The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow

Abstract

Cyclic electron flow around photosystem I (CEF) is critical for balancing the photosynthetic energy budget of the chloroplast by generating ATP without net production of NADPH. We demonstrate that the chloroplast NADPH dehydrogenase complex, a homolog to respiratory Complex I, pumps approximately two protons from the chloroplast stroma to the lumen per electron transferred from ferredoxin to plastoquinone, effectively increasing the efficiency of ATP production via CEF by 2-fold compared with CEF pathways involving non-proton-pumping plastoquinone reductases. By virtue of this proton-pumping stoichiometry, we hypothesize that NADPH dehydrogenase not only efficiently contributes to ATP production but operates near thermodynamic reversibility, with potentially important consequences for remediating mismatches in the thylakoid energy budget.

Regulation of cyclic electron flow by chloroplast NADPH‐dependent thioredoxin system

“…Reduction of plastoquinone by the thylakoid NDH complex is known to be coupled with the translocation of protons to the lumen, which contributes to the formation of pmf and enhances ATP synthesis (Strand, Fisher, & Kramer, ). We therefore investigated whether the generation of pmf during dark‐to‐light transitions and in plants illuminated with different light conditions is affected by deficiency or overexpression of NTRC.…”

“…However, controversy still exists over the molecular identity of FQR and the physiological function of PGR5 (Kanazawa et al., ; Leister & Shikanai, ; Tikkanen & Aro, ). The PGR‐ and NDH‐dependent pathways differ in their energetic properties; two protons per electron are translocated to the lumen (by the Q‐cycle) in the FQR‐pathway, whereas the NDH complex functions as a proton pump and additionally transfers two protons per electron to the lumen (Strand, Fisher, & Kramer, ; Strand, Livingston, et al., ). A third CEF pathway involving transfer of electrons from ferredoxin or FNR to PQ via heme c n in the Cyt b 6 f complex has also been proposed (Hasan, Yamashita, Baniulis, & Cramer, ).…”

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

“…transport may be denoted as "pseudolinear electron transport" (PLET). PLET is possible because the equilibrium of the reaction catalyzed by NDH is sensitive to pmf, given that its electron transport activity is coupled to transthylakoid H + transport (Strand et al, 2017). However, such reversal is only possible at high pmf and relatively high PQH 2 /Fd ratios, as determined by its thermodynamic properties (see Supplementary Text for details).…”

“…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).…”

“…Such simplifications prevent the study of the complex interactions that characterize the behavior of the system under natural conditions, such as the effect that changes in Rubisco activity would have on NPQ (Carmo-Silva and Salvucci, 2013;Kaiser et al, 2016). More comprehensive models have been published recently (Laisk et al, 2009;Zhu et al, 2013), but they still miss some of the mechanisms of interest in the regulation of PETC, such as NiR (Bloom et al, 2002) or NDH (Strand et al, 2017). Furthermore, the testing of these models with experimental data has been limited to a narrow range of experimental conditions and measurement techniques, and thus it is not known to what extent their simulations are physiologically reasonable.…”