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

AbstractCyclic electron flow around photosystem I (CEF) is critical for balancing the photosynthetic energy budget of the chloroplast, by generating ATP without net production of NADPH. We demonstrate that the chloroplast NADPH dehydrogenase complex (NDH), a homolog to respiratory Complex I, pumps approximately two protons from the chloroplast stroma to the lumen per electron transferred from ferredoxin to plastoquinone, effectively increasing the efficiency of ATP production via CEF by two-fold compared to CEF pathways involving non-proton-pumping plastoquinone reductases. Under certain physiological conditions, the coupling of proton and electron transfer reactions within NDH should enable a non-canonical mode of photosynthetic electron transfer, allowing electron transfer from plastoquinol to NADPH to be driven by the thylakoid proton motive force possibly helping to sense or remediate mismatches in the photosynthetic budget.

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ATP compartmentation in plastids and cytosol ofArabidopsis thalianarevealed by fluorescent protein sensing

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1711497115 ◽

2018 ◽

Vol 115 (45) ◽

pp. E10778-E10787 ◽

Cited By ~ 16

Author(s):

Chia Pao Voon ◽

Xiaoqian Guan ◽

Yuzhe Sun ◽

Abira Sahu ◽

May Ngor Chan ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Fluorescent Protein ◽

Higher Plants ◽

Electron Flow ◽

Cyclic Electron Flow ◽

Linear Electron ◽

Protein Sensing ◽

Atp Production ◽

Respiratory Inhibitors ◽

Sensor Protein

Matching ATP:NADPH provision and consumption in the chloroplast is a prerequisite for efficient photosynthesis. In terms of ATP:NADPH ratio, the amount of ATP generated from the linear electron flow does not meet the demand of the Calvin–Benson–Bassham (CBB) cycle. Several different mechanisms to increase ATP availability have evolved, including cyclic electron flow in higher plants and the direct import of mitochondrial-derived ATP in diatoms. By imaging a fluorescent ATP sensor protein expressed in livingArabidopsis thalianaseedlings, we found that MgATP2−concentrations were lower in the stroma of mature chloroplasts than in the cytosol, and exogenous ATP was able to enter chloroplasts isolated from 4- and 5-day-old seedlings, but not chloroplasts isolated from 10- or 20-day-old photosynthetic tissues. This observation is in line with the previous finding that the expression of chloroplast nucleotide transporters (NTTs) inArabidopsismesophyll is limited to very young seedlings. Employing a combination of photosynthetic and respiratory inhibitors with compartment-specific imaging of ATP, we corroborate the dependency of stromal ATP production on mitochondrial dissipation of photosynthetic reductant. Our data suggest that, during illumination, the provision and consumption of ATP:NADPH in chloroplasts can be balanced by exporting excess reductants rather than importing ATP from the cytosol.

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TO b OR NOT TO b: DIRECT REDUCTION OF CYTOCHROME b-563 BY FERREDOXIN IN HIGHER PLANT PHOTOSYNTHETIC CYCLIC ELECTRON FLOW IN VITRO?

Biochimica et Biophysica Acta (BBA) - Bioenergetics ◽

10.1016/j.bbabio.2018.09.314 ◽

2018 ◽

Vol 1859 ◽

pp. e106 ◽

Cited By ~ 1

Author(s):

Nick Fisher ◽

Vanessa Quevedo ◽

David M. Kramer

Keyword(s):

Cytochrome B ◽

Direct Reduction ◽

Electron Flow ◽

Cyclic Electron Flow ◽

Higher Plant

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

Biochimica et Biophysica Acta (BBA) - Bioenergetics ◽

10.1016/j.bbabio.2015.07.012 ◽

2016 ◽

Vol 1857 (1) ◽

pp. 1-6 ◽

Cited By ~ 32

Author(s):

Deserah D. Strand ◽

Nicholas Fisher ◽

Geoffry A. Davis ◽

David M. Kramer

Keyword(s):

Photosystem I ◽

Redox Regulation ◽

Electron Flow ◽

Cyclic Electron Flow ◽

Antimycin A ◽

Higher Plant

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Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system

10.1101/261560 ◽

2018 ◽

Author(s):

Lauri Nikkanen ◽

Jouni Toivola ◽

Andrea Trotta ◽

Manuel Guinea Diaz ◽

Mikko Tikkanen ◽

...

Keyword(s):

Carbon Fixation ◽

Electron Flow ◽

Proton Pumping ◽

Cyclic Electron Flow ◽

Light Conditions ◽

Oxidoreductase Activity ◽

Atp Production ◽

Fluctuating Light ◽

Thioredoxin System

ABSTRACTLinear electron transport in the thylakoid membrane drives both photosynthetic NADPH and ATP production, while cyclic electron flow (CEF) around photosystem I only promotes the translocation of protons from stroma to thylakoid lumen. The chloroplast NADH-dehydrogenase-like complex (NDH) participates in one CEF route transferring electrons from ferredoxin back to the plastoquinone pool with concomitant proton pumping to the lumen. CEF has been proposed to balance the ratio of ATP/NADPH production and to control the redox poise particularly in fluctuating light conditions, but the mechanisms regulating the NDH complex remain unknown. We have investigated potential regulation of the CEF pathways by the chloroplast NADPH-thioredoxin reductase (NTRC) in vivo by using an Arabidopsis knockout line of NTRC as well as lines overexpressing NTRC. Here we present biochemical and biophysical evidence showing that NTRC activates the NDH-dependent CEF and regulates the generation of proton motive force, thylakoid conductivity to protons and redox balance between the thylakoid electron transfer chain and the stroma during changes in light conditions. Further, protein–protein interaction assays suggest a putative thioredoxin-target site in close proximity to the ferredoxin binding domain of NDH, thus providing a plausible mechanism for regulation of the NDH ferredoxin:plastoquinone oxidoreductase activity by NTRC.One sentence summaryChloroplast thioredoxins regulate photosynthetic cyclic electron flow that balances the activities of light and carbon fixation reactions and improves plant fitness under fluctuating light conditions.

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