modulation of Cyclic Electron Flow around Photosystem I in C3 Plants journal November 2006
Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: Relevance to cyclic electron flow around photosystem I? journal December 2014
Cyclic electron flow in C3 plants journal May 2006
Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response journal September 2007
A Complex Containing PGRL1 and PGR5 Is Involved in the Switch between Linear and Cyclic Electron Flow in Arabidopsis journal January 2008
Understanding the cytochrome bc complexes by what they don't do. The Q-cycle at 30 journal January 2006
The Activity of the Chloroplastic Ndh Complex Is Regulated by Phosphorylation of the NDH-F Subunit journal April 2003
Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition? journal April 1999
The long-term responses of the photosynthetic proton circuit to drought journal March 2009
The proton pumping activity of H+-ATPases: An improved fluorescence assay journal November 1993
Cyclic electron flow is redox-controlled but independent of state transition journal June 2013
A qualitative analysis of the regulation of cyclic electron flow around photosystem I from the post-illumination chlorophyll fluorescence transient in Arabidopsis: a new platform for the in vivo investigation of the chloroplast redox state journal January 2010
Photosynthetic Measurements with the Idea Spec: an Integrated Diode Emitter Array Spectrophotometer/Fluorometer book January 2013
Regulation of cyclic electron flow in C3 plants: differential effects of limiting photosynthesis at ribulose-1,5-bisphosphate carboxylase/oxygenase and glyceraldehyde-3-phosphate dehydrogenase: Regulation of cyclic electron flow journal June 2010

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