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First published online July 27, 2007; 10.1104/pp.107.101733 Plant Physiology 145:258-265 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
A Bacterial Transgene for Catalase Protects Translation of D1 Protein during Exposure of Salt-Stressed Tobacco Leaves to Strong Light[OA]Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai, Osaka 599–8231, Japan (K.A.-T., T.I., A.W.); Department of Advanced Bioscience, Faculty of Agriculture, Kinki University, Nakamachi, Nara 631–8505, Japan (S.S., Y.Y.); and National Institute for Basic Biology, Myodaiji, Okazaki 444–8585, Japan (N.M.)
During photoinhibition of photosystem II (PSII) in cyanobacteria, salt stress inhibits the repair of photodamaged PSII and, in particular, the synthesis of the D1 protein (D1). We investigated the effects of salt stress on the repair of PSII and the synthesis of D1 in wild-type tobacco (Nicotiana tabacum ‘Xanthi’) and in transformed plants that harbored the katE gene for catalase from Escherichia coli. Salt stress due to NaCl enhanced the photoinhibition of PSII in leaf discs from both wild-type and katE-transformed plants, but the effect of salt stress was less significant in the transformed plants than in wild-type plants. In the presence of lincomycin, which inhibits protein synthesis in chloroplasts, the activity of PSII decreased rapidly and at similar rates in both types of leaf disc during photoinhibition, and the observation suggests that repair of PSII was protected by the transgene-coded enzyme. Incorporation of [35S]methionine into D1 during photoinhibition was inhibited by salt stress, and the transformation mitigated this inhibitory effect. Northern blotting revealed that the level of psbA transcripts was not significantly affected by salt stress or by the transformation. Our results suggest that salt stress enhanced photoinhibition by inhibiting repair of PSII and that the katE transgene increased the resistance of the chloroplast's translational machinery to salt stress by scavenging hydrogen peroxide.
Plants depend on light for survival, but light itself and, in particular, light in combination with other environmental stress can be harmful to plants (Boyer, 1982  ; Murata et al., 2007). Light stress interferes with oxygenic photosynthesis, a phenomenon known as photoinhibition (Powles, 1984). Some researchers suggested that the primary negative effect of photoinhibition might involve damage to the quinone-binding protein, known now as the D1, in the photochemical reaction center of PSII (Kyle et al., 1984; Ohad et al., 1984; Krieger et al., 1998). The reaction center of PSII contains D1 and D2 proteins, to which all the relevant redox cofactors, including P680, are bound (Nanba and Satoh, 1989; Loll et al., 2005). Vass et al. (1992) have suggested that an excess of light energy might generate oxidative stress that would disrupt the transfer of electrons through PSII by damaging D1. However, the extent of photoinhibition of PSII reflects a balance between the light-induced damage (photodamage) to PSII and the repair of photodamaged PSII. More recently, stimulation of photoinhibition by excess light energy has been explained in terms of the inhibition of the repair of PSII by the oxidative stress that results from absorption of the excess energy (Murata et al., 2007).
Photodamaged PSII is repaired by replacement of damaged D1 by newly synthesized D1 (Kyle et al., 1984
The synergistic effects of various stresses on photoinhibition have been studied extensively in cyanobacteria. Such studies are useful because it is possible to control the level of two or more kinds of stress much more precisely in suspension cultures of microorganisms than it is in plant leaves. For example, the use of Synechocystis sp. PCC 6803 (hereafter, Synechocystis) has allowed researchers to modulate various kinds of stress simultaneously and, thereby, to investigate the mechanisms of the effects of such stresses on the photodamage to PSII (Allakhverdiev and Murata, 2004
However, cyanobacteria do not contain chloroplasts, and D1 of Synechocystis is encoded by a small family of psbA genes, namely, psbA2, psbA3, and psbA7 (Jansson et al., 1987
In plants, the synergistic effects of light stress and other kinds of stress, such as salt stress and oxidative stress, have not been characterized. In previous studies, we introduced the katE for catalase of Escherichia coli into tobacco (Nicotiana tabacum) and into tomato (Solanum lycopersicon), with cDNA for a transit peptide that allowed the resultant catalase to enter the stroma of chloroplasts (Shikanai et al., 1998 The primary aim of this study was to investigate the effects of salt stress on photoinhibition in a higher plant and to elucidate the mechanism by which ROS in chloroplasts are involved in the stimulation of photoinhibition under salt stress. We also examined whether the conclusions derived from studies, in cyanobacteria, of the effects of salt stress on photoinhibition and the turnover of D1 can be applied to higher plants. Our results demonstrated that salt stress inhibits the repair but not the photodamage to PSII and that salt stress and oxidative stress are tightly linked in the mechanism for stimulation of photoinhibition.
Effects of Salt Stress on Photoinhibition of PSII
We characterized katE-transgenic tobacco plants in terms of the introduction of the katE gene for catalase and the nptII gene as a marker. The result of PCR amplification indicated that these genes had been inserted into the genome of transformed plants (Fig. 1
). In previous studies we demonstrated that katE-transgenic tobacco plants synthesized recombinant catalase and contained approximately 3-fold higher levels of catalase activity than wild-type ones (Shikanai et al., 1998
We examined the effects of salt stress due to NaCl at various concentrations on PSII activity (Fv/Fm) during exposure to light stress of leaf discs from wild-type and katE-transformed tobacco plants (Fig. 2 ). When leaf discs of wild-type plants were exposed for 3 h to light at 2,000 µE m–2 s–1 under low-salt conditions (50 mM NaCl), PSII activity fell by 25% of the original activity. In the presence of 0.5 M NaCl, inactivation was more marked and occurred more rapidly, such that 70% of the original activity disappeared during incubation for 3 h. In the presence of 1.0 M NaCl, PSII activity declined even more rapidly, with loss of 85% of the original activity over the course of 3 h (Fig. 2A). By contrast, exposure of katE-transformed plants to the same conditions resulted in less extensive inactivation of PSII, with only 20% inactivation at 50 mM NaCl. At 0.5 M and 1.0 M NaCl, inactivation during the 3-h incubation resulted in loss of 50% and 75% of the original activity, respectively (Fig. 2B). In darkness, incubation of leaf discs in the presence of 1.0 M NaCl did not inactivate PSII in either type of plant (Fig. 2, A and B). These results demonstrated that salt stress enhanced the photoinhibition of PSII and that katE-transformed leaves were more tolerant to salt stress than were wild-type leaves. In addition, although exposure of leaf discs separately to light stress and to salt stress inactivated PSII minimally, combination of the two kinds of stress induced marked inactivation of PSII, revealing apparent synergism between the effects of strong light and high concentrations of NaCl.
Effects of Salt Stress on Photoinhibition in the Presence of Lincomycin To examine the contribution of de novo synthesis of chloroplast genome-encoded proteins to the salt stress-enhanced photoinhibition of PSII, we treated leaves with lincomycin as described in "Materials and Methods." Figure 2, C and D, shows that inhibition of protein synthesis by lincomycin dramatically accelerated the inactivation of PSII in leaf discs from both wild-type and transgenic plants. Moreover, the inactivation observed in the presence of lincomycin was also unaffected by the concentration of NaCl. However, the extent of inactivation in the presence of lincomycin was only minimal when leaf discs were incubated in darkness in the presence of 1.0 M NaCl in both types of plant (Fig. 2, C and D). These observations suggested that the protein synthesis de novo might be involved in the synergistic effects of light stress and salt stress during the inactivation of PSII.
We performed western blotting to examine the effects of NaCl on the level of D1 during photoinhibition at 2,000 µE m–2 s–1 in leaf discs from wild-type and katE-transformed tobacco plants (Fig. 3 ). The level of D1 decreased as the concentration of NaCl was increased in leaf discs from both wild-type and transformed plants. Incubation of wild-type leaf discs in strong light for 3 h under salt-stress conditions at 50 mM, 0.5 M, and 1.0 M NaCl decreased the level of D1 to 65%, 30%, and 15% of the original level, respectively (Fig. 3C). By contrast, in leaf discs from katE-transformed plants, incubation for 3 h at 50 mM, 0.5 M, and 1.0 M NaCl decreased the level of D1 to 75%, 45%, and 25% of the original level, respectively (Fig. 3D). These results might reflect the respective declines in PSII activity under the same conditions (see Fig. 2B).
Effects of Salt Stress on the de Novo Synthesis of D1 The results in Figures 2 and 3 suggested that the original activity of PSII was maintained by active synthesis of the D1 protein under nonstress conditions (50 mM NaCl), as observed in cyanobacteria. To confirm this hypothesis, we examined the effects of NaCl on the de novo synthesis of D1 in quantitative detail. Figure 4, A and C , shows that, in wild-type thylakoid membranes, the incorporation of [35S]Met reached a maximum level after incubation for 3 h in the presence of 50 mM NaCl. However, the incorporation was markedly suppressed, falling to 10% of the original levels, in the presence of 0.5 M NaCl, which might have reflected the reduced level of PSII activity, under the same conditions, shown in Figure 2A. The synthesis of D1 was totally blocked in the presence of 1.0 M NaCl. However, in thylakoid membranes from transformed plants (Fig. 4, B and D), incorporation of [35S]Met similarly reached a maximum level after incubation for 3 h in the presence of 50 mM NaCl, but the rate of synthesis of D1 was reduced by approximately 50% in the presence of 0.5 M NaCl. This reduction reflects the 50% reduction in PSII activity shown in Figure 2B. At 1.0 M NaCl, the synthesis of D1 was inhibited completely. The phenomenon responsible for the inhibitory effect of NaCl on translation remains to be identified in future studies.
Effects of Salt Stress on the Level of the psbA Transcript To identify the step(s) in the de novo synthesis of D1 that was inhibited by high concentrations of NaCl, we examined the effects of NaCl on the level of the transcript of the psbA gene during photoinhibition in leaf discs of wild-type and katE-transformed tobacco plants at 2,000 µE m–2 s–1 (Fig. 5 ). The level of the psbA transcript increased rapidly at 50 mM NaCl (Fig. 5, C and D). The presence of 0.5 M NaCl markedly delayed the increase in the level of the transcript. However, the final level of the transcript, namely, the level after exposure of leaf discs to light at 2,000 µE m–2 s–1 for 3 h, was almost unaffected by 0.5 M NaCl in leaf discs from both wild-type and katE-transformed plants. At 1.0 M, NaCl almost completely prevented any increase in the level of the transcript. Thus, the katE transgene had no significant effect on the level of the psbA transcript under all tested conditions.
In this study, we demonstrated that salt stress due to NaCl stimulated photoinhibition of PSII. Salt stress might have acted directly on sites and/or steps that were essential for the protection of PSII against photoinhibition. However, it also seems possible that salt stress decreased the activity of Rubisco, with resultant inhibition of CO2 fixation, and a decrease in utilization of NADPH in the Calvin cycle would have stimulated the generation of ROS in PSI (Murata et al., 2007 ). An increase in ROS concentration might have enhanced the level of photoinhibition. To examine whether photoinhibition is stimulated by salt stress directly or indirectly via the generation of ROS, we generated the katE-transgenic tobacco plants (Fig. 1), in which the recombinant catalase was synthesized and translocated to chloroplasts. The results in Figure 2, A and B, show that the presence of recombinant catalase alleviated photoinhibition under salt-stress conditions; thus, we concluded that the ROS concentration was probably decreased. These findings may suggest that the indirect effect of salt stress via ROS is involved in the salt stress-induced stimulation of photoinhibition. However, the direct effect of salt stress on the stimulation of photoinhibition, in combination with the indirect effect, cannot be excluded.
In the presence of lincomycin (Fig. 2, C and D), which inhibits the expression of chloroplast genome-encoded genes, photoinhibition occurs in the absence of repair. Consequently, use of this drug allows separation of photodamage from photoinhibition. We found that salt stress had no effect on the photodamage to PSII in tobacco leaves. In addition, we confirmed the synergistic negative effects of light stress and salt stress on the PSII complex in tobacco leaves. This observation suggests that salt stress might inhibit repair, with a consequent apparent increase in the extent of photoinhibition. This result reflects a similar phenomenon in cyanobacteria (Allakhverdiev et al., 2002
Western blotting demonstrated that the level of D1 decreased during photoinhibition under salt stress (Fig. 3). However, the rate of decrease in the level of D1 was lower than the rate of loss of PSII activity. This difference was conspicuous in wild-type plants (Figs. 2A and 3C). The apparent discrepancy between PSII activity and the level of D1 might be explained by the fact that the antibodies that we used reacted with both active D1 and damaged D1 but before cleavage (Barber and Andersson, 1992
When we examined the incorporation of [35S]Met, we found that the translation of the psbA transcript to yield the D1 protein in leaves from wild-type plants was markedly suppressed in the presence of 0.5 M NaCl (Fig. 4C), while such translation was inhibited to a lesser extent in leaves from katE-transformed plants under the same conditions (Fig. 4D). The difference, in terms of incorporation of [35S]Met into D1, between wild-type and katE-transformed plants might be related to levels of catalase in the stroma, since catalases should protect the translational machinery by reducing levels of H2O2. The difference in extent of incorporation of the radiolabeled amino acid explains why the extent of photoinhibition in the presence of 0.5 M NaCl was higher in wild-type than in katE-transformed leaf discs (Fig. 2). These results are consistent with those obtained in Synechocystis by Nishiyama et al. (2001) Northern blotting indicated that there were only insignificant differences, in terms of levels of the psbA transcript in the presence of 0.5 M NaCl, between leaf disc from wild-type and katE-transformed plants. Moreover, whereas levels of the psbA transcript increased with some delay in wild-type leaves, as compared to those in transformed discs, the maximum levels of the transcript differed only slightly between the two types of leaf during incubation for 3 h (Fig. 5, C and D). Although light stress increased levels of the psbA transcript at 0.5 M NaCl in both types of leaf, the translation of the transcript was dramatically inhibited only in wild-type leaves. In other words, the de novo synthesis of D1 was suppressed in spite of elevated levels of the psbA transcript. It is reasonable to conclude that salt stress inhibited the translational machinery more effectively than the transcriptional machinery. It seems to be very plausible that the bacterial catalase that was expressed in the cytosol and transported to the stroma of chloroplasts decreased the concentration of H2O2 in the chloroplasts of transgenic plants and alleviated the inhibition of the protein synthesis.
In this study, we postulate that the translational machinery in chloroplasts might be inhibited by salt stress via the actions of ROS. The excess ROS, resulting from accumulated electrons in PSI, might attack two potential sites. The first potential site is the site of initiation of translation, at which the reduced form of RB60 activates the translation of psbA mRNA by binding to the 5' untranslated region (Danon and Mayfield, 1994
Plant Materials and Growth Conditions
The line of katE-transformed tobacco plants (Nicotiana tabacum ‘Xanthi’) that harbored the katE gene for catalase from Escherichia coli, driven by the promoter of the rbcS3C gene for the small subunit of tomato (Solanum lycopersicon) Rubisco, was generated as described previously (Shikanai et al., 1998
Genomic DNA was prepared from plant leaves (0.5–1 g fresh weight) by the method of Dellaporta et al. (1983)
Leaf discs (2 cm in diameter) were punched from healthy, fully expanded tobacco leaves from 4-week-old plants, and discs were floated, adaxial side up, in distilled water that contained 50 mM, 0.5 M, or 1.0 M NaCl and exposed for 1, 2, or 3 h to strong light at 2,000 µE m–2 s–1 from a tungsten lamp (Luminar Ace LA-150TX; Hayashi Watch-Works) for photoinhibition of PSII at 25°C. After photoinhibitory treatment and subsequent incubation in darkness for 30 min, PSII activity was monitored in terms of chlorophyll (Chl) fluorescence and expressed as Fv/Fm, as determined at 25°C with a fluorescence-monitoring system (Hansatech Instruments).
For experiments in the presence of lincomycin, intact tobacco leaves were incubated with of 0.6 mM lincomycin (Sigma) for 2 h in darkness as described by Aro et al. (1993)
Thylakoid membranes were isolated and solubilized from leaves of wild-type and katE-transformed plants as described by Suorsa et al. (2004)
The lower epidermis of tobacco leaf discs (diameter, 2 cm) was gently pressed against coarse sandpaper to facilitate the incorporation of [35S]Met. Leaf discs were then floated on a solution (one disc per 6 mL) that contained 3 nM [35S]Met (>30 TBq mmol–1; Institute of Isotopes) and 0.4% Tween 20. Discs were illuminated at 2,000 µE m–2 s–1 at 24°C for 1, 2, or 3 h in the presence of 50 mM, 0.5 M, or 1.0 M NaCl. At indicated times, the pulse-labeled leaf discs were rapidly frozen in liquid N2 and stored until two leaf discs from each time point were combined and thylakoid membranes were isolated with minimal delay. Chl was quantitated and SDS-PAGE was performed. For analysis of radioactivity in proteins of thylakoid membranes, gels were stained, destained, vacuum-dried, and then exposed for autoradiography to phosphor-imager screens for approximately 5 d. The screens were monitored with a phosphor imager (FLA-3000; Fuji Photo Film) and the amount of radioactivity in D1 was estimated densitometrically.
Northern blotting was performed with the digoxigenin (DIG) system in accordance with the manufacturer's instructions (Roche Molecular Biochemical DIG application manual for filter hybridization). Leaf discs that had been exposed to light stress were frozen immediately in liquid N2 and ground with a pestle and mortar. Then total RNA was extracted with the Sepasol-RNA I super reagent according to the manufacturer's instructions (Nakalai Tesque). Equal amounts of total RNA (5 µg) from each sample were mixed with loading buffer that contained 20 µg mL–1 ethidium bromide and denatured at 65°C for 10 min. Each denatured mixture was fractionated by electrophoresis in MOPS buffer on a 2% agarose gel that contained 2% formaldehyde at 100 mA/500 V/1.5 h per gel. The capillary transfer of RNA, hybridization of blots with DIG-labeled DNA probe, immunological detection, and chemiluminescent detection were performed according to the instruction from Roche Molecular Biochemicals (DIG application manual for filter hybridization). Signals from hybridized mRNAs were detected with a luminescence image analyzer (LAS-1000; Fuji Photo Film). For normalization, staining with ethidium bromide of 25S rRNA allowed as to confirm loading of equivalent amounts of each sample.
Total RNA was isolated from tobacco leaves by the CTAB method with the Sepasol-RNA I super reagent (see above). Five micrograms of total RNA was reverse transcribed with an oligo(dT)20 primer, and single-strand cDNAs were prepared with the SuperScript III First-Strand Synthesis System for RT-PCR (Invitrogen). PCR was then performed with gene-specific primers that were designed on the basis of the sequence of the psbA gene: forward primer, 5'-TTATTCCTACTTCTGCAGCTATAGG-3' (the underlined sequence is a PstI site); and reverse primer, 5'-CGATAGCAGCTAGGTCTAGAGGGAA-3' (the XbaI site is underlined; positions –245 to –269 and +1,015 to +1,039, respectively, counted from the first ATG of the plastid psbA gene [Sugita and Sugiura, 1984 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number X00616.
We thank Prof. Kimiyuki Satoh (Okayama University, Japan) for his generous gift of D1-specific antibodies and Prof. Masaaki Takahashi (Osaka Prefecture University) for his assistance with the pulse-labeling experiment. We also thank Dr. Ahmad Abdul Kader (General Commission for Scientific Agricultural Research, Syria) for his helpful comments on the original manuscript. Received May 1, 2007; accepted July 13, 2007; published July 27, 2007.
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: Akira Wadano (wadano{at}bioinfo.osakafu-u.ac.jp).
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.101733 * Corresponding author; e-mail wadano{at}bioinfo.osakafu-u.ac.jp.
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, 50 mM NaCl, light; 
, 0.5 M NaCl, light; 
, 1.0 M NaCl, light; 
, 1.0 M NaCl, dark. Each point and bar represent the average ± SE of results from three independent experiments. The absence of bar indicates that SE fell within the symbol in this and other figures.
), 0.5 M NaCl (
), and 1.0 M NaCl (
