Role of Thylakoid ATP/ADP Carrier in Photoinhibition and Photoprotection of Photosystem II in Arabidopsis 1[W][OA] Lan Yin, Bjo ¨rn Lundin 2 , Martine Bertrand, Markus Nurmi, Katalin Solymosi, Saijaliisa Kangasja ¨rvi, Eva-Mari Aro, Benoıˆt Schoefs, and Cornelia Spetea* Division of Molecular Genetics, Department of Physics, Chemistry, and Biology, Linko ¨ping University, 581 83 Linkoping, Sweden (L.Y., B.L., C.S.); National Institute for Marine Sciences and Techniques, Cnam, 50103 Cherbourg-Octeville cedex, France (M.B.); Department of Plant Anatomy, Eo ¨tvo ¨s University, 1117 Budapest, Hungary (K.S.); Department of Biochemistry and Food Chemistry, University of Turku, 20014 Turku, Finland (M.N., S.K., E.-M.A.); and UMR Plante-Microbe-Environnement, INRA-1088/CNRS-5184/Universite ´ de Bourgogne, 21065 Dijon cedex, France (B.S.) The chloroplast thylakoid ATP/ADP carrier (TAAC) belongs to the mitochondrial carrier superfamily and supplies the thylakoid lumen with stromal ATP in exchange for ADP. Here, we investigate the physiological consequences of TAAC depletion in Arabidopsis (Arabidopsis thaliana). We show that the deficiency of TAAC in two T-DNA insertion lines does not modify the chloroplast ultrastructure, the relative amounts of photosynthetic proteins, the pigment composition, and the photosynthetic activity. Under growth light conditions, the mutants initially displayed similar shoot weight, but lower when reaching full development, and were less tolerant to high light conditions in comparison with the wild type. These observations prompted us to study in more detail the effects of TAAC depletion on photoinhibition and photoprotection of the photosystem II (PSII) complex. The steady-state phosphorylation levels of PSII proteins were not affected, but the degradation of the reaction center II D1 protein was blocked, and decreased amounts of CP43-less PSII monomers were detected in the mutants. Besides this, the mutant leaves displayed a transiently higher nonphotochemical quenching of chlorophyll fluorescence than the wild-type leaves, especially at low light. This may be attributed to the accumulation in the absence of TAAC of a higher electrochemical H + gradient in the first minutes of illumination, which more efficiently activates photoprotective xanthophyll cycle-dependent and independent mechanisms. Based on these results, we propose that TAAC plays a critical role in the disassembly steps during PSII repair and in addition may balance the trans-thylakoid electrochemical H + gradient storage. In plants, the chloroplast thylakoid membrane is the site of light-driven photosynthetic reactions coupled to ATP synthesis. There are four major protein complexes involved in these reactions, namely, PSI, PSII, the cytochrome b 6 f, and the H + -translocating ATP synthase (for review, see Nelson and Ben-Shem, 2004). The photosystems and the cytochrome b 6 f complex also contain redox components and pigments bound to protein subunits. Their synthesis, assembly, optimal function, and repair during normal development and stress require a number of transport and regulatory mechanisms. In this context, the water-oxidizing PSII complex composed of more than 25 integral and peripheral proteins attracts special attention since its reaction center D1 subunit is degraded and replaced much faster than the other subunits under excess and even growth light conditions (for review, see Aro et al., 2005). Thus, the D1 protein turnover is the major event in the repair cycle of the PSII complex and occurs subsequently to the inactivation of PSII electron trans- port. D1 degradation is most likely performed by thylakoid FtsH and Deg proteases, operating on both sides of the thylakoid membrane (Lindahl et al., 2000; Haussu ¨ hl et al., 2001; Silva et al., 2003; Kapri-Pardes et al., 2007). The PSII repair cycle is regulated by reversible phosphorylation of several core subunits (Tikkanen et al., 2008). 1 This work was supported by grants from the Swedish Research Council, the Swedish Research Council for Environment, Agricul- ture, and Space Planning (Formas), the Graduate Research School in Genomics and Bioinformatics (C.S.), the Academy of Finland (to E.-M.A.), the French Ministe `re de l’Education Nationale de l’En- seignement Supe ´rieur et de la Recherche, and the Institut National de la Recherche Agronomique, the Centre National de la Recherche Scientifique (B.S.). 2 Present address: Graduate School of Natural Science and Tech- nology, Okayama University, 700–8530 Okayama, Japan. * Corresponding author; e-mail corsp@ifm.liu.se. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Cornelia Spetea (corsp@ifm.liu.se). [W] The online version of this article contains Web-only data. [OA] Open Access articles can be viewed online without a sub- scription. www.plantphysiol.org/cgi/doi/10.1104/pp.110.155804 666 Plant Physiology Ò , June 2010, Vol. 153, pp. 666–677, www.plantphysiol.org Ó 2010 American Society of Plant Biologists