Transfer of Redox Equivalents Between Subcellular Compartments of a Leaf Cell

Heldt, Hans W.; Heineke, Dieter; Heupel, Ralf; Krömer, Silke; Riens, Burgi

doi:10.1007/978-94-009-0511-5_633

Cited by 10 publications

(5 citation statements)

References 15 publications

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“…Redox equivalents can be exported from the chloroplasts by malate-oxaloacetate shuttle or DHAP-PGA shuttle (for detailed discussion see ref. 8). Although a blocking of mitochondrial oxidative phosphorylation would not totally inhibit mitochondrial respiration, due to the presence of the alternative pathway, the addition of oligomycin may reduce the capacity of the mitochondria to oxidize surplus redox equivalents from the chloroplasts and thus cause an increase in the reductive state of the stromal NADPH/NADP system and of the chloroplast electron transport carriers.…”

Section: Discussionmentioning

confidence: 99%

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

Krömer¹,

Heldt²

1991

Plant Physiol.

116

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Low concentrations of oligomycin, which strongly inhibit mitochondrial oxidative phosphorylation but do not affect chloroplast photophosphorylation, caused an inhibition of photosynthesis by 30 to 40% in barley (Hordeum vulgare L.) leaf protoplasts. This inhibition is reversed and the full rate of photosynthesis is regained when the protoplasts are ruptured so as to leave the chloroplasts intact. Oligomycin fed into barley leaves by the transpiration stream inhibited photosynthesis in these leaves by up to 60%. The measurement of metabolites in protoplast and leaf extracts showed that oligomycin caused a decrease in the ATP/ADP ratio and an increase in the content of glucose-and fructose 6-phosphate. Subcellular analysis of protoplasts revealed that the decrease in ATP/ADP ratio in the cytosol was larger than in the stroma and that the increase in hexose monophosphates was restricted to the cytosol, whereas the stromal hexosemonophosphates decreased upon the addition of oligomycin. Moreover, oligomycin caused an increase in the triosephosphate-3-phosphoglycerate ratio. It is concluded from these results that during photosynthesis of a plant leaf cell mitochondrial oxidative phosphorylation contributes to the ATP supply of the cell and prevents overreduction of the chloroplast redox carriers by oxidizing reductive equivalents generated by photosynthetic electron transport.It has been a matter of debate if in a plant leaf cell mitochondrial oxidative phosphorylation contributes to the supply of ATP during photosynthesis metabolism. In a previous publication (1 1), we investigated how to inhibit mitochondrial ATP synthesis in plant protoplasts without affecting photophosphorylation. A suitable inhibitor appeared to be oligomycin. It strongly inhibits mitochondrial oxidative phosphorylation (16) and has only a weak effect on photophosphorylation (10).Very low concentrations of oligomycin inhibiting mitochondrial oxidative phosphorylation caused a partial inhibition of protoplast photosynthesis that was observed only when the protoplasts were intact (1 1). When protoplasts that had been inhibited by oligomycin were ruptured by forcing them through a 5 ,um net, a procedure leaving chloroplasts and Supported by the Deutsche Forschungsgemeinschaft. mitochondria intact, photosynthesis of the released chloroplasts was recovered to the rate obtained in the absence of oligomycin.In a chloroplast suspension the volume of the external medium is about 1000 times larger than the stromal space of the chloroplasts. The phosphate in the medium functions as a reservoir for chloroplast photosynthesis and the products DHAP and PGA are diluted in the medium to such an extent that for the duration of the measurements photosynthesis is not affected by an accumulation of external products. In protoplasts, on the other hand, the volume of the cytosolic space is similar to the stromal one. Therefore, in the intact protoplasts photosynthesis can operate only if the products DHAP2 and PGA are further metabolized in the cytosol and th...

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Section: Discussionmentioning

confidence: 99%

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

Krömer¹,

Heldt²

1991

Plant Physiol.

116

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“…These pathways transfer reducing power from the chloroplast, through the cytosol, and into the mitochondria in a sort of 'bucket brigade' manner. One such shuttle involves the substrate couple, malate and oxaloacetate (Heber 1974;Heldt et al 1990;Raghavendra et al 1994;Hoefnagel et al 1998;Peltier & Cournac 2002). Currently, substrate shuttles are viewed as a minor component in overall ATP synthesis.…”

Section: Supply and Demandmentioning

confidence: 99%

Evolved physiological responses of phytoplankton to their integrated growth environment

Behrenfeld

Halsey

Milligan

2008

Phil. Trans. R. Soc. B

183

159

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Phytoplankton growth and productivity relies on light, multiple nutrients and temperature. These combined factors constitute the 'integrated growth environment'. Since their emergence in the Archaean ocean, phytoplankton have experienced dramatic shifts in their integrated growth environment and, in response, evolved diverse mechanisms to maximize growth by optimizing the allocation of photosynthetic resources (ATP and NADPH) among all cellular processes. Consequently, co-limitation has become an omnipresent condition in the global ocean. Here we focus on evolved phytoplankton populations of the contemporary ocean and the varied energetic pathways they employ to solve the optimization problem of resource supply and demand. Central to this discussion is the allocation of reductant formed through photosynthesis, which we propose has the following three primary fates: carbon fixation, direct use and ATP generation. Investment of reductant among these three sinks is tied to cell cycle events, differentially influenced by specific forms of nutrient stress, and a strong determinant of relationships between light-harvesting (pigment), photosynthetic electron transport and carbon fixation. Global implications of optimization are illustrated by deconvolving trends in the 10-year global satellite chlorophyll record into contributions from biomass and physiology, thereby providing a unique perspective on the dynamic nature of surface phytoplankton populations and their link to climate.

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“…In eukaryotes, separation of photosynthesis and respiration by NAD(P)H‐impermeable membranes of the chloroplast and mitochondria slightly complicates the situation. However, this problem is shared with carbohydrate metabolism in the cytosol and is solved in a “bucket brigade” fashion using “substrate shuttles” (Heber 1974, Heldt et al 1990, Raghavendra et al 1994, Hoefnagel et al 1998). Two prominent shuttle systems linking chloroplastic, cytosolic, and mitochondrial reductant pools are the “OAA‐malate shuttle” and the “dihydroxyacetone phosphate‐phosphoglyceric acid shuttle” (DHAP‐PGA).…”

Section: Life After Psii: Downstream Metabolic Pathwaysmentioning

confidence: 99%

IN SEARCH OF A PHYSIOLOGICAL BASIS FOR COVARIATIONS IN LIGHT‐LIMITED AND LIGHT‐SATURATED PHOTOSYNTHESIS¹

Behrenfeld

Prášil

Babin

et al. 2004

Journal of Phycology

227

198

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The photosynthesis‐irradiance (PE) relationship links indices of phytoplankton biomass (e.g. chl) to rates of primary production. The PE curve can be characterized by two variables: the light‐limited slope (αb) and the light‐saturated rate (Pbmax) of photosynthesis. Variability in PE curves can be separated into two categories: that associated with changes in the light saturation index, Ek (=Pbmax/αb) and that associated with parallel changes in αband Pbmax (i.e. no change in Ek). The former group we refer to as “Ek‐dependent” variability, and it results predominantly from photoacclimation (i.e. physiological adjustments in response to changing light). The latter group we refer to as “Ek‐independent” variability, and its physiological basis is unknown. Here, we provide the first review of the sporadic field and laboratory reports of Ek‐independent variability, and then from a stepwise analysis of potential mechanisms we propose that this important yet largely neglected phenomenon results from growth rate–dependent variability in the metabolic processing of photosynthetically generated reductants (and generally not from changes in the oxygen‐evolving PSII complexes). Specifically, we suggest that as growth rates decrease (e.g. due to nutrient stress), reductants are increasingly used for simple ATP generation through a fast (<1s) respiratory pathway that skips the carbon reduction cycle altogether and is undetected by standard PE methodologies. The proposed mechanism is consistent with the field and laboratory data and involves a simple new “twist” on established metabolic pathways. Our conclusions emphasize that simple reductants, not reduced carbon compounds, are the central currency of photoautotrophs.

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Transfer of Redox Equivalents Between Subcellular Compartments of a Leaf Cell

Cited by 10 publications

References 15 publications

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

Evolved physiological responses of phytoplankton to their integrated growth environment

IN SEARCH OF A PHYSIOLOGICAL BASIS FOR COVARIATIONS IN LIGHT‐LIMITED AND LIGHT‐SATURATED PHOTOSYNTHESIS¹

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Transfer of Redox Equivalents Between Subcellular Compartments of a Leaf Cell

Cited by 10 publications

References 15 publications

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

On the Role of Mitochondrial Oxidative Phosphorylation in Photosynthesis Metabolism as Studied by the Effect of Oligomycin on Photosynthesis in Protoplasts and Leaves of Barley (Hordeum vulgare)

Evolved physiological responses of phytoplankton to their integrated growth environment

IN SEARCH OF A PHYSIOLOGICAL BASIS FOR COVARIATIONS IN LIGHT‐LIMITED AND LIGHT‐SATURATED PHOTOSYNTHESIS1

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IN SEARCH OF A PHYSIOLOGICAL BASIS FOR COVARIATIONS IN LIGHT‐LIMITED AND LIGHT‐SATURATED PHOTOSYNTHESIS¹