Role of Ferredoxin in Photosynthetic Production of Oxygen and Phosphorylation by Chloroplasts

Arnon, Daniel I.; Tsujimoto, Harry Y.; McSwain, Berah D.

doi:10.1073/pnas.51.6.1274

Cited by 63 publications

(20 citation statements)

References 11 publications

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“…Experiments by Arnon et al [2] showed that on reduction of ferredoxin by illuminated chloroplasts one molecule of oxygen was evolved per four molecules of ferredoxin reduced, in agreement with the observation that spinach ferredoxin accepts one electron when it is reduced [3]. On reoxidation of the ferredoxin in the dark, one molecule of oxygen was taken up per four molecules of ferredoxin reoxidized.…”

Section: Introductionsupporting

confidence: 62%

“…1) a small amount of oxygen was evolved and on switching off the light a similar amount of oxygen was taken up. This was presumably associated with the reduction and reoxidation of ferredoxin, as in the experiments of Arnon et al [2]. Our experiments show that the initial product of ferredoxin-catalyzed electron transport is hydrogen peroxide and not water.…”

Section: Remits and Discussionmentioning

confidence: 48%

“…Our experiments show that the initial product of ferredoxin-catalyzed electron transport is hydrogen peroxide and not water. This was apparently not detected by Arnon et al [2] owing to the presence of catalase activity in their isolated chloroplasts. The chloroplasts used in our experiments showed only a very low level of endogenous eatalase acitivity.…”

Section: Remits and Discussionmentioning

confidence: 73%

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Hydrogen peroxide as the product of autoxidation of ferredoxin: Reduced either chemically or by illuminated chloroplasts

1970

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Section: Introductionsupporting

confidence: 62%

Section: Remits and Discussionmentioning

confidence: 48%

Section: Remits and Discussionmentioning

confidence: 73%

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Hydrogen peroxide as the product of autoxidation of ferredoxin: Reduced either chemically or by illuminated chloroplasts

1970

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“…Reduced ferredoxin can be reoxidized by oxygen (19,4) and may thus catalyze a pseudocyclic photophosphorylation which, like the true cyclic type, yields only ATP but in reality is a variant of noncyclic photophosphorylation that depends on continuous production and consumption of oxygen (20,10).…”

Section: Resultsmentioning

confidence: 99%

Regulation of ferredoxin-catalyzed photosynthetic phosphorylations.

Arnon¹,

Chain²

1975

Proc. Natl. Acad. Sci. U.S.A.

134

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Under aerobic conditions that are likely to prevail in chloroplasts in vivo, the optimal concentration of ferredoxin for cyclic photophosphorylation was found to be equal to that required for NADP reduction and about onetenth of that needed for cyclic photophosphorylation under anaerobic conditions. In the presence of ferredoxin and NADP, cyclic photophosphorylation operated concurrently with noncyclic photophosphorylation, producing an ATP: NADPH ratio of about 1.5. The effective operation of ferredoxin-catalyzed cyclic photophosphorylation by itself required a curtailment of the electron flow from water which was accomplished experimentally by the use of either an inhibitor or far-red monochromatic light. An unexpected discovery was that the operation of cyclic photophosphorylation by itself was also regulated by a back reaction of NADPH and ferredoxin with two components of chloroplast membranes, component C550 and cytochrome b559. The significance of these findings to photosynthesis in vivo is discussed.Solar energy is first converted into biologically useful chemical energy by photosynthetic phosphorylation (photophosphorylation), the process by which the photosynthetic apparatus transforms the electromagnetic energy of sunlight into phosphate bond energy of ATP, the universal energy carrier of living cells. The energy of the photochemically generated ATP and reducing power is conserved through the biosynthesis of organic compounds from CO2. When these are later degraded by fermentation and respiration, reducing power and ATP are regenerated to drive the multitude of endergonic reactions and activities of living cells.Chloroplasts, the photosynthetic organelles of green plants, have two types of photophosphorylation, cyclic and noncyclic, names devised to denote the coupling of ATP formation to a light-induced electron flow that is either of a closed (cyclic) type that yields only ATP or of a unidirectional (noncyclic) type that yields not only ATP but also NADPH as reducing power (1). Ferredoxin plays a key role in both. In cyclic photophosphorylation ferredoxin is the endogenous catalyst (2, 3) and in noncyclic photophosphorylation ferredoxin is the electron acceptor (4) that in turn reduces NADP by an enzymatic reaction that is independent of light (5).In this paper we report the concurrent operation of ferredoxin-dependent cyclic and noncyclic photophosphorylation under conditions that are likely to exist in chloroplasts in vivo. These experiments led to the discovery that noncyclic electron flow provides a regulatory mechanism that permits cyclic photophosphorylation to operate either concurrently with the noncyclic type (and thereby to increase the ratio of ATP to NADPH as needed for photosynthetic CO2 assimilation) or to operate by itself and produce only ATP for those endergonic reactions that do not require photochemically generated reducing power. Illumination. Incident monochromatic illumination was provided by a 250 W tungsten-halogen lamp (General Electric type EHN) and appropriate inte...

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“…The role assigned to ferredoxin as the terminal electron acceptor in the photochemical events that lead to NADP reduction was further documented when the photoreduction of substrate amounts of ferredoxin was found to be accompanied by stoichiometric oxygen evolution and ATP formation (79). Earlier formulations of noncyclic photophosphorylation (63,64) were now further refined to show that the omission of NADP did not affect ATP formation.…”

Section: Nadpmentioning

confidence: 99%

The Light Reactions of Photosynthesis

Arnon

1971

Proc. Natl. Acad. Sci. U.S.A.

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Historically, the role of light in photosvnthesis has been ascribed either to a photolysis of carbon dioxide or to a photolysis of water and a resultant rearrangement of constituent atoms into molecules of oxygen and glucose (or formaldehyde). The discovery of photophosphorylation demonstrated that photosynthesis includes a light-induced phosphorus metabolism that precedes, and is independent from, a photolysis of water or CO2. ATP formation could best be accounted for not by a photolytic disruption of the covalent bonds in C02 or water but by the operation of a light-induced electron flow that results in a release of free energy which is trapped in the pyrophosphate bonds of ATP.Photophosphorylation is now divided into (a) a noncyclic type, in which the formation of ATP is coupled with a light-induced electron transport from water to ferredoxin and a concomitant evolution of oxygen and (b) a cyclic type which yields only ATP and produces no net change in the oxidation-reduction state of any electron donor or acceptor. Reduced ferredoxin formed in (a) serves as an electron donor for the reduction of NADP by an enzymic reaction that is independent of light. ATP, from both cyclic and noncyclic photophosphorylation, and reduced NADP jointly constitute the assimilatory power for the conversion of C02 to carbohydrates (3 moles of ATP and 2 moles of reduced NADP are required per mole of C02).Investigations, mainly with whole cells, have shown that photosynthesis in green plants involves two photosystems, one (System II) that best uses light of "short" wavelength (X < 685 nm) and another (System I) that best uses light of "long" wavelength (X > 685 nm). Cyclic photophosphorylation in chloroplasts involves a System I photoreaction. Noncyclic photophosphorylation is widely held to involve a collaboration of two photoreactions: a short-wavelength photoreaction belonging to System II and a long-wavelength photoreaction belonging to System I. Recent findings, however, indicate that noncyclic photophosphorylation may include two short-wavelength, System II, photoreactions that operate in series and are joined by a "dark" electron-transport chain to which is coupled a phosphorylation site. Early conceptsThe first hypothesis about the role of light in photosynthesis came very appropriately from Jan Ingenhousz, who some years earlier had made the epochal discovery that it is "the influence of the light of the sun upon the plant" (1) that is responsible for the "restorative" effect of vegetation on "bad" air-an observation first made in 1771 by Joseph Priestley without reference to light (2). In 1796, Ingenhousz wrote that the green plant absorbs from "carbonic acid in the sunshine, the carbon, throwing out at that time the oxygen alone, and keeping the carbon to itself as nourishment" (3).The idea that light liberates oxygen by photodecomposing C02 had, with some modifications, persisted for well over a century. It seemed to have had a special attraction for some of the most illustrious chemists in their day, e.g., von ...

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Role of Ferredoxin in Photosynthetic Production of Oxygen and Phosphorylation by Chloroplasts

Cited by 63 publications

References 11 publications

Hydrogen peroxide as the product of autoxidation of ferredoxin: Reduced either chemically or by illuminated chloroplasts

Hydrogen peroxide as the product of autoxidation of ferredoxin: Reduced either chemically or by illuminated chloroplasts

Regulation of ferredoxin-catalyzed photosynthetic phosphorylations.

The Light Reactions of Photosynthesis

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