Journal of Experimental Botany, Vol. 52, No. 355, pp. 341-349,
February 2001
© 2001 Oxford University Press
Original Papers |
Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses
1 Department of Horticulture, Forestry and Recreational Resources, Kansas State University, Manhattan, KS 66506, USA
2 Department of Plant Science, Rutgers University, New Brunswick, NJ 08901, USA
Received 31 March 2000; Accepted 5 September 2000
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Abstract |
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Calcium (Ca2+) may be involved in plant tolerance to heat stress by regulating antioxidant metabolism or/and water relations. This study was designed to examine whether external Ca2+ treatment would improve heat tolerance in two C3, cool-season grass species, tall fescue (Festuca arundinacea L.) and Kentucky bluegrass (Poa pratensis L.), and to determine the physiological mechanisms of Ca2+ effects on grass tolerance to heat stress. Grasses were treated with CaCl2 (10 mM) or H2O by foliar application and then exposed to heat stress (35/30 °C) in growth chambers. Some of the Ca2+-untreated plants were maintained at 20/15 °C as the temperature control. Heat stress reduced grass quality, relative water content (RWC), and chlorophyll (Chl) content of leaves in both species, but Ca2+ treatment increased all three factors under heat stress. The Ca2+ concentration in cell saps increased with heat stress and with external Ca2+ treatment in both species. Osmotic potential increased with heat stress, but external Ca2+ treatment had no effect. Osmotic adjustment increased during short-term heat stress, but then decreased with a prolonged period of stress; it was not influenced by Ca2+ treatment. The activity of superoxide dismutase (SOD) in both species increased transiently at 12 d of heat stress and then remained at a level similar to that of the control. External Ca2+ treatment had no effect on SOD activity. The activities of catalase (CAT), ascorbate peroxidase (AP), and glutathione reductase (GR) of both species decreased during heat stress. Plants treated with Ca2+ under heat stress had higher CAT, GR and AP activities than untreated plants. Lesser amounts of malondialdehyde (MDA) accumulated in Ca2+-treated plants than in untreated plants during extended periods of heat stress. The results suggested that exogenous Ca2+ treatment enhanced heat tolerance in both tall fescue and Kentucky bluegrass. This enhancement was related to the maintenance of antioxidant activities and a decrease in membrane lipid peroxidation, but not to the regulation of osmotic potential and osmotic adjustment.
Key words: Antioxidant enzymes, Ca2+, tall fescue, Kentucky bluegrass, osmotic adjustment.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Heat stress is a major factor limiting growth of cool-season plant species in many areas. Growth suppression in cool-season grasses under heat stress involves many physiological and biochemical changes, including water deficit and oxidative stress (Tajima et al., 1976
; Lehman and Engelke, 1993; Liu and Huang, 2000), which are detrimental to plant survival under high temperature conditions. Previous studies have elucidated the importance of maintaining a favorable antioxidative level and water status in plant adaptation to heat stress (Ahmad et al., 1989; Graves et al., 1991; Ashraf et al., 1994; Jagtap and Bhargava, 1995; Gong et al., 1997; Kurganova et al., 1997).
Several studies have showed that Ca2+ is involved in the regulation of plant responses to various environmental stresses, including heat (Bramm, 1992; Biyaseheva et al., 1993; Colorado et al., 1994). Increasing cytosolic Ca2+ content under heat stress (Biyasheva et al., 1993; Gong et al., 1998) may alleviate heat injury and enable plant cells to better survive (Bamberg et al., 1998; Gong et al., 1998). However, excessive Ca2+ released into the cytosol and sustained high cytosolic Ca2+ concentration might be cytotoxic (Hepler and Wayne, 1985; Biyasheva et al., 1993; Wang and Li, 1999).
Limited research has been conducted concerning effects of exogenous Ca2+ on heat tolerance, and available results are contradictory. It was found that treatment of maize (Zea mays L.) seeds with 15 and 20 mM Ca2+ solution enhanced intrinsic heat tolerance of seedlings (Gong et al., 1997). External Ca2+ (5–10 mM) also reduced high temperature-induced membrane leakage in roots of beet (Beta vulgaris L.) (Toprover and Glinka, 1976; Cooke et al., 1986). In contrast, it has been reported that heat-induced growth retardation could not be alleviated by external Ca2+ treatment (1.9 mM) in excised coleoptiles of wheat (Triticum aestivum L.) (Onwueme and Laude, 1972).
The role of Ca2+ in the regulation of heat tolerance is still unclear. Some suggest that it may be involved in signal transduction (McAinsh et al., 1996) and gene expression (Bramm, 1992; Trofimova et al., 1999) under oxidative and heat stress. Others (Gong et al., 1997) found that Ca2+ increases antioxidant enzyme activities and reduces lipid peroxidation of cell membranes. Calcium has also been shown to regulate guard-cell turgor and stomatal aperture (Mansfield et al., 1990; Webb et al., 1996). Cell turgor maintenance depends on the accumulation of compatible, osmotically active solutes (osmotic adjustment) (Hare et al., 1998). External Ca2+ may interfere with cellular Ca2+ and affect osmotic adjustment of cells under stress conditions.
The objectives of this study were to investigate the involvement of Ca2+ in heat tolerance in cool-season grasses, and to examine the effects of external Ca2+ treatment on antioxidant enzymes and osmotic adjustment under heat stress. Two grass species, tall fescue and Kentucky bluegrass were examined to address these objectives.
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Materials and methods |
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Plant materials
Sod pieces of tall fescue (cv. Rebel Jr.) and Kentucky bluegrass (cv. Kenblue) were collected from field plots at the Rocky Ford Turfgrass Research Center, Kansas State University. Grasses were grown in polyvinylchloride tubes (10 cm in diameter, 60 cm long) filled with topsoil (fine, montmorillonitic, mesic, aquic arquidolls) in the greenhouse for 60 d and then transferred to growth chambers with a temperatures of 20/15 °C (day/night), a 14 h photoperiod, and a photosynthetically active radiation of 600 µmol m-2 s-1 at the canopy level. Grasses were well-watered and maintained at growth chamber conditions for 15 d to allow adaptation before heat stress was imposed.
Heat stress and Ca2+ treatment
The experiment included two temperatures regimes: optimum, control temperatures (20/15 °C, day/night) and high temperatures (35/30 °C). Each temperature regime was replicated in four growth chambers. A 20 ml CaCl2 solution (10 mM) was sprayed uniformly on foliage at 10.00 h using a spray bottle once daily during a 3 d period immediately before heat stress was imposed. No leaf burn was observed after Ca2+ spray. Control plants were sprayed with 20 ml deionized water. Each treatment consisted of four replicates and lasted for 30 d. The Ca2+-treated and untreated plants were arranged randomly in high-temperature growth chambers.
Analysis of variance was based on the general linear model procedure of the Statistical Analysis System (SAS Institute Inc., Cary, NC). Least significance difference (LSD) at a 0.05 probability level was used to detect the differences between treatment means.
Measurements
Grass quality, a criterion commonly used to evaluate physiological health and appearance, was rated visually as an integral of grass color, uniformity, and density on the scale of 0 (desiccated, brown leaves) to 9 (turgid, green leaves) (Turgeon, 1999). The minimum acceptable level was 6.
Leaf relative water content (RWC) was calculated as follows (Barrs and Weatherley, 1962): RWC=(FW-DW)/ (SW-DW)x100, where FW is the leaf fresh weight, DW is leaf dry weight at 85 °C for 3 d, and SW is turgid weight of leaves after soaking in water for 4 h at room temperature (approximately 20 °C).
Leaves were frozen and pressed with a hydraulic press to collect cell sap for Ca2+analysis and measurement of osmotic potential. The Ca2+concentration was assayed at a 1:100 (v/v) dilution of cell sap using an inductively coupled plasma spectrophotometer (Fisons Instruments Inc., Beverley, MA). Leaf osmotic potential of stressed, dehydrated (
o), and fully rehydrated (100) leaves was measured using a vapour pressure osmometer (Wescor, Inc., Logan, UT). Osmotic adjustment was calculated as the difference in osmotic potential at full turgor (100) between control and stressed plants (o) (Blum, 1989; Blum and Sullivan, 1986). Leaf chlorophyll (Chl) was extracted by soaking 0.05–0.1 g leaves in 20 ml dimethyl sulphoxide in the dark for 72 h (Hiscox and Israeltem, 1979). Absorbance of extracted Chl was measured at 663 and 645 nm using a spectrophotometer (Spectronic Instruments, Inc., Rochester, NY).
For enzyme extracts and assays, 0.2 g leaves were frozen in liquid nitrogen and then ground in 4 ml solution containing 50 mM phosphate buffer (pH 7.0), 1% (w/v) polyvinylpolypyrrolidone, and 0.2 mM ascorbic acid. The homogenate was centrifuged at 15 000 g for 30 min, and the supernatant was collected for enzyme assays.
The activity of SOD was measured as described previously (Giannopolities and Ries, 1977). The assay medium contained 50 mM phosphate buffer (pH 7.8), 13 mM methionine, 75 µm p-nitro blue tetrazolium chloride (NBT), 2 µm riboflavin, 0.1 mM EDTA, and 20–50 µl enzyme extract. Riboflavin was added last and the test tubes were placed under two 15 W fluorescent lamps. The reactions were terminated after 10 min by removal from light source. The absorbance was read at 560 nm. A non-irradiated reaction mixture did not develop colour and served as control. The reaction mixture lacking enzyme developed maximum colour as a result of maximum reduction of NBT. One unit of enzyme activity was determined as the amount of the enzyme to reach an inhibition of 50% NBT reduction rate.
The activity of CAT was determined as a decrease in absorbance at 240 nm for 1 min following the decomposition of H2O2 (Change and Maehly, 1955). The reaction mixture contained 50 mM phosphate buffer (pH 7.0) and 15 mM H2O2.
The activity of AP was measured as a decrease in absorbance at 290 nm for 1 min (Nakano and Asada, 1981). The assay mixture consisted of 0.5 mM ASA, 0.1 mM H2O2, 0.1 mM EDTA, 50 mM sodium phosphate buffer (pH 7.0), and 0.15 ml enzyme extract.
The activity of GR was determined by following the decrease in absorbance at 340 nm for 1 min due to the glutathione-dependence of NADPH (Cakmak et al., 1993). The reaction mixture contained 1 mM EDTA, 0.5 mM GSSG, 0.15 mM NADPH, 100 mM sodium phosphate buffer (pH 7.8), and 0.15 ml enzyme extract.
Enzyme activities were expressed on the basis of per unit protein weight. Protein content was determined using bovine serum albumin as a standard (Bradford, 1976).
Lipid peroxidation was measured in terms of MDA content (Dhindsa et al., 1981). A 1 ml aliquot of supernatant was mixed with 4 ml of 20% trichloroacetic acid containing 0.5% thiobarbituric acid. The mixture was heated at 100 °C for 30 min, quickly cooled, and then centrifuged at 10000 g for 10 min. The absorbance of the supernatant was read at 532 nm. The unspecific turbidity was corrected by A600 subtracting from A530. The concentration of MDA was calculated using an extinction coefficient of 155 mM-1 cm-1 (Heath and Packer, 1968).
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Results |
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Cell sap Ca2+ concentration
A rapid increase in Ca2+ concentration in the cell sap was observed during the first 15 d of heat stress in both species (Fig. 1
). After 15 d, heat-stressed plants still maintained higher Ca2+ concentration than the controls. External Ca2+treatment increased Ca2+ concentration in the cell sap before and after heat stress was imposed in both species, except for tall fescue at 30 d of heat stress.
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Grass quality, chlorophyll content and water relations
Heat stress reduced grass quality to below the control (20/15 °C) level for both species, starting at 12 d (Fig. 2). Plants treated with Ca2+ maintained a higher quality than untreated plants after exposure to heat stress for 18 d in tall fescue and for 24 d in Kentucky bluegrass. At 30 d of heat stress, Ca2+-treated Kentucky bluegrass still had acceptable quality (6.0), whereas quality of untreated plants had declined to below the acceptable level.
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Leaf RWC decreased to below the control level, starting at 12 d of heat stress for tall fescue and 24 d for Kentucky bluegrass (Fig. 3
). The Ca2+-treated plants had higher RWC than untreated plants after 18 d and 24 d for tall fescue and Kentucky bluegrass, respectively. Kentucky bluegrass treated with Ca2+under heat stress maintained RWC similar to the level of control plants without Ca2+treatment during most of the experimental period, except at 30 d of heat stress.
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Leaf Chl content increased to above the control level at 6 d of heat stress in both species and then decreased to below the control level at 24 d for tall fescue and 18 d for Kentucky bluegrass (Fig. 4
). The Ca2+-treated plants had higher Chl content than untreated plants after 24 d and 30 d for tall fescue and Kentucky bluegrass, respectively.
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Heat stress significantly increased leaf osmotic potential in both species, starting at 7 d (Fig. 5
). Osmotic adjustment increased within the first 15 d of heat stress and then gradually decreased in both species (Fig. 6). External Ca2+ treatment had no significant effects on osmotic potential and osmotic adjustment (Figs 5, 6).
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Antioxidant enzyme activities
The activity of SOD increased to above the control level at 12 d of heat stress in both species and then decreased to a level similar to that of the control (Fig. 7). The Ca2+ treatment had no effects on SOD activity under heat stress. Unlike SOD, CAT decreased to below the control level, beginning at 12 d of heat stress for tall fescue and 18 d for Kentucky bluegrass (Fig. 8). The activity of GR without Ca2+ treatment decreased to below the control level, starting at 6 d of heat stress for tall fescue and 12 d for Kentucky bluegrass (Fig. 9). The Ca2+-treated plants had higher CAT and GR activities than untreated plants after 24 d of heat stress for both species. The AP activity decreased to below the control level after 18 d of heat stress for both species without Ca2+ treatment (Fig. 10). The Ca2+ treatment enhanced AP activity of heat-stressed plants to a level similar to that of control plants without Ca2+ treatment.
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Lipid peroxidation
The MDA content in heat-stressed plants was higher than that in control plants, starting at 12 d in tall fescue and 18 d in Kentucky bluegrass (Fig. 11). The Ca2+ treatment considerably reduced MDA contents under heat stress at 12 d and 18 d for tall fescue and 18, 24 and 30 d for Kentucky bluegrass. The inhibitory effect of Ca2+on MDA accumulation was more dramatic and lasted longer in Kentucky bluegrass than in tall fescue.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Heat stress caused significant declines in grass quality, RWC and leaf Chl content. External Ca2+ application alleviated heat injury, as manifested by increases in these three factors compared to untreated plants. The responses of both cool-season species to heat stress and Ca2+ application followed the same pattern. These results are consistent with those reported for several other species. Application of 5–10 mM Ca2+reduced thermal damage in beet root (Cooke et al., 1986
) and potato (Solanum tuberosum L.) tubers (Coria et al., 1998). Similar concentrations of external Ca2+also increased drought resistance in Vigna catjang (Mukherjee and Choudhuri, 1985), soybean (Glycine max L.) (Yang et al., 1993), and cotton (Gossypium hirsutum L.) (Cheng et al., 1997), and increased salinity tolerance in bean (Phaseolus vulgaris L.) roots (Cachorro et al., 1993). Heat stress significantly increased Ca2+concentration in cell sap of both tall fescue and Kentucky bluegrass, especially during the early period of stress. Accumulation of cytosolic free Ca2+ also has been found under heat shock in other species (Klein and Ferguson, 1987; Biyaseheva et al., 1993; Gong et al., 1998; Wang and Li, 1999).
Osmotic adjustment is an important mechanism of plant tolerance to drought and heat stress (Smith et al., 1989; Ludlow et al., 1990). Osmotic adjustment increased during short-term heat stress in both species, but was not affected by external Ca2+ treatment under heat stress conditions. These results indicated that the enhancing effects of external Ca2+ on leaf water status and heat tolerance in both tall fescue and Kentucky bluegrass were not due to its regulation of osmotic potential and osmotic adjustment.
Short-term heat stress caused a transient increase in Chl content. However, prolonged periods of heat stress resulted in the loss of Chl and might have been related to damage to reaction centres (Kyle, 1987). External Ca2+ treatment inhibited the loss of chlorophyll under heat stress, possibly by its reducing photo-oxidation (Wise and Naylor, 1987) or maintaining membrane integrity (Coria et al., 1998).
Heat stress induces oxidative injury and alters the activities of antioxidant enzymes including SOD, CAT, AP, and GR in many plant species (Burke and Oliver, 1992; Foyer et al., 1994; Jagtap and Bhargava, 1995; Gong et al., 1997). The SOD activity increased transiently during initial stress periods in tall fescue and Kentucky bluegrass. This increase might have been due to a rapid and large accumulation of Cu/Zn SOD mRNA, as was found in tobacco leaves during heat shock (Tsang et al., 1991). The external Ca2+ treatment did not affect SOD activity under heat stress, suggesting that SOD was not related to the effects of Ca2+ on heat-induced oxidative stress. However, it has been found that external Ca2+ increased SOD activity in maize seedlings (Gong et al., 1997). The increased SOD activity also might reflect the increased production of O2-. (Thompson et al., 1987). Limited studies have suggested that calcium loading in root cells induces a dramatic increase in O2-. release during wound stress (Minibayeva et al., 1998), but there is no direct evidence of the effect under heat stress.
Activity of CAT continued to decline with prolonged periods of heat stress in both species. Reduction in CAT activity also has been reported in other plants during heat shock (Willekens et al., 1995; Foyer et al., 1997; Dat et al., 1998), which paralleled increases in H2O2 content (Dat et al., 1998). External Ca2+ treatment helped maintain higher CAT activity under heat stress. This enhanced CAT activity could reduce the accumulation of H2O2 and alleviate the damage to cell membranes. Ascorbate peroxidase located in both the cytosol and the chloroplasts, can also remove H2O2 (Cakmak et al., 1993). Gong et al. reported that external Ca2+ treatment increased activity of AP in maize seedlings during heat stress and this enhanced activity could be related to improvement of heat tolerance (Gong et al., 1997). These results agreed with this observation in cool-season grasses. External Ca2+ treatment resulted in a transient increase in cytosolic Ca2+ concentration during heat stress (Gong et al., 1998) and the inhibitors of AP modify H2O2-induced transients in cytosolic Ca2+ concentration (Price et al., 1994), suggesting some relationship among AP activity, cytosolic Ca2+ and oxidative stress. Glutathione reductase also plays an important role in maintaining the cellular antioxidant/ prooxidant ratio. Heat stress decreased GR activity, but Ca2+-treated plants had higher GR activity than untreated plants. Calcium deprivation strongly inhibited GR activity in cell culture of Digitalis thapsi and changed the redox state of cells (Paranhos et al., 1999). Thus, the enhancement of GR activity by external Ca2+ treatment could protect the chloroplastic components against oxidation by H2O2.
The content of MDA often is used as an indicator of lipid peroxidation resulting from oxidative stress (Smirnoff, 1995). Heat stress increased MDA contents in both tall fescue and Kentucky bluegrass. The Ca2+ treatment reduced lipid peroxidation, as indicated by less accumulation of MDA compared to untreated plants. This result agreed with those for maize seedlings (Gong et al., 1997). Calcium is known to reduce membrane permeability and maintain membrane integrity under heat stress (Cooke et al., 1986; Coria et al., 1998). External Ca2+ treatment not only could affect membrane structure, but also could be involved in oxidative signal transduction concomitant with the regulation of antioxidant enzymes under heat stress (McAinsh et al., 1996; Gong et al., 1997). The results show that application of Ca2+ would reduce loss of grasses in hot environments by mitigating oxidative stress.
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Acknowledgments |
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The authors thank Dr Mary Beth Kirkham for reviewing the manuscript. Funds for this study were provided by Kansas Turfgrass Foundation and Kansas Agricultural Experiment Station. Contribution No. 00-341-J from the KAES.
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Notes |
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3 To whom correspondence should be addressed. Fax: +1 732 932 9441. E-mail: huang{at}aesop.rutgers.edu
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Abbreviations |
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RWC; relative water content; Chl; chlorophyll content; SOD; superoxide dismutases; CAT; catalase; AP; ascorbate peroxidase; GR; glutathione reductase; MDA; malondialdehyde..
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References |
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