Journal of Experimental Botany, Vol. 52, No. 359, pp. 1179-1190,
June 1, 2001
© 2001 Oxford University Press
Original Papers |
Anoxic stress leads to hydrogen peroxide formation in plant cells
Department of Biosciences, Division of Plant Physiology, Viikki Biocenter, PO Box 56, FIN-00014 Helsinki University, Finland
Received 19 October 2000; Accepted 5 February 2001
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Abstract |
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Hydrogen peroxide (H2O2) was detected cytochemically in plant tissues during anoxia and re-oxygenation by transmission electron microscopy using its reaction with cerium chloride to produce electron dense precipitates of cerium perhydroxides. Anoxia-tolerant yellow flag iris (Iris pseudacorus) and rice (Oryza sativa), and anoxia-intolerant wheat (Triticum aestivum) and garden iris (Iris germanica) were used in the experiments. In all plants tested, anoxia and re-oxygenation increased H2O2 in plasma membranes and the apoplast. In the anoxia-tolerant species the response was delayed in time, and in highly tolerant I. pseudacorus plasma membrane associated H2O2 was detected only after 45 d of oxygen deprivation. Quantification of cerium precipitates showed a statistically significant increase in the amount of H2O2 caused by anoxia in wheat root meristematic tissue, but not in the anoxia-tolerant I. pseudacorus rhizome parenchyma. Formation of H2O2 under anoxia is considered mainly an enzymatic process (confirmed by an enzyme inhibition analysis) and is due to the trace amount of dissolved oxygen (below 10-5 M) present in the experimental system. The data suggest oxidative stress is an integral part of oxygen deprivation stress, and emphasize the importance of the apoplast and plasma membrane in the development of the anoxic stress response.
Key words: Anoxia, apoplast, hydrogen peroxide, hypoxia, oxidative stress, reactive oxygen species.
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Introduction |
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The recent hypothesis that a decrease in oxygen concentration and the formation of reactive oxygen species (ROS) may be recognized through the same sensing mechanism in the cell (Semenza, 1999
) makes adaptation to anoxic stress an important model for the investigation of this mechanism. The experiments reported here are based on recent data on the generation of (ROS) under various stress conditions (Noctor and Foyer, 1998), their effects on metabolically active macromolecules and on cell structures, and their involvement in the regulation of adaptive response. These effects are all important for understanding stress physiology and the underlying signalling mechanisms.
Direct and indirect evidence has accumulated on the involvement of ROS in the anoxic stress response. A term ‘re-oxygenation injury’ has been introduced to acknowledge the detrimental effect of ROS on anoxically pretreated tissue (Crawford et al., 1994). Most of the studies in this field characterize the consequences of oxidative stress, i.e. membrane damage, lipid peroxidation (LP) and antioxidant status with respect to anoxia-tolerant and intolerant species. In previous studies evidence has been obtained of ROS engagement in the etiology of anoxic stress: enhanced formation of LP products—conjugated dienes, trienes and thiobarbituric acid reactive substances (TBARS), changes in superoxide dismutase (SOD) activity and a decrease in antioxidant content (Chirkova et al., 1998; Blokhina et al., 1999, 2000).
It has been shown earlier that anoxia leads to changes in lipid content and composition, membrane fluidity (Hetherington et al., 1982; Chirkova et al., 1989), decrease in the adenylate energy charge (Chirkova et al., 1984; Hanhijärvi and Fagerstedt, 1994), cytoplasmic acidosis (Roberts et al., 1984), and changes in the patterns of protein synthesis (Chang et al., 2000). Most of these changes favour ROS production and the successive peroxidation of lipids (Crawford et al., 1994; Crawford and Braendle, 1996; Chirkova et al., 1998).
Formation of ROS occurs through several univalent reduction steps, yielding first the superoxide anion, then hydrogen peroxide and the hydroxyl radical, and finally water (Elstner, 1991). Of the above-mentioned chemical species only hydrogen peroxide is relatively stable and able to penetrate the plasma membrane as an uncharged molecule. Thus, it could act as a second messenger under stress conditions (Foyer et al., 1997). To achieve signal specificity three important components of the signalling pathway via ROS have to be considered: The source of the signal, target susceptibility and the antioxidant status of the cell (Alscher et al., 1997; Lander, 1997). Other than antioxidant-associated mechanisms can be involved in the fine adjustment of ROS action such as local elevations in Ca2+-concentration (Subbaiah et al., 1998) and changes in the redox status and pH of the cell.
The role and place of ROS in the sequence of events leading to metabolic changes under oxygen deprivation stress is not yet clear. The aim of this study is to show direct ROS (e.g. hydrogen peroxide) generation under anoxia and re-oxygenation, and to localize the sites of H2O2 formation and reveal its possible enzymatic sources. Since the effect of ROS on the cell is non-specific, an attempt has been made to investigate any possible association between ROS accumulation, LP and redox state of the cell, and anoxia-induced metabolic changes.
In this investigation the anoxia-intolerant wheat and the more tolerant rice represent agriculturally important species. Their behaviour is compared with the naturally evolved anoxia-intolerant and tolerant species, Iris germanica and Iris pseudacorus, respectively. Study of native species capable of tolerance of anoxia for long periods, and the comparison of these with the intolerant agricultural plant cultivars, is important since it reveals the tolerance mechanisms which have appeared during evolution.
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Materials and methods |
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Plant material and growth conditions
Seeds of wheat (Triticum aestivum L. cv. Leningradka) and rice (Oryza sativa L. cv.VNIIR) were planted in plastic trays and grown at 23/20 °C (day/night) with a 16 h photoperiod and illumination at 40 µmol s-1 m-2 for 7 d (wheat) or 10 d (rice). Iris pseudacorus L. rhizomes were collected by the Nupuri lake in southern Finland in a wet riverside meadow at the end of May and June in 1998. Iris germanica L. rhizomes were kindly supplied by the Botanical Garden of Helsinki University. Only current year rhizomes were used in the experiments. Before treatment the rhizomes were washed and roots and leaves removed. Experimental plants represent pairs of anoxia-intolerant–anoxia-tolerant plants: wheat–rice and I. germanica–I. pseudacorus, respectively. Plant organs which are susceptible to O2 deprivation under natural conditions (the roots of cereals and the rhizomes of Iris spp.) were used in the experiments.
Anoxic stress treatment
Plants (rhizomes or whole seedlings) were placed in glass jars (1.5 l) on moist filter paper. Anoxic conditions were created with gas generating kits (Oxoid BR 10, Unipath Ltd., Basingstoke, UK) and anaerobic palladium catalysts (Oxoid BR 42). Hydrogen released by the kit immediately reacts with oxygen on the palladium catalyst to form water, and, therefore removes oxygen from the system. In addition, the kit causes carbon dioxide concentration inside the jars to rise to c. 7–10%. High CO2 under anoxia is a natural condition in soil resulting from root and microbial anaerobic respiration. Absence of oxygen was checked with anaerobic indicators (Oxoid BR 55, sensitive down to 12 µM oxygen). Aerobic samples were placed into moistened quartz sand (rhizomes) or wrapped in several layers of moist filter paper (seedlings). Both anoxic and control samples were kept at room temperature in the dark. The duration of anoxia was chosen individually for each species based on their tolerance of anoxia to achieve physiologically equal treatment: wheat 1 and 3 d, rice 7 d, I. germanica 8 d, and I. pseudacorus 15 and 45 d. Investigations were undertaken earlier to establish the limit of anoxia tolerance and ultrastructural, physiological and biochemical changes in the experimental material in the time-course of anoxia (i.e. monitoring of cell plasmolysis as an integral parameter of cell damage under stress, measurement of electrolyte leakage and cytoplasmic pH changes) (Chirkova et al., 1991; Hanhijärvi and Fagerstedt, 1994).
Cytochemical localization of hydrogen peroxide
The assay is based on the reaction of H2O2 with CeCl3, which produces electron-dense insoluble precipitates of cerium perhydroxides Ce(OH)2OOH and Ce(OH)3OOH (Bestwick et al., 1997). To visualize H2O2 accumulation under oxygen deprivation, vessels containing anoxic samples were transferred to a gas tight chamber and samples were treated with CeCl3 under a continuous flow of nitrogen (hypoxia). To evaluate the impact of re-oxygenation on the intensity of H2O2 formation, similar specimens were kept in air at room temperature for 2 h in the dark after the anoxic period (anoxia+2 h re-oxygenation). Plant tissues (whole seedlings of the cereals or fresh cuts of Iris rhizome core c. 2x2 mm) were treated with 5 mM CeCl3 in 50 mM HEPES pH 7.3 for 1 h at room temperature. To test the effect of added H2O2 on cerium precipitate formation, some tissue samples were treated with 5 mM H2O2, rinsed several times and stained as were the other samples. After three washing steps (50 mM HEPES, 5–10 ml), tissue specimens were fixed in 2.5% glutaraldehyde in the same buffer for 1 h. After fixation c. 2 mm long root tips were removed. Both the root tips and the rhizome core samples were post-fixed in 1% osmium tetroxide (EMS, Washington, PA, USA). After dehydration in an ethanol series (50%, 70%, 96%, and 100%) tissue specimens were embedded in Epon LX 112 (Ladd Research Industries Inc., Williston, VT, USA) and polymerized. Root tips were sectioned starting from the tip. The first sections (60 nm) containing the root cap were discarded and only the meristematic cells were processed further. Both the rhizome and root specimen sections were stained with uranyl acetate for 0.5 h (Ultrastain-1, Leica, Austria) and lead citrate for 1.2 min (Ultrastain-2, Leica, Austria) in Leica EM Staining automat. Another similar set of sections was left unstained for better visualization of the cerium perhydroxide deposits. The samples were viewed at an accelerating voltage 60 kV with a transmission electron microscope (Jeol JEM-1200EX, Jeol Ltd, Tokyo, Japan). The I. pseudacorus rhizome contains concentric amphivasal vascular bundles spread in parenchymal tissue. In the electron micrographs only parenchymal cells were examined to eliminate H2O2 associated with lignification of xylem elements.
Inhibition analysis
To verify H2O2 formation under anoxia and to confirm the reliability of the cerium perhydroxide precipitate method, one of the experiments (wheat 3 d under anoxia+2 h aeration) was combined with the following 1 h treatments: 8 µM diphenyleneiodonium (DPI, an NADPH oxidase inhibitor), 3 mM KCN (superoxide dismutase and peroxidase inhibitor) and 1 mM NaN3 (peroxidase inhibitor) and 25 µg ml-1 (1200 U ml-1) of catalase (H2O2 removal). Each inhibitor treatment was given separately in 25 ml volume. After this treatment, the plant samples were washed and incubated with CeCl3 as described above.
Quantification of cerium perhydroxide precipitates in electron micrographs by Image Pro® Plus
To compare the results on the amount of H2O2 (as judged by the cerium precipitates) in an anoxia-intolerant and an anoxia-tolerant plant species, wheat and Iris pseudacorus samples were processed further to quantify the amount of cerium precipitates in the electron micrographs. Original unprocessed scans from electron micrographs taken with the same magnification (x6000) were used for the quantification of H2O2. Micrographs were taken randomly of the sections; however, in Iris rhizome sections areas containing only parenchymal tissues were photographed and areas with vascular tissues were not used. The Image Pro® Plus programme differentiated cerium perhydroxide precipitates from the background by the difference in contrast. Threshold intensity values and area limits were chosen manually for each calculation, depending on the density of cerium perhydroxide accumulation and plant species. Calculation of precipitates was based on area and percentage of total area parameters, measured in pixels and as a percentage of the whole image area, respectively. To eliminate artefacts originating from uneven light distribution in the original micrographs, a ‘flatten background’ operation was performed. Statistical analyses were carried out to establish differences between aerated and anoxic material.
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Results |
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Amount of hydrogen peroxide during anoxic stress and re-oxygenation
Comparison of samples treated (Figs 1b, e, f, 2b) or not treated (Fig. 2c
) with cerium chloride (and not stained by uranyl acetate) indicated the formation of cerium precipitates. This result combined with the inhibition analysis (Fig. 5) confirmed the presence of cerium perhydroxides and hence H2O2. The cerium precipitates appeared in some samples as needle-like crystals (Figs 1f, 2f, 3e) possibly indicating a larger amount of H2O2. Treatment of the tissue samples with 5 mM H2O2 prior to cerium chloride staining resulted in intensive formation of precipitates at the plasma membrane (Fig. 1c).
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In the aerated control plants H2O2 accumulation was observed as electron dense cerium precipitates mainly in the cell wall of the root tip meristematic cells and rhizome core parenchyma (Figs 1a, b, 2a, b, 3a, b, 4a). In some cases better visualization of cerium precipitates was achieved when the standard staining of thin sections with uranyl acetate and lead citrate was excluded from the procedure for electron microscopy (Figs 1b, c, e, f; 2a versus b, 3d, e, 4a–c, 5a–e). Cerium perhydroxides appear in the photographs as electron dense spots in association with the plasma membrane (Figs 1b–e, 2a, b, 3e, 4b, c) or as crystal-like matter when detected in the cell wall (Figs 1f, 2f) and intercellular spaces of I. pseudacorus (Fig. 3d
, e). Some cerium perhydroxide deposits were detected in the cytoplasm of the anoxic samples (Figs 1f
, 2f), which confirmed the penetration of CeCl3 into the cells.
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Inhibition analysis confirmed enzymatic origins of a large part of the H2O2 detected. The most efficient in H2O2 elimination were treatments with catalase (Fig. 5b
) and diphenyleneiodonium (NADPH oxidase inhibitor, Fig. 5c) in comparison with anoxic tissue not treated with inhibitors (Fig. 5a). Peroxidase inhibitors KCN and NaN3were less efficient (Fig. 5d, e, respectively), although they can act not only as enzyme inhibitors but also as direct reductants of H2O2 (Ros Barcelo, 1998). KCN also inhibits CuZn-SOD and Fe-SOD, which could have contributed to H2O2 production in the control sample.
In the cereals, imposition of anoxia increased H2O2 associated with the plasma membrane (Figs 1d, e, 2f). Both the enhancement of stress and the restoration of normoxic conditions caused plasmolysis and membrane degradation and an increase in the amount of H2O2 (Figs 1f, 2d–f). Figures 1e and f and 2e and f represent the result of re-oxygenation injury. Both wheat and rice roots showed deteriorated membrane structures and increased amount of H2O2 not only on the plasma membrane but inside the protoplast as well (Figs 1f, 2f). The difference in anoxia tolerance between the rhizomatous Iris species, estimated as the amount of H2O2, was more pronounced than that of the cereals (Figs 3, 4 ). In the cells of the anoxia-intolerant I. germanica intensive presence of H2O2 was detected on the plasma membrane and a less intensive presence in the cell wall after 8 d of oxygen deprivation (Fig. 4b, c). Anoxia-tolerant I. pseudacorus showed no increase in the H2O2 presence on the plasma membrane after 15 d of anoxia (Fig. 3b versus c). Re-oxygenation after 15 d of treatment did not cause any changes either in the cell ultrastructure or in H2O2 amount (Fig. 3c). In the rhizomes of I. pseudacorus the intercellular space was a notable site of H2O2 presence both under aeration and anoxia (Fig. 3d, e). Anoxia for 45 d led to increased cerium precipitation in the cell wall (Fig. 3e).
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Results on the quantification of cerium precipitates by Image Pro® Plus are presented in Table 1
. The high values of deviation in the areas of the precipitates are due to the large magnification needed: in some pictures cell walls, containing most of the precipitates, covered more of the image area resulting in a larger area of the precipitates. Application of the Student's t-test revealed a statistically significant difference at the 1% level between aerated and anoxic wheat samples, while in the anoxia-tolerant I. pseudacorus the difference was not significant.
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Ultrastructural changes caused by anoxic stress
Anoxic treatment brought about both H2O2 accumulation and changes in cell ultrastructure. The ability to maintain cell intactness correlated positively with anoxia tolerance. I. pseudacorus rhizome tissue showed undisturbed structures after 15 d (Fig. 3c) and even after 45 d of anoxia (Fig. 3e, f) with thin layers of cytoplasm along the cell walls and amorphous fructan stores in the vacuoles (Fig. 3b, e, f). In the roots of the anoxia-intolerant wheat, plasmolysis could be observed after 1 d of oxygen deprivation (Fig. 1e). In rice, continued stress led to swelling of mitochondria (Fig. 2d, e) and to plasmolysis (Fig. 2d, e, f) and finally to the disintegration of the plasma membrane after 7 d of anoxia (Fig. 2f). Due to the large number of treatments, not all micrographs from every experiment can be shown.
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Discussion |
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Anatomical and ultrastructural features
Incubation of the anoxia-intolerant plant tissues under oxygen deprivation caused plasmolysis and disintegration of organelles. Such changes have been described in detail earlier (Vartapetian and Zakhmilova, 1990
). The anatomy and ultrastructure of Iris pseudacorus rhizome parenchyma containing much of storage fructan have been described earlier (Hanhijärvi and Fagerstedt, 1994). In this study, I. pseudacorus rhizome parenchymal cells showed no signs of damage at the ultrastructural level even after 45 d of anoxic incubation. According to this investigation and earlier biochemical studies (Chirkova, 1988; Hanhijärvi and Fagerstedt, 1994; Chirkova et al., 1998; Blokhina et al., 1999), the plant species used in the present paper can be placed in the following order of increasing anoxia tolerance: wheat, rice, I. germanica, I. pseudacorus.
Source of H2O2
The increased appearance of cerium perhydroxide deposits in the samples under anoxia can be due to the inhibition of H2O2 utilization by antioxidant enzymes, or to an enhancement of H2O2 production via an enzymatic or a chemical mechanism. Under severe stress conditions both processes can be present. The sensitivity of the oxygen indicators used in the anoxic jars, and hence the concentration of O2 in the experiments, was below 12 µM. However, this concentration is still enough for the functioning of plant terminal oxidases (Km 10-6 M for oxygen; Skulachev, 1997) and for the formation of ROS. Non-enzymatic one-electron O2 reductions can occur at about 10-4 M and higher oxygen concentrations (Skulachev, 1997). H2O2 accumulation under anoxia employs the very low amount of dissolved oxygen present in the experimental system presented here, and therefore, was mostly of enzymatic origin. The inhibition analysis of H2O2 production (Fig. 5) supports this fact.
Earlier investigations on H2O2 accumulation in barley and wheat have shown an increase in H2O2 in the roots suffering from hypoxia (Kalashnikov et al., 1994; Biemelt et al., 2000). In the present experiments the comparison between aerated and anoxic samples revealed the same tendency: accumulation of H2O2 in anoxic samples of the intolerant wheat (Table 1).
H2O2 is a constitutive metabolite in the cell wall. Some apoplastic enzymes may contribute to H2O2 production under normal and under stress conditions, for example, an extracellular germin-like oxalate oxidase and an amine oxidase capable of H2O2 production have been localized in the apoplast (Reggiani and Bertani, 1989; Hurkman and Tanaka, 1996). The presence of a stress-induced plasma membrane NADPH oxidase, capable of H2O2 formation, has also been indicated in plants (Dwyer et al., 1996). According to this study's data, sites of hydrogen peroxide production in tissues suffering from oxygen deprivation are mainly associated with the plasma membrane (Figs 1d, e, 2f), and are possibly an indication of NADPH oxidase activity. This was confirmed by inhibition of H2O2 formation by diphenyleneiodonium (DPI) (Fig. 5c), an inhibitor of NADPH oxidase.
Disturbance of H2O2 decomposition by apoplastic peroxidases can lead to H2O2 appearing in the cell wall. However, some isozymes of cell wall peroxidases with an optimum in the neutral or alkaline pH-region can be responsible for H2O2 production under hypoxia through the reduction of Compound III of peroxidase (Dunford, 1993).
In these experiments, a decrease in cerium perhydroxide precipitates in the apoplast was observed upon treatment with peroxidase (NaN3 and KCN) and superoxide dismutase (KCN) inhibitors suggesting the involvement of these enzymes in H2O2 production and decomposition under anoxia. According to the results of this study, the rise in H2O2 amount under anoxia is mainly due to the combined action of NADPH oxidase and peroxidases.
Antioxidant status of the cells
Reduced activity of the enzymes of the ascorbate-glutathione cycle can be responsible for H2O2 accumulation. Earlier results on the depletion of the reduced forms of ascorbate and glutathione suggest an imbalance in the glutathione-ascorbate cycle under anoxia (Blokhina et al., 2000), a condition which affects the redox state of the cell and redox-dependent reactions. Enzymatic turnover of ascorbate and glutathione is problematic for plants under anoxic stress, and a decrease in enzyme activities has been observed under hypoxia and anoxia by several authors (Yan et al., 1996; Chirkova et al., 1998; Biemelt et al., 1998; Boo and Jung, 1999). O2 availability is a necessary condition for ROS formation and for the induction of protective reactions i.e. ROS-scavenging and antioxidant-regenerating enzymes. Such induction is probably achieved through redox changes. From that point of view, a decrease in ascorbic acid/dehydroascorbic acid and GSH/GSSG ratios in our experiments (Blokhina et al., 2000) represents one of the possible redox signals in anoxically damaged tissue undergoing oxidative stress.
Is H2O2 a stress signal under anoxia?
H2O2 is considered to act as a signalling molecule in plants in the pathogen defence reaction and wounding stress (Mehdy, 1994; Bowler and Fluhr, 2000). Recently, the participation and place of H2O2 in a particular signalling cascade has been demonstrated: H2O2 can act as a potent activator of a mitogen-activated protein kinase cascade in Arabidopsis, initiating a protein phosphorylation cascade, which induces stress-responsive genes (Kovtun et al., 2000). Also, it is known that oxidation of an exposed SH-group of the OxyR transcription factor of Escherichia coli activates transcription of genes involved in the detoxification of ROS (Lander, 1997). Recently, ozone-induced H2O2 production has been shown on the plasma membrane and cell wall of silver birch (Betula pendula) leaves. In that investigation an inhibition analysis suggested participation of both NADPH-dependent superoxide synthase and the cell wall peroxidases in H2O2 formation (Pellinen et al., 1999).
Under anoxia, H2O2 is localized mainly in the apoplast and may be responsible for the generation of the stress response together with the peroxidation products of the plasma membrane lipids. The importance of the apoplast as the site of environmental sensing has been shown earlier for light, submergence, hypergravity and water deficiency stresses (Hoson, 1998). Indeed, in these experiments cerium perhydroxides were detected not only in the anoxic material, but also in the apoplast of the aerated control samples (Fig. 1a, b, 2a, b, 3 d). The amount of precipitates detected under aeration was lower than that found in the anoxic samples. These results favour the suggestion that the apoplast is involved in the perception of different signals and acts in co-operation with the plasma membrane (Hoson, 1998). Signal specificity could be achieved with a particular balance of other anoxia-induced metabolic changes such as shifts in the reduction state of the key redox-active metabolites (i.e. ascorbate, glutathione, NAD(P)H, ions of transition metals), cytoplasmic acidification, elevation in cytosolic free Ca2+ concentration, disruption of the energy metabolism and generation of ROS (Fig. 6). The importance of a combination of factors has been shown for H2O2-induced apoptosis, where a certain intracellular superoxide anion concentration and an increase in the chemical reduction state and acidification of the intracellular environment are needed for the signal to proceed (Clement et al., 1998).
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Under natural conditions anoxic stress necessarily includes several transition states (hypoxia, anoxia and subsequent oxidative stress) characterized by different O2 concentrations and particular physiological states of the tissue. Excessive generation of ROS, the first sign of oxidative stress, is essential for the induction of a stress response. Changes in the steady-state equilibrium between ROS formation and utilization in the cell (Fig. 6
) can induce both adaptive responses (ROS signalling, Lander, 1997) and detrimental changes in the cell structure and metabolism (LP). The sequence of events in ROS sensing is not known but several existing models (Semenza, 1999) employ redox changes and suggest that hypoxia (low oxygen concentration) and ROS could be sensed through the same mechanism. In plants undergoing anoxic stress factors, which can affect ROS formation and cell redox potential, have been described (Fig. 6). The exact place of H2O2 in anoxic signalling has yet to be identified, however, the localization of H2O2 in the apoplast and plasma membrane in the present study emphasizes the physiological importance of the apoplast in sensing/response to anoxic stress.
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Acknowledgments |
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We wish to acknowledge the technical support of the Electron Microscopy Unit of the Institute of Biotechnology, University of Helsinki. This work was supported by the Academy of Finland project 164346 on Plant Molecular Biology and Forest Biotechnology (Finnish Centre of Excellence Programme 2000–2005).
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Notes |
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1 Present address: Department of Plant Physiology and Biochemistry, Universitetskaya nab. 7/9, University of St Petersburg, 199034 Russia.
2 To whom correspondence should be addressed. Fax: +358 9 19159552. E-mail: kurt.fagerstedt{at}helsinki.fi
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Abbreviations |
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LP; lipid peroxidation; ROS, reactive oxygen species; SOD, superoxide dismutase; TBARS, thiobarbituric acid reactive substances.
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