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The Role of Superoxide Dismutase in Combating Oxidative Stress in Higher Plants.

I. Abstract

Superoxide dismutase (SOD) isozymes are compartmentalized in higher plants and play a major role in combating oxygen radical mediated toxicity. In this review we evaluate the mode of action and effects of the SOD isoforms with respect to oxidative stress resistance, correlating age, species, and specificity of plants during development.

II. Introduction

Superoxide dismutase (EC; SOD) catalyzes the dismutation of superoxide radicals to hydrogen peroxide and oxygen. In higher plants, SOD plays a major role in combating oxygen radical mediated toxicity. The sources of superoxide radical generation may be natural--that is, by-products of metabolic activities, including the electron-transport chain--or induced by external agents--including ozone, UV B, gamma rays, light-induced photoinhibitory conditions, or chemicals like paraquat or methyl viologen. Three classes of SOD have been identified, depending on the metals present at the active site: copper/zinc SOD, manganese SOD, and iron SOD. In higher plants the FeSOD has been isolated from plastids; MnSOD, from the mitochondrial matrix; and Cu/ZnSOD, from the cytosol. Another isoform is also present in chloroplast of some plants (Bannister et al., 1987).

In this article we consider retrospective as well as recent reports, in order to evaluate the mode of action and tissue specificity of SOD isozymes under environmental stress conditions. The condition that causes damage to plants by the active oxygen species is referred to as oxidative stress.

III. Effect of Gamma Rays on SOD Isozymes in Vitro

Pramanik et al. (1996) used 10-1,600 Gy doses of gamma rays to induce damage to seeds of Plantago ovate. The seeds, when germinated aseptically, showed a dose-dependent decrease in seedling height with increasing doses of radiation. Such seedling injury has also been noted in Planeago (Frolova et al., 1991, 1993) and in barley (Sah et al., 1996) in vivo. Pramanik et al. (1996) correlated morphological damage caused by gamma rays with the changes in SOD isozyme patterns in callus tissue obtained from irradiated seeds. SOD activity PAGE gels showed an extra band (Rf value 0.59) in all of the irradiated samples of calli, which was absent in the control. This overexpression of SOD is an indication of radioprotection in vitro.

In the shoot tips propagated in vitro, the SOD showed a new band with an Rf value of 0.58 in the 10 Gy sample, which was absent from the control and also in the other irradiated samples. It is interesting to note that the same isoform of SOD (same Rf value) was expressed in all irradiated samples in calli but was present only in shoot tip with a 10 Gy dose and not expressed in the higher doses of gamma rays. This indicated that the radiation treatments disrupted the physiological balance in the callus tissues or axillary buds differentially, resulting in a disturbance in the regulatory system controlling gene expression. The complex control mechanism of enzyme activity and expression may have a regulatory effect on the concentrations of [H.sub.2][O.sub.2] produced during stress conditions in different tissues (Dc Marco & Roubelakis Angelakis, 1996). A distinct in vitro tissue-specific expression has been documented, even under the same dosage of gamma ray employed.

IV. Oxidative Stress Induced by UV B and Ozone

The effect of UV B and ozone exposure has been evaluated in higher plants by many authors (Krupa & Kickert, 1989; Runeckles & Krupa, 1994; Van Camp et al., 1996). In spite of their potential differences as stress factors, both UV B and ozone share a feature in generating active oxygen species. It has been suggested that ozone enters the mesophyll cells through the stomata and is converted to superoxide anion ([O.sub.2]), hydroxyl radical (OH), and [H.sub.2][O.sub.2] (Grimes et al., 1983; Mehlhorn et al., 1990). Plants metabolize active oxygen species (AOS) by generating the antioxidant (Foyer et al., 1994a; Kangasjarvi et al., 1994), including both enzymic and nonenzymic counterparts (Alscher & Hess, 1993; Bowler et al., 1994).

Rao et al. (1996) investigated the ability of Arabidopsis thaliana ecotype "Landsberg erecta" and its flavonoid-deficient mutant transparent testa (tt5) to metabole UV B and ozone-induced activated oxygen species by producing similar antioxidant enzymes. Earlier studies (Rao & Ormrod, 1995a, 1995b; Rao et al., 1995) showed that exposure of tt5 plants to UV B for 6 to 7 days and LER to ozone for 9 to 10 days resulted in visible injury symptoms. Hence they modified the experiments to 5 days of UV B and 8 days of ozone exposure to evaluate plant responses. Ozone exposure enhanced SOD, peroxidase, glutamate reductase, and ascorbate peroxidase. Both UV B and ozone exposure enhanced similar Cu/Zn isoforms. The overall results showed that UV B exposure preferentially induces peroxidase-related enzymes, whereas ozone exposure invokes enzymes of the superoxide dismutase ascorbate glutathione cycle. According to these authors, UV B- and ozone-induced SOD activities are due to preferential expression of Cu/Zn SOD 3,-4 and -5 isoforms.

Conklin and Last (1995) monitored the accumulation of mRNAs encoding both cytosolic and the chloroplastic antioxidant isozymes[integral of] using two different ozone-exposure protocols. In both cases, the levels of three mRINAs encoding cytosolic antioxidant isozymes (ascorbate peroxidase, copper/zinc superoxide dismutase, and glutathione S transferase) increased. According to these authors, the glutathione S transferase mRNA responds very quickly to the oxidative stress and is elevated to very high levels. In contrast, ozone exposure caused a decline in the levels of two chloroplastic antioxidant mRNAs (iron superoxide dismutase and glutathione reductase) and two photosynthetic protein mRNAs (chlorophyll a/b binding protein and ribulose 1,5 biphosphate carboxylase/oxygenase small subunit). Conklin and Last have advanced two hypotheses regarding the differential accumulation of proteins.

During adaptation to a situation that leads to increased oxidative stress, antioxidant enzyme activities would be expected to increase. However, this response is variable and dependent on plant species, stage of development, and dose of ozone (Decleire et al., 1984; Krupa & Manning, 1988; Price et al., 1990). According to Conklin and Last (1995), of the cytosolic antioxidant mRNAs elevated by ozone, the amplitude of the change in glutathione S transferase mRNA was the largest. This is supported by the findings of Sharma and Davies (1994).

According to Conklin and Last (1995), ozone causes a decline in the level of Arabidopsis thaliana nuclear-encoded mRNA for two chloroplastic antioxidant enzymes FeSOD and glutathione reductase. Similar observations have been made in Nicotiana plumbaginifolia and N. tabacum. According to Willekens et al. (1994), ozone exposure causes steady-state FeSOD mRNA levels in these two species to decrease. Exposure to UV B also causes a reduction in Nicotiana FeSOD mRNA (Willekens et al., 1994) and Pisum sativum chloroplastic Cu/Zn SOD mRNA (Strid et al., 1994).

Conklin and Last (1995) have put forward two hypotheses to explain this decline in antioxidant function in response to ozone. Their first model is supported by published works of other authors. Chloroplast-localized antioxidants detoxify the free radicals produced by photosynthetic electron transport (Foyer et al., 1994a). In N. p1umbaginifo1ia, the mRNA encoding FeSOD appeared to be regulated by the level of chloroplast-generated free radicals. An increase in photoinhibitory conditions by paraquat treatment results in an elevation of FeSOD mRNA, whereas blockage of photosynthetic electron transport caused FeSOD mRNA levels to decline (Willekens et al., 1994). Ozone is also known to depress photosynthetic activity by triggering inactivation and proteolysis of rubisco and by decreasing the level of RbcS mRNAs (Pell et al., 1994). This response is common to other agents, such as UV B and drought, that cause oxidative stress (Jordan et al., 1992; Williams et al., 1994). All these reports are consistent with the notion that the ozone-induced decline in photosynthetic activity could trigger reduction in Arabidopsis thaliana FeSOD and glutathione reductase mRNAs. This hypothesis assumes that there is an overall decline in free radicals in the chloroplasts of ozone-exposed plants. However, there is evidence that ozone actually causes enhanced oxidative stress within the chloroplasts (Floyd et al., 1989). Furthermore, reports suggest that transgenic tobacco overexpressing chloroplastic SOD is more resistant to ozone (Van Camp et al., 1996).

The alternative hypothesis advocated by Conklin and Last (1995) was that ozone triggers a senescence-related mechanism that globally decreases accumulation of transcripts encoding photosynthetic protein and chloroplastic antioxidant enzymes. According to these authors, ozone activates a senescence pathway that overrides the plant to upregulate both FeSOD and GR mRNAs in response to increased oxidative stress and actually causes the observed decline in these mRNAs. This model is supported by Pell et al. (1994) in the fact that ozone causes accelerated aging in mature leaves and predisposes young leaves to senescence. Exposure of barley to conditions of moderate photo-oxidative stress causes a reduction in chloroplastic FeSOD mRNA in mature senescent leaves that are still competent for photosynthesis, whereas this mRNA increases in younger leaves after photoinhibition. In contrast, the mRNAs for both a cytosolic and a mitochondrial SOD are elevated in senescent leaves under the same stress conditions. Hence, a senescence-related signal could trigger a decline in chloroplastic antioxidant function in ozone-exposed plants despite an elevation in oxidative stress.

V. Induction of SOD by White Light

Tsang et al. (1991) reported changes in SOD mRNA levels that occur under a variety of stress treatments, including light. According to these authors, the diverse responses of the SOD mRNAs indicated that active oxidative stress is an influencing component of environmental stress. Because the SOD isoforms are compartmentalized in different organelles, the SOD mRNA levels indicated how each stress affects the different subcellular compartments.

The effects of white light on SOD transcript abundance in both green leaves and etiolated seedlings revealed that FeSOD chi is the most strongly affected by white light. During illumination, oxygen radicals are generated mainly by leakage of electrons from PSI and from ferredoxin (Asada & Takahashi, 1987). According to Tsang et al. (1991), it is not light per se but the oxidative stress arising from photosynthetic electron transport that modulates FeSOD chl gene expression.

VI. Induction of SOD by Temperature Stress

Differential regulation of SOD mRNAs were found by Tsang et al. (1991) during temperature stress. From the experiments involving a temperature stress designed by these authors, Cu/Zn SOD cyt appeared to be the most responsive of the SOD mRNAs. It is the only one to be strongly induced by heat shock and during the recovery period after chilling stress, In both cases, the response is essentially independent of light. This indicates that the cytosol may be the chief site of oxyradical formation under these conditions. In Salmonella typhimurium many of the proteins induced by oxidative stress are also induced by heat shock (Morgan et al., 1986), leading to the proposal that heat shock may itself be a form of oxidative stress. This has been further supported by the finding that SOD was induced by heat shock in Escherichia coli (Privalle & Fridovich, 1987). Hydrogen peroxide has been found to the heat-shock response in Drosophila (Becker et al., 1990) and to induce thermotolerance in Neurospora crassa (Kapoor et a l., 1990). According to Tsang et al (1991), it is possible that in addition to eliminating excess superoxide Cu/Zn SOD cyt raises cytoplasmic levels of [H.sub.2][O.sub.2] during heat shock, which can then activate the defense mechanism of the cell.

Three-day-old chill-sensitive maize inbred seedlings were exposed to 4[degrees]C for 7 days and did not survive chilling stress unless they were preexposed to 14[degrees]C for 3 days. cDNAs representing three chilling acclimation responsive (CAR) genes were isolated by subtraction hybridization and differential screening and found to be differentially expressed during acclimation. Hydrogen peroxide levels were elevated during both acclimation and chilling of nonacclimated seedlings. However, SOD activity was not affected but the levels of cat 3 transcripts, and the activities of catalase 3 and guiacolperoxidase were elevated in mesocotyls during acclimation (Prasad et al., 1994).

Two highly similar Cu/Zn SOD (Sod 4 and Sod 4a) have been isolated from maize (Kernodle & Scandalios, 1996). Sod 4A contains 8 exons and 7 introns. The Sod 4 partial sequence contains 5 introns. The introns in the two genes are located in the same position and have highly homologous sequences in several regions. The largest (1,200 bp) interrupts the 5' leader sequence. The presence of different regulatory motifs in the promoter region of each gene may indicate distinct responses to various conditions. Zymogram and RNA blot analyses show that Sod 4 and Sod 4A are expressed in all the tissues of the maize plant. The developmental profiles of Sod 4 and Sod 4A mRNA accumulation differ in scutella during sporophytic development. RNA blot analysis of the respective Sod mRNAs indicates a differential, tissue-specific response of each gene to certain stressors. RNA isolated from stem tissue of ethephon-treated seedlings shows an increase in the Sod 4 but not the Sod 4A transcript; there is no change in transcripts o f either gene in seedlings. Other agents that can cause oxidative stress were also tested for differential expression of the genes.

VII. Induction of SOD by Paraquat

Paraquat, a bipyridyl herbicide, is a redox active compound that becomes reduced within the cell and subsequently transfers its electrons to oxygen, forming the superoxide anion (Asada & Takahashi, 1987; Halliwell & Gutteridge, 1989). On exposure to white light the electrons are donated from photosystem I, ensuring that superoxide is formed primarily in the chloroplasts. Paraquat can also mediate toxic effects in the dark. The major electron donor may be a microsomal NADPH cytochrome P450 reductase, as in animal cells (Halliwell & Gutteridge, 1989). It was found that FeSOD chl transcript abundance is increased greatly by paraquat in the light (approximately fortyfold), as are MnSOD mit and Cu/ZnSOD cyt mRNA (by thirtyfold and fifteenfold, respectively). According to Tsang et al. (1991), paraquat caused a twelvefold increase in Cu/Zn Sod cyt, whereas MnSOD mit and FeSOD chl transcripts were unaffected. Although the combined action of paraquat and light imposes an oxidative stress mainly upon the chloroplasts, it was found that both MnSOD mit and Cu/Zn SOD cyt mRNA abundance increased, in addition to FeSOD chl. It is likely, therefore, that, although superoxide is generated within a specific compartment, the ensuing damage can affect other compartments in the cell. The formation of oxidative stress within the different compartments can by itself mediate changes in steady-state SOD mRNA levels.

VIII. Oxidative Stress Induced by Methyl Viologen

Methyl viologen (MV) is a herbicide that passes electrons from various electron-transport chains to oxygen, generating superoxide (Van Camp et al., 1996). During illumination, MV generates superoxide in the chloroplasts (Halliwell, 1984; Slooten et al., 1995) and thus stimulates the oxidative stress component of the environmental stress.

Transgenic tobacco plants that express a chimeric gene that encodes chloroplastic Cu/Zn SOD from pea was developed by Sengupta et al. (1993). Transgenic SOD plants exhibited increased resistance to oxidative damage caused by exposure to low concentrations of MV, but at higher concentrations this protective effect disappeared. Tepperman and Dunsmuir (1990) were unable to detect any significant differences in resistance to MV between tobacco plants that expressed high levels of petunia chloroplast Cu/Zn SOD and control plants. It has been reported that moderate, but not large, increases of Cu/ZnSOD provide MV resistance in human and mouse cells.

Expression of higher plant mitochondrial MnSOD in the chloroplasts of transgenic Nicotiana tabacum cv SRl and cv PB6 reduces cellular damage caused by treatment with MV (Bowler et al., 1991; Slooten et al., 1995). In PB 6, overproduction of MnSOD had a protective effect on MV-induced ion leakage and also inactivation of the PSII reaction center (Slooten et al., 1995). The antioxidant defense, as determined by the overproduction of SOD, was stronger at the plasmalemma than at PSII. It is noteworthy that the overproduced MnSOD is located in the chloroplast. It has been suggested (Van Camp et al., 1996) that the pathway from MV-mediated superoxide generation at PSI to damage at PSII is poorly accessible to plant mitochondrial MnSOD expressed in the chloroplasts. According to these authors, this lack of protection of PSII may be specific for overproduced plant mitochondrial MnSOD, because chloroplastic overproduction of Cu/Zn SOD in potato and of E. coli MnSOD in tobacco (Foyer et al., 1994a, 1994b) does allevia te the inhibition of photosynthesis by MV.

A chimeric gene consisting of the coding sequence for chloroplast FeSOD from Arabidopsis thaliana, coupled with the chloroplast targeting sequence from the pea RU1,5,DP carboxylase/oxygenase small subunit, was expressed in N. tabaccum cv "Petit Havana SRl." Expression of the transgenic FeSOD protected both the plasmalemma and photosystem II against superoxide generated during illumination of leaf discs containing MV. This indicates that FeSOD provides better protection of chloroplasts than MnSOD. According to these authors, this is due to the fact that FeSOD is indigenous to chloroplast. Hopkin et al. (1992) pointed out the functional differences between the FeSOD and MnSOD enzymes of Escherichia coli, with regard to protection of DNA and proteins. In plant chloroplasts FeSOD and MnSOD have different protective properties that may be related to their subcellular location. Overproduction of FeSOD interferes with signal pathways, leading to induction of cytosolic Cu/ZnSOD during salt stress. Overproduction of FeSOD leads to induction of chloroplastic ascorbic peroxidase during salt stress (Van Camp et al., 1996). It is interesting to note that transgenic plants with different levels of FeSOD overproduction did not differ significantly with respect to enhancement of MV tolerance. The lowest levels of SOD overproduction, around 11 units/mg chlorophyll, was already sufficient to relieve the rate limitation of superoxide scavenging by endogenous chloroplastic SOD.

IX. Responses of Antioxidative Systems to Drought Stress

The effects of an enhanced [CO.sub.2] concentration, either alone or in combination with drought stress, on antioxidative systems of Quercus rober and Pinus pinaster was studied by Schwanz et al. (1996). The seedlings were grown for a season in a greenhouse in tunnels supplied with 350 or 700 microliter [CO.sub.2]. Antioxidants, protective enzymes, soluble protein, and pigments showed considerable fluctuations in different years. Elevated concentration of [CO.sub.2] caused significant reductions in the activities of superoxide dismutases in both oak and pine. When the trees were subjected to drought stress by withholding water, the activities of antioxidative enzymes decreased in leaves of pine and oak grown at ambient [CO.sub.2] and increased in plants grown at elevated [CO.sub.2] levels. Growth in elevated carbon dioxide may reduce oxidative stress to which leaf tissues are generally exposed and enhance metabolic flexibility to encounter increased stress by increasing antioxidative capacity.

X. Age--Specific Changes in SOD Isozymes during Development

The role of SOD in combating the toxic effects of oxygen free radicals has been studied by various authors in different species of plants. It has been shown that SOD is developmentally regulated (White et al., 1990; Perl Treves & Galun, 1991; Herouart et al., 1993, 1994; Zhu & Scandalios, 1993; Pramanik et al., 1995, 1996). Pen Treves and Galun (1991) have reported that SOD genes of tomato are developmentally regulated and respond to light and stress. Shoot tips, flower buds, seedlings, and young leaves of tomato contained high levels of mRNA transcripts of SOD. Developmental control of Cu/Zn SOD has also been recorded by Herouart et al. (1993) in transgenic tobacco. According to White et al. (1990), Cu/Zn SOD mRNA levels remain constant, but SOD3 (MnSOD) mRNA levels increased throughout postgermination scutellar development. In maize, total SOD activity increased in kernel extracts after 10 days postpollination. SOD 3 and Cu/Zn SOD activity increased during kernel development. Pramanik et al. (1996) describ ed a new molecular form of SOD that appears in vitro in multiplying shoot tips. According to these authors, this particular form of SOD is developmentally regulated and may arise due to de novo synthesis, or it may represent posttranscriptional modification of genes. According to Zhu and Scandalios (1993), accumulation of the MnSOD transcripts is tissue specific and could be correlated with developmental stages. De Marco and Roubelakis Angelakis (1996) hold the view that oxidative stress is compartment specific and that the localization of hydrogen peroxide, rather than its absolute concentration, may be responsible for oxidative stress and that controlled amounts of hydrogen peroxide are necessary to allow proper cell-wall reconstitution and subsequent cell division.

To investigate the molecular mechanism of SOD induction, the promoter of the N. plumbaginifolia cytosolic Cu/Zn SOD was fused to the GUS reporter gene gusA (Herouart et al., 1993). Studies of Cu/Zn SOD cyt expression in protoplasts revealed that sulfhydryl antioxidants induce the expression of the fused gene. On the contrary, no induction of the chimeric gene was found in protoplast treated with hydrogen peroxide or paraquat (Herouart et al., 1993). In a later paper (Herouart et al., 1994) the same authors demonstrated that Cu/Zn cyt expression is strictly developmentally regulated and highly induced in response to various environmental stress conditions.

All the different forms of environmental stresses discussed above demonstrated changes in different isoforms of SOD levels, both in vivo and in vitro. This change is compartment specific and also tissue specific. Studies with expression of SOD mRNAs gave a clear picture of SOD induction under oxidative stress. Transgenic plants overexpressing SOD would provide an important material to study cooperative effects between overproduced antioxidant enzymes in scavenging toxic oxygen species.

Responses to paraquat exposure from three different leaf age classes of pea were studied by Donahue et al. (1997). Resistance was correlated with leaf age, photosynthetic rates, enzyme activities, and pretreatment levels of plastid glutathione reductase and plastid Cu/Zn SOD transcripts. No increase of mRNA for the plastid glutathione reductase or Cu/Zn SOD was found. According to these authors, developmentally controlled mechanisms determining basal antioxidant enzyme activities, and not inductive responses, are the critical factors for short-term oxidative stress resistance.

XI. Conclusion

The role of SOD in combating oxidative stress has been well documented by various authors. During adaptation to increased oxidative stress, SOD levels may increase, depending on the species of plant, stage of development, and degree of the stress condition (Decleire et al., 1984; Krupa & Manning, 1988; Pramanik, 1996; Pramanik et al., 1996). Because of the compartmentation of different isozymes, SOD is more effective in stress tolerance.

XII. Acknowledgments

The senior author is grateful to the University of Calcutta for the grant of study leave to work as a visiting scientist at Yale University during 1996-1997.

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Publication:The Botanical Review
Geographic Code:1USA
Date:Jan 1, 2000
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