Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts

Fisher, Nicholas; Bricker, Terry M.; Kramer, David M.

doi:10.1016/j.bbabio.2019.148081

Title: Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts

Abstract

Cylic electron flow (CEF) around Photosystem I in photosynthetic eukaryotes is anticipated to be necessary to augment ATP production, rapidly- and precisely balancing the plastid ATP/NADPH energy budget to meet the demands of downstream metabolism. Many regulatory aspects of this process are unclear. In this work, we demonstrate that the higher plant plastid NADH/Fd:plastoquinone reductase (NDH) and proposed PGR5/PGRL1 ferredoxin:plastoquinone reductase (FQR) pathways of CEF are strongly, rapidly and reversibly inhibited in vitro by ATP with K_i values of 670 μM and 240 μM respectively, within the range of physiological changes in ATP concentrations. Control experiments ruled out effects on secondary reactions, e.g. FNR- and cytochrome b₆f activity, nonphotochemical quenching of chlorophyll fluorescence etc., supporting the view that ATP is an inhibitor of CEF and its associated pmf generation and subsequent ATP production. The effects are specific to ATP, with the ATP analog AMP-PNP showing little inhibitory effect, and ADP inhibiting only at higher concentrations. For the FQR pathway, inhibition was found to be classically competitive with Fd, and the NDH pathway showing partial competition with Fd. We propose a straightforward model for regulation of CEF in plants in which CEF is activated under conditions when stromal ATP low, butmore »« less

Authors:: Fisher, Nicholas; Bricker, Terry M.; Kramer, David M.

Publication Date:: Fri Nov 01 00:00:00 EDT 2019

Research Org.:: Louisiana State Univ., Baton Rouge, LA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division

OSTI Identifier:: 1703107

Alternate Identifier(s):: OSTI ID: 1593968

Grant/Contract Number:: FG02-98ER20310; FG02-91ER20021

Resource Type:: Published Article

Journal Name:: Biochimica et Biophysica Acta - Bioenergetics

Additional Journal Information:: Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1860 Journal Issue: 11; Journal ID: ISSN 0005-2728

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; photosynthesis; cyclic electron flow; regulation; enzymology

Citation Formats


                    Fisher, Nicholas, Bricker, Terry M., and Kramer, David M. Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts.  Netherlands: N. p., 2019. 
Web.  doi:10.1016/j.bbabio.2019.148081.

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                    Fisher, Nicholas, Bricker, Terry M., & Kramer, David M. Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts.  Netherlands.  https://doi.org/10.1016/j.bbabio.2019.148081

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                    Fisher, Nicholas, Bricker, Terry M., and Kramer, David M. Fri .  
"Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts".  Netherlands.  https://doi.org/10.1016/j.bbabio.2019.148081.

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@article{osti_1703107,

  title        = {Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts},

  author       = {Fisher, Nicholas and Bricker, Terry M. and Kramer, David M.},

  abstractNote = {Cylic electron flow (CEF) around Photosystem I in photosynthetic eukaryotes is anticipated to be necessary to augment ATP production, rapidly- and precisely balancing the plastid ATP/NADPH energy budget to meet the demands of downstream metabolism. Many regulatory aspects of this process are unclear. In this work, we demonstrate that the higher plant plastid NADH/Fd:plastoquinone reductase (NDH) and proposed PGR5/PGRL1 ferredoxin:plastoquinone reductase (FQR) pathways of CEF are strongly, rapidly and reversibly inhibited in vitro by ATP with Ki values of 670 μM and 240 μM respectively, within the range of physiological changes in ATP concentrations. Control experiments ruled out effects on secondary reactions, e.g. FNR- and cytochrome b6f activity, nonphotochemical quenching of chlorophyll fluorescence etc., supporting the view that ATP is an inhibitor of CEF and its associated pmf generation and subsequent ATP production. The effects are specific to ATP, with the ATP analog AMP-PNP showing little inhibitory effect, and ADP inhibiting only at higher concentrations. For the FQR pathway, inhibition was found to be classically competitive with Fd, and the NDH pathway showing partial competition with Fd. We propose a straightforward model for regulation of CEF in plants in which CEF is activated under conditions when stromal ATP low, but is downregulated as ATP levels build up, allowing for effective ATP homeostasis. The differences in Ki values suggest a two-tiered regulatory system, where the highly efficient proton pumping NDH is activated with moderate decreases in ATP, with the less energetically-efficient FQR pathway being activated under more severe ATP depletion.},

  doi          = {10.1016/j.bbabio.2019.148081},

  journal      = {Biochimica et Biophysica Acta - Bioenergetics},

  number       = 11,

  volume       = 1860,

  place        = {Netherlands},

  year         = {Fri Nov 01 00:00:00 EDT 2019},

  month        = {Fri Nov 01 00:00:00 EDT 2019}

}

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Title: Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts

Abstract

Citation Formats

Characterization of Factors Affecting the Activity of Photosystem I Cyclic Electron Transport in Chloroplasts journal, March 2008

The value of ΔG° for the hydrolysis of ATP journal, May 1972

Evaluation of the Specific Roles of Anions in Electron Transport and Energy Transfer Reactions in Photosynthesis journal, September 2001

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

Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii journal, February 2002

Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes journal, February 1998

Adenine Nucleotide Levels in the Cytosol, Chloroplasts, and Mitochondria of Wheat Leaf Protoplasts journal, October 1982

Plasticity in light reactions of photosynthesis for energy production and photoprotection journal, November 2004

The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow journal, May 2017

An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal, January 2010

Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability journal, October 2013

Activation of cyclic electron flow by hydrogen peroxide in vivo journal, April 2015

NAD(P)H Dehydrogenase-Dependent, Antimycin A-Sensitive Electron Donation to Plastoquinone in Tobacco Chloroplasts journal, November 1998

Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5′-triphosphate journal, March 1981

TROL-FNR interaction reveals alternative pathways of electron partitioning in photosynthesis journal, June 2015

Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions journal, January 2010

Novel insights into the function of LHCSR3 in Chlamydomonas reinhardtii journal, December 2015

Stromal Phosphate Concentration Is Low during Feedback Limited Photosynthesis journal, October 1989

Calcium-dependent regulation of photosynthesis journal, September 2015

PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition journal, November 2002

ATP-induced increase in chlorophyll fluorescence. Characterization of rapid and slow induction phases journal, October 1984

The glucose 6-phosphate shunt around the Calvin–Benson cycle journal, November 2015

Calredoxin represents a novel type of calcium-dependent sensor-responder connected to redox regulation in the chloroplast journal, June 2016

Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I journal, February 2016

Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain journal, January 2003

Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex journal, October 2012

Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I journal, August 1998

Towards Characterization of the Chloroplast NAD(P)H Dehydrogenase Complex journal, November 2009

Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: Relevance to cyclic electron flow around photosystem I? journal, December 2014

Cyclic electron transfer in plant leaf journal, July 2002

A Complex Containing PGRL1 and PGR5 Is Involved in the Switch between Linear and Cyclic Electron Flow in Arabidopsis journal, January 2008

Structure of the complex I-like molecule NDH of oxygenic photosynthesis journal, February 2019

Quantification of the electrochemical proton gradient and activation of ATP synthase in leaves journal, July 2008

Balancing the central roles of the thylakoid proton gradient journal, January 2003

Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction journal, December 1973

Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids journal, January 2016

From The Cover: Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis journal, November 2005

Post-illumination Reduction of the Plastoquinone Pool in Chloroplast Transformants in which Chloroplastic NAD(P)H Dehydrogenase was Inactivated journal, January 2002

Photosynthetic Measurements with the Idea Spec: an Integrated Diode Emitter Array Spectrophotometer/Fluorometer book, January 2013

Improving photosynthesis and crop productivity by accelerating recovery from photoprotection journal, November 2016

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

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

State 1-state 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching journal, November 1981

State transitions and light adaptation require chloroplast thylakoid protein kinase STN7 journal, February 2005

Structure of the Chloroplast NADH Dehydrogenase-Like Complex: Nomenclature for Nuclear-Encoded Subunits journal, July 2011

Characterization of Factors Affecting the Activity of Photosystem I Cyclic Electron Transport in Chloroplasts
journal, March 2008

The value of ΔG° for the hydrolysis of ATP
journal, May 1972

Evaluation of the Specific Roles of Anions in Electron Transport and Energy Transfer Reactions in Photosynthesis
journal, September 2001

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

Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii
journal, February 2002

Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes
journal, February 1998

Adenine Nucleotide Levels in the Cytosol, Chloroplasts, and Mitochondria of Wheat Leaf Protoplasts
journal, October 1982

Plasticity in light reactions of photosynthesis for energy production and photoprotection
journal, November 2004

The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow
journal, May 2017

An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex
journal, January 2010

Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability
journal, October 2013

Activation of cyclic electron flow by hydrogen peroxide in vivo
journal, April 2015

NAD(P)H Dehydrogenase-Dependent, Antimycin A-Sensitive Electron Donation to Plastoquinone in Tobacco Chloroplasts
journal, November 1998

Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5′-triphosphate
journal, March 1981

TROL-FNR interaction reveals alternative pathways of electron partitioning in photosynthesis
journal, June 2015

Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions
journal, January 2010

Novel insights into the function of LHCSR3 in Chlamydomonas reinhardtii
journal, December 2015

Stromal Phosphate Concentration Is Low during Feedback Limited Photosynthesis
journal, October 1989

Calcium-dependent regulation of photosynthesis
journal, September 2015

PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition
journal, November 2002

ATP-induced increase in chlorophyll fluorescence. Characterization of rapid and slow induction phases
journal, October 1984

The glucose 6-phosphate shunt around the Calvin–Benson cycle
journal, November 2015

Calredoxin represents a novel type of calcium-dependent sensor-responder connected to redox regulation in the chloroplast
journal, June 2016

Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I
journal, February 2016

Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain
journal, January 2003

Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex
journal, October 2012

Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I
journal, August 1998

Towards Characterization of the Chloroplast NAD(P)H Dehydrogenase Complex
journal, November 2009

Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: Relevance to cyclic electron flow around photosystem I?
journal, December 2014

Cyclic electron transfer in plant leaf
journal, July 2002

A Complex Containing PGRL1 and PGR5 Is Involved in the Switch between Linear and Cyclic Electron Flow in Arabidopsis
journal, January 2008

Structure of the complex I-like molecule NDH of oxygenic photosynthesis
journal, February 2019

Quantification of the electrochemical proton gradient and activation of ATP synthase in leaves
journal, July 2008

Balancing the central roles of the thylakoid proton gradient
journal, January 2003

Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction
journal, December 1973

Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids
journal, January 2016

From The Cover: Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis
journal, November 2005

Post-illumination Reduction of the Plastoquinone Pool in Chloroplast Transformants in which Chloroplastic NAD(P)H Dehydrogenase was Inactivated
journal, January 2002

Photosynthetic Measurements with the Idea Spec: an Integrated Diode Emitter Array Spectrophotometer/Fluorometer
book, January 2013

Improving photosynthesis and crop productivity by accelerating recovery from photoprotection
journal, November 2016

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

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

State 1-state 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching
journal, November 1981

State transitions and light adaptation require chloroplast thylakoid protein kinase STN7
journal, February 2005

Structure of the Chloroplast NADH Dehydrogenase-Like Complex: Nomenclature for Nuclear-Encoded Subunits
journal, July 2011