A bestrophin‐like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis

Abstract

During photosynthesis, photosynthetic electron transport generates a proton motive force (pmf) across the thylakoid membrane, which is used for ATP biosynthesis via ATP synthase in the chloroplast. The pmf is composed of an electric potential (ΔΨ) and an osmotic component (ΔpH). Partitioning between these components in chloroplasts is strictly regulated in response to fluctuating environments. However, our knowledge of the molecular mechanisms that regulate pmf partitioning is limited. Here, we report a bestrophin‐like protein (AtBest), which is critical for pmf partitioning. While the ΔpH component was slightly reduced in atbest, the ΔΨ component was much greater in this mutant than in the wild type, resulting in less efficient activation of nonphotochemical quenching (NPQ) upon both illumination and a shift from low light to high light. Although no visible phenotype was observed in the atbest mutant in the greenhouse, this mutant exhibited stronger photoinhibition than the wild type when grown in the field. AtBest belongs to the bestrophin family proteins, which are believed to function as chloride (Cl−) channels. Thus, our findings reveal an important Cl− channel required for ion transport and homeostasis across the thylakoid membrane in higher plants. These processes are essential for fine‐tuning photosynthesis under fluctuating environmental conditions.

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

“…S13 and S14) suggests that NPQ deficiency does not have a deleterious effect on plant vegetative growth acclimation under long-term fluctuating light conditions. In contrast, NPQ was demonstrated to play a crucial role in rapid adjustments of photosynthesis to artificial fluctuating light and shading (49)(50)(51)(52). Although npq mutants suffered higher photoinhibition and had less seeds relative to the wild type in field experiments, they did not display visible vegetative growth defects (53,54).…”

An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis

“…It was only in the recent years that genes have been annotated with functions that may correspond to the reported activities. The two‐pore K + channel TPK3 (Carraretto et al ) and two bestrophin‐like anion channels AtBest1 and AtBest2 (Duan et al ) that were renamed voltage‐dependent chloride channels VCCN1 and VCCN2 (Herdean et al ) have been localized to the thylakoid membrane in Arabidopsis . AtBest1/VCCN1 is the major form in Arabidopsis leaves, whereas AtBest2/VCCN2 is mostly expressed in flowers (Duan et al , Herdean et al ).…”

“…The two‐pore K + channel TPK3 (Carraretto et al ) and two bestrophin‐like anion channels AtBest1 and AtBest2 (Duan et al ) that were renamed voltage‐dependent chloride channels VCCN1 and VCCN2 (Herdean et al ) have been localized to the thylakoid membrane in Arabidopsis . AtBest1/VCCN1 is the major form in Arabidopsis leaves, whereas AtBest2/VCCN2 is mostly expressed in flowers (Duan et al , Herdean et al ). Electrophysiological experiments in planar lipid bilayers have revealed TPK3 as a K + selective channel regulated by Ca 2+ and pH (Carraretto et al ).…”

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

“…In any case, the balancing of Δψ/ΔpH, and its kinetics, are dependent on the regulation of counter-ion homeostasis in the chloroplast (34), and recent work from several labs has identified putative components of these ion homeostatic machineries, including a thylakoid potassium channel (35), a K + /H + antiporter (36), as well as transporters for other charged species (37)(38)(39)(40)(41). There are also indications that the Δψ/ΔpH balance is controlled by the synthesis of membrane permeable weak bases, such as putrescene, that effectively increase the proton buffering capacity of the lumen (42).…”