Investigation of the apparent inefficiency of the coupling between Photosystem II electron transfer and ATP formation

Susan Flores, Donald Richard Ort

Research output: Contribution to journalArticle

Abstract

The maximum phosphorylation efficiency achieved with synchronous turnovers of Photosystem II (PS II) in spinach chloroplast lamellae is 0.3 molecules of ATP per pair of electrons transferred. This is the same as the efficiency observed for PS II operating alone in continuous light and would seem to indicate less than 50% coupling efficiency. Flash-induced ATP synthesis associated with both photosystems acting in unison closely approaches twice the flash-induced ATP synthesis associated with the Photosystem-I-dependent oxidation of duroquinol (itself 0.6) and comes close to equalling the highest efficiency observed in steady-state PS I + PS II electron transport. The anomalously low coupling efficiency seen when PS II is operating alone can be overcome by a ΔpH of two units imposed before flash illumination, or by a prior flash series involving the entire electron transfer chain. In contrast, prior electron transport through PS II alone is only slightly effective in enhancing the coupling efficiency of subsequent PS II turnovers. (It should be noted that in all cases where supplementary energy was provided, either by a proton gradient or by prior illumination, this supplementary energy was always below the energetic threshold for phosphorylation. Furthermore, the enhancement of PS II coupling efficiency by supplementary energy persisted even after a large number of subsequent PS II-inducing flashes). The efficiency of flash-induced ATP synthesis associated with whole-chain electron transfer or with PS-I-dependent duroquinol oxidation is also enhanced by the supplementary energy, but only during the first few inefficient flashes, suggesting that in this case the supplementary energy may simply be contributing to the initial build-up of an energetic threshold for ATP synthesis. This cannot be the case when the same supplementary energy contributes to the efficiency of the PS II reaction, since the enhancement then persists for a long time and contributes to an essentially constant flash yield of ATP. Our results imply that during electron transfer involving both photosystems, PS II participates in generating about half of the total ATP, whereas it operates inefficiently only when operating alone. Since hydrogen ions produced by PS I are able to raise the efficiency of subsequent PS-II-dependent phosphorylation, at least some cooperation between the two photosystems takes place and this suggests some donation of protons from PS I to PS II. However, the inability of PS II alone to achieve high efficiency, even with prolonged pre-illumination, would seem to indicate some functional distinction of protons from the two photosystems.

Original languageEnglish (US)
Pages (from-to)289-302
Number of pages14
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume766
Issue number2
DOIs
StatePublished - 1984

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Photosystem II Protein Complex
Adenosine Triphosphate
Electrons
Phosphorylation
Protons
Lighting
Electron Transport
Photosystem I Protein Complex
Oxidation
Spinacia oleracea
Chloroplasts

Keywords

  • 2,5 or 2,6-dimethylbenzoquinone
  • 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone
  • 3(N-morpholino)-2-hydroxypropanesulfonic acid
  • 3-(3,4-dichlorophenyl)-1,1-dimethylurea
  • 4-morpholineethanesulfonic acid
  • ATP formation
  • ATP/e
  • Chl
  • chlorophyll
  • Coupling efficiency
  • DAD
  • DBMIB
  • DCMU
  • diiminodurene
  • DMQ
  • Electron transfer
  • Heppso
  • Mes
  • Mopso
  • N-hydroxyethylpiperazine-N′-2-hydroxypropanesulfonic acid
  • N-[2-hydroxy-1,1-bis(hydroxymethyl)ethyl]glycine
  • oxidized N′,N′,N,N-tetramethyl-p-phenylenediamine
  • phosphorylation efficiency, number of ATP molecules synthesized per pair of electrons transferred
  • Photosystem I
  • Photosystem II
  • Photosystem II
  • protonmotive force
  • PS I
  • PS II
  • Spinach chloroplast
  • TMPD
  • transmembrane proton activity difference
  • Tricine
  • Δp
  • ΔpH

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Cell Biology

Cite this

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title = "Investigation of the apparent inefficiency of the coupling between Photosystem II electron transfer and ATP formation",
abstract = "The maximum phosphorylation efficiency achieved with synchronous turnovers of Photosystem II (PS II) in spinach chloroplast lamellae is 0.3 molecules of ATP per pair of electrons transferred. This is the same as the efficiency observed for PS II operating alone in continuous light and would seem to indicate less than 50{\%} coupling efficiency. Flash-induced ATP synthesis associated with both photosystems acting in unison closely approaches twice the flash-induced ATP synthesis associated with the Photosystem-I-dependent oxidation of duroquinol (itself 0.6) and comes close to equalling the highest efficiency observed in steady-state PS I + PS II electron transport. The anomalously low coupling efficiency seen when PS II is operating alone can be overcome by a ΔpH of two units imposed before flash illumination, or by a prior flash series involving the entire electron transfer chain. In contrast, prior electron transport through PS II alone is only slightly effective in enhancing the coupling efficiency of subsequent PS II turnovers. (It should be noted that in all cases where supplementary energy was provided, either by a proton gradient or by prior illumination, this supplementary energy was always below the energetic threshold for phosphorylation. Furthermore, the enhancement of PS II coupling efficiency by supplementary energy persisted even after a large number of subsequent PS II-inducing flashes). The efficiency of flash-induced ATP synthesis associated with whole-chain electron transfer or with PS-I-dependent duroquinol oxidation is also enhanced by the supplementary energy, but only during the first few inefficient flashes, suggesting that in this case the supplementary energy may simply be contributing to the initial build-up of an energetic threshold for ATP synthesis. This cannot be the case when the same supplementary energy contributes to the efficiency of the PS II reaction, since the enhancement then persists for a long time and contributes to an essentially constant flash yield of ATP. Our results imply that during electron transfer involving both photosystems, PS II participates in generating about half of the total ATP, whereas it operates inefficiently only when operating alone. Since hydrogen ions produced by PS I are able to raise the efficiency of subsequent PS-II-dependent phosphorylation, at least some cooperation between the two photosystems takes place and this suggests some donation of protons from PS I to PS II. However, the inability of PS II alone to achieve high efficiency, even with prolonged pre-illumination, would seem to indicate some functional distinction of protons from the two photosystems.",
keywords = "2,5 or 2,6-dimethylbenzoquinone, 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, 3(N-morpholino)-2-hydroxypropanesulfonic acid, 3-(3,4-dichlorophenyl)-1,1-dimethylurea, 4-morpholineethanesulfonic acid, ATP formation, ATP/e, Chl, chlorophyll, Coupling efficiency, DAD, DBMIB, DCMU, diiminodurene, DMQ, Electron transfer, Heppso, Mes, Mopso, N-hydroxyethylpiperazine-N′-2-hydroxypropanesulfonic acid, N-[2-hydroxy-1,1-bis(hydroxymethyl)ethyl]glycine, oxidized N′,N′,N,N-tetramethyl-p-phenylenediamine, phosphorylation efficiency, number of ATP molecules synthesized per pair of electrons transferred, Photosystem I, Photosystem II, Photosystem II, protonmotive force, PS I, PS II, Spinach chloroplast, TMPD, transmembrane proton activity difference, Tricine, Δp, ΔpH",
author = "Susan Flores and Ort, {Donald Richard}",
year = "1984",
doi = "10.1016/0005-2728(84)90244-5",
language = "English (US)",
volume = "766",
pages = "289--302",
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TY - JOUR

T1 - Investigation of the apparent inefficiency of the coupling between Photosystem II electron transfer and ATP formation

AU - Flores, Susan

AU - Ort, Donald Richard

PY - 1984

Y1 - 1984

N2 - The maximum phosphorylation efficiency achieved with synchronous turnovers of Photosystem II (PS II) in spinach chloroplast lamellae is 0.3 molecules of ATP per pair of electrons transferred. This is the same as the efficiency observed for PS II operating alone in continuous light and would seem to indicate less than 50% coupling efficiency. Flash-induced ATP synthesis associated with both photosystems acting in unison closely approaches twice the flash-induced ATP synthesis associated with the Photosystem-I-dependent oxidation of duroquinol (itself 0.6) and comes close to equalling the highest efficiency observed in steady-state PS I + PS II electron transport. The anomalously low coupling efficiency seen when PS II is operating alone can be overcome by a ΔpH of two units imposed before flash illumination, or by a prior flash series involving the entire electron transfer chain. In contrast, prior electron transport through PS II alone is only slightly effective in enhancing the coupling efficiency of subsequent PS II turnovers. (It should be noted that in all cases where supplementary energy was provided, either by a proton gradient or by prior illumination, this supplementary energy was always below the energetic threshold for phosphorylation. Furthermore, the enhancement of PS II coupling efficiency by supplementary energy persisted even after a large number of subsequent PS II-inducing flashes). The efficiency of flash-induced ATP synthesis associated with whole-chain electron transfer or with PS-I-dependent duroquinol oxidation is also enhanced by the supplementary energy, but only during the first few inefficient flashes, suggesting that in this case the supplementary energy may simply be contributing to the initial build-up of an energetic threshold for ATP synthesis. This cannot be the case when the same supplementary energy contributes to the efficiency of the PS II reaction, since the enhancement then persists for a long time and contributes to an essentially constant flash yield of ATP. Our results imply that during electron transfer involving both photosystems, PS II participates in generating about half of the total ATP, whereas it operates inefficiently only when operating alone. Since hydrogen ions produced by PS I are able to raise the efficiency of subsequent PS-II-dependent phosphorylation, at least some cooperation between the two photosystems takes place and this suggests some donation of protons from PS I to PS II. However, the inability of PS II alone to achieve high efficiency, even with prolonged pre-illumination, would seem to indicate some functional distinction of protons from the two photosystems.

AB - The maximum phosphorylation efficiency achieved with synchronous turnovers of Photosystem II (PS II) in spinach chloroplast lamellae is 0.3 molecules of ATP per pair of electrons transferred. This is the same as the efficiency observed for PS II operating alone in continuous light and would seem to indicate less than 50% coupling efficiency. Flash-induced ATP synthesis associated with both photosystems acting in unison closely approaches twice the flash-induced ATP synthesis associated with the Photosystem-I-dependent oxidation of duroquinol (itself 0.6) and comes close to equalling the highest efficiency observed in steady-state PS I + PS II electron transport. The anomalously low coupling efficiency seen when PS II is operating alone can be overcome by a ΔpH of two units imposed before flash illumination, or by a prior flash series involving the entire electron transfer chain. In contrast, prior electron transport through PS II alone is only slightly effective in enhancing the coupling efficiency of subsequent PS II turnovers. (It should be noted that in all cases where supplementary energy was provided, either by a proton gradient or by prior illumination, this supplementary energy was always below the energetic threshold for phosphorylation. Furthermore, the enhancement of PS II coupling efficiency by supplementary energy persisted even after a large number of subsequent PS II-inducing flashes). The efficiency of flash-induced ATP synthesis associated with whole-chain electron transfer or with PS-I-dependent duroquinol oxidation is also enhanced by the supplementary energy, but only during the first few inefficient flashes, suggesting that in this case the supplementary energy may simply be contributing to the initial build-up of an energetic threshold for ATP synthesis. This cannot be the case when the same supplementary energy contributes to the efficiency of the PS II reaction, since the enhancement then persists for a long time and contributes to an essentially constant flash yield of ATP. Our results imply that during electron transfer involving both photosystems, PS II participates in generating about half of the total ATP, whereas it operates inefficiently only when operating alone. Since hydrogen ions produced by PS I are able to raise the efficiency of subsequent PS-II-dependent phosphorylation, at least some cooperation between the two photosystems takes place and this suggests some donation of protons from PS I to PS II. However, the inability of PS II alone to achieve high efficiency, even with prolonged pre-illumination, would seem to indicate some functional distinction of protons from the two photosystems.

KW - 2,5 or 2,6-dimethylbenzoquinone

KW - 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone

KW - 3(N-morpholino)-2-hydroxypropanesulfonic acid

KW - 3-(3,4-dichlorophenyl)-1,1-dimethylurea

KW - 4-morpholineethanesulfonic acid

KW - ATP formation

KW - ATP/e

KW - Chl

KW - chlorophyll

KW - Coupling efficiency

KW - DAD

KW - DBMIB

KW - DCMU

KW - diiminodurene

KW - DMQ

KW - Electron transfer

KW - Heppso

KW - Mes

KW - Mopso

KW - N-hydroxyethylpiperazine-N′-2-hydroxypropanesulfonic acid

KW - N-[2-hydroxy-1,1-bis(hydroxymethyl)ethyl]glycine

KW - oxidized N′,N′,N,N-tetramethyl-p-phenylenediamine

KW - phosphorylation efficiency, number of ATP molecules synthesized per pair of electrons transferred

KW - Photosystem I

KW - Photosystem II

KW - Photosystem II

KW - protonmotive force

KW - PS I

KW - PS II

KW - Spinach chloroplast

KW - TMPD

KW - transmembrane proton activity difference

KW - Tricine

KW - Δp

KW - ΔpH

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