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TURFGRASS SCIENCE

Heat Stress Injury in Relation to Membrane Lipid Peroxidation in Creeping Bentgrass

^a Dep. of Horticulture, Forestry and Recreation Resources, Kansas State Univ., Manhattan, KS, 66506 USA

bhuang{at}oz.oznet.ksu.edu

	ABSTRACT

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Understanding physiological and biochemical factors involved in heat-stress injury would help improve heat tolerance of cool-season grasses. The objective of this study was to investigate lipid peroxidation of cell membranes in relation to heat-stress tolerance in creeping bentgrass (Agrostis palustris Huds.) . Two creeping bentgrass cultivars differing in heat tolerance, L-93 (heat tolerant) and Penncross (heat sensitive) were grown under two temperature regimes: 22/16°C (day/night) and 35/25°C for 56 d in growth chambers. Photochemical efficiency (Fv/Fm) and chlorophyll content of leaves; and electrolyte leakage (EL); content of the lipid peroxidation product, malondialdehyde (MDA); and activities of antioxidant enzymes including superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) in leaves and roots were determined biweekly during heat stress. Leaf Fv/Fm ratio and chlorophyll content decreased, whereas EL and MDA contents of both leaves and roots increased under heat stress in both cultivars, but to a greater extent in Penncross. The activities of SOD and CAT decreased, whereas POD activity increased in both leaves and roots, which occurred to a greater extent for Penncross. The increases in MDA content and POD activity under heat stress were greater for leaves than for roots in both cultivars. These results suggest that decreased activities of antioxidant enzymes could result in an increased level of lipid peroxidation. Thus, decreased activities of antioxidant enzymes could contribute to damage of cell membranes and to leaf senescence as demonstrated by increased EL and reduced Fv/Fm, and by decreased chlorophyll content during heat stress. Cultivar variations in antioxidant enzyme activities were associated with their differences in heat tolerance as evidenced by Fv/Fm ratio, chlorophyll content, and EL.

Abbreviations: CAT, catalase • EL, electrolyte leakage • Fv/Fm, photochemical efficiency • LSD, least significance difference • MDA, malondialdehyde • POD, peroxidase • SOD, superoxide dismutase

	INTRODUCTION

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GROWTH INHIBITION, leaf senescence, and even death of shoots and roots occur under heat stress in many cool-season grass species, especially creeping bentgrass at low mowing heights (Duff and Beard, 1974; Huang et al., 1998a, b; Martin and Wehner, 1987; Wehner and Watschke, 1981). Many physiological factors could be involved in heat stress injury. For example, heat stress inhibits photosynthesis (Paulsen, 1994; Santarius, 1975; Schreiber and Bilger, 1987); limits carbohydrate accumulation (Howard and Watschke, 1991; Huang and Gao, 1999, unpublished data; Liu and Huang, 1999, unpublished data); and can damage cell membranes (Blum and Ebercon, 1981; Marcum, 1998), leading to cell death (Abernethy et al., 1989). The adverse effects of heat stress also may be related to oxidative damage to cell membranes by active oxygen species, as found with low temperature, drought, and salinity stress (Bowler et al., 1992; Dhindsa and Matowe, 1981; Elstner, 1982; Zhang and Kirkham, 1994).

In aerobic biological systems, superoxide , hydrogen peroxide (H₂O₂), hydroxyl free radical (·OH), and singlet oxygen (¹O₂) are species of active oxygen derivatives that may attack and damage macromolecules in living cells (Foyer et al., 1994; Halliwel, 1984; Scandalios, 1993, 1994; Smirnoff, 1993). Plants have developed enzymatic and nonenzymatic scavenging systems to quench active oxygen, and to eliminate the detrimental effects of active oxygen. Superoxide dismutase (SOD) and catalase (CAT) break down and H₂O₂, respectively (Asada, 1992; Bowler et al, 1992; Elstner, 1982; Scandalios, 1993, 1994). The ascorbate-glutathione cycle is an alternative pathway to scavenge active oxygen (Alscher, 1989; Creissen et al., 1994; Foyer, 1993; Foyer et al., 1994). When plants are subjected to adverse conditions such as high or low temperature, drought, and salinity stresses, the scavenging system may lose its function and the balance between producing and quenching active oxygen species can be disturbed, resulting in oxidative damage (Bowler et al., 1992; Hodgson and Raison, 1991; Price et al., 1989; Zhang and Han, 1997; Zhang and Kirkham, 1994). Whether lipid peroxidation of cell membranes is associated with heat-stress injury in cool-season grasses, especially creeping bentgrass under close mowing conditions, is not clear.

The objective of this study was to examine changes in photochemical efficiency, cell membrane stability, activities of antioxidant enzymes, and lipid peroxidation level in leaves and roots during heat stress in two creeping bentgrass cultivars, L-93 and Penncross, which contrast in heat tolerance.

	Materials and methods

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Plant Materials
Sod of L-93 and Penncross was collected from a 2-yr-old field plot in the Rocky Ford Turfgrass Research Center, Kansas State University, and planted in polyvinyl chloride tubes (20 cm in diameter and 60 cm in length) filled with a mixture of 10% fritted clay (Profile, AIMCOR, Deerfield, IL) and 90% coarse sand. Turf was mowed daily to a 4-mm height with an electric clipper, watered daily until water drained from the bottom of tubes, and fertilized weekly with 40 mL of full-strength Hoagland's nutrient solution (Hoagland and Arnon, 1950).

Treatments
Grasses were maintained in growth chambers at 22/16°C (day/night) for about 2 mo, and then half of the plants were left at 22/16°C (control), and half of the plants were transferred to growth chambers of high temperature (35/25°C, day/night) by increasing the temperature by 4 to 5°C each day in a 3-d period. Grasses were exposed to 35/25°C for 56 d.

Measurements
Leaf photochemical efficiency, leaf chlorophyll content, cell membrane stability, activities of antioxidant enzymes, and levels of lipid peroxidation in leaves and roots were determined biweekly during heat stress. At 14, 28, 42, and 56 d of treatment, leaves were collected with an electric clipper, and roots were washed free of sand. Bulk samples of leaves and roots were stored separately for analysis.

Leaf photochemical efficiency was estimated by measuring chlorophyll fluorescence (Fv/Fm) with a plant photosynthesis efficiency analyzer (Hansatech, Hansatech Instrument LTD, Kings Lynn, England). Leaf chlorophyll was extracted by soaking 0.1 g of leaves in 8 mL of dimethyl sulfoxide in the dark for 72 h. Absorbance of the extractant at 663 nm and 645 nm was measured with a spectrophotometer (Hitachi U-1100, Hitachi Ltd, Tokyo, Japan). Chlorophyll content was calculated by the formula of Arnon (1949).

Cell membrane stability was estimated by measuring electrolyte leakage (EL). Samples of 0.1 g of leaves or roots were rinsed with deionized water, immersed in 20 mL of deionized water, and subjected to a vacuum of 48 kPa for 15 min. Then leaves and roots were shaken in flasks of deionized water on a shaker table (Lab-Line Instruments, Inc., Melrose Park, IL) for 24 h. The conductivity of the solution (C_initial) was measured using a conductivity meter (YSI Model 32, Yellow Spring, OH). Leaves and roots then were killed by autoclaving at 140°C for 20 min. The conductivity of killed tissues (C_max) was measured. Relative EL was calculated as the percentage of C_initial over C_max.

To extract antioxidant enzymes, 0.5 g fresh leaves and 1.0 g fresh roots randomly sampled from plants in each container were ground using a tissue grinder in 8 mL of 50 mM cool phosphate buffer [pH 7.0, containing 1% (w/v) polyvinylpyrrolidone] and 0.2 g of white quartz sand in tubes that were placed in an ice bath. The homogenate was centrifuged at 15000 x g for 20 min at 4°C. The supernatant was used for assays of enzyme activity and the level of lipid peroxidation.

The activity of SOD was determined by measuring its ability to inhibit the photoreduction of nitro blue tetrazolium (NBT) following the method of Giannopolitis and Ries (1977). The reaction solution (3 mL) contained 50 µM NBT, 1.3 µM riboflavin, 13 mM methionine, 75 nM EDTA, 50 mM phosphate buffer (pH 7.8), and 20 to 50 µL enzyme extract. Test tubes containing the reaction solution and leaves or roots were irradiated under a light bank (15 fluorescent lamps) at 78 µmol m^-2 s^-1 for 15 min. The absorbance of the irradiated and nonirradiated solution at 560 nm was determined with a spectrophotometer (Hitachi U-1100, Tokyo, Japan). One unit of SOD activity was defined as the amount of enzyme that would inhibit 50% of NBT photoreduction.

Activities of CAT and peroxidase (POD) were measured using the method of Chance and Maehly (1955) with modification. The CAT reaction solution (3 mL) contained 50 mM phosphate buffer (pH 7.0), 15 mM H₂O₂, and 0.1 mL enzyme extract. Reaction was initiated by adding enzyme extract. Changes in absorbance of the reaction solution at 240 nm were read every 20 s. One unit CAT activity was defined as an absorbance change of 0.01 units per min. The POD reaction solution (3 mL) contained 50 mM sodium acetate buffer (pH 5.0), 20 mM guaiacol, 40 mM H₂O₂, and 0.1 mL enzyme extract. Changes in absorbance of the reaction solution at 470 nm were determined every 20 s. One unit POD activity was defined as an absorbance change of 0.01 units per min.

The activity of each enzyme was expressed on a protein basis. Protein concentration of the crude extract was measured by the method of Bradford (1976).

The lipid peroxidation level was determined in terms of malondialdehyde (MDA) content by the method of Dhindsa et al. (1981) and Zhang and Kirkham (1994). A 2-mL aliquot of enzyme solution was added to a tube containing 1 mL 20% (v/v) trichloroacetic acid and 0.5% (v/v) thiobarbituric acid. The mixture was heated in a water bath at 95°C for 30 min, cooled to room temperature and then centrifuged at 10 000 x g for 10 min. The absorbance of supernatant at 532 nm was determined and the nonspecific absorbance at 600 nm was subtracted. The MDA content was calculated by the extinction coefficient of 155 mM^-1 cm^-1 (Heath and Packer, 1968).

Experimental Design and Statistical Analysis
Two cultivars were arranged randomly in each temperature treatment. Each temperature treatment was repeated four times in four growth chambers. The experimental design was considered to be a series of experiments repeated over temperatures (i.e., an experiment involved a specific temperature) with four tubes for each cultivar at each sampling time nested within temperature as described by Kempthorne (1952). Each measurement was replicated four times.

Effects of temperature, cultivars, days of sampling (time), and their interactions were determined by analysis of variance according to the general linear model procedure of Statistical Analysis System (SAS Institute, Cary, NC). Variation was partitioned into cultivar, temperature, and time as main effects and their corresponding interactions. Cultivar x temperature and cultivar x temperature x time interactions were significant at 0.05 probability for all the parameters. To define how each cultivar responded to heat stress over time, the analysis of temperature effects was conducted separately within each cultivar. Differences among treatment means were separated by the least significance difference (LSD) test at 0.05 probability level.

	Results

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Leaf Photochemical Efficiency (Fv/Fm) and Chlorophyll Content
The Fv/Fm ratio (Fig. 1) and chlorophyll content (Fig. 2) of both cultivars decreased under heat stress at 14, 28, 42, and 56 d of treatment. By 56 d, Fv/Fm and chlorophyll content of stressed plants were 34% and 51% lower than those of control plants, respectively, for L-93, and 36% and 72% lower, respectively, for Penncross. The cultivar L-93 retained significantly higher Fv/Fm and chlorophyll content than Penncross during heat stress.

View larger version (20K): [in this window] [in a new window]   Fig. 1 Leaf photochemical efficiencies (Fv/Fm) of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (20K): [in this window] [in a new window]   Fig. 2 Leaf chlorophyll contents of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (22K): [in this window] [in a new window]   Fig. 3 Cell membrane permeabilities in leaves and roots of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (23K): [in this window] [in a new window]   Fig. 4 Malondialdehyde (MDA) contents in leaves and roots of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (23K): [in this window] [in a new window]   Fig. 5 Superoxide dismutase activities in leaves and roots of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (24K): [in this window] [in a new window]   Fig. 6 Catalase activities in leaves and roots of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

View larger version (22K): [in this window] [in a new window]   Fig. 7 Peroxidase activities in leaves and roots of two creeping bentgrass cultivars as affected by high temperature (HT). Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

	Discussion

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The declines in Fv/Fm and chlorophyll content and increase in EL during heat stress were greater in Penncross than in L-93. Previous studies (Huang et al., 1998a, b) reported that L-93 was more tolerant to heat stress than Penncross, because L-93 was able to maintain higher turf quality, higher photosynthetic capacity, and more active root growth than Penncross during elevated temperatures. The cultivar L-93 also maintained a higher concentration of TNC in both shoots and roots during heat stress than Penncross (unpublished results). The results of this and other studies suggest that damage to the photosynthetic apparatus and cell membranes could be among the major physiological factors contributing to the decline of growth and quality in creeping bentgrass during heat stress. The detrimental effects of heat stress and cultivar variation in heat tolerance could be associated with levels of lipid peroxidation and activities of antioxidant enzymes. Under optimum temperature conditions, plants maintain a balance between producing and scavenging active oxygen species (Bowler et al., 1992). Heat stress may disturb this balance and promote lipid peroxidation, either by increasing the production of active oxygen or by decreasing the O₂ radical scavenging ability in the cell (Bowler et al., 1992).

The level of lipid peroxidation has been used as an indicator of free radical damage to cell membranes under stress conditions. Malondialdehyde (MDA) is a product of peroxidation of unsaturated fatty acids in phospholipids and is responsible for cell membrane damage (Halliwel and Gutteridge, 1989). Peroxidases constitute a set of enzymes that catalyze the oxidation of substrates by H₂O₂ (Asada, 1992). The MDA content and POD activity increased with heat stress in leaves and roots of both bentgrass cultivars. Such increases have been found in other species under drought (Zhang and Kirkham, 1994) and salt stress (Wang et al., 1988). The increases in POD activity suggests an accelerated production of activated oxygen species in tissues and high MDA content indicate membrane lipid peroxidation (Okuda et al., 1991). High POD activity could be associated with chlorophyll degradation during leaf senescence, and was likely induced by increased levels of superoxide radicals (Kato and Shimizu, 1985), resulting from the decline in SOD and CAT activities. The higher MDA content and POD activity in leaves and roots for Penncross than for L-93 under heat stress indicate that L-93 was better able to curtail lipid peroxidation. Furthermore, lipid peroxidation was greater in leaves than in roots of either cultivar. Lipid peroxidation can occur in both chloroplasts and mitochondria (Bowler et al, 1992; Elstner, 1982). Our results indicated that the higher MDA level in leaves than in roots may have been due to oxidative damage affecting both organelles in leaves; however, in roots only mitochondria were damaged because of the exposure to both high temperature and light.

Superoxide dismutase is the key enzyme in the active oxygen scavenger system because it catalyzes superoxide free radical dismutation into H₂O₂ and O₂ (Elstner, 1982; Bowler et al., 1992; Scandalios, 1993). The SOD activity increased at 14 d of heat stress and then decreased in leaves and roots of both cultivars starting at 28 d. Increased activity of SOD during short-term heat stress may provide protection from oxidative stress. However, MDA content increased in leaves and roots of both cultivars during the entire stress period. Apparently, the increase in SOD activity was less than the increase of production. Hence, a net increase of lipid peroxidation occurred within the first 14 d and was maintained after SOD activities decreased, particularly for Penncross. The damage to leaves and roots during prolonged periods of heat stress could be related to the reduction in SOD activity, which caused accumulation of , especially in chloroplasts and mitochondria.

The physiological role of CAT is to break down H₂O₂ in the cell (Scandalios, 1994). Thus, decreases in CAT activity would result in H₂O₂ accumulation, which can react with to produce hydroxyl-free radicals via the Herbert-Weiss reaction (Bowler et al, 1992; Elstner, 1982). The hydroxyl-free radicals can directly attack unsaturated fatty acids of lipid to induce lipid peroxidation in the cell. The CAT activity decreased in leaves and roots in both cultivars during the entire heat stress period, but occurred to a greater extent for Penncross than L-93. This also could have contributed to increases in lipid peroxidation as indicated by high MDA content. The decreases in activities of SOD and CAT and increases in POD activity indicated that the scavenger ability in the cells of leaves and roots was inhibited under heat stress conditions, which occurred to a greater extent for Penncross than L-93.

In summary, the results reported here, combined with previous research (Huang et al., 1998a, b; Huang and Gao, 1999, unpublished data), suggest that the decline in turf quality of creeping bentgrass cultivars with increasing temperature was associated with oxidative stress. The cultivar L-93 likely sustained a higher active O₂ scavenger ability during heat stress and thus experienced less lipid peroxidation and cell damage. This was manifested in higher cell membrane stability, higher chlorophyll content, and increased photochemical efficiency in L-93. Therefore, selection of grasses on the basis of these criteria may help to develop heat-tolerant creeping bentgrass cultivars and thereby reduce summer decline.

	ACKNOWLEDGMENTS

 
Research was supported by the Golf Course Superintendent's Association of America, Kansas Turfgrass Foundation, and Alfred Sloan Foundation. This is contribution no. 99-457-J from the Kansas Agricultural Experiment Station.

Received for publication May 27, 1999.

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