Regulation of light energy conversion between linear and cyclic electron flow within photosystem II controlled by the plastoquinone/quinol redox poise

Colin Gates, Gennady Ananyev, Shatabdi Roy-Chowdhury, Petra Fromme, G. Charles Dismukes

Research output: Contribution to journalArticlepeer-review

Abstract

Ultrapurified Photosystem II complexes crystalize as uniform microcrystals (PSIIX) of unprecedented homogeneity that allow observation of details previously unachievable, including the longest sustained oscillations of flash-induced O2 yield over > 200 flashes and a novel period-4.7 water oxidation cycle. We provide new evidence for a molecular-based mechanism for PSII-cyclic electron flow that accounts for switching from linear to cyclic electron flow within PSII as the downstream PQ/PQH2 pool reduces in response to metabolic needs and environmental input. The model is supported by flash oximetry of PSIIX as the LEF/CEF switch occurs, Fourier analysis of O2 flash yields, and Joliot-Kok modeling. The LEF/CEF switch rebalances the ratio of reductant energy (PQH2) to proton gradient energy (H+o/H+i) created by PSII photochemistry. Central to this model is the requirement for a regulatory site (QC) with two redox states in equilibrium with the dissociable secondary electron carrier site QB. Both sites are controlled by electrons and protons. Our evidence fits historical LEF models wherein light-driven water oxidation delivers electrons (from QA) and stromal protons through QB to generate plastoquinol, the terminal product of PSII-LEF in vivo. The new insight is the essential regulatory role of QC. This site senses both the proton gradient (H+o/H+i) and the PQ pool redox poise via e/H+ equilibration with QB. This information directs switching to CEF upon population of the protonated semiquinone in the Qc site (QH+)C, while the WOC is in the reducible S2 or S3 states. Subsequent photochemical primary charge separation (P+QA) forms no (QH2)B, but instead undergoes two-electron backward transition in which the QC protons are pumped into the lumen, while the electrons return to the WOC forming (S1/S2). PSII-CEF enables production of additional ATP needed to power cellular processes including the terminal carboxylation reaction and in some cases PSI-dependent CEF.

Original languageEnglish (US)
JournalPhotosynthesis research
DOIs
StateAccepted/In press - 2022
Externally publishedYes

Keywords

  • Electron acceptors
  • Kok model
  • Microcrystals
  • Oxygen evolution
  • Photosystem II
  • VZAD
  • Water-oxidizing complex

ASJC Scopus subject areas

  • Biochemistry
  • Plant Science
  • Cell Biology

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