Cyclic electron flow is redox-controlled but independent of state transition

Abstract

Photosynthesis is the biological process that feeds the biosphere with reduced carbon. The assimilation of CO2 requires the fine tuning of two co-existing functional modes: linear electron flow, which provides NADPH and ATP, and cyclic electron flow, which only sustains ATP synthesis. Although the importance of this fine tuning is appreciated, its mechanism remains equivocal. Here we show that cyclic electron flow as well as formation of supercomplexes, thought to contribute to the enhancement of cyclic electron flow, are promoted in reducing conditions with no correlation with the reorganization of the thylakoid membranes associated with the migration of antenna proteins towards Photosystems I or II, a process known as state transition. We show that cyclic electron flow is tuned by the redox power and this provides a mechanistic model applying to the entire green lineage including the vast majority of the cases in which state transition only involves a moderate fraction of the antenna.

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…S5). Incidentally, our measurements of a transient PSI-CEF under state II provide, to our knowledge, the first in vivo support to the occurrence of PSI-CEF without any direct correlation with state transitions (Takahashi et al, 2013;Alric, 2014).…”

“…NADPH to PQ; Alric, 2014), as well as the PSI electron transfer due to acceptor side limitation (Takahashi et al, 2013). It is tempting to propose that hydrogenase activity, by partially reoxidizing the PQ pool and FDX, might directly contribute to set the redox poise, allowing the PSI-CEF to operate.…”

“…In anoxia, both PQ and PSI acceptor pools are almost fully reduced (Bennoun, 1982;Ghysels et al, 2013;Godaux et al, 2013;Takahashi et al, 2013), which might hamper the putative limiting step of PSI-CEF electron transfer (i.e. NADPH to PQ; Alric, 2014), as well as the PSI electron transfer due to acceptor side limitation (Takahashi et al, 2013).…”

Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of ƊATPase pgr5 and ƊrbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii

“…In the green Chlorophyte alga, C. reinhardtii, supercomplex formation between PGRL1 and PSI-LHCI (for Light-Harvesting Complex)-LHCII-Fd-NADPH reductasecytochrome b 6 f (Iwai et al, 2010;Takahashi et al, 2013) as well as the Ca 2+ sensor protein and the protein Anaerobic Response1 (ANR1; Terashima et al, 2012) is promoted under anoxic conditions. Anoxia reduces the redox poise of the stroma, which has been shown to enhance CEF [measured in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU)] in the wildtype line but not pgrl1 mutant cells (Tolleter et al, 2011).…”

Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants

“…[35]). In C. reinhardtii, the formation of a supercomplex including PSI-LHCI and cytochrome b 6 f, which also involves the association of ferredoxin-NADPH oxidoreductase, PGRL1, Ca 2+ sensor protein, and anaerobic response 1 protein, is shown to mediate cyclic electron flow [36][37][38].…”