JXB Advance Access originally published online on April 25, 2005
Journal of Experimental Botany 2005 56(416):1439-1447; doi:10.1093/jxb/eri158
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FOCUS PAPER |
Redox regulation in the chloroplast thylakoid lumen: a new frontier in photosynthesis research
Department of Plant and Microbial Biology, 111 Koshland Hall, University of California, Berkeley, CA 94720, USA
* To whom correspondence should be addressed. Fax: +1 510 642 7356. E-mail: view{at}nature.berkeley.edu
Received 1 February 2005; Accepted 10 March 2005
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Abstract |
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Top
Abstract
IntroductionInitially linked to photosynthesis, regulation by change in the redox state of thiol groups (S-S
2SH) is now known to occur throughout biology. Thus, in addition to serving important structural and catalytic functions, it is recognized that, in many cases, disulphide bonds can be broken and reformed for regulation. Several systems, each linking a hydrogen donor to an intermediary disulphide protein, act to effect changes that alter the activity of target proteins by change in the thiol redox state. Pertinent to the present discussion is the chloroplast ferredoxin/thioredoxin system, comprised of photoreduced ferredoxin, a thioredoxin, and the enzyme ferredoxin-thioredoxin reductase, that occur in the stroma. In this system, thioredoxin links the activity of enzymes to light: those enzymes functional in biosynthesis are reductively activated by light via thioredoxin (S-S2SH), whereas counterparts acting in degradation are deactivated under illumination conditions and are oxidatively activated in the dark (2SHS-S). Recent research has uncovered a new paradigm in which an immunophilin, FKBP13, and potentially other enzymes of the chloroplast thylakoid lumen are oxidatively activated in the light (2SHS-S). The present review provides a perspective on this recent work. Key words: Chloroplast thylakoid lumen, immunophilin, redox regulation, thiol-disulphide exchange, thioredoxin
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Introduction |
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Recent studies have opened a new area of photosynthesis research in extending redox regulation to an enzyme of the chloroplast thylakoid lumen. The lumenal immunophilin FKBP13, earlier shown to be essential in the formation of a functional Rieske complex for the photosynthetic transport of electrons, lost its peptidyl-prolyl-cis-trans isomerase (PPIase) enzymatic activity on reduction (or mutagenesis) of its two disulphide (S-S) groups, one located at the carboxyl and the other at the amino terminus as demonstrated by X-ray structural analysis. Both disulphides were reduced by thioredoxin (Trx), a regulatory protein long known to link light to the activity of enzymes of the chloroplast stroma. The results suggest a previously unrecognized paradigm for redox regulation in photosynthesis, in which activation by light is achieved in concert with oxygen evolution by the oxidation of sulphydryl groups (conversion of SH to S-S). Such a mechanism, occurring in the thylakoid lumen, is in striking contrast to regulation in the stroma, where reduction of disulphides of biosynthetic enzymes targeted by Trx (S-S converted to SH) leads to an increase in activity in the light. Specifics relevant to these new findings are summarized below.
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Background on thioredoxins |
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Trxs are 12 kDa proteins with a characteristic structural motif—four alpha helixes surrounding a beta sheet composed of five strands—common to most, if not all, protein disulphide (S-S) oxidoreductase family members (for recent reviews on plant Trxs see Schürmann and Jacquot, 2000
; Balmer and Buchanan, 2002; Baumann and Juttner, 2002; Buchanan et al., 2002; Schürmann, 2003; Gelhaye et al., 2004b; Izui et al., 2004; Buchanan and Balmer, 2005). Trxs appear to be present in all living cells with the exception of a fastidious human pathogen (Renesto et al., 2003). In plants, unlike bacteria and animals, a large number of genes encode Trxs—19 different isoforms have been identified in the genome of Arabidopsis thaliana that can be grouped into six subfamilies (Mestres-Ortega and Meyer, 1999; Laloi et al., 2001; Lemaire et al., 2003, 2004; Lemaire and Miginiac-Maslow, 2004) (Fig. 1). Chloroplasts contain four types of Trx—f, m, x, and y—whereas Trx o is located in mitochondria. The h representatives are distributed in multiple cell compartments: cytosol, nucleus, and ER as well as mitochondria (Florencio et al., 1988; Schürmann and Jacquot, 2000; Brugiere et al., 2004; Gelhaye et al., 2004a, b). The evidence suggests that individual organs express characteristic members of the Trx h family.
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Trxs contain a conserved redox active site with the sequence WC(G/P)PC. In plants, the disulphide bond formed between the two cysteines can be reduced either by (i) ferredoxin and the iron-sulphur/disulphide enzyme, ferredoxin-thioredoxin reductase (FTR), in chloroplasts, and (ii) NADPH via a flavin enzyme, NADP-thioredoxin reductase (NTR), in other organelles. By reducing disulphide groups, Trxs, in turn, function as electron (hydrogen) donors for the reduction of either chemical substrates or, for what seems to be a broader role, the regulation of enzymes.
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Thioredoxins of chloroplast stroma |
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In chloroplasts, two types of Trxs—f and m—are central to enzyme regulation (Buchanan, 1980
; Schürmann and Jacquot, 2000; Buchanan and Balmer, 2005). More recently, two less abundant Trxs, x and y, have been described for chloroplast stroma (Mestres-Ortega and Meyer, 1999; Lemaire et al., 2003). Their function is being defined (Collin et al., 2003, 2004). In the reduction of Trx in chloroplasts, the participating enzyme, FTR, receives electrons from photoreduced ferredoxin, thereby providing a link between light and enzyme activity (equations 1–4). In this system, biosynthetic enzymes of the stroma are activated by reduction (S-S2SH).
 | (1) |
 | (2) |
 | (3) |
 | (4) |
By contrast, enzymes of carbohydrate degradation are active in the disulphide (S-S) state and are deactivated on reduction (SH state). Chloroplast Trxs function in regulating the Calvin cycle, and, as found in recent studies discussed below, a spectrum of other processes. In this regulatory network, now a part of standard biology and biochemistry texts, Trx acts as an ‘eye,’ informing enzymes that the light is off (S-S state) or on (SH state) (Fig. 2). In a complementary capacity, recent evidence indicates that Trx also links enzyme activity to the level of oxidants generated under stress conditions via a mechanism designated ‘oxidative regulation’ (Balmer et al., 2003).
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Stromal thioredoxin targets |
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Since the discovery of a role for Trx in the activation of fructose-1,6 bisphosphatase (Buchanan, 1980
), the number of known Trx-linked enzymes has steadily increased (Schürmann and Jacquot, 2000; Buchanan et al., 2002; Buchanan and Balmer, 2005). Almost all of the Trx-linked proteins identified before 2000 were found either by chance or by following up on prior indicative observations, i.e. metabolite changes reported for in vivo light/dark transition experiments or increased enzyme activity found in vitro after adding dithiothreitol (DTT), a non-physiological substitute for Trx. Studies during the first 25 years following their discovery in chloroplasts led to the identification of a total of about 16 proteins regulated by Trx.
The development of the affinity chromatography procedure with mutated Trx, in combination with proteomics, has enabled the identification of numerous new Trx-linked proteins in chloroplasts. The affinity procedure takes advantage of the mechanism by which Trx reduces a specific regulatory disulphide bond (Brandes et al., 1996; Verdoucq et al., 1999; Balmer and Schürmann, 2001; Motohashi et al., 2001; Goyer et al., 2002). The mechanism requires the formation of a transient heterodisulphide bond between Trx and the interacting enzyme prior to complete reduction of the targeted disulphide. Mutation of one of the two cysteines of the Trx active site (the one buried in the molecule) stabilizes the normally transient heterodisulphide, thereby covalently linking the target protein to Trx via a bond that can be cleaved by DTT. This property was used earlier to generate covalent complexes between Trx f and both phosphoribulokinase and fructose bisphosphatase (Brandes et al., 1996; Balmer and Schürmann, 2001). Further experiments in which the buried Cys of the active site of extraplastidic Trx h was mutated to serine led to the identification of a new type of peroxidase as a target protein in yeast two-hybrid experiments (Verdoucq et al., 1999). In a subsequent development, mutated Trx m was immobilized on a resin and used in conjunction with proteomics to screen chloroplast stroma for potential target proteins (Motohashi et al., 2001). This approach led to the identification of eight Trx targets: five known (Rubisco activase, sedoheptulose bisphosphatase, glyceraldehyde 3-phosphate dehydrogenase, glutamine synthetase, and 2-Cys peroxiredoxin) and three new (peroxiredoxin-Q, cyclophilin CYP 20-3, and Rubisco small subunit). A similar experiment with mutated Trx h led to the identification of a peroxiredoxin from Chlamydomonas (Goyer et al., 2002).
Further application of the affinity column technique led to the identification of additional new soluble Trx targets in chloroplasts (Balmer et al., 2003). This approach confirmed the identity of nine out of 16 known soluble Trx-regulated enzymes and led to more than a doubling in the number of potential Trx-interacting proteins. Fifteen potential new targets functional in 10 chloroplast processes not known to be regulated by Trx (Fig. 3) were identified. Most of the new targets contain conserved cysteines and are members of processes not previously known to be redox regulated. It should be noted that, while the mutant affinity column approach has provided new insight in the field, one of its shortcomings is the loss of specificity observed in vitro, i.e. it seems not to matter which chloroplast Trx (f or m) is bound to the column matrix in isolating potential targets (Balmer et al., 2003). Nonetheless, the method has been successfully applied to identify 50 potential new targets in plant mitochondria (Balmer et al., 2004). Additional evidence that these mitochondrial proteins were authentic targets was provided by the finding that each is reduced specifically by Trx. Further, the column technique has been used to uncover new target proteins in wheat starchy endosperm (Wong et al., 2003, 2004), barley seeds (Maeda et al., 2004) and Arabidopsis thaliana seedlings (Marchand et al., 2004; Yamazaki et al., 2004). At present, approximately 180 established and potential Trx targets have been identified in land plants (Buchanan and Balmer, 2005). The procedure has also been applied to a cyanobacterium, Synechocystis sp. PCC 6803 (Lindahl and Florencio, 2004) and Chlamydomonas reinhardtii (Lemaire et al., 2004), leading to the identification of additional potential new targets. This same type of mutagenesis technique was also recently successfully applied to the identification of targets of the chloroplast drought-induced stress protein, CDSP32 (Rey et al., 2005).
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Immunophilins and their function in animals |
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Immunophilins were discovered as cellular receptors for immunosuppressive drugs, including cyclosporin A and FK506, that are used clinically to prevent graft rejection. Recent studies have revealed that, among other processes, these proteins function at the crossroads of protein folding and trafficking, and signal transduction in animals. Earlier work with animal systems demonstrated that, cyclosporin A (a cyclic decapeptide) and FK506 (a macrocyclic lactone) suppress the immune response by blocking the activation of T lymphocytes (Kunz and Hall, 1993
; Schreiber, 1991). As a part of this work, the cellular receptors for cyclosporin A and FK506 were purified and, respectively, named cyclophilin (CYP) and FKBP (FK506-Binding Proteins). Their receptors identified, the CYPs, and FKBPs, are collectively referred to as immunophilins (Schreiber, 1991). The complexes formed between immunophilins and their cognate ligands are the functional modules for immunosuppression. The FKBP12-FK506 and CYP-cyclosporin A complexes, but not their separate components, bind and inhibit the activity of calcineurin, a Ca2+, calmodulin-dependent protein phosphatase (Liu et al., 1991). Studies have demonstrated that inhibition of calcineurin activity is necessary for the immunosuppressive effect of cyclosporin A and FK506 (Clipstone and Crabtree, 1992; Liu et al., 1992; O'Keefe et al., 1992; Rao et al., 1997).
During the past decade, a growing number of immunophilins have been characterized from mammals as well as a variety of other organisms, ranging from bacteria and yeast to plants (reviewed in Rosen and Schreiber, 1992; Fruman et al., 1994; Luan, 1998). The high level of conservation and ubiquitous distribution of the members of this family among divergent organisms, together with their presence in almost all subcellular compartments, attests to a broad role in fundamental processes. The finding of PPIase activity associated with immunophilins suggested that they facilitate protein folding. Evidence for this role is accumulating in animal systems (Luan, 1998). For example, cyclosporin A, a specific inhibitor of the PPIase activity of CYPs, delayed collagen triple helix assembly in chick embryo fibroblasts (Steimann et al., 1991). Further, a CYP member has been shown to promote protein folding in mitochondria (Matouschek et al., 1995) and in vitro studies with carbonic anhydrase indicated that CYPs can act as chaperones (Freskgard et al., 1992; Freeman et al., 1996). However, it has not been possible to separate the chaperone and PPIase roles in vivo, making it difficult to conclude if immunophilins are rotamase-dependent or independent chaperones.
Several studies suggest that immunophilins play a role in protein trafficking. Brown et al. (2001) showed that CYPA is required for vacuole targeting of fructose bisphosphatase in yeast. In another study with fruit flies, a genetic analysis showed that a CYP homologue, NinaA, is required for transit of rhodopsin isoforms from the ER (Stamnes et al., 1991). Again, it is not known if foldase or rotamase activity (or both) are essential for these trafficking processes.
Other intriguing findings suggest that each immunophilin interacts specifically with a given protein. Such a function may or may not be related to protein folding. Examples of this specificity include the finding that FKBP12 associated with the Ca2+-releasing ryanodine receptor in striated muscle cells and modified its activity (Jayaraman et al., 1992; Brillantes et al., 1994). Mutant mice devoid of a functional FKBP12 developed a cardiac defect (Shou et al., 1998). In another study, CYP40, was shown to interact with HSP90 in the steroid hormone receptor complex (Kieffer et al., 1993). Regulation of steroid hormone signal transduction by these high molecular weight immunophilins has now been established (reviewed in Pratt, 1998). CYPA and Ess1 (another PPIase) associated with each other and with the chromatin remodelling complex and general transcriptional machinery (Wu et al., 2000). Such an interaction regulates gene silencing (Arevalo-Rodriguez et al., 2000). Although individual immunophilins act in different processes, they all seem to take part in the regulation of ‘super-molecular complexes’. It is not known how immunophilins facilitate assembly or maintain these complexes.
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Immunophilins and their function in plants |
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In work initiated about 10 years ago, a cyclosporin A-/FK506-sensitive process was identified in plants (fava bean) (Luan et al., 1993
). The use of immunosuppressants as an affinity tool led to a systematic effort to purify plant immunophilins (Luan et al., 1993, 1994a). The members of the immunophilin family most typical of plants were found to be localized in the chloroplast (Luan et al., 1994a). Since that time, a number of plant CYP genes have been characterized (Lippuner et al., 1994; Luan et al., 1994b; Marivet et al., 1994, 1995; Chou and Gasser, 1997). These include CYPB/CYP20-3 (ROC4), encoding a chloroplast CYP (Lippuner et al., 1994; Luan et al., 1994b). The first FKBP-type immunophilin identified (FKBP15), cloned from both Arabidopsis and fava bean, was shown to be located in the endoplasmic reticulum, ER (Luan et al., 1996) (T Ting and S Luan, unpublished results). There are at least two isoforms of FKBP15 in Arabidopsis and, consistent with findings in yeast, they are responsive to heat shock (Partaledis and Berlin, 1993; Sykes et al., 1993). A cytosolic FKBP12 has been characterized from fava bean and Arabidopsis (Faure et al., 1998; Xu et al., 1998). High molecular weight FKBP members have also been identified, two from wheat (FKBP73 and FKBP77) and one from Arabidopsis (FKBP77) (Blecher et al., 1996; Vucich and Gasser, 1996; Aviezer et al., 1998; Kurek et al., 1999). These large FKBPs contain the putative domains reported for interaction with Hsp90 in animals (Pratt, 1998).
A recent analysis of the Arabidopsis genome database revealed at least 52 genes encoding putative immunophilins (He et al., 2004). This is by far the largest immunophilin family found in organisms whose genomes have been sequenced, for example, 12 members have been found in yeast and 23 in C. elegans and Drosophila. Investigators have begun to address the function of the plant immunophilins. In one case, in which an Arabidopsis mutant had an abnormal developmental pattern, the responsible gene encoded an FKBP-like protein (Vittorioso et al., 1998). Another immunophilin, a CYP40-like protein, was shown to be necessary for normal leaf development (Berardini et al., 2001). Finally, in yet another study a CYP was found to interact with VirD2, an endonuclease acting in T-DNA transfer from Agrobacterium to host plant cells (Deng et al., 1998). The evidence suggests that, as in animals, individual members of the immunophilin family play different roles in plants.
Among the 52 immunophilins in Arabidopsis, about 20 are predicted to be in chloroplasts (He et al., 2004). The first chloroplast FKBP identified, pFKBP13, was purified from fava bean plants (Luan et al., 1994a). This protein was subsequently characterized biochemically and genetically in Arabidopsis (Gupta et al., 2002b). Arabidopsis FKBP13 (AtFKBP13) is localized in the thylakoid lumen where it interacts with the Rieske protein, an iron–sulphur protein in the cytochrome b6f complex that is part of the photosynthetic electron transport chain (Cramer et al., 1997). Silencing the AtFKBP13 gene in Arabidopsis altered the accumulation of the Rieske protein, suggesting that AtFKBP13 regulates import or assembly of the Rieske protein (Gupta et al., 2002b). A second protein found to be targeted by AtFKBP13 is novel and bears low, but recognizable homology to cytochrome c6—an electron carrier known to substitute for the copper protein, plastocyanin, in cyanobacteria and algae grown under copper-deficient conditions (Merchant and Dreyfuss, 1998). A cytochrome c6-like protein had not previously been found in land plants, which are unable to survive in copper-deficient environments. As a result, it was generally believed that land plants do not have a component to replace plastocyanin (Merchant and Dreyfuss, 1998). Extensive biochemical and genetic analyses prompted a change in this view in demonstrating that Arabidopsis contained a cytochrome c6 that could assist plastocyanin in electron transport (Gupta et al., 2002a).
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Summary of immunophilin function |
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Studies in both animal and plant systems show that immunophilins have diverse functions linked to activity as protein foldases, chaperones, and scaffolding facilitators or possible unknown catalytic capabilities. Immunophilins differ from other types of protein foldases and molecular chaperones in that each appears to have its own function and cellular target. This property is consistent with the finding that the sequence and structure of immunophilins are rather divergent, although a drug-binding core is conserved in all cases, including members of the family in plants. The specific sequence motif in each immunophilin may provide the structural basis for interacting with a given target. Another general rule for function is an association with ‘super-molecular complexes’ in animals as well as plants. It is possible that each immunophilin plays a role in the ‘biogenesis’ and/or ‘maintenance’ of these complexes.
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Regulation of immunophilins |
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Since their discovery in the early 1990s, one of the unanswered questions has been whether immunophilins are post-translationally regulated. Recent work with chloroplasts has provided an affirmative answer to this question. Initially, a resident of the stroma, AtCYP20-3 (ROC4) was shown to be activated post-translationally by chloroplast thioredoxin m following oxidation of its thiol groups with CuCl2 (Motohashi et al., 2003
). The results are in keeping with its regulation via the ferredoxin/thioredoxin system. More recently, a role for redox has also been linked to the regulation of FKPB13, an immunophilin of the thylakoid lumen (Gopalan et al., 2004). The thylakoid lumen has historically been considered a vacant compartment exclusively used to accommodate the evolution of oxygen in photosynthesis. Recent advances in proteomics and genomics have prompted a change in this view through the finding that this compartment contains numerous enzymes in addition to those directly associated with the light reactions (Gupta et al., 2002a, b; Peltier et al., 2002; Schubert et al., 2002; Spetea et al., 2004). Prominent among the lumen inhabitants are more than a dozen immunophilins, including AtFKBP13. Of note, the three-dimensional structure of AtFKBP13 revealed a unique pair of disulphide bonds that are absent in animal and bacterial homologues (Cys 5,17 and Cys 106,111) (Fig. 4). FKPB13 thus joins a growing group of redox-regulated chloroplast enzymes that, unlike their animal or heterotrophic counterparts, contain disulphide bonds functional in regulation (Buchanan and Balmer, 2005).
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atom backbone of Arabidopsis thaliana FKBP13 with the human and Legionella pneumophilia counterparts (from Gopalan et al., 2004The experiments revealed that Trxs from either chloroplasts (m-type) or E. coli specifically reduced both FKBP13 disulphides in concert with the loss of PPIase activity. That evidence, together with similar results obtained with derivatives harbouring Cys
Ser mutations, suggests that lumenal AtFKPB13 resembles a stromal CYP counterpart, AtCYP20-3, in undergoing thiol redox modulation (Motohashi et al., 2001, 2003). The lumen differs from the stroma, however, in one fundamental respect: activation of an immunophilin residing in the lumen (FKBP13) is achieved by oxidation (conversion of 2SH to S-S) rather than reduction (S-S to 2SH) as for the stromal immunophilin, AtCYP20-3, and numerous other biosynthetic enzymes in the stroma (Gopalan et al., 2004). The results support the view that, in contrast to stromal counterparts, biosynthetic enzymes of the lumen such as AtFKPB13 are activated by oxidation in the light (compare equations 5 and 6). The evidence suggests that the response of a regulatory enzyme to redox change in general depends on the redox milieu of the host compartment, i.e. whether the milieu is reducing or oxidizing under a prescribed environmental condition. An interesting question is whether the type of control depicted in equation 6 applies to other enzymes in the lumen.
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| (5) |
 | (6) |
Figure 5 summarizes the current view of the mechanism by which lumenal FKBP13 is regulated relative to stromal enzymes (Gopalan et al., 2004). It is noted that details of the mechanism of oxidation are not clear, i.e. whether an intermediary protein, designated redox protein, facilitates the oxidative activation of the target enzyme. It is also not known whether oxidative activation is diurnal or whether it occurs sporadically, for example, following import of reduced FKPB13 into the lumen. The elucidation of the details of the activation mechanism, including the extent of dependency of the activation mechanism on light, is a future goal in this work.
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A final question raised by recent work relates to the regulation of immunophilins via thiol/disulphide exchange compared with those lacking a disulphide group. It seems possible that the situation may resemble that established for chloroplast enzymes (that are regulated by thioredoxin via a redox active disulphide, such as fructose 1,6-bisphosphatase) and cytosolic counterparts (that lack a disulphide and are regulated by other mechanisms) (Schürmann and Jacquot, 2000
). According to this view, chloroplast immunophilins containing regulatory disulphide elements would be controlled by light via redox, whereas members lacking these elements would be regulated by other mechanisms, possibly independently of light. This question will also be addressed in the future. |
Concluding remarks |
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Recent findings have extended the capacity for redox regulation, long known for the chloroplast stroma, to the immunophilin AtFKBP13, a resident of the thylakoid lumen. The results suggest that the regulatory response of an enzyme to redox change depends not only on its function, but also on its location within the cell. Further, while specifics are not known, the above experiments raise the possibility that the observed oxidative activation mechanism reflects a general pattern of regulation operative in the lumen. According to this view, the precursor form of AtFKBP13 and perhaps other redox-regulated proteins bound for the lumen, such as polyphenol oxidase and violaxanthin de-epoxidase, are photoreduced by thioredoxin m via photosystem I on entering and traversing the stroma. Once imported into the lumen, the reduced, inactive form of the enzyme is converted to the active form by oxidation (Fig. 6). Such a mode of activation, in which an enzyme of the lumen is rendered active when oxidized, a reaction facilitated by oxygen produced in the light, contrasts with the mechanism functional in the stroma. The relation of electron transfer proteins resident in the lumen (Friso et al., 2004
)—HCF164 (Lennartz et al., 2001), thylakoid lumenal protein (Lee et al., 2004), oxygen-evolving enhancer protein (Heide et al., 2004), and CcdA (Page et al., 2004)—to the proposed scheme awaits further work.
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References |
|---|
Arevalo-Rodriguez M, Cardenas ME, Wu X, Hanes SD, Heitman J. 2000. Cyclophilin A and Ess1 interact with and regulate silencing by the Sin3-Rpd3 histone deacetylase. EMBO Journal 19, 3739–3749.[CrossRef][Web of Science][Medline]
Aviezer K, Kurek I, Erel N, Blecher O, Devos K, Breiman A. 1998. Studies on the expression of the wheat prolyl isomerase FKBP73 during plant development. Plant Science 139, 149–158.
Balmer Y, Buchanan BB. 2002. Yet another plant thioredoxin. Trends in Plant Scienceence 7, 191–193.
Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB. 2003. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proceedings of the National Academy of Sciences, USA 100, 370–375.
Balmer Y, Schürmann P. 2001. Heterodimer formation between thioredoxin f and fructose 1,6-bisphosphatase from spinach chloroplasts. FEBS Letters 492, 58–61.[CrossRef][Web of Science][Medline]
Balmer Y, Vensel WH, Tanaka CK, et al. 2004. Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proceedings of the National Academy of Sciences, USA 101, 2642–2647.
Baumann U, Juttner J. 2002. Plant thioredoxins: the multiplicity conundrum. Cell and Molecular Life Science 59, 1042–1057.
Berardini TZ, Bollman K, Sun H, Poethig RS. 2001. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291, 2405–2407.
Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A. 1996. A novel plant peptidyl-prolyl-cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Molecular Biology 32, 493–504.[CrossRef][Web of Science][Medline]
Brandes HK, Larimer FW, Hartman FC. 1996. The molecular pathway for the regulation of phosphoribulokinase by thioredoxin f. Journal of Biological Chemistry 271, 3333–3335.
Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR. 1994. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513–523.[CrossRef][Web of Science][Medline]
Brown CR, Cui D-Y, Hung GG-C, Chiang H-L. 2001. Cyclophilin A mediates Vid22p function in the import of fructose-1,6-bisphosphatase into Vid vesicles. Journal of Biological Chemistry 276, 48017–48026.
Brugière S, Kowalski S, Ferro M, et al. 2004. The hydrophobic proteome of mitochondrial membranes from Arabidopsis cell suspensions. Phytochemistry 65, 1693–1707.[CrossRef][Web of Science][Medline]
Buchanan BB. 1980. Role of light in the regulation of chloroplast enzymes. Annual Review of Plant Physiology 31, 341–347.[Web of Science]
Buchanan BB, Balmer Y. 2005. Redox regulation: a broadening horizon. Annual Review of Plant Biology (In press).
Buchanan BB, Schürmann P, Wolosiuk RA, Jacquot J-P. 2002. The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynthesis Research 73, 215–222.[CrossRef][Web of Science][Medline]
Chou IT, Gasser CS. 1997. Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Molecular Biology 35, 873–892.[CrossRef][Web of Science][Medline]
Clipstone NA, Crabtree GR. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357, 695–657.[CrossRef][Medline]
Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M. 2003. The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. Journal of Biological Chemistry 278, 23747–23752.
Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, Issakidis-Bourguet E. 2004. Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiology 136, 4088–4095.
Cramer WA, Soriano GM, Zhang H, Ponomarev MV, Smith JL. 1997. The cytochrome b6f complex. Novel aspects. Physiologia Plantarum 100, 852–862.
Deng W, Chen L, Wood DW, Metcalfe T, Liang X, Gordon MP, Comai L, Nester EW. 1998. Agrobacterium VirD2 protein interacts with plant host cyclophilins. Proceedings of the National Academy of Sciences, USA 95, 7040–7045.
Faure JD, Gingerich D, Howell SH. 1998. An Arabidopsis immunophilin, AtFKBP12, binds to AtFIP37 (FKBP interacting protein) in an interaction that is disrupted by FK506. The Plant Journal 15, 783–789.[CrossRef][Web of Science][Medline]
Florencio FJ, Yee BC, Johnson TC, Buchanan BB. 1988. An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach. Archives of Biochemistry and Biophysics 266, 496–507.[CrossRef][Web of Science][Medline]
Freeman BC, Toft DO, Morimoto RI. 1996. Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274, 1718–1720.
Freskgard PO, Bergenhem N, Jonsson BH, Svensson M, Carlsson U. 1992. Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258, 466–468.
Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, Wijk KJ. 2004. In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. The Plant Cell 16, 478–499.
Fruman DA, Burakoff SJ, Bierer BE. 1994. Immunophilins in protein folding and immunosuppression. FASEB Journal 8, 391–400.[Abstract]
Gelhaye E, Rouhier N, Gérard J, et al. 2004a. Thioredoxin h regulates enzymes of plant mitochondria. Proceedings of the National Academy of Sciences, USA 101, 14545–14550.
Gelhaye E, Rouhier N, Jacquot J-P. 2004b. The thioredoxin h system of higher plants. Plant Physiology and Biochemistry 42, 265–271.[CrossRef][Web of Science][Medline]
Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Héroux A, Buchanan BB, Kunchithapadam S, Luan S. 2004. Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proceedings of the National Academy of Sciences, USA 101, 13945–13950.
Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot JP, Decottignies P. 2002. Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. European Journal of Biochemistry 269, 272–282.[Web of Science][Medline]
Gupta R, He Z, Luan S. 2002a. Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis. Nature 417, 567–571.[CrossRef][Medline]
Gupta R, Mould RM, He Z, Luan S. 2002b. A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proceedings of the National Academy of Sciences, USA 99, 15806–15811.
He Z, Li L, Luan S. 2004. Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiology 134, 1248–1267.
Heide H, Kalisz HM, Follmann H. 2004. The oxygen evolving enhancer protein 1 (OEE) of photosystem II in green algae exhibits thioredoxin activity. Journal of Plant Physiology 161, 139–149.[CrossRef][Web of Science][Medline]
Izui K, Matsumura H, Furumoto T, Kai Y. 2004. Phosphoenolpyruvate carboxylase: a new era of structural biology. Annual Review of Plant Biology 55, 69–84.[CrossRef][Medline]
Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). Journal of Biological Chemistry 267, 9474–9477.
Kieffer LJ, Seng TW, Li W, Osterman DG, Handschumacher RE, Bayney RM. 1993. Cyclophilin-40, a protein with homology to the P59 component of the steroid receptor complex. Cloning of the cDNA and further characterization. Journal of Biological Chemistry 268, 12303–12310.
Kunz J, Hall MN. 1993. Cyclosporin A, FK506 and rapamycin—more than just immunosuppression. Trends in Biochemical Science 18, 334–338.
Kurek I, Aviezer K, Erel N, Herman E, Breiman A. 1999. The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiology 119, 693–704.
Laloi C, Rayapuram N, Chartier Y, Grienenberger J-M, Bonnard G, Meyer Y. 2001. Identification and characterization of a mitochondrial thioredoxin system in plants. Proceedings of the National Academy of Sciences, USA 98, 14144–14149.
Lee K, Lee J, Kim Y, Bae D, Kang KY, Yoon SC, Lim D. 2004. Defining the plant disulfide proteome. Electrophoresis 25, 532–541.[CrossRef][Web of Science][Medline]
Lemaire SD, Collin V, Keryer E, Quesada A, Miginiac-Maslow M. 2003. Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Letters 543, 87–92.[CrossRef][Web of Science][Medline]
Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P. 2004. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, USA 101, 7475–7480.
Lemaire SD, Miginiac-Maslow M. 2004. The thioredoxin superfamily in Chlamydomonas reinhardtii. Photosynthesis Research 82, 203–220.[CrossRef][Web of Science][Medline]
Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K. 2001. HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b6f complex in Arabidopsis. The Plant Cell 13, 2539–2551.
Lindahl M, Florencio FJ. 2004. Systematic screening of reactive cysteine proteomes. Proteomics 4, 448–450.[CrossRef][Web of Science][Medline]
Lippuner V, Chou IT, Scott SV, Ettinger WF, Theg SM, Gasser CS. 1994. Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana. Journal of Biological Chemistry 269, 7863–7868.
Liu J, Albers MW, Wandless TJ, Luan S, Alberg DG, Belshaw PJ, Cohen P, MacKintosh C, Klee CB, Schreiber SL. 1992. Inhibition of T cell signaling by immunophilin–ligand complexes correlates with loss of calcineurin phosphatase activity. Biochemistry 31, 3896–3901.[CrossRef][Medline]
Liu J, Farmer Jr JD, Lane WS, Friedman J, Weissman I, Schreiber SL. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807–815.[CrossRef][Web of Science][Medline]
Luan S. 1998. Immunophilins in animals and higher plants. Botanical Bulletin of Academia Sinica 39, 217–223.
Luan S, Albers MW, Schreiber SL. 1994a. Light-regulated, tissue-specific immunophilins in a higher plant. Proceedings of the National Academy of Sciences, USA 91, 984–988.
Luan S, Kudla J, Gruissem W, Schreiber SL. 1996. Molecular characterization of a FKBP-type immunophilin from higher plants. Proceedings of the National Academy of Sciences, USA 93, 6964–6969.
Luan S, Lane WS, Schreiber SL. 1994b. pCyP B: a chloroplast-localized, heat shock-responsive cyclophilin from fava bean. The Plant Cell 6, 885–892.[Abstract]
Luan S, Li W, Rusnak F, Assmann SM, Schreiber SL. 1993. Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. Proceedings of the National Academy of Sciences, USA 90, 2202–2206.
Maeda K, Finnie C, Svensson B. 2004. Cy5 maleimide-labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochemistry Journal 378, 497–507.[CrossRef][Web of Science][Medline]
Marchand C, Le Marechal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P. 2004. New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4, 2696–2706.[CrossRef][Web of Science][Medline]
Marivet J, Frendo P, Burkard G. 1995. DNA sequence analysis of a cyclophilin gene from maize: developmental expression and regulation by salicylic acid. Molecular and General Genetics 247, 222–228.[CrossRef]
Marivet J, Margis-Pinheiro M, Frendo P, Burkard G. 1994. Bean cyclophilin gene expression during plant development and stress conditions. Plant Molecular Biology 26, 1181–1189.[CrossRef][Web of Science][Medline]
Matouschek A, Rospert S, Schmid K, Glick BS, Schatz G. 1995. Cyclophilin catalyzes protein folding in yeast mitochondria. Proceedings of the National Academy of Sciences, USA 92, 6319–6323.
Merchant S, Dreyfuss BW. 1998. Post-translational assembly of photosynthetic metalloproteins. Annual Review of Plant Physiology and Plant Molecular Biology 49, 25–51.[CrossRef][Web of Science][Medline]
Mestres-Ortega D, Meyer Y. 1999. The Arabidopsis thaliana genome encodes at least four thioredoxins m and a new prokaryotic-like thioredoxin. Gene 240, 307–316.[CrossRef][Web of Science][Medline]
Motohashi K, Kondoh A, Stumpp MT, Hisabori T. 2001. Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proceedings of the National Academy of Sciences, USA 98, 11224–11229.
Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T. 2003. Chloroplast cyclophilin is a target protein of thioredoxin. Thiol modulation of the peptidyl-prolyl cis-trans isomerase activity. Journal of Biological Chemistry 278, 31848–31852.
Nelson DK, Cox MM. 2004. Lehninger principles of biochemistry. Worth Publishers.
O'Keefe SJ, Tamura J, Kincaid RL, Tocci MJ, O'Neill EA. 1992. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692–694.[CrossRef][Medline]
Page ML, Hamel PP, Gabilly ST, Zegzouti H, Perea JV, Alonso JM, Ecker JR, Theg SM, Christensen SK, Merchant S. 2004. A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. Journal of Biological Chemistry 279, 32474–32482.
Partaledis JA, Berlin V. 1993. The FKB2 gene of Saccharomyces cerevisiae, encoding the immunosuppressant-binding protein FKBP-13, is regulated in response to accumulation of unfolded proteins in the endoplasmic reticulum. Proceedings of the National Academy of Sciences, USA 90, 5450–5454.
Peltier JB, Emanuelsson O, Kalume DE, et al. 2002. Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. The Plant Cell 14, 211–236.
Pratt WB. 1998. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proceedings of the Society for Experimental Biology and Medicine 217, 420–434.[CrossRef][Medline]
Rao A, Luo C, Hogan PG. 1997. Transcription factors of the NFAT family: regulation and function. Annual Review of Immunology 15, 707–747.[CrossRef][Web of Science][Medline]
Renesto P, Crapoulet N, Ogata H, La Scola B, Vestris G, Claverie JM, Raoult D. 2003. Genome-based design of a cell-free culture medium for Tropheryma whipplei. Lancet 362, 447–449.[CrossRef][Web of Science][Medline]
Rey P, Cuiné S, Eymery F, Garin J, Court M, Jacquot JP, Rouhier N, Broin M. 2005. Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. The Plant Journal 41, 31–42.[CrossRef][Web of Science][Medline]
Rosen MK, Schreiber SL. 1992. Natural products as probes to cellular functions: studies of immunophilins. Angewandte Chemie 31, 384–400.
Schreiber SL. 1991. Chemistry and biology of immunophilin s and their immunosuppressive ligands. Science 251, 283–287.
Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T. 2002. Proteome map of the chloroplast lumen of Arabidopsis thaliana. Journal of Biological Chemistry 277, 8354–8365.
Schürmann P. 2003. Redox signaling in the chloroplast: the ferredoxin/thioredoxin system. Antioxidant Redox Signal 5, 69–78.[CrossRef][Web of Science][Medline]
Schürmann P, Jacquot J-P. 2000. Plant thioredoxin systems revisited. Annual Review of Plant Physiology and Plant Molecular Biology 51, 371–400.[CrossRef][Web of Science][Medline]
Shou W, Aghdasi B, Armstrong DL, Guo Q, Bao S, Charng MJ, Mathews LM, Schneider MD, Hamilton SL, Matzuk MM. 1998. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391, 489–492.[CrossRef][Medline]
Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B. 2004. Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proceedings of the National Academy of Sciences, USA 101, 1409–1414.
Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS. 1991. The cyclophilin homolog ninaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell 65, 219–227.[CrossRef][Web of Science][Medline]
Steimann B, Bruckner P, Superti-Furga A. 1991. Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans isomerase. Journal of Biological Chemistry 266, 1299–1303.
Sykes K, Gething MJ, Sambrook J. 1993. Proline isomerases function during heat shock. Proceedings of the National Academy of Sciences, USA 90, 5853–5857.
Verdoucq L, Vignols F, Jacquot J-P, Chartier Y, Meyer Y. 1999. In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family. Journal of Biological Chemistry 274, 19714–19722.
Vittorioso P, Cowling R, Faure JD, Caboche M, Bellini C. 1998. Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Molecular and Cell Biology 18, 3034–3043.
Vucich VA, Gasser CS. 1996. Novel structure of a high molecular weight FK506 binding protein from Arabidopsis thaliana. Molecular and General Genetics 252, 510–517.
Wong JH, Balmer Y, Cai N, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB. 2003. Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics. FEBS Letters 547, 151–156.[CrossRef][Web of Science][Medline]
Wong JH, Cai N, Balmer Y, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB. 2004. Thioredoxin targets of developing cereal seeds using complementary proteomic approaches. Phytochemistry Special Proteomics Issue 65, 1629–1640.
Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J, Hanes SD. 2000. The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO Journal 19, 3727–3738.[CrossRef][Web of Science][Medline]
Xu Q, Kudla J, Luan S. 1998. A novel FKBP12 that does not mediate action of immunosuppressive drugs FK506 and rapamycin. The Plant Journal 15, 811–820.
Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T. 2004. Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiology 45, 18–27.
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