scholarly journals Efficient cooperation of chloroplasts and mitochondria enhances ATP and sucrose production

2020 ◽  
Author(s):  
Chia Pao Voon ◽  
Yee-Song Law ◽  
Xiaoqian Guan ◽  
Zhou Xu ◽  
Wing-Tung Chu ◽  
...  
Keyword(s):  
Carbon Fixation ◽  
Electron Flow ◽  
Redox Balance ◽  
Purple Acid Phosphatase ◽  
Linear Electron ◽  
Atp Production ◽  
Outer Membranes ◽  
Production And Consumption ◽  
Seed Yields ◽  
Reducing Equivalents

ABSTRACTEfficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts as the linear electron flow generates a higher NADPH/ATP ratio than that is consumed by the Calvin-Benson-Bassham cycle. Recent works suggested that ATP importation into mature chloroplasts of Arabidopsis thaliana is negligible, and therefore the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow. A higher rate of ATP and NADPH production from the linear electron flow, a higher capacity of carbon fixation by the Calvin-Benson-Bassham cycle and a greater consumption of NADH in mitochondria, enhance photosynthesis in the chloroplasts, ATP production in the mitochondria, sucrose synthesis in the cytosol, and eventually boosting plant growth and seed yields in the overexpression lines.Significance StatementThis study demonstrates the importance of chloroplast-mitochondria cooperation in redox balance and illustrates that an optimized function of mitochondria can enhance the efficiency of photosynthesis.

scholarly journals Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth

2021 ◽  
Vol 2 ◽  
Author(s):  
Chia P. Voon ◽  
Yee-Song Law ◽  
Xiaoqian Guan ◽  
Shey-Li Lim ◽  
Zhou Xu ◽  
...  
Keyword(s):  
Plant Growth ◽  
Carbon Fixation ◽  
Electron Flow ◽  
Purple Acid Phosphatase ◽  
Atp Production ◽  
Outer Membranes ◽  
Production And Consumption ◽  
Adenosine Triphosphate Production ◽  
Seed Yields ◽  
Reducing Equivalents

Abstract Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow (LEF). A higher rate of ATP and NADPH production from the LEF, a higher capacity of carbon fixation by the Calvin–Benson–Bassham (CBB) cycle and a greater consumption of NADH in mitochondria enhance photosynthesis in the chloroplasts, ATP production in the mitochondria and sucrose synthesis in the cytosol and eventually boost plant growth and seed yields in the overexpression lines.

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 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 A Balance between the Activities of Chloroplasts and Mitochondria Is Crucial for Optimal Plant Growth

Antioxidants ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 935
Author(s):  
Zhou Xu ◽  
Renshan Zhang ◽  
Meijing Yang ◽  
Yee-Song Law ◽  
Feng Sun ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Plant Growth ◽  
Seed Yield ◽  
Optimal Growth ◽  
Purple Acid Phosphatase ◽  
Outer Membranes ◽  
Transgenic Lines ◽  
Growth Promoting ◽  
High Level ◽  
Reducing Equivalents

Energy metabolism in plant cells requires a balance between the activities of chloroplasts and mitochondria, as they are the producers and consumers of carbohydrates and reducing equivalents, respectively. Recently, we showed that the overexpression of Arabidopsis thaliana purple acid phosphatase 2 (AtPAP2), a phosphatase dually anchored on the outer membranes of chloroplasts and mitochondria, can boost the plant growth and seed yield of Arabidopsis thaliana by coordinating the activities of both organelles. However, when AtPAP2 is solely overexpressed in chloroplasts, the growth-promoting effects are less optimal, indicating that active mitochondria are required for dissipating excess reducing equivalents from chloroplasts to maintain the optimal growth of plants. It is even more detrimental to plant productivity when AtPAP2 is solely overexpressed in mitochondria. Although these lines contain high level of adenosine triphosphate (ATP), they exhibit low leaf sucrose, low seed yield, and early senescence. These transgenic lines can be useful tools for studying how hyperactive chloroplasts or mitochondria affect the physiology of their counterparts and how they modify cellular metabolism and plant physiology.

Photosystem I-abhängige Phosphorylierung isolierter Chloroplasten mit Ascorbat/2.6-Dichlorphenolindophenol als Elektronendonator und Methylviologen als Elektronenakzeptor / Photosystem I Dependent Phosphorylation of Isolated Chloroplasts with Ascorbate/2,6-Dichlorophenolindophenol as Electron Donor and Methylviologen as Electron Acceptor

1972 ◽  
Vol 27 (4) ◽  
pp. 445-455 ◽  
Author(s):  
Heinrich Strotmann ◽  
Christa Von Gösseln
Keyword(s):  
Electron Transport ◽  
Linear System ◽  
Photosystem I ◽  
Electron Acceptor ◽  
Electron Flow ◽  
Phosphorylation Site ◽  
Cyclic System ◽  
Atp Production ◽  
Proton Uptake ◽  
Isolated Chloroplasts

Photosystem I related phosphorylation of isolated chloroplasts was investigated with special reference to the stoichiometry between ATP production and electron transprt (ATP: 2e⊖). The system studied contained DCMU to inhibit electron flow from photosystem II, ascorbate and DPIP to supply electrons to photosystem I, and methylviologen as electron acceptor. The following results were obtained:1. Basal electron transport is stimulated by the addition of the phosphorylating system, indicating that phosphorylation is really coupled to non-cyclic electron flow. The ratio ATP: 2e⊖ is 1, when the increase of electron flow obtained by the addition of ADP and phosphate is correlated to phosphorylation. This ratio is constant upon varying several parameters including DPIP concentration and light intensity.2. In the absence of methylviologen a DPIP catalyzed cyclic phosphorylation takes place (cf. I. c.7, 11, 12). Phosphorylation is not increased by the addition of methylviologen, indicating that both, the cyclic DPIP mediated and the non-cyclic system are coupled to the same phosphorylation site and limited by the same reaction step.3. In the absence of oxygen a methylviologen supported cyclic phosphorylation occurs. Comparing optimum rates, phosphorylation under these conditions is about twice as high as in the noncyclic system. Therefore we conclude that two phosphorylation sites are involved in methylviologen catalyzed cyclic electron transport. This system is sensitive against trypsin treatment of the chloroplasts, whereas the linear system is not.4. The two cyclic systems as well as the non-cyclic system are coupled to reversible proton uptake. Furthermore the linear system exhibits an irreversible uptake of hydrogen ions, which is stoichiometric to electron flow. From the reversible and the irreversible components of the pH changes the ratio of the proton pump to electron transprt can be calculated. Under steady state conditions the ration H⨁ : e⊖ approaches 1.

Maintenance of Photophosphorylation Despite Inhibition of the Transthylakoid pH Gradient by Tetracaine

1992 ◽  
Vol 47 (9-10) ◽  
pp. 717-725 ◽  
Author(s):  
Henrik Laasch
Keyword(s):  
Salt Concentration ◽  
Spinacia Oleracea ◽  
Electron Flow ◽  
Energy Coupling ◽  
Ph Gradient ◽  
Proton Pumps ◽  
Linear Electron ◽  
Ps Ii ◽  
Spinacia Oleracea L ◽  
Low Salt

The inhibition of the transthylakoid pH gradient, ΔpH, and of photophosphorylation by the local anesthetic tetracaine was investigated with isolated chloroplasts from Spinacia oleracea L. Tetracaine strongly inhibited ΔpH in the presence of low salt concentrations. In the presence of high salt concentrations, the inhibition of ΔpH was much smaller. This effect of salt concentration was observed only when both, cation and anion were easily membrane permeable. It was concluded that the effect of salts on ΔpH inhibition was excerted on the inside of the thylakoid membrane. The rate of photophosphorylation, Vp, driven by the PS Idependent artificial proton carrier phenazine methosulfate decreased with ΔpH in the presence of both, high and low salt concentrations. In contrast, Vp driven by the endogenous proton pumps of PS II + I-dependent linear electron flow was largely independent of ΔpH changes in the presence of low salt concentration. It appeared that energy coupling during linear electron transport, in contrast to artificially produced PS I-dependent coupling, may be localized to membrane-bound proton domains which are not accessible to the employed indicators of ΔpH. The data were discussed with respect to recent hypotheses on localized energy coupling in chloroplasts.

The Effect of an Antiserum to Plastocyanin on Various Chloroplast Preparations

1975 ◽  
Vol 30 (3-4) ◽  
pp. 201-212 ◽  
Author(s):  
Georg Schmid ◽  
Alfons Radunz ◽  
Wilhelm Menke
Keyword(s):  
Electron Transport ◽  
Thylakoid Membrane ◽  
Electron Flow ◽  
Linear Electron ◽  
Wild Type ◽  
Lamellar System ◽  
Spinach Chloroplasts ◽  
Monospecific Antiserum ◽  
Cyclic Photophosphorylation ◽  
Aurea Mutant

Abstract A monospecific antiserum to tobacco plastocyanin agglutinates strom a-free sw ellable chloroplasts from wild type tobacco, (Nicotia na tabacum var. John William’s Broadleaf) from the tobacco aurea mutant Su/su2, (Nicotiana tabacum var. Su/su2) from Antirrhinum majus and spinach (Spi-nacia oleracea). In this condition the antiserum inhibits linear photosynthetic electron flow in tobacco and spinach chloroplasts. This inhibition of electron transport as well as the agglutination are not observed if the chloroplasts have been sonicated prior to antiserum addition. This is due to the fact that plastocyanin is removed by ultrasonication. The antiserum stimulates a number of photophosphorylation reactions in tobacco chloroplasts. This stimulation is always larger in the aurea mutant chloroplasts and in chloroplasts from yellow leaf patches of a variegated tobacco mutant (N . tabacum , var. NC95) than in the green type chloroplasts. The stimulation appears to be a consequence of the inhibition of linear electron transport. The antiserum does not affect PMS-mediated cyclic photophosphorylation in tobacco chloroplasts from the wild type whereas the reaction appears stimulated in the tobacco mutant chloroplasts. However, menadione-mediated cyclic photo­ phosphorylation is inhibited upon addition of the antiserum. The same is true for noncyclic photo­ phosphorylation coupled to electron transport in the aerobic system diaminodurene/ascorbate → methylviologen in the presence of N-tetraphenyl-p-phenylenediamine in spinach chloroplasts. If the lamellar system of Antirrhinum and spinach has lost its swellability neither agglutination nor inhibition of electron transport is observed. However, also in this state antibodies to plasto­ cyanin are specifically adsorbed onto the surface of the thylakoid membrane. This state which is characterized by a morphologically well preserved lamellar system is realized in chloroplast prepa­ rations from Antirrhinum and spinach and is termed stroma-freed, chloroplasts. In both states of the molecular structure of the thylakoid membrane, plastocyanin is located in the outer surface of the thylakoid. However, it cannot be excluded that functioning plastocyanin is also located in the interior of the thylakoid membrane.

scholarly journals A Genome-Scale Metabolic Model of Thalassiosira pseudonana CCMP 1335 for a Systems-Level Understanding of Its Metabolism and Biotechnological Potential

2020 ◽  
Vol 8 (9) ◽  
pp. 1396
Author(s):  
Ahmad Ahmad ◽  
Archana Tiwari ◽  
Shireesh Srivastava
Keyword(s):  
Carbon Fixation ◽  
Electron Flow ◽  
Single Gene ◽  
Metabolic Model ◽  
Thalassiosira Pseudonana ◽  
Marine Diatom ◽  
Omega 3 ◽  
Biotechnological Potential ◽  
A Genome ◽  
Genome Scale

Thalassiosira pseudonana is a transformable and biotechnologically promising model diatom with an ability to synthesise nutraceuticals such as fucoxanthin and store a significant amount of polyglucans and lipids including omega-3 fatty acids. While it was the first diatom to be sequenced, a systems-level analysis of its metabolism has not been done yet. This work presents first comprehensive, compartmentalized, and functional genome-scale metabolic model of the marine diatom Thalassiosira pseudonana CCMP 1335, which we have termed iThaps987. The model includes 987 genes, 2477 reactions, and 2456 metabolites. Comparison with the model of another diatom Phaeodactylum tricornutum revealed presence of 183 unique enzymes (belonging primarily to amino acid, carbohydrate, and lipid metabolism) in iThaps987. Model simulations showed a typical C3-type photosynthetic carbon fixation and suggested a preference of violaxanthin–diadinoxanthin pathway over violaxanthin–neoxanthin pathway for the production of fucoxanthin. Linear electron flow was found be active and cyclic electron flow was inactive under normal phototrophic conditions (unlike green algae and plants), validating the model predictions with previous reports. Investigation of the model for the potential of Thalassiosira pseudonana CCMP 1335 to produce other industrially useful compounds suggest iso-butanol as a foreign compound that can be synthesized by a single-gene addition. This work provides novel insights about the metabolism and potential of the organism and will be helpful to further investigate its metabolism and devise metabolic engineering strategies for the production of various compounds.

scholarly journals In silico-guided engineering of Pseudomonas putida towards growth under micro-oxic conditions

2019 ◽  
Vol 18 (1) ◽  
Author(s):  
Linde F. C. Kampers ◽  
Ruben G. A. van Heck ◽  
Stefano Donati ◽  
Edoardo Saccenti ◽  
Rita J. M. Volkers ◽  
...  
Keyword(s):  
Pseudomonas Putida ◽  
In Silico ◽  
Redox Balance ◽  
Industrial Applications ◽  
Strictly Aerobic ◽  
Class Iii ◽  
Adaptive Laboratory Evolution ◽  
Laboratory Evolution ◽  
Atp Production ◽  
Lactobacillus Lactis

Abstract Background Pseudomonas putida is a metabolically versatile, genetically accessible, and stress-robust species with outstanding potential to be used as a workhorse for industrial applications. While industry recognises the importance of robustness under micro-oxic conditions for a stable production process, the obligate aerobic nature of P. putida, attributed to its inability to produce sufficient ATP and maintain its redox balance without molecular oxygen, severely limits its use for biotechnology applications. Results Here, a combination of genome-scale metabolic modelling and comparative genomics is used to pinpoint essential $$\text {O}_{2}$$ O 2 -dependent processes. These explain the inability of the strain to grow under anoxic conditions: a deficient ATP generation and an inability to synthesize essential metabolites. Based on this, several P. putida recombinant strains were constructed harbouring acetate kinase from Escherichia coli for ATP production, and a class I dihydroorotate dehydrogenase and a class III anaerobic ribonucleotide triphosphate reductase from Lactobacillus lactis for the synthesis of essential metabolites. Initial computational designs were fine-tuned by means of adaptive laboratory evolution. Conclusions We demonstrated the value of combining in silico approaches, experimental validation and adaptive laboratory evolution for microbial design by making the strictly aerobic Pseudomonas putida able to grow under micro-oxic conditions.

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