JXB Advance Access originally published online on May 13, 2003
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Journal of Experimental Botany, Vol. 54, No. 388, pp. 1665-1673,
July 1, 2003
© 2003 Oxford University Press
Role of visible light in the recovery of photosystem II structure and function from ultraviolet-B stress in higher plants
Received 22 October 2002; Accepted 19 March 2003
1 Dipartimento di Biologia, Università di Padova, Italy
2 Dipartimento di Biologia, Universitá di Milano, Italy
3 Dipartimento di Scienze e Tecnologie Avanzate, Università del Piemonte Orientale, ‘Amedeo Avogadro’, Corso Borsalino 54, 15100 Alessandria, Italy
* To whom correspondence should be addressed. Fax: +39 0131 254410. E-mail: roberto.barbato{at}unipmn.it
Abbreviations: DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; PAGE, polyacrylamide gel electrophoresis; PSII, photosystem II.
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Abstract |
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The effect of visible light on photosystem II reaction centre D1 protein in plants treated with ultraviolet-B light was studied. It was found that a 20 kDa C-terminal fragment of D1 protein generated during irradiation with ultraviolet-B light was stable when plants were incubated in the dark, but was degraded when plants were incubated in visible light. In this condition the recovery of photosynthetic activity was also observed. Even a low level of white light was sufficient to promote both further degradation of the fragment and recovery of activity. During this phase, the D1 protein is the main synthesized thylakoid polypeptide, indicating that other photosystem II proteins are recycled in the recovery process. Although both degradation of the 20 kDa fragment and resynthesis of D1 are light-dependent phenomena, they are not closely related, as degradation of the 20 kDa fragment may occur even in the absence of D1 synthesis. Comparing chemical and physical factors affecting the formation of the fragment in ultraviolet-B light and its degradation in white light, it was concluded that the formation of the fragment in ultraviolet-B light is a photochemical process, whereas the degradation of the fragment in white light is a protease-mediated process.
Key words: D1 protein, photosynthesis, photosystem II, ultraviolet-B.
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Introduction |
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Although plants depend on light for their survival, in many cases light can be harmful to them. An excess of light brings about the inactivation of oxygenic photosynthesis, a phenomenon known as photoinhibition (Powles, 1984). The molecular target of photoinhibition is photosystem II (PSII), a thylakoid multisubunit pigment–protein complex capable of light-induced water splitting, with concomitant reduction of plastoquinone molecules. The reaction centre of PSII is composed of the D1 and D2 polypeptides to which all redox cofactors, including P680, are bound (Nanba and Satoh, 1989). An excess of light is thought to impair electron transfer through PSII, causing oxidative damage to the protein D1 (Vass et al., 1992). However, not only the quantity but also the quality of light is important in determining the actual extent of photoinhibition. It has long been known that wavelengths in the ultraviolet-B region of the spectrum (280–320 nm) are very effective in inactivating photosynthesis, and that the molecular target is again PSII (Jones and Kok, 1966). An increasing body of evidence indicates that photoinactivation due to ultraviolet-B light and that due to visible light are only partially related phenomena, as inactivation occurs at different sites of the photosynthetic electron transfer chain. In visible light, inactivation of PSII takes place either at the acceptor or donor side. In the first case, over-reduction of QA promotes the formation of the P680 triplet from which singlet oxygen is formed, with the subsequent induction of oxidative damage to the D1 protein (Vass et al., 1992). Proteins are then degraded by the recently discovered DegP2 (Haussuhl et al., 2001) and FtsH proteases (Spetea et al., 1999; Lindhal et al., 2000), hereafter referred to as FtsH1; DegP2 initially cleaves the D1 protein in the loop connecting the fourth and fifth transmembrane segments, originating the 23 kDa N-terminal fragment first described by Greenberg et al. (1987), whereas FtsH1 degrades this, and possibly other fragments, further. In donor-side photoinhibition, the accumulation of highly oxidizing cations such as P680+ and/or TyrZ+ may provide the driving force for direct photochemical cleavage of the protein (Barber and Andersson, 1992) occurring between the first and second transmembrane segments (Barbato et al., 1991), giving rise to a C-terminal fragment of about 24 kDa. In ultraviolet-B light, the main site of damage is thought to be the Mn-cluster involved in the oxidation of water (Melis et al., 1992; Vass et al., 1996), and its damage prompts the breakdown of D1 protein, which is cleaved in (or near) the second transmembrane segment by an as yet unidentified mechanism. This event originates 20 kDa C-terminal and 10 kDa N-terminal fragments (Barbato et al., 1995). Other sites of secondary damage inside PSII, such as QA, QB, bound/unbound plastoquinone/plastoquinol, P680, and TyrZ have also been reported (Greenberg et al., 1989; Renger et al., 1989; Melis et al., 1992; Vass et al., 1992).
Irrespective of the underlying mechanism of damage, recovery from photoinhibition depends on the synthesis of new protein D1 and on the reassembly of repaired PSII centres. Recovery of activity requires a low level of visible light and is prevented by the presence of inhibitors of plastidial protein synthesis, such as lincomycin. Reactivation of PSII is a complex process, requiring lateral migration of damaged complexes from grana partitions to stroma-exposed regions of the thylakoid membrane, their partial dismantling (Adir et al., 1990; Barbato et al., 1992), reassembly with pigments and other inorganic cofactors (van Wijk et al., 1994) and, lastly, back-migration of the repaired centres to grana regions of the thylakoid membrane (van Wjik et al., 1997; Baena-Gonzalez et al., 1999). Additional phenomena such as reversible phosphorylation of certain subunits and dimerization of repaired PSII centres may also be involved (Baena-Gonzalez et al., 1999). Recovery from exposure to ultraviolet-B light may be an even more complex phenomenon, as PSII damaged by this radiation stay in the grana and do not migrate to stroma-exposed lamellae, so that the repair cycle is not activated (Barbato et al., 1992).
As depletion of stratospheric ozone is causing renewed concern about the increased level of ultraviolet-B radiation reaching the Earth’s surface (Smith et al., 1995), it is important to understand how biological organisms cope, at the molecular level, with this enhanced environmental risk. This work investigated how the D1 protein and photosystem II, affected by treatment with ultraviolet-B light, behave during further incubation with visible light, a condition known to allow recovery of photosynthetic activity (Sass et al., 1997). Evidence is presented here for the following: (i) the formation in ultraviolet-B light of the well-defined 20 kDa C-terminal fragment of the D1 protein is a photochemical process; (ii) subsequent incubation of ultraviolet-B-treated plants in white light brings about the proteolytic degradation of this photochemically generated fragment; (iii) this occurs both in vitro and in vivo, even when protein synthesis is blocked by the presence of lincomycin; (iv) recovery of photosynthetic activity is observed only when white light is present and absolutely depends on protein synthesis.
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Materials and methods |
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Plant material, thylakoid isolation and subfractionation
Growth of barley (Hordeum vulgare L.), and the fah1 mutant of Arabidopsis thaliana L. (ferulic acid hydroxylase; Landry et al., 1995), and the isolation of thylakoids were carried out as described previously (Barbato et al., 2000; Casazza et al., 2001). For ultraviolet-B irradiation of isolated thylakoids, 20% (v/v) glycerol was added. Photosystem II membranes and octyl-ß-D-glucopyranoside-derived oxygen-evolving PSII cores were obtained as described previously by Ghanotakis et al. (1989).
Irradiation with ultraviolet-B and visible light
A Vilbert-Lourmat 215M lamp was used as the source of ultraviolet-B light. The ultraviolet-C component of the lamp was screened out by two layers of 0.15 mm thick cellulose diacetate. Irradiation with ultraviolet-B light was performed essentially as described previously (Barbato et al., 2000). For irradiation of thylakoids at different temperatures, a thermostatted beaker was used. Irradiation at a low oxygen concentration (about 2 µM) was carried out in a tightly stoppered quartz cuvette purged with nitrogen. To minimize oxygen intake, samples were withdrawn under a nitrogen stream. Low oxygen concentration was achieved by a chemical trap consisting of 10 mM glucose, 0.2 mg ml–1 glucose oxidase and 0.2 mg ml–1 catalase. Irradiation with white light was performed with a slide projector giving a light intensity of 50 µmol m–2 s–1 at the surface of the sample. For experiments with protease inhibitor, the CompleteTM Mini Protease Inhibitors cocktail (Roche) was used, which contains inhibitors to all five main classes of protease. For 3.5 ml of thylakoids at a chlorophyll concentration of 100 µg ml–1, half a tablet was used.
In vivo labelling
For in vivo labelling, plants which had been treated for 3 h with ultraviolet-B light, were incubated in white light (50 µmol m–2 s–1) in the presence of 67 µCi ml–1 of [35S]methionine as described previously (Barbato et al., 2000). At the desired time, leaves were harvested and washed with distilled water several times, and the thylakoids isolated as described above.
Protein analysis
SDS-PAGE in the presence of 6 M urea was performed in 12.5% polyacrylamide gels (Barbato et al., 2000). After electroblotting of proteins (Dunn, 1986) to poly(vinylidenedifluoride) membranes (Gelman), D1 protein and its primary 20 kDa fragment, as well as other PSII subunits, were detected with specific polyclonal antibodies. For immunodetection of D1 protein, two different antibodies to D1 were used, one specific for the C-terminus of the protein (Barbato et al., 1991), the second, a kind gift from Professor Aro (University of Turku, Finland) raised to a synthetic peptide corresponding to residues 234–242 of the D1 protein sequence. Antiserum to CP43 was raised in mouse; the properties of other antibodies have been described previously (Barbato et al., 1992). Blots were incubated in peroxidase-conjugated goat-anti mouse (or anti-rabbit) IgG and immunoreaction visualized by an enhanced-chemiluminescence kit (SuperSignal, Pierce). For quantification of proteins, 0.2 µg of chlorophyll was applied per gel lane; for detection of breakdown fragments of D1 protein, a larger amount of chlorophyll was applied (1–2 µg). For autoradiography, gels were stained with Coomassie Blue R-250, destained in 7.5% acetic acid/10% methanol, incubated with Amplify (Amersham), vacuum-dried and exposed to X-ray film at –80 °C.
Lincomycin treatment
Whole rosette leaves from 20-d-old Arabidopsis plants were used. They were cut at the petiole level, dipped and kept either in distilled water or in a 1 mM lincomycin for 1.5 h in the dark at room temperature. Plants were there transferred in the light or kept in the dark further for the desired periods of time.
Fluorescence analysis
The fluorescence parameters of the fah1 mutant of A. thaliana leaves treated or not with lincomycin, were recorded using a Photosynthetic Efficiency Analyser (PEA, Hansatech) as described previously (Tarantino et al., 1999).
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Results |
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Degradation of thylakoid proteins in leaves induced by ultraviolet-B light
The major effect of ultraviolet-B light on thylakoid proteins is breakdown of the reaction centre D1 protein, giving rise to a relatively stable fragment of about 20 kDa (Trebst and Depka, 1990; Friso et al., 1994; Barbato et al., 1995) which consists of the C-terminus of the protein (Friso et al., 1994). When barley leaves were irradiated with ultraviolet-B light in these experimental conditions (Fig. 1A, UVB), this fragment was detected after only 1 h exposure, peaked after 2–8 h, and decreased upon longer exposure. After 24 h, pronounced loss of both the D1 protein and the 20 kDa fragment was observed, together with the loss of other thylakoid subunits such as CP43 and OEE1 (Fig. 1B), CP47 and D2 (Fig. 1C). However, the loss of these proteins was not paralleled by the appearance of any specific degradation product (see also Fig. 1 in Barbato et al., 1995). No loss of either D1 protein or of any other thylakoid polypeptides was observed when plants were kept for 24 h either in the dark (Fig. 1, lane D) or in growth light (data not shown).
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Further degradation of the primary breakdown fragment requires visible light
When the ultraviolet-B lamp was turned off, the fate of the 20 kDa breakdown fragment depended on whether visible light was supplied to the system or not. Figure 2 shows that, when plants previously irradiated for 3 h with ultraviolet-B light were exposed to 50 µmol m–2 s–1 of white light, the level of the fragment decreased with time and, after 3 h, almost disappeared from the membrane (Fig. 2, visible). By contrast, the amount of fragment did not vary when plants were kept in the dark (Fig. 2, D). It was found that even a very low level of white light was effective in determining further decrease in the 20 kDa breakdown fragment (data not shown). These results suggest that the fate of this fragment is that of full degradation, and that this process needs light.
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Synthesis of D1 protein during degradation of the 20 kDa breakdown fragment
After 3 h exposure to ultraviolet-B light, barley leaves were incubated in white light in the presence of [35S]methionine, and the level of radioactivity incorporated into the D1 protein was evaluated by SDS-PAGE and autoradiography (Fig. 3). In this experimental condition, the D1 protein (as identified by immunoblotting; see Barbato et al., 2000), was mainly labelled. Labelling of other polypeptides was detected after longer exposure, but their level was much lower than that of the D1 protein (see Fig. 3).
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Lincomycin prevents recovery from photoinactivation but allows degradation of the 20 kDa fragment
Incubation with a low level of white light is usually associated with the recovery of photochemical efficiency from photoinactivation, a process requiring de novo synthesis of D1 protein and reassembly of functional PSII centres. Thus, a low level of visible light is required for the repair cycle of PSII units and the 20 kDa fragment of damaged D1 subunits to be further metabolized. The aim of the following experiments was to determine whether there is a link between these two phenomena. Recovery of photosynthetic efficiency after ultraviolet-B irradiation was measured by means of the Fv/Fm parameter. The experiment was performed on the fah1 mutant of A. thaliana. This carryies a lesion in the phyenylpropanoid biosynthetic pathway, the leaves of which do not contain ultraviolet-B-absorbing flavonoids. As a result, this mutant is particularly sensitive to this radiation (Landry et al., 1995; Booij-James et al., 2000) and a relatively low level of ultraviolet-B light induces inactivation of photosynthesis without damage to DNA (C Soave, unpublished results), making the mutant excellent material for recovery experiments. The same result was obtained with barley although with a slower recovery kinetics. The result of a typical experiment is reported in Fig. 4A, in which the loss and recovery of Fv/Fm are compared in the presence or absence of lincomycin. In the experimental conditions used here, which were similar to those used for barley, the presence of the antibiotic did not affect the extent of PSII inactivation (loss of about 50% of activity after 3 h of irradiation in both cases). However, when plants were moved to visible light, the effect of lincomycin became evident: recovery occurred, at least to some extent, when lincomycin was absent, whereas no recovery was observed in its presence. In the latter case, further loss of activity was evident and, after 24 h, variable fluorescence was no longer detectable. In the second part of the experiment, thylakoids were isolated from both samples, and the levels of D1 protein and breakdown fragments were evaluated by immunoblotting with polyclonal antibodies. As shown in Fig. 4B, the D1 protein in A. thaliana did not give a simple degradation pattern as in barley, but a number of fragments were detected with apparent masses between 25 and 16 kDa (Fig. 4B). With barley, a similar degradation pattern was observed when a higher level of ultraviolet-B light was used. As in the case of barley, the amount of breakdown fragments decreased upon incubation in white light (Fig. 4B) and, after 24 h, they were absent or barely detectable. When lincomycin was present during incubation in white light (Fig. 4C), removal of fragments still occurred, although to a slightly lower extent. Thus, synthesis of new D1 protein is not necessary for breakdown fragments to be further degraded.
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Metabolism of D1 protein in vitro
Up to now it has been established that a low level of visible light has two effects on leaves previously exposed to ultraviolet-B radiation: recovery of photosynthetic activity by de novo synthesis of D1 protein is activated, and further metabolism of the fragments produced by ultraviolet-B light is promoted. In leaves and thylakoids, identical degradation patterns were observed for the D1 protein (Barbato et al., 1995); however, in isolated thylakoids, recovery dependent on protein synthesis cannot occur. Isolated thylakoids irradiated with ultraviolet-B light and then incubated either at a low level of visible light or in the dark, gave the results shown in Fig. 5A. The fragment forming upon irradiation with ultraviolet-B light (Fig. 5A) was stable in the dark (Fig. 5A, dark) but then further degraded when thylakoids were incubated with a low level (50 µmol m–2 s–1) of visible light (Fig. 5A, visible), in a similar way as described for leaves. Even a very low level of visible light (5 µmol m–2 s–1) induced degradation of the fragment (data not shown), suggesting that this phenomenon does not require electron transfer. Accordingly, the presence of 10 µM DCMU during incubation in white light did not affect the degradation of the 20 kDa fragment (Fig. 5A, visible+DCMU). These results confirm that breakdown of the 20 kDa fragment does not require concomitant D1 synthesis. When oxygen-evolving PSII preparations such as PSII membranes (Fig. 5B, PSII membranes) or highly resolved PSII cores (Fig. 5B, PSII cores) were irradiated with ultraviolet-B light, formation of the typical 20 kDa fragment was still observed, in the same way as reported in leaves or isolated thylakoids (Barbato et al., 1995). However, further incubation in white light of these ultraviolet-B-treated preparations, at variance with what occurred in leaves and thylakoids, did not promote further degradation of the fragment (Fig. 5B). Therefore, further metabolism of the fragment probably requires factor(s) that are present in intact leaves or even in whole thylakoids, but not in simpler detergent-derived PSII preparations.
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In order to characterize the nature of the molecular processes responsible for the generation of the 20 kDa C-terminal fragment in ultraviolet-B light and that of its degradation in visible light, the effects of temperature, protease inhibitors and oxygen were further investigated. As shown in Fig. 6A, the 20 kDa fragment is formed by ultraviolet-B light in similar amounts at 0 and 20 °C. When thylakoids containing the fragment were exposed to white light, the fragment disappeared much faster at 20 °C (Fig. 6B, 20 °C) than at 0 °C (Fig. 6B, 0 °C). When irradiation with ultraviolet-B light was performed in the presence of a cocktail of protease inhibitors, neither the loss of D1 protein (Fig. 7A) nor the appearance of the 20 kDa fragment (Fig. 7B) was prevented. Instead, when thylakoids containing the 20 kDa fragment were further incubated in white light (Fig. 7C) in the presence of the protease inhibitors, degradation of the fragment was almost completely prevented. Lastly, in anaerobic conditions, the visible-light-induced degradation of the fragment (Fig. 8A) was much-less pronounced than in the presence of oxygen (Fig. 8B).
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Discussion |
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The reported loss of the D1 protein observed during irradiation with ultraviolet-B light (Barbato et al., 1995) is linked to an increased rate of degradation and a decreased rate of synthesis. The D1 protein, when cleaved by ultraviolet-B light, gives rise to a specific 20 kDa C-terminal fragment (Friso et al., 1994; Barbato et al., 1995). Three main observations must be considered in relation to degradation and resynthesis of the D1 protein: (i) the fate of the ultraviolet-B-generated 20 kDa D1 fragment is quite straightforward—both in vitro and in vivo further metabolism of this fragment needs light, but is independent of concomitant synthesis of D1 protein; (ii) as in the case of photoinhibition induced by visible light, recovery from ultraviolet-B stress is dependent on the synthesis of new D1 protein, a process requiring visible light; recovery is in fact completely prevented by conditions in which synthesis of the D1 protein does not take place; (iii) incubation with radioactive methionine during recovery from ultraviolet-B light stress in a low level of visible light leads to rather specific labelling of the D1 protein, radioactivity in other subunits being barely detectable in our labelling and autoradiography conditions. Some conclusions may be reached by bringing together these observations. First, during recovery from ultraviolet-B stress, low levels of visible light are required for the synthesis of new D1 protein, and for the removal from the membrane of the 20 kDa fragment generated by ultraviolet-B light. Although these two processes are both light-dependent, they do not seem to be closely related. New synthesis of D1 protein occurs continuously, independently of the damage induced by ultraviolet-B radiation. It is known that the synthesis and insertion of new D1 protein depends on visible light at the level of transcription, translation and elongation of the nascent peptide (Zhang and Aro, 2002). Instead, ultraviolet-B radiation simply decreases the rate of synthesis (Barbato et al., 2000). Light-induced degradation of the 20 kDa fragment occurs irrespective of whether D1 protein synthesis is active or prevented. Secondly, it has previously been shown that the 20 kDa fragment is located in grana membranes where it may be detected together with other PSII proteins in structurally defined although not functional centres (Barbato et al., 2000). During recovery from ultraviolet-B stress, only the D1 protein is synthesised de novo (Fig. 3), suggesting the possibility that other undamaged PSII subunits are recycled to reconstitute functional PSII centres. Recovery of photosynthetic activity needs the fragment to be removed from the damaged centres, in order to make them available for reassembly of new PSII units. In this context, visible light-dependent degradation of the 20 kDa fragment may be seen as the first step in repair from ultraviolet-B stress.
As for the mechanism by which the 20 kDa fragment is produced, it must be noted that it is generated both in vivo and in vitro, and that its production is blocked neither at 0 °C nor by the presence of protease inhibitors. This makes enzymatic cleavage at the origin of the 20 kDa fragment highly improbable, at variance with the case in which breakdown of the D1 protein is induced by visible light (Aro et al., 1990). In fact, primary cleavage in ultraviolet-B and visible light occurs on different sides of the thylakoid membrane, i.e. on the lumenal (Friso et al., 1994; Barbato et al., 1995) or stromal sides (De Las Rivas et al., 1992; Spetea et al., 1999), respectively. In visible light, the primary cleavage of D1 protein is carried out by the recently discovered DegP2 protease (Haussuhl et al., 2001), an enzyme bound to the stroma-exposed surface of thylakoids. As this enzyme does not have access to the lumenal side of thylakoids, it cannot be responsible for primary cleavage of D1 in ultraviolet-B light. Proteolytic activity located on the lumenal side of the membrane is due to DegP1 protease (Itzhaki et al., 1998). However, this protein has not been directly involved in the metabolism of the D1 protein. Although the activity of recently discovered plastidial proteases such as DegP2 and FtsH1 is relatively independent of temperature, it is nevertheless strongly inhibited at 0 °C (Haussuhl et al., 2001).
The visible-light induced degradation of D1 is a two-step process: a light-dependent (and temperature- independent) triggering event is followed by light- independent (and temperature-dependent) proteolysis; and these two steps can be resolved by performing irradiation at low temperatures (Aro et al., 1990; Spetea et al., 1999). Instead, in ultraviolet-B light, the protein is cleaved in just one photocleavage event, which is not inhibited by low temperatures or protease inhibitors. Its further degradation requires white light both in vitro and in vivo. The light intensity required to degrade the 20 kDa fragment is unable to induce degradation of the D1 protein in itself, not even in thylakoids previously inactivated on their donor side and, therefore, extremely sensitive to photoinhibition. Since anaerobic conditions slow down degradation of the fragment, it is proposed that visible light is required to prepare the photochemically generated fragment for proteolytic degradation, possibly by the action of singlet oxygen or other oxygen radicals. If this is the case, the FtsH1 protease may be responsible for the breakdown of the 20 kDa fragment, as in the case of the 23 kDa N-terminal fragment of D1 generated during acceptor-side photoinhibition (Lindhal et al., 2000). Accordingly, PSII preparations still able to photogenerate the 20 kDa fragment in ultraviolet-B light are incapable of further degradation of this fragment in visible light, indicating that the proteolytic activity responsible for this phenomenon was lost during the fractionation process: as in the case of visible light, this finding may be taken as evidence that the enzyme is not closely associated to the reaction centre complex, but is stroma-located or peripherically bound to the thylakoid surface.
Alternatively, light may play a regulatory role: the activity involved in the degradation of the 20 kDa fragment may be due to a light-activated protease, and therefore different from the FtsH1 protease, unless FtsH1 itself is light-activated. Evidence for the presence of plastidial light-activated protease(s) has been reported (Ostersetzer and Adam, 1997) during import studies with in vitro synthesized Rieske protein; in that case, FtsH1 was involved. Given the low level of light required, together with the lack of any effect of DCMU, it seems that electron transport is not involved in the phenomenon.
From the results reported in this paper, it seems clear that the metabolism of D1 protein in light is a very complex issue, depending both on qualitative and quantitative aspects of light. In visible light, the metabolism of D1 is a two-step phenomenon, in which the protein is oxidatively damaged and removed by the combined action of DegP2 and FtsH1 proteases. Shifting towards ultraviolet-B, the primary degradative process may be photolytic in nature, and photocleaved D1 generates the 20 kDa C-terminus. This then becomes the substrate of a protease the activity of which, directly or indirectly, is regulated by visible light. In natural conditions, in which ultraviolet and visible light are mixed, a rather complex picture emerges, in which turnover of D1 protein is differently affected by the two kinds of light.
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Acknowledgements |
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This work was supported by the Italian Ministry of University and Scientific and Technological Research Grant-Cofin (CIP MM5153929; RB, CS), National Program for Antarctic Research (PNRA), and CNR Target Project on Biotechnology. Financial support by the Dipartimento di Scienze e Tecnologie Avanzate to RB is acknowledged.
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