Significance of PGR5-dependent cyclic electron flow for optimizing the rate of ATP synthesis and consumption in Arabidopsis chloroplasts

Abstract

The proton motive force (PMF) across the chloroplast thylakoid membrane that is generated by electron transport during photosynthesis is the driving force for ATP synthesis in plants. The PMF mainly arises from the oxidation of water in photosystem II and from electron transfer within the cytochrome bf complex. There are two electron transfer pathways related to PMF formation: linear electron flow and cyclic electron flow. Proton gradient regulation 5 (PGR5) is a major component of the cyclic electron flow pathway, and the Arabidopsis pgr5 mutant shows a substantial reduction in the PMF. How the PGR5-dependent cyclic electron flow contributes to ATP synthesis has not, however, been fully delineated. In this study, we monitored in vivo ATP levels in Arabidopsis chloroplasts in real time using a genetically encoded bioluminescence-based ATP indicator, Nano-lantern(ATP1). The increase in ATP in the chloroplast stroma of pgr5 leaves upon illumination with actinic light was significantly slower than in wild type, and the decrease in ATP levels when this illumination stopped was significantly faster in pgr5 leaves than in wild type. These results indicated that PGR5-dependent cyclic electron flow around photosystem I helps to sustain the rate of ATP synthesis, which is important for growth under fluctuating light conditions.

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

“…However, there would be insufficient ATP from the LET during certain multiple stress situations. Plants could compensate for the deficiency of ATP/NADPH in the LET by using the CET around the PSI ( Sato et al, 2019 ; Ma et al, 2021 ), the water-water cycle (Mehler reaction; Asada et al, 1999 ) and the mitochondrial alternative oxidase respiration ( Meng et al, 2012 ).…”

Interaction of zinc and IAA alleviate aluminum-induced damage on photosystems via promoting proton motive force and reducing proton gradient in alfalfa

“…In the present study, Zn addition increased CEF values of Al-stressed alfalfa, which increased pmf and proton transfer from lumen to stroma (g H + ), as well as decreased ROS generation (Fig.6f). The generation of pmf links to ATP synthesis and balances ATP/NADPH ratio [22,24]. The increased pmf and g H + in Al-stressed seedlings activated chloroplastic ATP synthase located in thylakoid membrane (Fig.6a), consequently increased ATP synthesis accompanying with H + transfer from lumen to stroma, which leads to a reduction of ΔpH pmf between lumen and stroma.…”

Higher order photoprotection mutants reveal the importance of ΔpH-dependent photosynthesis-control in preventing light induced damage to both photosystem II and photosystem I

“…Furthermore, unlike wild type and npq4-1 plants, the photosynthesis-control depleted mutants are not able to photo-accumulate P700 + , as their Y(ND) is near zero at any light intensity due to the low values of both thylakoid proton gradient (ΔpH) and proton motive force (pmf) they can develop 44 . At the same time, they are characterized by the overreduction of PSI acceptors, observed as an increase of Y(NA).…”

“…On the other hand, damages to PSI are relevant in inducing inactivation of PSII: the acceptor side of PSII becomes over-reduced and this, in turn, increases the rate of charge recombination with formation of 3 P680 35 and PSII inactivation. In addition, the absence of ΔpH-dependent photosynthesis-control affects the value of pmf 44 , and this could alter the electron transfer between Q A and Q B , promoting PSII inactivation.…”