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

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.

scholarly journals Electron flow through NDH-1 complexes is the major driver of cyclic electron flow-dependent proton pumping in cyanobacteria

2020 ◽  
Author(s):  
Neil T. Miller ◽  
Michael D. Vaughn ◽  
Robert L. Burnap
Keyword(s):  
Electron Flow ◽  
Proton Pumping ◽  
Cyclic Electron Flow ◽  
Pumping Rate ◽  
Photosynthetic Organisms ◽  
Photosynthetic Electron Flow ◽  
Flow Through ◽  
Pumping Rates ◽  
Kinetics Of

AbstractCyclic electron flow (CEF) around Photosystem I is vital to balancing the photosynthetic energy budget of cyanobacteria and other photosynthetic organisms. The coupling of CEF to proton pumping has long been hypothesized to occur, providing proton motive force (PMF) for the synthesis of ATP with no net cost to [NADPH]. This is thought to occur largely through the activity of NDH-1 complexes, of which cyanobacteria have four with different activities. While a much work has been done to understand the steady-state PMF in both the light and dark, and fluorescent probes have been developed to observe these fluxes in vivo, little has been done to understand the kinetics of these fluxes, particularly with regard to NDH-1 complexes. To monitor the kinetics of proton pumping in Synechocystis sp. PCC 6803, the pH sensitive dye Acridine Orange was used alongside a suite of inhibitors in order to observe light-dependent proton pumping. The assay was demonstrated to measure photosynthetically driven proton pumping and used to measure the rates of proton pumping unimpeded by dark ΔpH. Here, the cyanobacterial NDH-1 complexes are shown to pump a sizable portion of proton flux when CEF-driven and LEF-driven proton pumping rates are observed and compared in mutants lacking some or all NDH-1 complexes. It is also demonstrated that PSII and LEF are responsible for the bulk of light induced proton pumping, though CEF and NDH-1 are capable of generating ∼40% of the proton pumping rate when LEF is inactivated.Highlights statementNDH-1 is essential for proton pumping during cyclic photosynthetic electron flow in cyanobacteria

scholarly journals The Higher Plant Plastid Complex I (NDH) is a Reversible Proton Pump that increases ATP production by Cyclic Electron Flow Around Photosystem I

2016 ◽  
Author(s):  
Deserah D. Strand ◽  
Nicholas Fisher ◽  
David M. Kramer
Keyword(s):  
Electron Transfer ◽  
Photosystem I ◽  
Complex I ◽  
Electron Flow ◽  
Proton Pumping ◽  
Cyclic Electron Flow ◽  
Higher Plant ◽  
Atp Production ◽  
Respiratory Complex I ◽  
Chloroplast Stroma

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.

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

2018 ◽  
Vol 115 (45) ◽  
pp. E10778-E10787 ◽  
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.

scholarly journals PsaE Is Required for in Vivo Cyclic Electron Flow around Photosystem I in the Cyanobacterium Synechococcus sp. PCC 7002

1993 ◽  
Vol 103 (1) ◽  
pp. 171-180 ◽  
Author(s):  
L. Yu ◽  
J. Zhao ◽  
U. Muhlenhoff ◽  
D. A. Bryant ◽  
J. H. Golbeck
Keyword(s):  
Photosystem I ◽  
Electron Flow ◽  
Cyclic Electron Flow ◽  
Synechococcus Sp

scholarly journals Cyclic electron flow and light partitioning between the two photosystems in leaves of plants with different functional types

2019 ◽  
Vol 142 (3) ◽  
pp. 321-334 ◽  
Author(s):  
Julius Ver Sagun ◽  
Murray R. Badger ◽  
Wah Soon Chow ◽  
Oula Ghannoum
Keyword(s):  
Electron Flux ◽  
Electron Flow ◽  
Cyclic Electron Flow ◽  
Plant Functional Groups ◽  
Accurate Estimation ◽  
Total Electron ◽  
Membrane Inlet Mass Spectrometry ◽  
Fern Species ◽  
Light Partitioning

Abstract Cyclic electron flow (CEF) around photosystem I (PSI) is essential for generating additional ATP and enhancing efficient photosynthesis. Accurate estimation of CEF requires knowledge of the fractions of absorbed light by PSI (fI) and PSII (fII), which are only known for a few model species such as spinach. No measures of fI are available for C4 grasses under different irradiances. We developed a new method to estimate (1) fII in vivo by concurrently measuring linear electron flux through both photosystems $$\left( {{\text{LEF}}_{{{\text{O}}_{ 2} }} } \right)$$LEFO2 in leaf using membrane inlet mass spectrometry (MIMS) and total electron flux through PSII (ETR2) using chlorophyll fluorescence by a Dual-PAM at low light and (2) CEF as ETR1—$${\text{LEF}}_{{{\text{O}}_{ 2} }}$$LEFO2. For a C3 grass, fI was 0.5 and 0.4 under control (high light) and shade conditions, respectively. C4 species belonging to NADP-ME and NAD-ME subtypes had fI of 0.6 and PCK subtype had 0.5 under control. All shade-grown C4 species had fI of 0.6 except for NADP-ME grass which had 0.7. It was also observed that fI ranged between 0.3 and 0.5 for gymnosperm, liverwort and fern species. CEF increased with irradiance and was induced at lower irradiances in C4 grasses and fern relative to other species. CEF was greater in shade-grown plants relative to control plants except for C4 NADP-ME species. Our study reveals a range of CEF and fI values in different plant functional groups. This variation must be taken into account for improved photosynthetic calculations and modelling.

Sign in / Sign up

Export Citation Format

Share Document