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

Susan Flores, Donald R. Ort

Research output: Contribution to journalArticlepeer-review

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 - Jan 1 1984

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
  • Coupling efficiency
  • DAD
  • DBMIB
  • DCMU
  • DMQ
  • Electron transfer
  • Heppso
  • Mes
  • Mopso
  • N-[2-hydroxy-1,1-bis(hydroxymethyl)ethyl]glycine
  • N-hydroxyethylpiperazine-N′-2-hydroxypropanesulfonic acid
  • PS I
  • PS II
  • Photosystem I
  • Photosystem II
  • Photosystem II
  • Spinach chloroplast
  • TMPD
  • Tricine
  • chlorophyll
  • diiminodurene
  • oxidized N′,N′,N,N-tetramethyl-p-phenylenediamine
  • phosphorylation efficiency, number of ATP molecules synthesized per pair of electrons transferred
  • protonmotive force
  • transmembrane proton activity difference
  • Δp
  • ΔpH

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Cell Biology

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