Plant Physiol. (1998) 116: 1351-1357

Parallel Changes in H₂O₂ and Catalase during Thermotolerance Induced by Salicylic Acid or Heat Acclimation in Mustard Seedlings¹

James F. Dat, Humberto Lopez-Delgado², Christine H. Foyer, and Ian M. Scott^*

Institute of Biological Sciences, University of Wales, Aberystwyth, Ceredigion SY23 3DA, United Kingdom (J.F.D., H.L.-D., I.M.S.); and Environmental Biology Department, Institute of Grassland and Environmental Research, Aberystwyth, Ceredigion SY23 3EB, United Kingdom (J.F.D., C.H.F.)

	ABSTRACT

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Spraying mustard (Sinapis alba L.) seedlings with salicylic acid (SA) solutions between 10 and 500 µm significantly improved their tolerance to a subsequent heat shock at 55°C for 1.5 h. The effects of SA were concentration dependent, with higher concentrations failing to induce thermotolerance. The time course of thermotolerance induced by 100 µm SA was similar to that obtained with seedlings acclimated at 45°C for 1 h. We examined the hypothesis that induced thermotolerance involved H₂O₂. Heat shock at 55°C caused a significant increase in endogenous H₂O₂ and reduced catalase activity. A peak in H₂O₂ content was observed within 5 min of either SA treatment or transfer to the 45°C acclimation temperature. Between 2 and 3 h after SA treatment or heat acclimation, both H₂O₂ and catalase activity significantly decreased below control levels. The lowered H₂O₂ content and catalase activity occurred in the period of maximum thermoprotection. It is suggested that thermoprotection obtained either by spraying SA or by heat acclimation may be achieved by a common signal transduction pathway involving an early increase in H₂O₂.

	INTRODUCTION

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Plants have evolved various ways of coping with their changing surroundings. Adaptive responses are directly regulated by genetic and biochemical characteristics, which may be manipulated. An understanding of the biochemical changes involved in plant-stress responses will enable the development of genetically engineered plant material with enhanced resistance to biotic and abiotic stress. Because high temperature is one of the major abiotic stresses limiting plant yield and distribution in many regions of the world (Ong and Baker, 1985; Criddle et al., 1994), it has been the focus of much research, particularly since the discovery and characterization of HSPs. The heat-shock response is not unique to plants and has been described for a wide range of organisms, including bacteria (Vierling, 1991). In cyanobacteria oxidative stress can induce the synthesis of some HSPs (Mittler and Tel-Or, 1991), suggesting that HSPs and oxidative stress-induced proteins may share one or several common regulatory operons (Lee et al., 1983; Van Bogelen et al., 1987). However, to date very little research has been undertaken to elucidate the nature of the common responses to heat shock and oxidative stress in plants.

In recent years SA has been the focus of much attention because of its ability to induce protection against plant pathogens (Raskin, 1992). However, the mode of action of SA during pathogenesis and its role in the transient increase of active oxygen species, including H₂O₂, characteristic of incompatible plant-pathogen interactions (the oxidative burst), is still a matter for debate (Levine et al., 1994; Ryals et al., 1995). The in vitro inhibition of catalase (Chen et al., 1993; Sanchez-Casas and Klessig, 1994; Conrath et al., 1995) and ascorbate peroxidase by SA (Durner and Klessig, 1995) provided the first indications of the existence of a link between SA and the oxidative burst. Other workers, however, suggest that catalase inhibition may not be the main mechanism by which SA induces H₂O₂ accumulation (Rüffer et al., 1995; Ryals et al., 1995). A direct role for SA in potentiating H₂O₂ production by a plasma membrane NAD(P)H oxidase has been proposed (Kauss and Jeblick, 1995, 1996; Willekens et al., 1995; Mur et al., 1996; Shirasu et al., 1997). In addition, H₂O₂ may regulate SA accumulation (Bi et al., 1995; León et al., 1995; Neuenschwander et al., 1995; Summermatter et al., 1995).

Generation of active oxygen species, particularly H₂O₂, during abiotic stresses has also been proposed as part of the signaling cascade leading to protection from these stresses (Doke et al., 1994; Prasad et al., 1994; Foyer et al., 1997). SA also accumulates during exposure to ozone or UV light (Yalpani et al., 1994; Sharma et al., 1996), whereas pretreatment of leaves with SA can protect them from paraquat-induced oxidative stress (Strobel and Kuc, 1995). Therefore, it is interesting to explore whether SA and H₂O₂ may be involved in the induction of protective mechanisms involved in tolerance to abiotic and biotic stresses.

Tissues from potato (Solanum tuberosum) microplants grown on acetylsalicylic acid in our laboratory were shown to have enhanced thermotolerance (Lopez-Delgado et al., 1998). The following experiments were designed to determine whether SA could also induce thermotolerance in whole seedlings. Thermoprotection was induced by spraying SA and was compared with heat acclimation. Tissue H₂O₂ contents and catalase activities were determined to assess their possible involvement in induced thermotolerance.

	Materials and Methods

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Mustard (Sinapis alba L.) seeds (Kings Seeds, Essex, UK) were germinated in Levington's Universal compost (Fisons, Ipswich, UK) (15 seedlings per 15- × 21-cm tray) and grown for 8 d in a growth room with RH at 70% under a 16-h photoperiod on a 24/18°C day/night cycle at 100 µmol m² s¹ PAR.

Treatments

Assessment of Heat Tolerance

Measurement of H₂O₂

Plant tissue (approximately 0.5 g), consisting of the apical region of the shoot including the cotyledons, was ground in liquid N₂ and extracted in 3 mL of ice-cold 5% TCA (Fisher Scientific). The crude extracts were centrifuged for 20 min at 1400g. A sample of supernatant (0.5 mL) was passed through a column containing 0.5 g of Dowex resin (1X1-100, chloride form, 1% cross-linked, Sigma) previously equilibrated with 5% TCA. The column was washed with a further 3.5 mL of 5% TCA; all eluates were collected together. H₂O₂ content was measured by adding 0.5 mL of eluate to 0.5 mL of 0.5 mm luminol (Aldrich) and the volume was made to 5.5 mL with 0.2 m NH₄OH (pH 9.0). This mixture (0.5 mL) in a borosilicate glass tube (6 × 50 mm, Laboratory Sales, Ltd., Rochdale, UK) was analyzed using a chemiluminescence meter (model A6100, Pico-Lite Luminometer Analyzer, Packard, Meriden, CT). Chemiluminescence was initiated by injecting 50 µL of 0.5 mm potassium ferricyanide (Sigma) in 0.2 m NH₄OH. The emitted photons were counted for 5 s. Recovery estimates (which consisted of adding a known concentration of H₂O₂ to aliquots of the initial extracts that were then processed in parallel) indicated that on average 93% (sd = 2.5%; n = 38) of the H₂O₂ was recovered, and were used as correction factors for each sample (Warm and Laties, 1982).

Catalase Activity

Statistical Analysis

	RESULTS

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Effects of Heat Acclimation and SA on Survival from Heat Shock

View larger version (19K): [in this window] [in a new window]   Figure 1. A, Percentage survival of mustard seedlings heat shocked at various times after spraying with 100 µm SA () or with water () at 24°C. B, Percentage survival of mustard seedlings heat shocked at various times after 1 h of acclimation treatment (45°C) in the dark (); controls () were kept at 24°C during the acclimation period (light- or dark-incubated controls were not significantly different). Bars represent se of at least four experiments (n  4), each with 12 to 15 seedlings.

A period of 1.5 h after spraying was adopted for assessment of the concentration dependence of the SA treatments (Fig. 2). SA solutions between 10 to 500 µm significantly increased (P < 0.007) thermotolerance to heat shock in comparison with controls sprayed with water (Fig. 2). In contrast, spraying with SA concentrations of 1 µm or 1 mm did not improve survival of heat shock (Fig. 2). By comparison, the heat-acclimation treatment shown in Figure 2, consisting of 1 h at 45°C in the dark followed by a 1-h recovery period in the light, increased survival of heat shock by 4-fold compared with nonacclimated plants.

View larger version (23K): [in this window] [in a new window]   Figure 2. Percentage survival of mustard seedlings heat shocked for 1.5 h at 55°C either 1.5 h after spraying with water (C) or various concentrations of SA at 24°C, or 1 h after acclimation (1 h at 45°C) in the dark (Accl D). Bars represent se of at least four experiments (n  4), each with 12 to 15 seedlings.

SA can affect stomatal opening under certain conditions (Larque-Saavedra, 1979; Rai et al., 1986). Cs measurements were therefore made to examine whether changes in Cs could have been responsible for the observed thermoprotection of SA-sprayed plants (Fig. 3). Spraying with either H₂O or 100 µm SA solution increased Cs during the next hour (probably because of increased humidity at the leaf surface), but Cs then decreased back to levels of nonsprayed control plants after 2 h. There were no significant differences in Cs between plants sprayed with either water or SA (Fig. 3).

View larger version (40K): [in this window] [in a new window]   Figure 3. Cs of mustard seedlings at intervals following spraying with either distilled water (white bars) or with 100 µm SA solution (gray bars) in comparison with nonsprayed controls (black bars) (n = 8).

Effects of Heat Shock on H₂O₂ Content and Catalase Activity

View larger version (15K): [in this window] [in a new window]   Figure 4. A, H2O2 content (µmol g1 fresh weight) of mustard seedlings following a 1-h heat-shock treatment in the dark at 55°C. Bars represent the se (n = 9). B, Catalase activity (µmol O2 min1 g1 fresh weight) of mustard seedlings following a 1-h heat-shock treatment in the dark at 55°C. Bars represent se (n = 12).

H₂O₂ Content and Catalase Activity during the 1-h HeatAcclimation Treatment and the 1st h after SA Spray

View larger version (16K): [in this window] [in a new window]   Figure 5. A, H2O2 content (µmol g1 fresh weight) of mustard seedlings either during the 1st h immediately after spraying with a 100 µm SA solution at 24°C (), or during a 1-h temperature-acclimation treatment at 45°C (). B, Catalase activity (µmol O2 min1 g1 fresh weight) of mustard seedlings either during the 1st h immediately after spraying with a 100 µm SA solution at 24°C (), or during a 1-h temperature-acclimation treatment at 45°C (). Bars represent se (n = 8).

The H₂O₂ content of mustard plants increased by more than 90% 5 min after spraying with a 100 µm SA solution. Fifteen and 30 min after spraying, H₂O₂ levels were still significantly (P < 0.05) higher (28-35%) than in the control plants. After 45 min the H₂O₂ content had returned to control values. Thus, both SA and heat acclimation caused a rapid increase in H₂O₂, which then declined toward control values.

Catalase activity was determined during the 1-h acclimation treatment and during the 1st h following the SA spray. In both cases the catalase activity fluctuated but was significantly increased (P < 0.05) after 60 min (Fig. 5B).

H₂O₂ Content and Catalase Activity during the Period of Thermotolerance

View larger version (16K): [in this window] [in a new window]   Figure 6. A, H2O2 content (µmol g1 fresh weight) of mustard seedlings during the thermoprotection period following either spraying with a 100 µm SA solution at 24°C (), or a 1-h temperature-acclimation treatment (45°C) in the dark (). Controls () were kept at 24°C without spraying (light- or dark-incubated controls were not significantly different). Bars represent se (n = 8). B, Catalase activity (µmol O2 min1 g1 fresh weight) of mustard seedlings during the thermoprotection period following either spraying with a 100 µm SA solution () at 24°C, or a 1-h temperature-acclimation treatment (45°C) in the dark (). Controls () were kept at 24°C without spraying (light- or dark-incubated controls were not significantly different). Bars represent se (n  8).

Catalase activity was determined during the same period (Fig. 6B). Both treatments resulted in a significant (P < 0.032), transient decrease in extractable catalase activity of more than 15% 2 to 3 h after treatment, followed by an increase back to control levels by 6 h. Catalase activity was therefore significantly lower during the period of thermotolerance; the decreased catalase activity was not due to co-extracted SA, because there was no inhibition when SA concentrations up to 10 mm were added to the in vitro assay.

	DISCUSSION

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To our knowledge, this is the first report of thermoprotection obtained by spraying SA on seedlings. The increased thermotolerance obtained following spraying mustard seedlings with SA solutions (Fig. 2) extends our recent observation that tissues of potato (Solanum tuberosum L.) microplants grown on culture medium containing low concentrations of acetylsalicylic acid were more thermotolerant than tissues of microplants grown on acetylsalicylic acid-free medium (Lopez-Delgado et al., 1998). Thermoprotection obtained in SA-treated mustard seedlings was temporary, being maximal from 1.5 to 4 h after spraying (Fig. 1A). Heat-acclimation treatment also gave effective protection over the same time period (Fig. 1B). Howarth and Skøt (1994) found that sorghum (Sorghum bicolor L.) seedlings were significantly more thermotolerant 2 and 4 h after a 2-h 45°C acclimation treatment, but thermotolerance was completely lost by 6 h.

Exogenous applications of SA, either by direct injection or by spraying, have been reported to cause a multitude of effects on the morphology and physiology of plants (Raskin, 1992; Pierpoint, 1994; Pancheva et al., 1996). SA is known to affect stomatal opening (Larque-Saavedra, 1979; Rai et al., 1986). However, in this study no significant effect of SA on Cs was observed during the first 3 h following application (Fig. 3), which is similar to previous observations in barley (Pancheva et al., 1996). Stomatal regulation was therefore probably not involved in the acquired thermotolerance following spraying with a SA solution.

If heat shock generates oxidative stress, SA may mimic temperature acclimation by also generating H₂O₂. It has been suggested that heat shock may produce oxidative stress in plant cells, as well as in human and in animal cells (Lee et al., 1983; Privalle and Fridovich, 1987; Bowler et al., 1992), although evidence of H₂O₂ accumulation during heat shock was only recently reported in cell-suspension cultures (Doke et al., 1994) and in planta in tobacco (Nicotiana tabacum L.) seedlings (Foyer et al., 1997). Indirect evidence linking oxidative stress and heat shock has often combined high light and heat shock, resulting in photoinhibition and/or photooxidation (Tsang et al., 1991; Bowler et al., 1992). The present study clearly indicates that heat shock can result in increased oxidant accumulation in plants (Fig. 4A), even when applied in the dark. H₂O₂ accumulation after heat shock in the dark is probably independent of photosynthesis and may be produced in a manner similar to H₂O₂ in plants chilled and acclimated in the dark (Okuda et al., 1991; Purvis and Shewfelt, 1993; Prasad et al., 1994), where the site of H₂O₂ synthesis is unresolved. The increase in H₂O₂ following heat shock in the dark could be explained by the model of Doke et al. (1994; Doke, 1997) in which abiotic stresses are accompanied by an oxidative burst, similar to that involved in signaling during plant-pathogen interactions (Levine et al., 1994; Mehdy, 1994; Baker and Orlandi, 1995).

Although H₂O₂ increased by over 65% following a 1-h heat shock in mustard seedlings, catalase activity decreased by about 10% (Fig. 4). There are several reports of decreased activities of key antioxidant enzymes (superoxide dismutase and catalase) following heat shock; the antioxidant defenses may thus be impaired by heat shock and lead to increased oxidant concentrations (Matters and Scandalios, 1986; Feierabend et al., 1992; Streb et al., 1993; Willekens et al., 1995; Foyer et al., 1997; Polle, 1997). Such perturbations in oxidant concentrations may be a prerequisite for redox signaling-induced changes in gene expression (Foyer et al., 1997). Heat shock suppresses translation of many proteins, except HSPs (Vierling, 1991). As catalase has a rapid turnover, conditions inhibiting catalase synthesis will lower the steady-state level of this enzyme (Streb et al., 1993; Streb and Feierabend, 1996; Scandalios et al., 1997). Thus, heat shock and oxidative stress will enhance inactivation of catalase by preventing synthesis of new enzyme (Hertwig et al., 1992; Feierabend and Dehne, 1996), resulting in a decline in catalase activity. Because the heat shock was applied in the dark, catalase photoinactivation (Feierabend and Engel, 1986; Polle, 1997) is not the cause of the reduction in catalase activity in the present study (Fig. 4B).

H₂O₂ increased during heat acclimation and following SA treatment. An increase in H₂O₂ content was measured 5 min after the start of the heat acclimation and after the SA spray treatments (Fig. 5A). This early peak in H₂O₂ is similar to that observed by Doke et al. (1994) during heat shock of cell suspensions. The amplitude of the H₂O₂ increase is also similar to that reported by Chen et al. (1993), following a continuous 24-h injection of a 1 mm SA solution into petioles of tobacco plants. It is tempting to associate this H₂O₂ increase with an oxidative burst similar to that observed during other forms of abiotic stress (Shimada et al., 1991; Doke et al., 1994; Sgherri et al., 1996; Sharma et al., 1996), including chilling (Omran, 1980; Okuda et al., 1991; Prasad et al., 1994), and during incompatible pathogen interactions (Apostol et al., 1989; Chen et al., 1993; Doke et al., 1994; Tenhaken et al., 1995). Recent work by Lopez-Delgado et al. (1998) also implicates H₂O₂ in the signal transduction sequence inducing thermotolerance, since tissues of potato microplants grown from explants incubated with H₂O₂ showed enhanced thermotolerance. The increase in H₂O₂ during temperature acclimation and immediately following SA spray (Fig. 5A) may thus be part of the signaling cascade involved in inducing protection against a subsequent stress.

The biochemical changes responsible for the transient period of induced thermoprotection (Fig. 1) are of considerable interest, as they may be manipulated to enhance thermotolerance in plants. The metabolic and molecular mechanisms associated with the observed decline in H₂O₂ content and in catalase activity during this period (Fig. 6) are unknown, but the parallel changes in the acclimated and SA-treated plants suggest that these parameters may be relevant to thermotolerance. The decline in H₂O₂ content may be indicative of an enhanced antioxidant potential in the tissues, which would contribute to enhanced thermotolerance. Catalase activity reached a minimum during the thermoprotection period following either treatment (Fig. 6B), although its activity was higher at the start of this period (Figs. 5B and 6B). Other antioxidants such as GSH may prove to be involved during high-temperature acclimation, as observed by Nieto-Sotelo and Ho (1986) during heat shock. Although SA can inhibit catalase and ascorbate peroxidase in vitro (Chen et al., 1993; Conrath et al., 1995; Durner and Klessig, 1995; Rüffer et al., 1995), this mechanism would not explain the lower catalase activity extracted from our SA-treated mustard plants. It may also be worth investigating possible links between the thermotolerance induced with SA and the role of this compound in thermogenicity (Raskin et al., 1987; Van der Straeten et al., 1995).

In conclusion, the present study shows that SA treatment induces thermoprotection in mustard seedlings, and that the period of induced thermoprotection is similar to that obtained by heat acclimation. Both the SA and heat-acclimation treatments induced a transient initial increase in H₂O₂, but both resulted in decreased H₂O₂ and catalase contents during the period of induced thermoprotection. Since SA and H₂O₂ have recently been shown to induce thermoprotection in potato microplants (Lopez-Delgado et al., 1998), we suggest that both SA and H₂O₂ could be involved in signal transduction leading to acclimation during heat stress.

	FOOTNOTES

   Received July 25, 1997; accepted December 16, 1997.

	ABBREVIATIONS

Abbreviations: Cs, stomatal conductance. HSP, heat-shock protein. SA, salicylic acid.

	ACKNOWLEDGMENTS

We are grateful for technical advice from Dr. A. Kingston-Smith and Prof. J. Barrett.

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