Regulatory electron transport pathways in cyclic photophosphorylation

A major breakthrough in our understanding of how plants oxidize water to molecular 02 was the discovery by P. Joliot and co-workers that the 02 yield per flash, in a series of light flashes, oscillates with a periodicity of 4. This led to the concept by B. Kok and co-workers that these reactions involve accumulation of four positive charges in independent "02-evolving centers," which undergo a series of changes in their redox state (the so-called S states). In the present paper, we have applied optical techniques (such as thermoluminescence and delayed light emission, both discovered by W. Arnold and co-workers) to monitor charge storage on the 02-evolving system in leaves from higher plants. We observed a period of four oscillations in both thermoluminescence and delayed light emission, with maxima on flashes 2 and 6, establishing a relationship with the charge accumulation process in photosynthesis. These measurements provided additional new information: the deactivation of the "02-evolving centers," which cannot be measured by the 02 method in the leaves, is in the 20-to 30-s range; and in the dark-adapted leaves, the secondary bound plastoquinone molecule (the so-called secondary electron acceptor QB) is in equal concentration in its reduced and oxidized forms. The origin of thermoluminescence and delayed light emission, in terms of the recombination of charges on the 02-evolving and plastoquinone sides, is also discussed.In spite of some new developments, the chemistry of oxidation of water to molecular 02 remains a poorly understood process (1, 2). Joliot et al. (3) (11) and by Lavorel (7), respectively. The flash-induced TL in control thylakoids has been identified as arising from S2QBor S3Q-recombination (12). This TL corresponds to a slow phase of DLE (decaying in the seconds-to-minutes time scale) recorded after flash excitation of thylakoids at room temperature (13). When diuron, which inhibits electron flow from QX to QB, is added to thylakoids, the flash-induced TL band is shifted to a lower temperature (11,12,14) and the 30-s phase of DLE is replaced by one decaying within a few seconds (13,15). The DLE in the presence of diuron is attributed to S2QA and S3QX recombination (12)(13)(14)(15)(16). These recent advances have allowed the measurement of slow DLE and TL to be used as probes of PS II photochemistry in thylakoids.Luminescence techniques have one great advantage over the majority of other probes of PS II: they can be adapted easily to the study of leaves. In this work, the recent developments in our understanding of DLE and TL have been applied to a study of PS II in leaves, and several of the phenomena associated with PS II that previously have been reported only in isolated thylakoids and algal cells have been measured in leaves. (i) Charge storage on the oxygen-evolving enzyme has been monitored as a period of four oscillations of a TL band at around 30'C and of a slow phase of DLE after a series of flashes. The luminescence is attributed to recombination of S2Q-and S3QB. (ii) Fr...

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“…This is thought to be due to a feedback of electrons into the PQ pool (e.g., refs. [30][31][32]. Such a system may be functional also in leaves.…”

Section: Resultsmentioning

confidence: 99%

Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission

Rutherford

Govindjee

Inoue

1984

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

122

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“…Electron transport results in ferredoxin reduction; proton transport results in the stoichiometrically coupled ATP formation (2). Reduced ferredoxin is the carrier ofphotosynthetic reducing power (35) that provides (directly or via NADP+) a conduit for massive electron flow for bioreductions [of CO2 (as phosphoglycerate), NO2-, SO32-] or a trickle of electron flow for regulation, as in cyclic photophosphorylation (36,37) or in thioredoxin-regulated chloroplast enzymes (38). By contrast, the role of the anoxygenic photosystem is limited to ATP production.…”

Section: Resultsmentioning

confidence: 99%

Proton transport in photooxidation of water: A new perspective on photosynthesis

Arnon

Tsujimoto

Tang

1981

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

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The currently prevalent concept of the generation of photosynthetic reducing power in oxygen-evolving cells envisions a linear (noncyclic) electron flow from water to ferredoxin (and thence to NADP+) that requires the collaboration of photosystems I and 11 (PSI and PSII) joined by plastoquinone and other electron carriers (the Z scheme). The essence of the Z scheme is that only PSI can reduce ferredoxin-i.e., that, after being energized to an intermediate reducing potential by PSII, electrons from water are transported via plastoquinone to PSI which energizes the electrons to their ultimate reducing potential adequate for the reduction of ferredoxin. Basic to the Z scheme is the function of plastoquinone as the obligatory link in electron transport from PSIl to PSI. However, we have found that, when plastoquinone function was inhibited, ferredoxin was photoreduced by water without the collaboration of PSI. We now report evidence for an important function of plastoquinone in the translocation of protons liberated inside the thylakoid membrane by photooxidation of water. When the oxygenic photoreduction (i.e., by water) of ferredoxin was blocked by plastoquinone inhibitors, dibromothymoquinone or dinitrophenol ether of iodonitrothymol, the photoreduction of ferredoxin was restored by each of four chemically diverse uncouplers, similar only in their ability to facilitate proton movement across membranes. Similar results were obtained for the oxygenic reduction of NADP'. Our results suggest that the light-induced electron flow from water cannot be maintained unless the simultaneously liberated protons are removed from inside the membrane via plastoquinone. The new evidence is embodied in a concept of an oxygenic photosystem for photosynthetic electron and proton transport, which we propose as an alternative to the Z scheme, to account for photoreduction offerredoxin-NADP+ by water and the coupled oxygenic (formerly noncyclic) ATP formation without involving PSI. The role of the anoxygenic photosystem (formerly called PSI) is ATP formation by cyclic photophosphorylation.Photooxidation of water, 2H20-) 4 e-+ 4H + 02, is a key reaction in plant photosynthesis. Aside from its all-important by-product, oxygen, the liberated electrons eventually reduce ferredoxin (1, 2) and then NADP+ (3), thereby accounting for photosynthetic reducing power; the liberated protons contribute to the protonmotive force (4, 5) which accounts for the ("noncyclic") ATP formation that is coupled to NADP+ reduction (6).Photooxidation of water takes place inside the thylakoid membranes (7). These contain two photocenters identified with photosystems I and II (PSI and PSII) and a chain of carriers responsible for the transport ofelectrons and protons within and across the membrane. According to the now-prevalent concepts embodied in the so-called Z scheme (8, 9), PSII photooxidizes water but cannot reduce ferredoxin because it can energize the released electrons only to an intermediate potential; the electrons are transported from PSII t...

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“…It is proposed that, as the name 'reductant-dependent oxidation' implies, reducing equivalents generated in the light by photosystem I drive the oxidation of cytochrome b-563 as illustrated in scheme (B). If reduced ferredoxin functions as an electron donor to PQ rather than to cytochrome b-563 as proposed in [3,8,25,26], then illumination might be expected to initiate this oxidation. As electrons enter PQ from ferredoxin and cytochrome b-563, the requirement for ferredoxin in cyclic photophosphorylation is fulfilled [lo] along with ATP formation under long wavelength illumination [lo].…”

Section: Discussionmentioning

confidence: 99%

Regulatory electron transport pathways in cyclic photophosphorylation

Cited by 40 publications

References 38 publications

Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission

Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission

Proton transport in photooxidation of water: A new perspective on photosynthesis

Evidence for a reluctant‐dependent oxidation of chloroplast cytochrome b‐563

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