The Arabidopsis thylakoid chloride channel ClCe regulates ATP availability for light-harvesting complex II protein phosphorylation

Emilija Dukic; Peter J Gollan; Steffen Grebe; Virpi Paakkarinen; Andrei Herdean; Eva-Mari Aro; Cornelia Spetea

doi:10.3389/fpls.2022.1050355

The Arabidopsis thylakoid chloride channel ClCe regulates ATP availability for light-harvesting complex II protein phosphorylation

Front Plant Sci. 2022 Nov 22:13:1050355. doi: 10.3389/fpls.2022.1050355. eCollection 2022.

Authors

Emilija Dukic¹, Peter J Gollan², Steffen Grebe², Virpi Paakkarinen², Andrei Herdean³, Eva-Mari Aro², Cornelia Spetea¹

Affiliations

¹ Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
² Molecular Plant Biology Unit, Department of Life Technologies, University of Turku, Turku, Finland.
³ Climate Change Cluster, University of Technology Sydney, Ultimo, NSW, Australia.

Abstract

Coping with changes in light intensity is challenging for plants, but well-designed mechanisms allow them to acclimate to most unpredicted situations. The thylakoid K⁺/H⁺ antiporter KEA3 and the voltage-dependent Cl^- channel VCCN1 play important roles in light acclimation by fine-tuning electron transport and photoprotection. Good evidence exists that the thylakoid Cl^- channel ClCe is involved in the regulation of photosynthesis and state transitions in conditions of low light. However, a detailed mechanistic understanding of this effect is lacking. Here we report that the ClCe loss-of-function in Arabidopsis thaliana results in lower levels of phosphorylated light-harvesting complex II (LHCII) proteins as well as lower levels of the photosystem I-LHCII complexes relative to wild type (WT) in low light conditions. The phosphorylation of the photosystem II core D1/D2 proteins was less affected either in low or high light conditions. In low light conditions, the steady-state levels of ATP synthase conductivity and of the total proton flux available for ATP synthesis were lower in ClCe loss-of-function mutants, but comparable to WT at standard and high light intensity. As a long-term acclimation strategy, expression of the ClCe gene was upregulated in WT plants grown in light-limiting conditions, but not in WT plants grown in standard light even when exposed for up to 8 h to low light. Taken together, these results suggest a role of ClCe in the regulation of the ATP synthase activity which under low light conditions impacts LHCII protein phosphorylation and state transitions.

Keywords: ATP synthase; Arabidopsis thaliana; chloride channel (ClC); light-harvesting complex II (LHCII); low light acclimation; photosystem II; protein phosphorylation; proton motive force (PMF).