Solute transporters in plant thylakoid membranes

Abstract

Plants utilize sunlight to drive photosynthetic energy conversion in the chloroplast thylakoid membrane. Here are located four major photosynthetic complexes, about which we have great knowledge in terms of structure and function. However, much less we know about auxiliary proteins, such as transporters, ensuring an optimum function and turnover of these complexes. The most prominent thylakoid transporter is the proton-translocating ATP-synthase. Recently, four additional transporters have been identified in the thylakoid membrane of Arabidopsis thaliana, namely one copper-transporting P-ATPase, one chloride channel, one phosphate transporter, and one ATP/ADP carrier. Here, we review the current knowledge on the function and physiological role of these transporters during photosynthesis and light stress in plants. Subsequently, we make a survey on the outlook of thylakoid activities awaiting identification of responsible proteins. Such knowledge is necessary to understand the thylakoid network of transporters, and to design strategies for bioengineering crop plants in the future.

Acknowledgements

The authors would like to acknowledge the Swedish Research Council, the Swedish Research Council for Environment, Agriculture and Space Planning (Formas) and Linköping University (to Cornelia Spetea), the French Ministére de l’Education Nationale de l’Enseignement Supérieur et de la Recherche, the Institut National de la Recherche Agronomique (INRA), the Centre National de la Recherche Scientifique (CNRS) and the University of Burgundy (to Benoît Schoefs).

dio]Figures and Tables

Figure 1 Flow scheme for experimental validation of putative transporters using a functional genomics approach in Arabidopsis thaliana.

Figure 2 Current picture of thylakoid solute transporters from Arabidopsis thaliana. Chloroplasts are structurally organized in three membrane compartments (outer envelope, inner envelope and thylakoid membrane), and two soluble compartments (stroma and thylakoid lumen). The diagram shows the following transporters, that have been localized to the thylakoid membrane, and functionally characterized: the H⁺-translocating ATP synthase CF₀F₁, the Cu²⁺-transporting P-type ATPase PAA2, the thylakoid ATP/ADP carrier TAAC, the Na⁺-dependent Pi transporter ANTR1, and the chloride channel CLCe.

Figure 3 Schematic model of ATP transport and GTP-mediated signaling during high light stress. The active photosystem II (PSII ) is a multisubunit and dimeric complex, containing an intact reaction center D1 protein (yellow). As a result of high-light-induced inactivation, the D1 protein is oxidatively damaged (red), and needs to be replaced. The ATP-synthase CF₀F₁ supplies ATP in the stroma, from where it is translocated by the thylakoid ATP/ADP carrier (TAAC) into the lumen in exchange for ADP. The lumenal nucleoside diphosphate kinase NDPK3 converts ATP to GTP, which is subsequently bound and hydrolyzed by the PSII extrinsic subunit PsbO (blue). This leads to PsbO dissociation, partial disassembly of PSII complex (CP43 subunit shown in green), and D1 proteolysis by Deg and FtsH proteases in a highly controlled manner. The resulting phosphate (Pi) is exported back to the stroma by the Na⁺- dependent Pi transporter (ANTR1). The various nucleotides and Pi are highlighted as red text.

Table 1 Thylakoid solute transporters from Arabidopsis thaliana