Role of Ions in the Regulation of Light-Harvesting

Abstract

Regulation of photosynthetic light harvesting in the thylakoids is one of the major key factors affecting the efficiency of photosynthesis. Thylakoid membrane is negatively charged and influences both the structure and the function of the primarily photosynthetic reactions through its electrical double layer (EDL). Further, there is a heterogeneous organization of soluble ions (K+, Mg2+, Cl−) attached to the thylakoid membrane that, together with fixed charges (negatively charged amino acids, lipids), provides an electrical field. The EDL is affected by the valence of the ions and interferes with the regulation of “state transitions,” protein interactions, and excitation energy “spillover” from Photosystem II to Photosystem I. These effects are reflected in changes in the intensity of chlorophyll a fluorescence, which is also a measure of photoprotective non-photochemical quenching (NPQ) of the excited state of chlorophyll a. A triggering of NPQ proceeds via lumen acidification that is coupled to the export of positive counter-ions (Mg2+, K+) to the stroma or/and negative ions (e.g., Cl−) into the lumen. The effect of protons and anions in the lumen and of the cations (Mg2+, K+) in the stroma are, thus, functionally tightly interconnected. In this review, we discuss the consequences of the model of EDL, proposed by Barber (1980b) Biochim Biophys Acta 594:253–308) in light of light-harvesting regulation. Further, we explain differences between electrostatic screening and neutralization, and we emphasize the opposite effect of monovalent (K+) and divalent (Mg2+) ions on light-harvesting and on “screening” of the negative charges on the thylakoid membrane; this effect needs to be incorporated in all future models of photosynthetic regulation by ion channels and transporters.

Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non‐model organism aided by transcriptomic data integration

“…CAS is a calcium‐sensing receptor localized in the thylakoid membrane, and, in agreement with photosynthesis‐related functions, its phosphorylation state is light dependent (Vainonen et al ., ). Since Ca 2+ ion fluxes across the thylakoid membrane can modulate the regulatory capacity of the pmf (Carraretto et al ., ; Kaňa and Govindjee, ), accumulation of CAS in HL plants (Figure ) indicates that this protein functions as a luminal sink for Ca 2+ (Nomura and Shiina, ), whose release ultimately contributes to control of the ETC. SOQ1 is a membrane protein with a lumenal thioredoxin‐like domain that plays a role in NPQ, although not in a pH‐ or PsbS‐dependent manner (Brooks et al ., ) but by interacting with the chloroplast lipocalin (CHL) protein during light‐stress response (Malnoë et al ., ).…”

Chloroplast Acetyltransferase NSI Is Required for State Transitions in Arabidopsis thaliana

“…Interestingly, the grana in the nsi were more tightly packed than in the wild type ( Figure 3C). On the other hand, as chloroplast ion content is known to be a key determinant of thylakoid membrane stacking, it can play an important role in state transitions in conjunction with LHCII phosphorylation (Kaňa and Govindjee, 2016). Indeed, one of the most drastically downregulated Lys acetylation sites in the nsi mutants was found in the PSBP-1 protein, where acetylation was more than 12-fold less abundant than in the wild type ( Figure 2C).…”

Lipid‐polymorphism of plant thylakoid membranes. Enhanced non‐bilayer lipid phases associated with increased membrane permeability

“…They might be correlated with some changes in the ultrastructure of the thylakoid membrane system. The fact that the lipid phase behaviour of the thylakoid membrane system, similarly to the (macro‐)organization of the grana, depends on the ionic strength of the medium (Garab et al , Ünnep et al , Kana and Govindjee ), would suggest a correlation with the membrane ultrastructure and/or the macro‐organization of the protein complexes. However, as pointed out by Garab et al (), these changes must be relatively small and thus difficult to identify.…”