Role of Thylakoid ATP/ADP Carrier in Photoinhibition and Photoprotection of Photosystem II in Arabidopsis    

Abstract

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 transport. D1 degradation is most likely performed by thylakoid FtsH and Deg proteases, operating on both sides of the thylakoid membrane (Lindahl et al., 2000;Haussü hl et al., 2001;Silva et al., 2003;Kapri-Pardes et al., 2007). The PSII repair cycle is regulated by reversible phosphorylation of sever...

The Arabidopsis Thylakoid ADP/ATP Carrier TAAC Has an Additional Role in Supplying Plastidic Phosphoadenosine 5′-Phosphosulfate to the Cytosol

“…In fact, ATP is required in thylakoids for phosphorylation, translocation, correct folding, and degradation of proteins. Moreover, its requirement in the repair of photoinactivated photosystem II would explain why mutant plants lacking TAAC exhibit lower high light tolerance than the wild type (Yin et al, 2010).…”

“…T-DNA insertions in these homozygous mutant plants named papst1-1 (SALK_039194) and papst1-2 (FLAG 443D03) are depicted in Figure 6A. Under ambient conditions, both mutant lines were slightly retarded in growth compared with corresponding wild-type plants (Col-0 or Ws-4) (Thuswaldner et al, 2007;Yin et al, 2010) ( Figure 6B). This growth phenotype resembles that of plants lacking the plastidic APK isoforms apk1 apk2 and apk1 apk2 apk4 (Mugford et al, , 2010.…”

Adenine nucleotide transporters in organelles: novel genes and functions

“…8), including protein phosphorylation, folding, import, and degradation [85]. It is also converted to GTP, which is involved in the turnover and repair of the photosystem II complex, which is mainly inactivated under high light stress conditions [86]. TAAC knock-out plants displayed lower shoot weight when reaching full development and were less tolerant of high light conditions in comparison with the wild type, apparently by a deficient repair of photosystem II under light stress in the mutants [86].…”

“…It is also converted to GTP, which is involved in the turnover and repair of the photosystem II complex, which is mainly inactivated under high light stress conditions [86]. TAAC knock-out plants displayed lower shoot weight when reaching full development and were less tolerant of high light conditions in comparison with the wild type, apparently by a deficient repair of photosystem II under light stress in the mutants [86]. Mutants also show a 40% reduction in the thylakoid content, resulting in pale green leaves, and uptake of ATP into isolated thylakoids is reduced around 30-40% [85].…”

Identification of a Dual-Targeted Protein Belonging to the Mitochondrial Carrier Family That Is Required for Early Leaf Development in Rice

“…4). At5g01500 is the TAAC protein and is found in thylakoids (Thuswaldner et al, 2007;Yin et al, 2010); however, the protein encoded by At3g51870 is likely located in the envelopes of plastids according to proteomics-based analysis (Ferro et al, 2003(Ferro et al, , 2010Sun et al, 2009). …”