The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light

Abstract

Plants use sunlight as their primary energy source. During photosynthesis, absorbed light energy generates reducing power by driving electron transfer reactions. These are coupled to the transfer of protons into the thylakoid lumen, generating a proton motive force (pmf) required for ATP synthesis. Sudden alterations in light availability have to be met by regulatory mechanisms to avoid the over-accumulation of reactive intermediates and maximize energy efficiency. Here, the acidification of the lumen, as an intermediate product of photosynthesis, plays an important role by regulating photosynthesis in response to excitation energy levels. Recent findings reveal pmf regulation and the modulation of its composition as key determinants for efficient photosynthesis, plant growth, and survival in fluctuating light environments.

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

“…Accordingly, a high NADPH/NADP + ratio has been shown to activate CEF (Breyton et al, 2006;Okegawa et al, 2008). A high NADPH/NADP+ ratio together with high accumulation of reduced Fd may also explain the activation of NDH-dependent CEF by H 2 O 2 (Strand et al, 2015;Strand et al, 2017), since oxidative treatment decreases the activation of redox-regulated CBC enzymes, and consequently the consumption of NADPH in illuminated chloroplasts. Accordingly, the ntrc mutant has a higher accumulation of H 2 O 2 than WT (Suppl.…”

“…Light drives the electron flow from water through PSII, plastoquinone (PQ), cytochrome b6f, plastocyanin (PC) and PSI to ferredoxin and ultimately to NADP + , producing NADPH. These photosynthetic electron transfer reactions are coupled to ATP synthesis via translocation of protons to the thylakoid lumen, generating a proton gradient over the thylakoid membrane (ΔpH), which together with membrane potential (ΔΨ) constitutes the proton motive force (pmf) (Hangarter and Good, 1982;Armbruster et al, 2017). Δ pH also contributes to induction of the energy-dependent qE component of NPQ, a photoprotective mechanism that dissipates excess excitation energy from the electron transfer chain (Niyogi and Truong, 2013;Ruban, 2016), and maintains photosynthetic control at Cyt b6f (Joliot and Johnson, 2011;Johnson, 2011).…”

“…However, controversy still exists over the molecular identity of FQR and the physiological function of PGR5 (Leister and Shikanai, 2013;Tikkanen and Aro, 2014;Kanazawa et al 2017). 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 2H+ per electron to the lumen (Strand et al, 2017). 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 et al, 2013).…”

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

“…Light drives the electron flow from water through PSII, plastoquinone (PQ), cytochrome b6f , plastocyanin (PC), and PSI to ferredoxin and ultimately to NADP + , producing NADPH. These photosynthetic electron transfer reactions are coupled with ATP synthesis via translocation of protons to the thylakoid lumen, generating a proton gradient over the thylakoid membrane (ΔpH), which together with membrane potential (ΔΨ) constitutes the proton motive force ( pmf ) (Armbruster, Correa Galvis, Kunz, & Strand, ; Hangarter & Good, ). ΔpH also contributes to induction of the energy‐dependent qE component of NPQ, a photoprotective mechanism that dissipates excess excitation energy from the electron transfer chain (Niyogi & Truong, ; Ruban, ), and maintains photosynthetic control at Cyt b6f (Johnson, ; Joliot & Johnson, ).…”

Multilevel regulation of non‐photochemical quenching and state transitions by chloroplast NADPH‐dependent thioredoxin reductase

“…One of these mechanisms is non‐photochemical quenching (NPQ), which dissipates excitation energy absorbed by the light‐harvesting antenna of photosystem II (PSII) as heat (Niyogi and Truong ). Induction of the major, energy‐dependent component of NPQ (qE) requires acidification of the thylakoid lumen via translocation of protons from stroma to lumen by linear and cyclic electron flow (CEF), which then results in downregulation of thylakoid electron flow (Demmig‐Adams et al , Armbruster et al ). Low lumenal pH causes protonation of the photosystem II Subunit S (PsbS; Li et al ) and activation of the lumenal xanthophyll cycle enzyme VIOLAXANTHIN DE‐EPOXIDASE (VDE), resulting in accumulation of zeaxanthin (Zx, Jahns and Holzwarth ).…”