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First published online October 29, 2004; 10.1104/pp.104.046656 Plant Physiology 136:3784-3794 (2004) © 2004 American Society of Plant Biologists
Investigations into the Role of the Plastidial Peptide Methionine Sulfoxide Reductase in Response to Oxidative Stress in Arabidopsis1Intercollege Program in Plant Physiology (H.M.R., E.J.P., M.T.), Department of Plant Pathology (P.J.J., E.J.P.), and Department of Biochemistry and Molecular Biology (M.T.), The Pennsylvania State University, University Park, Pennsylvania 16802; and National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland 20892 (B.S.B.)
Peptidyl Met residues are readily oxidized by reactive oxygen species to form Met sulfoxide. The enzyme peptide Met sulfoxide reductase (PMSR) catalyzes the reduction of Met sulfoxides back to Met. In doing so, PMSR is proposed to act as a last-chance antioxidant, repairing proteins damaged from oxidative stress. To assess the role of this enzyme in plants, we generated multiple transgenic lines with altered expression levels of the plastid form of PMSR (PMSR4). In transgenic plants, PMSR4 expression ranged from 95% to 40% (antisense) and more than 600% (overexpressing lines) of wild-type plants. Under optimal growing conditions, there is no effect of the transgene on the phenotype of the plants. When exposed to different oxidative stress conditions—methyl viologen, ozone, and high light—differences were observed in the rate of photosynthesis, the maximum quantum yield (Fv/Fm ratio), and the Met sulfoxide content of the isolated chloroplast. Plants that overexpressed PMSR4 were more resistant to oxidative damage localized in the chloroplast, and plants that underexpressed PMSR4 were more susceptible. The Met sulfoxide levels in proteins of the soluble fraction of chloroplasts were increased by methyl viologen and ozone, but not by high-light treatment. Under stress conditions, the overexpression of PMSR4 lowered the sulfoxide content and underexpression resulted in an overall increase in content.
The generation of reactive oxygen species (ROS), especially under conditions of metabolic stress, is an unavoidable side effect of life in an oxygen atmosphere. These species include singlet oxygen, hydrogen peroxide, superoxide, and hydroxyl radical. To protect against ROS, aerobic organisms have evolved both enzymatic and nonenzymatic scavenging systems (Scandalios, 1993  ; Smirnoff and Wheeler, 2000). The enzymatic systems include superoxide dismutases (Scandalios, 1993), catalases, and peroxidases (Defelipe et al., 1988). The nonenzymatic systems include antioxidants such as glutathione, vitamin E, carotene, and vitamin C. ROS that escape the scavenging system can cause oxidative damage to virtually all biomolecules (Klatt and Lamas, 2000). Once damaged, certain macromolecules, such as DNA, may be repaired by the cell. Research within the past decade has shown that proteins can also be repaired.
Amino acids vary in susceptibility to oxidative damage, with Met residues the most vulnerable followed by Cys and Tyr (Levine et al., 1996
Plant PMSR activity in turnip and bean leaves was first reported in 1966 by Doney and Thompson (1966) To examine the role of PMSR in plants, we have transformed Arabidopsis plants to alter expression levels of the plastid form of PMSR (PMSR4). Multiple lines were generated expressing different levels of PMSR4 ranging from 95% to 40% (antisense) and more than 600% (overexpressing lines) of wild-type plants. Our results show that PMSR4 plays a role in protection from ROS in the chloroplast.
Oxidative Stress and Wild-Type PMSR4 Activity Wild-type plants were exposed to three agents that have been shown to cause oxidative stress: ozone, methyl viologen, and high-light intensity. The PMSR4 activity was measured in chloroplasts isolated from foliage after these treatments and compared to nontreated controls. Because the PMSR activity was measured in isolated chloroplasts, other nonchloroplastic isozymes do not contribute to the total measured enzyme activity. Figure 1 shows PMSR4 expression as measured by western blot (Fig. 1A) and by enzyme activity (Fig. 1B) after the oxidative stress treatments. The intensity of the immunoblots was measured and revealed that PMSR content was 3.5 times higher after high-light treatment and 4.5 times higher after methyl viologen treatment. In contrast, PMSR4 content was only 1.6 times higher in plants exposed to ozone. The pattern in PMSR4 enzyme activity was similar to that obtained from the western blots.
Purity of Chloroplast Preparations Because our studies of transgenic plants involve characterization of the chloroplast, we needed to initially determine the integrity of our chloroplast preparations. The NADP-dependent glyceraldehyde-3-phosphate dehydrogenase (G3PDH) activity is a marker enzyme for the chloroplast, whereas phosphoenolpyruvate carboxylase (PEPC) is a marker enzyme for the cytosol. Transgenic and wild-type plants were grown under optimal growth conditions and the activity of these enzymes in the crude (chloroplast-containing) extracts and chloroplast preparations of the different lines was determined (Table I). After chloroplast isolation, the activity of the marker enzyme G3PDH was 2 to 3 times higher than in the crude extract, showing that the procedure enriched for the targeted organelle. When assaying the isolated chloroplast for the cytosolic marker PEPC, a maximum of 5% of the activity was recovered in the plastidial preparation. This shows the high purity of the isolated chloroplasts.
The purity of the chloroplast was confirmed by Asp aminotransferase (AAT) activity gels. This method separates the cytosolic and the chloroplastic isoforms of the enzyme (Schultz and Coruzzi, 1995 ) and detects their activity in the gels. Both isoforms were detected in the crude extract, but only one band corresponding to the chloroplastic form of AAT is present in the isolated chloroplasts (Figs. 1C, 3B, and 4B). Since the results obtained with the AAT activity gels were consistent with those of the marker enzymes, we decided to use AAT gel activity assay to routinely monitor the purity of the chloroplast preparations. Furthermore, PEPC activity was determined in several more chloroplast isolations and in no case was it detected more than 5% of cytosolic contamination (data not shown).
Characterization of Transgenic Plants To study the role of PMSR4 in the response of Arabidopsis plants to oxidative stress conditions, we obtained transgenic plants with altered expression of PMSR4. A full-length PMSR4 cDNA was placed in the sense (overexpression) and in the antisense (underexpression) direction, behind the cauliflower mosaic virus 35S promoter (35S::PMSR4 and 35S::anti-PMSR4, respectively) and transformed into Arabidopsis. The presence of the construct was confirmed by PCR analysis in several lines, and the independence of the lines was assessed by Southern-blot analysis. Three of the lines of each construct were further characterized. The expression level of PMSR4 in the transgenic plants was analyzed by semiquantitative reverse transcription (RT)-PCR and by western blot. For overexpressing plants with the construct in the sense orientation (Fig. 2), RT-PCR showed a large increase in the PMSR message. Using specific primers (see "Materials and Methods") that amplified only the mRNA transcribed from the transgene, we confirmed that the increase in the PMSR4 mRNA levels was due exclusively to the effect of the transformation. Furthermore, analysis of the plants showed that the transformation did not induce gene silencing by cosuppression. All of the lines showed overexpression of PMSR4 mRNA (Fig. 2A). Similar analysis of the transgenic antisense lines showed a considerable reduction in the PMSR4 mRNA as seen by RT-PCR analysis (Fig. 3A). The reduction in the mRNA levels was in accord with the decrease observed in the protein levels (Fig. 3A).
The peptidyl PMSR activity in the chloroplast extracts from these transgenic lines was measured using 9-fluorenylmethyloxycarbonyl (Fmoc)-MetSO as the peptide mimic substrate (Fig. 4). The overexpressing lines (Fig. 4A) expressed higher PMSR4-specific activity than the untransformed wild-type plants. The PMSR4-specific activity in the overexpressing line 1001 was nearly 6 times higher than the activity of the untransformed wild-type plants. The enzyme activity of line 202 was almost 3 times that of the wild type. Consistent with the results of the western blot shown in Figure 2, the activity of line 802 was not much higher than that of the wild type, but the difference was statistically significant (P  0.05). In contrast, the PMSR4-specific activities of the underexpressing lines (Fig. 4B) were significantly lower than that of the untransformed wild type, ranging from 0.15 nmol min–1 mg–1 protein in line 1003 to 0.27 nmol min–1 mg–1 protein in line 801.
MetSO content in the soluble fraction of the chloroplast preparations was also measured (Table II). Under optimal growing conditions, there were no statistical differences (P
PMSR4 Overexpression and Oxidative Stress The wild-type and transgenic plants underexpressing and overexpressing PMSR4 were subjected to the oxidative stress treatments of high-light/low-temperature methyl viologen and ozone. Photosynthetic rates and chlorophyll a fluorescence were measured and the percentage reduction was calculated (see "Materials and Methods"). Under optimal growing conditions, no phenotypic variations between the transgenic overexpressing lines and the untransformed wild-type plants were observed (data not shown). The photosynthetic activity ranged from 7.1 to 7.6 µmol CO2 m–2 s–1 and the maximum quantum yield (Fv/Fm ratio) was around 0.83. However, oxidative stress treatments induced a reduction in the photosynthetic rate (Fig. 5A) and in the Fv/Fm ratio (Fig. 5B) in wild-type and overexpressing plants. The overexpression of PMSR4 reduced the severity of the stress-induced impact on the photosynthetic rate and the Fv/Fm ratio. The treatment that resulted in the largest difference in response between the wild-type and the overexpressing lines was methyl viologen (i.e. overexpression of the chloroplast PMSR4 afforded the most protection from methyl viologen stress). Whereas the photosynthetic rate and maximum quantum yield were inhibited 67% and 27%, respectively, in wild-type plants, these functions were inhibited only 38% and 19% in the overexpressing line 802; 16% and 8% in the overexpressing line 202, and 0.5% and 11% in the overexpressing line 1001.
PMSR4 overexpression also enhances the resistance of the plants against the oxidative stress imposed by the treatment of high-light intensity under low temperature. The inhibition caused by high-light treatment in wild-type plants was 59% in photosynthetic rate and 24% in Fv/Fm ratio. In plants overexpressing PMSR4, lines 802, 202, and 1001, the photosynthetic rate was inhibited to a lesser extent at 38%, 34%, and 28%, respectively. The reduction of Fv/Fm ratio was 18% (line 802), 15% (line 202), and 12% (line 1001). Treatment with ozone resulted in statistically significant differences in the photosynthetic rate between the wild-type and the transgenic lines, but not in the Fv/Fm ratio (Fig. 5B) or in the stomatal conductance (Fig. 6). The inhibition of photosynthesis in the wild type was 33%, and in the overexpressing plants, it was 16%, 14%, and 10% in lines 802, 202, and 1001, respectively.
PMSR4 Underexpression and Oxidative Stress Underexpression of PMSR4 resulted in greater sensitivity to high light and to methyl viologen, but not to ozone (Fig. 7). In plants exposed to high light under low temperature, photosynthesis and Fv/Fm ratio were reduced 55% and 23%, respectively, in the wild type, whereas the reduction in the transgenic lines was 70% and 24% (line 801), 68% and 23% (line 1002), and 66% and 23% (line 1003). The reduction in photosynthesis and Fv/Fm ratio in the plants treated with methyl viologen was 59% and 46% (wild type), 74% and 54% (line 801), 74% and 55% (line 1002), 71% and 57% (line 1003).
MetSO Content of Chloroplasts The MetSO content of the soluble fraction of chloroplasts was also determined in wild-type and transgenic lines after treatment with oxidative stress agents. The MetSO contents of the overexpressing lines 202 and 1001 after high-light treatment were slightly, but significantly, lower than that of wild type (Fig. 8A). The percent MetSO was 30% in wild-type plants and 25% in line 1001. No statistical differences were observed between the wild-type and the other overexpressing line 802. Treatment of the plants with methyl viologen resulted in a large increase in the MetSO content of all plants; however, in the overexpressing plants, the MetSO content was lower (50%) than in the wild-type plants (58%). A similar MetSO pattern was observed when plants were treated with ozone. Whereas the wild-type plants contained 56% MetSO, the overexpressing lines contained statistically significant lower amounts of MetSO (approximately 35% for all lines).
In plants underexpressing PMSR4 (Fig. 8B), the high-light treatment resulted in formation of approximately 30% MetSO in all the lines. There were no significant differences among them. In plants underexpressing PMSR4, methyl viologen treatment resulted in MetSO content significantly increasing to a much higher value (as much as 80% in line 1003) relative to wild type. A similar MetSO profile was also observed when plants were treated with ozone. Plants underexpressing PMSR4 contained as much as 85% MetSO content after ozone treatment, a value much higher than that observed in wild-type plants.
Plant Oxidative Stress and PMSR
Due to the ease of Met oxidation to yield MetSO and the ability of PMSR to repair the MetSO, Met has been proposed to act as a last-chance antioxidant for proteins (Levine et al., 1999
Our results show that wild-type plants increase PMSR4 expression in response to oxidative stress (Fig. 1). This expression is dependent upon the type of oxidative stress and where it is localized. Oxidative stress, localized in the chloroplast and induced by high light and methyl viologen, caused an increase in PMSR4 expression. In contrast, ozone, which probably reacts before reaching the chloroplast, had little, if any, effect on PMSR4 expression. Similar results were found by Sadanandom et al. (2000)
High-light stress caused a decrease in both photosynthetic rate and in chlorophyll a fluorescence (Table III). However, no change was observed in the MetSO content of the soluble proteins. These results are actually consistent with the known mechanism of high-light damage. Upon high-light stress, there is a decrease in quantum yield and photosynthetic productivity referred to as photoinhibition. This has been suggested to be caused by ROS oxidation of PSII proteins (Aro et al., 1993
Consistent with the findings from the overexpressing lines, with plants underexpressing PMSR4, the reduction of the photosynthetic rate is not accompanied by an increase in MetSO content. This again suggests that when plants are exposed to high light, PMSR4 plays a key role in repairing membrane proteins in the chloroplast. Aro et al. (1993) found that the degradation and replacement of the D1 protein (and at lower level D2 protein) in PSII play a protective role against photodamage under both stress and nonstress conditions. Both of these are membrane proteins that have high turnover rates (replaced quickly in the cell) and Met residues may play a key role in this turnover. Both proteins have several Met residues, which, upon oxidation, can induce structural changes in the protein triggering the signaling for proteolysis (Aro et al., 1993; Satoh, 1998). Such oxidation of D1 and D2 Met residues after high-light stress has been observed with purified proteins from pea plants (Sharma et al., 1997b). If oxidation of these Met residues facilitates their proteolysis, then PMSR4 may play a key role in regulating D1 and D2 turnover and, in turn, in the integrity of PSII.
Due to its reactivity, ozone is proposed not to reach the chloroplast, reacting in the apoplast and the cytosol of plant cells (Langebartels et al., 2002
The finding that ozone caused a decrease in photosynthesis but not in Fv/Fm ratio indicates that ozone has little impact on the proteins of PSII. In contrast, the changes in MetSO content indicate that ozone treatment results in oxidation of the soluble proteins of the chloroplast. Because Rubisco is the major protein of the chloroplast, it is a likely target for Met oxidation and repair in vivo. Previous research has attributed the decrease in photosynthesis after ozone treatment to be due to a decrease in Rubisco content (Pell et al., 1992
Another possible mechanism for protection is the ability of PMSR4 overexpression to protect guard cells in the stomata. Ozone treatment has been shown to cause a guard cell-dependent decrease in CO2 exchange and thus in photosynthetic rates mainly due to changes in stomatal conductance (Torsethaugen et al., 1999
Upon illumination, methyl viologen is reduced by PSI. Reduced methyl viologen, in turn, reduces O2 yielding superoxide. The resulting superoxide, in the presence of iron or copper, can lead to generation of the hydroxyl radical. Thus, methyl viologen has the capacity to oxidize all soluble and membrane-associated proteins of the chloroplast. Indeed, among the different oxidative stress treatments, methyl viologen caused the strongest inhibition of photosynthesis and of maximum quantum yield. Methyl viologen also caused the largest increase in MetSO content of chloroplast-soluble proteins. Our results indicate that PMSR4 plays a significant role in plant response to methyl viologen. Underexpression caused a greater decrease in the Fv/Fm ratio, a greater increase in MetSO formation in the chloroplast, and a greater decrease in assimilation capacity. In contrast, plants overexpressing PMSR4 were more resistant to methyl viologen as demonstrated by lower MetSO formation, higher Fv/Fm ratio, and higher photosynthetic rates (line 1001, Fig. 5C).
The apparently wide range of functions of PMSR4 is still not clearly resolved and the natural substrates for the enzyme are yet to be identified. For example, Gustavsson et al. (1999)
The lack of phenotypic variation between underexpressing and wild-type plants under nonstress conditions suggests that PMSR4 does not play a crucial role in ROS metabolism under low-stress conditions. However, PMSR4 appears to play a key role in plant response under conditions of oxidative stress. Our findings also indicate that, under basal nonoxidative stress conditions, plant chloroplasts contain a high level of MetSO and appear to be tolerant of these high levels. The average value of 27% to 33% MetSO in the soluble fraction of the chloroplasts of different lines under optimal growing conditions is considerably higher than the protein MetSO content reported for yeast (Saccharomyces cerevisiae), bacteria (Moskovitz et al., 1997
Plant Material Arabidopsis (Arabidopsis thaliana) ecotype Columbia seeds were planted in a commercial soil mix (Redi-earth Plug and Seedling mix; Scotts-Sierra, Marysville, OH) and grown in lighted growth chambers, with approximately 120 µmol photon m–2 s–1 on a 23°C/21°C, 12-h day/night cycle. Plants were fertilized weekly with 20:20:20 fertilizer (Peters Professional; Scotts-Sierra).
The full-length cDNA encoding PMSR4 from Arabidopsis (expressed sequence tag 226P20T7; GenBank accession no. X97326) was obtained from the Arabidopsis Biological Resource Center (Columbus, OH). The cDNA was cloned in the sense (overexpressing) and the antisense (underexpressing) direction into the pBI121 vector after removal of the
RNA was extracted from 10-d-old plants grown in solid medium (0.5x Murashige and Skoog, 1% Suc, 0.7% bacto-agar). Leaf tissue was ground in liquid nitrogen and total RNA was extracted from 100 mg of tissue (RNeasy; Qiagen, Chatsworth, CA). RNA (1 µg) was treated with DNAse I and reverse transcribed to synthesize the first-strand cDNA using the Retroscript System (Ambion, Austin, TX) in a two-step reaction with previous denaturing of the RNA at 80°C and cDNA synthesis at 44°C using oligo(dT). The synthesized cDNA (2 µL) was used for PCR amplification of the genes of interest using gene-specific primers as in Zhong et al. (2003)
Methyl viologen was applied to mature rosettes of 4-week-old plants by spraying with 10 µM methyl viologen with 0.05% Tween 20. Approximately 3 mL of methyl viologen per plant were applied 3 h before the beginning of the light period. The plants were then returned to the growth chamber. Ozone was applied to 4-week-old plants at 0.46 µL L–1 for 6 h during 4 d. Ozone was generated by passing oxygen through an ozonator (OREC V1-0, Ozone Research and Equipment, Phoenix), and O3 concentrations in the growth chamber were monitored continuously with a UV photometric O3 analyzer (model 49; Thermo Environmental Instruments, Franklin, MA). To determine the effect of high light, 4-week-old plants were exposed to 600 µmol photon m–2 s–1 light intensity at 8°C for 48 h. Photosynthetic rates, stomatal conductance, and the maximal quantum yield of PSII photochemistry (Fv/Fm ratio) were measured 24 h before and after treatments. Photosynthetic rates and stomatal conductance were measured with a LI-COR 6400 gas exchange system fitted with an Arabidopsis chamber (LI-COR, Lincoln, NE). The gas exchange cuvette was maintained at 23°C block temperature, 400 µL L–1 CO2, and 600 ± 30 µmol photon m–2 s–1 light intensity. Chlorophyll a fluorescence was measured using a pulse amplitude-modulated fluorometer PAM-2000 equipped with an Arabidopsis chamber and clip (Walz, Effeltrich, Germany). Photosynthesis, stomatal conductance, and chlorophyll a fluorescence were determined in leaves 4 and 5 from the apex of at least 8 (photosynthesis) or 12 (fluorescence) plants. Photosynthesis and stomatal conductance were measured 4 h after the beginning of the light period. Fv/Fm ratio was determined in dark-adapted leaves before the beginning of the light period. The percentage of reduction in photosynthesis and in Fv/Fm ratio was calculated as the reduction in the variable after the treatment in relation to the value measured before the treatment. After measuring photosynthesis, plants were placed in the dark for 6 h and then leaves were harvested for chloroplast isolation.
Chloroplasts were isolated from fully expanded leaves of 4-week-old plants (32/preparation). The purity of the preparations was determined by Asp aminotransferase activity gels according to the organelle preparation protocol (Weigel and Glazebrook, 2002
Isolated chloroplasts were resuspended in 50 mM Tris-Cl, pH 7.5, 0.1% Triton X-100, 10% glycerol, 5 mM
Lysed chloroplasts (100 µL) were centrifuged at 16,000g at 4°C and the supernatant proteins were isolated according to the method of Ferguson and Burke (1994)
PMSR activity was measured as per Ferguson and Burke (1994)
Data were subjected to ANOVA using statistical software (SAS System for Windows version 8.2; SAS Institute, Cary, NC). Means were compared by Duncan's test at P Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requester. Received May 18, 2004; returned for revision August 10, 2004; accepted August 30, 2004.
1 This work was supported in part by the Instituto Colombiano Para el Desarrollo de la Ciencia y la Tecnología "Francisco José de Caldas"–COLCIENCIAS and the Universidad Nacional de Colombia (doctoral fellowship to H.M.R).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.046656. * Corresponding author; e-mail mxt3{at}psu.edu; fax 814–863–8616.
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Zhong R, Morrison III WH, Freshour GD, Hahn MG, Ye Z (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol 132: 786–795 This article has been cited by other articles:
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ABSTRACT
RESULTS
-subunit of cytochrome b559 and the psbI gene product of PSII have four and two oxidizable residues, respectively. However, upon light treatment, only one specific Met residue in each protein is oxidized (Sharma et al., 1997a
