Regulation of cyclic and linear electron flow in higher plants

Abstract

Cyclic electron flow is increasingly recognized as being essential in plant growth, generating a pH gradient across thylakoid membrane (ΔpH) that contributes to ATP synthesis and triggers the protective process of nonphotochemical quenching (NPQ) under stress conditions. Here, we report experiments demonstrating the importance of that ΔpH in protecting plants from stress and relating to the regulation of cyclic relative to linear flow. In leaves infiltrated with low concentrations of nigericin, which dissipates the ΔpH without significantly affecting the potential gradient, thereby maintaining ATP synthesis, the extent of NPQ was markedly lower, reflecting the lower ΔpH. At the same time, the photosystem (PS) I primary donor P700 was largely reduced in the light, in contrast to control conditions where increasing light progressively oxidized P700, due to down-regulation of the cytochrome bf complex. Illumination of nigericin-infiltrated leaves resulted in photoinhibition of PSII but also, more markedly, of PSI. Plants lacking ferredoxin (Fd) NADP oxidoreductase (FNR) or the polypeptide proton gradient regulation 5 (PGR5) also show reduction of P700 in the light and increased sensitivity to PSI photoinhibition, demonstrating that the regulation of the cytochrome bf complex (cyt bf) is essential for protection of PSI from light stress. The formation of a ΔpH is concluded to be essential to that regulation, with cyclic electron flow playing a vital, previously poorly appreciated role in this protective process. Examination of cyclic electron flow in plants with a reduced content of FNR shows that these antisense plants are less able to maintain a steady rate of this pathway. This reduction is suggested to reflect a change in the distribution of FNR from cyclic to linear flow, likely reflecting the formation or disassembly of FNR–cytochrome bf complex.

Photosynthesis Control: An underrated short-term regulatory mechanism essential for plant viability

“…In agreement with previous data, 30 this is likely due to a reduced capacity of the pgr5 mutants to cope with fluctuations in light intensity and to protect PSI from photodamage. The PSI core protein PsaB was strongly depleted in the pgr5 mutant when grown under fluctuating light conditions, whereas accumulation of subunits of the PSII-core, the Cyt b 6 f complex, and the ribulose-1,5-bisphosphate carboxylase/oxygenase did not show major differences.…”

“…Indeed, uncontrolled electron flow from PSII during high-light phases causes damage to PSI in pgr5, as shown by a decline in PM, the maximum oxidizable amount of P700. 30 Although the indispensable role of the PGR5 protein in the maintenance of Photosynthesis Control appears to be clear, the molecular details of this mechanism remain to be elucidated. Indeed, the roles of the PGR5 and PGRL1 proteins in Arabidopsis CET are still under debate.…”

“…Some reports provide evidence that, to some extent, the pgr5 and pgrl1 mutants are also capable of performing CET, and CET was found to be impaired in these mutants only under specific conditions, such as high light or CO 2 limitation. 30,32,50,51 Thus, it is likely that rather than being absolute requirements, the PGR5 and PGRL1 proteins are important to regulate and facilitate CET.…”

“…Most probably, acidification of the lumen impedes the oxidation of PQH 2 , because the protons accumulated inside the thylakoids cause the protonation of the proton-accepting groups in the Q o -center, thereby decreasing the probability of PQH 2 oxidation. 15 Despite the discovery of Photosynthesis Control dates back to the 1960s, 18 its physiological importance has been recognized only recently, thanks to the work of Joliot and Johnson (2011), 30 where the pH-dependent downregulation of Cyt b 6 f activity was shown to be essential for protection of PSI from light stress. Indeed, leaves infiltrated with low concentrations of nigericin, which prevents thylakoid lumen acidification, and exposed to high light intensities for 20 min resulted in photoinhibition of almost 70% of PSI and only 30% of PSII complexes.…”

Quantitative Local Photosynthetic Flux Measurements at Isolated Chloroplasts and Thylakoid Membranes Using Scanning Electrochemical Microscopy (SECM)

“…[67][68][69][70] Therefore, at the reasonably short time periods, which we probe herein, oxygen production largely depends on the overall oxidation state of the PQ pool. [71][72][73][74] Oxygen Generation at Chloroplast Films: We develop FEM simulations based on a kinetic model in which the rate of oxygen generation at the chloroplast film depends on the concentration of oxidized PQ species (N t ) which are consumed (kinetic constant k f ) to produce a reduced PQ species (R s ), but are also regenerated (kinetic constant k b ) to produce the oxidized species. …”