Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids

Abstract

The chloroplast must regulate supply of reducing equivalents and ATP to meet rapid changes in downstream metabolic demands. Cyclic electron flow around photosystem I (CEF) is proposed to balance the ATP/NADPH budget by using reducing equivalents to drive plastoquinone reduction, leading to the generation of proton motive force and subsequent ATP synthesis. While high rates of CEF have been observed in vivo, isolated thylakoids show only very slow rates, suggesting that the activity of a key complex is lost or down-regulated upon isolation. We show that isolation of thylakoids while in the continuous presence of reduced thiol reductant dithiothreitol (DTT), but not oxidized DTT, maintains high CEF activity through an antimycin A sensitive ferredoxin:quinone reductase (FQR). Maintaining low concentrations (~2 mM) of reduced DTT while modulating the concentration of oxidized DTT leads to reversible activation/inactivation of CEF with an apparent midpoint potential of -306 mV (±10 mV) and n=2, consistent with redox modulation of a thiol/disulfide couple and thioredoxin-mediated regulation of the plastoquinone reductase involved in the antimycin A-sensitive pathway, possibly at the level of the PGRL1 protein. Based on proposed differences in regulatory modes, we propose that the FQR and NADPH:plastoquinone oxidoreductase (NDH) pathways for CEF are activated under different conditions and fulfill different roles in chloroplast energy balance.

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…Recently, evidence for redox regulation has emerged for many other processes, including PET. Cyclic electron flow (CEF) via ferredoxin-dependent quinone reductase is sensitive to antimycin A and is stimulated by thiol-reducing conditions, with a redox midpoint potential of 2306 mV (Strand et al, 2016). In a converse manner, the NADPH dehydrogenase-dependent CEF pathway is activated by oxidizing conditions in vivo after H 2 O 2 infiltration or in mutants with enhanced production of chloroplast H 2 O 2 (Strand et al, 2015).…”

In Silico Analysis of the Regulation of the Photosynthetic Electron Transport Chain in C3 Plants

“…1). NDH and FQR are modeled taking into account the effect of pmf on NDH (Strand et al, 2017) and the redox regulation of FQR (Strand et al, 2016). WWC and NiR are simulated by constructing rate equations based on published kinetics, whereas MDH and export of malate are modeled as proposed by Fridlyand et al (Fridlyand et al, 1998).…”

“…Although several experimental techniques are available to study CET and ANCET (Bloom et al, 2002;Munekage et al, 2002;Driever and Baker, 2011;Walker et al, 2014;Strand et al, 2016), little is known about the interactions among the different mechanisms involved. Similarly, recent technological developments (Sacksteder et al, 2000) have led to a better understanding of the regulation of ATPase (Kanazawa and Kramer, 2002), the partitioning of pmf into DC and DpH (Cruz et al, 2001;Takizawa et al, 2007), and the range of lumen pH that is physiologically feasible (Kramer et al, 1999), but the interactions among the reactions that determine pmf have not been fully elucidated .…”

Photosynthesis of microalgae in outdoor mass cultures and modelling its effects on biomass productivity for fuels, feeds and chemicals

“…The FQR/pgr5 pathway is fast, generates a rapid proton motive force and is believed to be the main contributor to ATP production (Johnson et al, 2014). In contrast, the NDH pathway is relatively slow but is considered as a major stress response signaled by H2O2, such as in cases where large ATP deficiencies and / or redox imbalances occur (Strand et al, 2016).…”

“…Under optimal steady state light flux, a balance of mostly linear and some cyclic electron flows create a high ΔpH in the lumen needed to power ATP synthase and ensure the strict stoichiometry of ATP:NADPH required by the Calvin-Benson-Bassham (CBB) cycle such that carbon assimilation runs at near maximum efficiency (Strand et al, 2016, Cardol et al, 2011. In contrast, light fluctuations, particularly from light to total darkness and vice versa, disrupt the strong pH gradient of the thylakoid lumen and consequently slow down the ATP synthase upon returning into the light, relative to the rate of electron transfer (Rochaix, 2011).…”