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Crop Science 41:430-435 (2001)
© 2001 Crop Science Society of America

TURFGRASS SCIENCE

Supraoptimal Soil Temperatures Induced Oxidative Stress in Leaves of Creeping Bentgrass Cultivars Differing in Heat Tolerance

Bingru Huanga, Xiaozhong Liub and Qingzhang Xub

a Dep. of Plant Science, Foran Hall, 59 Dudley Rd., Rutgers Univ., New Brunswick, NJ 08901
b Dep. of Horticulture, Forestry, and Recreation Resources, Kansas State Univ., Manhattan, KS 66506-5506

Corresponding author (Huang{at}aesop.rutgers.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
High temperature is a major factor limiting growth of cool-season grasses during summer months. The objective of this study was to determine whether oxidative stress is involved in leaf injury induced by high soil temperatures in two creeping bentgrass (Agrostis palustris Huds.) cultivars, heat-tolerant L-93 and heat-sensitive Penncross. Shoots and roots were exposed to four differential temperature regimes in growth chambers and water baths: (i) 20/20°C (control); (ii) 20/35°C (high soil temperature); (iii) 35/20°C (high air temperature); and (iv) 35/35°C (high shoot/soil temperatures). Turf quality, leaf photochemical efficiency (Fv/Fm), electrolyte leakage (EL), content of a lipid peroxidation product (malondialdehyde, MDA), and activities of the antioxidants superoxide dismutase (SOD) and catalase (CAT) were determined. Turf quality and leaf Fv/Fm ratio decreased, whereas EL and MDA contents increased under high soil temperature alone or in combination with high air temperature regimes in both cultivars, but to a greater extent in Penncross than in L-93. Decreases in turf quality and Fv/Fm ratio and increases in EL and MDA were more pronounced at 20/35°C than at 35/20°C. The activities of SOD and CAT decreased with prolonged periods of high temperatures and to a greater extent for Penncross than for L-93. The reductions in SOD and CAT activities were more severe at 20/35 than at 35/20°C. These results suggest that high soil temperature caused more severe oxidative damage to leaves than high air temperature by limiting antioxidant activities and inducing lipid peroxidation. This oxidative stress was associated with accelerated leaf senescence under high temperature conditions. Maintenance of antioxidant activities and low levels of lipid peroxidation was related to the better tolerance of creeping bentgrass to high soil temperature stress imposed on roots or high air temperature on shoots.

Abbreviations: CAT, catalase • Cinitial, initial conductivity • Cmax, maximum conductivity • EL, electrolyte leakage • Fv/Fm, photochemical efficiency • LSD, least significance difference • MDA, malondialdehyde • SOD, superoxide dismutase


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
IN WARM CLIMATE REGIONS, plant roots often are exposed to soil temperatures that reach injuriously high levels, which strongly influences shoot growth and even survival of whole plants especially for cool-season species (Paulsen, 1994). High soil temperatures inhibit growth and physiological activities of shoots (Aldous and Kaufmann, 1979; Kuroyanagi and Paulsen, 1988; Udomprasert et al., 1995; Xu and Huang, 2000a,b) and accelerate leaf senescence (Aldous and Kaufmann, 1979; Kuroyanagi and Paulsen, 1988). Kuroyanagi and Paulsen (1988) found that high soil temperatures induced shoot senescence directly in winter wheat (Triticum aestivum L.).

Leaf injury under high soil temperatures has been attributed to direct inhibition of root growth (Xu and Huang, 2000), hormone synthesis and transport (Udomprasert, et al., 1995), water uptake (Graves et al., 1991; Huang et al., 1991), and nutrient uptake (Gur and Shulman, 1979; Huang and Xu, 2000). Other biochemical processes may be involved in leaf senescence at high soil temperatures. They may damage shoots by inducing oxidative damage to cell membranes by active oxygen species, as do low temperature, drought, and salinity stress (Bowler et al., 1992; Zhang and Kirkham, 1994).

Environmental stresses induce production of active oxygen species such as superoxide , hydrogen peroxide (H2O2), hydroxyl radical (OH·), and singlet oxygen (1O2). They are highly reactive and can damage many important cellular components such as lipids, proteins, and nucleic acids in living cells (Smirnoff, 1993; Foyer et al., 1994). Plants have developed enzymatic and nonenzymatic scavenging systems to quench active oxygen species. When plants are subjected to stresses such as high temperatures, the scavenging system may lose its function and the balance between producing and quenching active oxygen species can be disturbed, resulting in oxidative damage (Price et al., 1989; Bowler et al., 1992; Zhang and Kirkham, 1994). Leaf injury and even death of whole plants occur as soil temperature exceeds the optimum range for root growth in creeping bentgrass (Huang et al., 1998; Liu and Huang, 2000). Whether leaf injury at high soil temperatures is associated with changes in antioxidant metabolism and oxidation of cell membranes in cool-season grasses is not clear.

The objectives of this study were (i) to compare the relative effects of high shoot, root, and shoot/soil temperatures on leaf physiological status and antioxidant metabolism in two creeping bentgrass cultivars, L-93 and Penncross, differing in heat tolerance; and (ii) to determine whether leaf injury induced at supraoptimal soil temperatures was related to oxidative stress. Leaf injury was evaluated by measuring leaf photochemical efficiency and membrane stability. Previous studies found that L-93 was more heat tolerant than Penncross (Huang et al., 1998; Liu and Huang, 2000).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Sods of creeping bentgrass cv. Penncross (heat sensitive) and cv. L-93 (heat tolerant) were collected from the Rocky Ford Turfgrass Research Center, Manhattan, KS, and transplanted to a mixture (9:1, v/v) of sand and fritted clay (Profile Products LLC., Deerfield, IL) in clear polyethylene bags (5 cm in diameter and 40 cm in length, with holes drilled at the bottom for drainage). The polyethylene bags were placed in polyvinylchloride (PVC) tubes of the same diameter and length, which were installed vertically in water baths with the lower open end exposed from the bottom of the water bath for drainage. These were designed in a way that enabled plant growth in well-drained soil, while soil temperature was controlled at a constant, predetermined level. Plants were kept in growth chambers at 20/15°C (day/night), a photosynthetic photon flux density of 400 µmol m-2 s-1, and a 13-h photoperiod for 40 d before differential shoot/soil temperature treatments were imposed. Before and during temperature treatments, turf was mowed daily at 3- to 4-mm height with electric hair clippers, watered daily until water drainage freely from the bottom of PVC tubes, and fertilized weekly with a full-strength Hoagland's nutrient solution (Hoagland and Arnon, 1950).

Shoots and roots were exposed to four air/soil temperature regimes: 20/20, 20/35, 35/20, and 35/35°C for 56 d. These test temperatures were chosen because 20°C is within the optimum range for the growth of cool-season grasses, and 35°C commonly occurs in the transitional and warm climatic regions during midsummer. Shoots were maintained at the ambient temperature (20 or 35°C) of the growth chambers, which was regulated by a temperature controller. Soil temperature was controlled by maintaining the entire root zone (40-cm-long soil column in a polyethylene bag) in water baths with predetermined temperatures (20 or 35°C). The low temperature was controlled by circulating cool water (18–20°C), and the high temperature with an immersion circulating heater (IC-2100, Fisher Scientific Inc. Pittsburgh, PA). Water was circulated continuously to maintain constant and uniform temperatures. Water levels were maintained at the top edges of both water baths during the experimental period.

Air temperatures at various distances from the canopy and soil temperatures at different depths from the soil surface were measured with thermocouples connected to a thermometer. The detailed temperature profile was described in Xu and Huang (2000a). In the 20/20°C treatment, both shoots and roots were maintained around 20°C; in the 20/35°C treatment, air temperature ranged from 23 to 25°C, and root-zone temperature was approximately 35°C; in the 35/20°C treatment, air temperature ranged from 32 to 35°C, whereas root-zone temperature ranged from 18 to 21°C; and in the 35/35°C treatment, air and root-zone temperatures were maintained at 33 to 36°C.

Temperature treatments were arranged in a completely randomized design with four replicates in repeated measurements randomly sampled each time as described in Xu and Huang (2000a)(b). Each of the two air temperatures (20 and 35°C) was replicated randomly in four growth chambers. High temperature and low temperature treatments were conducted sequentially in four chambers at each time. Each of two soil temperatures was replicated randomly in four water baths. Two water baths were placed in each growth chamber, with one being controlled at high soil temperature (35°C) and one at low soil temperature (20°C). All measurements were taken on four replicates sampled randomly from four chambers in each treatment at each measurement time. Effects of temperature and days of treatment (time) and their interactions were determined by analysis of variance (Kempthorne, 1952), according to the general linear model procedure of Statistical Analysis System (SAS Institute, Cary, NC). Differences between treatment means were determined by the least significance difference (LSD) test at the 0.05 probability level.

Turf quality was visually rated based on color, density, and uniformity on a scale of 0 (worst, all plant were dead and brown) to 9 (best, all plants were healthy and green).

Leaf photochemical efficiency was estimated by measuring chlorophyll fluorescence (Fv/Fm) with a plant photosynthesis efficiency analyzer (Hansatech Instrument LTD, Kings Lynn, England). Attached leaves were covered in a leaf chamber and adapted in dark for 20 min before Fv/Fm was measured.

Cell membrane stability was estimated by measuring electrolyte leakage (EL). Samples (0.1 g) of leaves were rinsed with deionized water, immersed in 20 mL deionized water, and subjected to a vacuum of 48 kPa for 15 min. Then leaves 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 (Cinitial) was measured with a conductivity meter (YSI Model 32, Yellow Spring, OH). Leaves then were killed by autoclaving at 140°C for 20 min, and the conductivity of killed tissues (Cmax) was measured. Relative EL was calculated as the percentage of Cinitial over Cmax.

Antioxidant responses were evaluated by measuring activities of catalase (CAT) and superoxide dismutase (SOD), the two most significant antioxidant enzymes in scavenging active oxygen species. Samples of 0.5 g fresh leaves were collected randomly from plants in each container and ground with a tissue grinder in 8 mL of 50 mM cool phosphate buffer [pH 7.0, containing 1% (w/v) polyvinylpyrrolidone] and 0.2 g white quartz sand. The homogenate was centrifuged at 15 000 g for 20 min at 4°C. The supernatant was used for assays of enzyme activity and also 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 were irradiated under a light bank (15 fluorescent lamps) at 78 µmol m-2 s-1 for 15 min. Absorbances of the irradiated and nonirradiated solutions at 560 nm were determined with a spectrophotometer (Hitachi U-1100, Tokyo, Japan). One unit of SOD activity was defined as the amount of enzyme that inhibits 50% of NBT photoreduction.

Activities of CAT were measured by the method of Chance and Maehly (1955) with modification. The 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 at 240 nm were read every 20 s. One unit of CAT activity was defined as an absorbance change of 0.01 per min.

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

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 of enzyme solution was added to a tube containing 1 mL of 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 g for 10 min. The absorbance of the supernatant at 532 nm was determined, and the nonspecific absorbance at 600 nm was subtracted. The MDA content was calculated with the extinction coefficient of 155 mM-1 cm-1 (Heath and Packer, 1968).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Turf Quality
Turf quality of both cultivars grown at 35/20°C was not different from the control at 20/20°C but was higher than that at 20/35°C and 35/35°C during the experimental period (Fig. 1) . At 35/35°C, quality of both cultivars declined to below the control level at 14 d of treatment. Turf quality at 20/35°C decreased to the level lower than the control, beginning at 14 d for Penncross and 28 d for L-93. Turf quality of both cultivars at 20/35 or 35/20°C was higher than that at 35/35°C from 14 to 42 d of treatment.



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  		Fig. 1. Turf visual quality of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 
There was no difference in turf quality between L-93 and Penncross at 20/20°C. However, L-93 had significantly higher quality than Penncross after 14 d at 35/20, 20/35, and 35/35°C.

Leaf Photochemical Efficiency and Electrolyte Leakage
Leaf Fv/Fm ratio of both cultivars was less than the control level (20/20°C) when roots (20/35°C), shoots (35/20°C), or both (35/35°C) were exposed to high temperatures; the decline was earlier and more severe at 35/35°C than at 20/35 and 35/20°C and at 20/35 than at 35/20 (Fig. 2) . The Fv/Fm ratios of L-93 and of Penncross were not significantly different at 20/20°C. However, L-93 had significantly higher Fv/Fm than Penncross after 30 d at 35/20, 20/35, and 35/35°C.



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  		Fig. 2. Leaf photochemical efficiencies (Fv/Fm) of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 
Leaf EL of both L-93 and Penncross increased at 20/35, 35/20, and 35/35°C but remained constant at 20/20°C during the entire experimental period (Fig. 3) . By 42 d, EL of heat-stressed plants was approximately 2, 3, and 4 times higher than that of the control plants (at 20/20°C) at 35/20, 20/35, and 35/35°C, respectively, for L-93, and 3, 4, and 5 times higher, respectively, for Penncross. At 14, 28, and 42 d of treatment, EL was significantly lower for L-93 than for Penncross at 20/35, 35/20, and 35/35°C. There was no difference in EL between the two cultivars at 20/20°C.



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  		Fig. 3. Cell membrane permeability expressed as electrolyte leakage of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 
Antioxidant Activity
At 14 d, SOD activity increased at 35/20°C, was unchanged at 20/35°C, and decreased at 35/35°C compared to that at 20/20°C for both cultivars (Fig. 4) . The SOD activity then declined to below the control level at 28 d at 20/35°C and 42 d at 35/20°C. The reductions in SOD activity were greater at 35/35°C than at 20/35 and 35/20°C and at 20/35°C than at 35/20°C. L-93 had higher SOD activity than Pencross under all three high temperature regimes.



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  		Fig. 4. Superoxide dismutase activity in leaves of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 
The CAT activities decreased significantly below their respective control levels, beginning at 14 d of all three high temperature regimes for both cultivars (Fig. 5) . The activity of CAT was significantly lower at 35/35°C than at 20/35 and 35/20°C and at 20/35 than at 35/20°C. The CAT activities were significantly higher for L-93 than Penncross at all high temperature regimes.



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  		Fig. 5. Catalase activity in leaves of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 
Lipid Peroxidation
The MDA contents increased significantly above their respective control levels under all three high temperature regimes for both cultivars, beginning at 14 d of treatment (Fig. 6) . By 42 d, MDA contents were 3.2, 1.9, and 1.6 times high than that of control plants at 35/35, 20/35, and 35/20°C, respectively, for L-93. For Penncross, the corresponding figures were 5.1, 2.5, and 2.0 times. L-93 maintained a significantly lower MDA content than Penncross under all three high temperature regimes.



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  		Fig. 6. Lipid peroxidation expressed as malondialdehyde content in leaves of two creeping bentgrass cultivars, L-93 (solid line and symbol) and Penncross (dotted line and open symbol), in response to differential air/soil temperature. Vertical bars indicate LSD values (P = 0.05) for treatment and cultivar comparisons at a given day

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Leaf photochemical efficiency as indicated by Fv/Fm ratio reflects the integrity of chloroplasts and is proportional to photosynthetic capacity (Schreiber and Bilger, 1987). Electrolyte leakage indicates cell membrane stability (Blum and Ebercon, 1981). Both parameters are used widely as indicators of stress injury or senescence in leaves (Schreiber and Bilger, 1987). The decreases in Fv/Fm and increases in EL under supraoptimal soil temperature alone or the combined high air/soil temperatures in both L-93 and Penncross corresponded to turf quality decline, which indicated that high temperatures, particularly high soil temperature or combined high air and soil temperatures, caused damage to leaves and accelerated leaf senescence. Heat-tolerant L-93 was able to maintain a higher turf quality and Fv/Fm ratio and lower EL under high temperatures than heat-sensitive Penncross. Leaf injury and turf quality was accentuated by heating roots while maintaining shoots at low temperatures and alleviated by lowering soil temperature while exposing shoots to high temperatures. The results suggested that shoot responses to soil temperatures were regulated by root responses in creeping bentgrass. Kuroyanagi and Paulsen (1988) reported that shoot growth and leaf senescence of winter wheat were influenced more by soil temperature than by air temperature.

The adverse effects of high soil temperature on shoot growth and physiological activities have been attributed to direct inhibition of root growth and activity and, therefore, limitation of water and nutrient supplies to the shoot (Kramer, 1983) and disruption of cytokinin synthesis in roots (Al-Khatib and Paulsen, 1984; Kuroyanagi and Paulsen, 1988; Smart et al., 1991). High soil temperature also promoted leaf senescence by increasing transport of root abscisic acid to the shoots (Udomprasert et al., 1995). Carbohydrate accumulation and translocation to roots is inhibited severely under high soil temperatures (Xu and Huang, 2000b). The present study suggested that injury in leaves induced by high soil temperature, as manifested by decreases in cell membrane stability and photochemical efficiency, could be attributed at least partially to oxidative stress. Environmental stresses such as drought, salinity, and high or low air temperatures are known to induce the production of active oxygen species, which are highly reactive and can bring about peroxidation of membrane lipids, leading to membrane damage (Levitt, 1980; Dhindsa et al., 1981). However, how high soil temperature causes oxidative stress in leaves merits investigation.

Plants normally develop antioxidant defense systems that scavenge active oxygen species and protect cells against oxidative stress injury (Bowler et al., 1992). Superoxide dismutase and CAT are the most effective antioxidant enzymes, and their combined effect averts cellular damage. Changes in the levels of antioxidants may be indicative of the levels of oxidative stress and stress resistance. Superoxide dismutase is responsible for scavenging O-2 to produce H2O2 and O2 (Bowler et al., 1992). In this study, SOD activity increased transiently during the initial periods of high air temperature but decreased rapidly at high root and shoot/soil temperatures. This indicated that the dismutation ability of SOD was able to increase transiently when shoots only were exposed to high temperature. However, heating roots while exposing shoots to low temperature impaired SOD activity, which could cause accumulation of O-2 and severe oxidative damage.

Catalase breaks down H2O2. Thus, decreases in CAT activity would result in accumulation of H2O2, which can react with O-2 to produce hydroxyl radicals via the Herbert-Weiss reaction (Bowler et al., 1992). The hydroxyl radicals can directly attack unsaturated fatty acids of lipid to induce lipid peroxidation in cells. The CAT activity decreased in both cultivars during the entire period of exposure to high shoot, root, or shoot/soil temperatures but to a greater extent at high soil temperature than high air temperature and for Penncross than L-93. A reduction in CAT activity also has occurred during short-time heat shock (Willekens et al., 1995; Dat et al., 1998).

The decreases in activities of SOD and CAT indicated that the scavenging ability in the cells of leaves was lowered under high temperature conditions. High soil temperature caused lower SOD and CAT activities than high air temperature. L-93 was better able to maintain SOD and CAT activities than Penncross during high temperature stress. Low CAT and SOD activities could be attributed to photoinactivation (Polle, 1997; Feierabend and Engel, 1986) or inhibition of their de novo synthesis in the dark (Dat et al., 1998), which favors the accumulation of active oxygen species and causes damage to cell membranes (Dhindsa et al., 1981).

The level of lipid peroxidation has been used as an indicator of free radical damage to cell membranes under stress conditions. Malondialdehyde is a final product of peroxidation of unsaturated fatty acids in phospholipids that often is used as a measure of level of lipid peroxidation (Halliwell and Gutteridge, 1989). The MDA contents in leaves of both cultivars increased under all three high temperature regimes. High soil temperature induced more severe lipid oxidation than high air temperature. L-93 was better able to curtail lipid peroxidation than Penncross at high shoot or/and soil temperatures. Even though SOD activity increased transiently when shoots only were exposed to high temperature, lipid peroxidation occurred during the initial stress period. Apparently, the transient increase in SOD activity at high air temperature was less than the increase of O-2 production or the decrease in CAT activity. An increasing MDA content indicates that membrane lipid peroxidation has occurred.

In summary, our results suggested that high soil temperature induced more damage to leaves and accelerated more severe leaf senescence, as demonstrated by reductions in leaf cell membrane stability and photochemical efficiency, than high air temperature in creeping bentgrass. Leaf injury under heat stress was associated with pronounced lipid peroxidation and decreases in antioxidative activity, particularly from exposing roots to high temperatures. Reducing soil temperature alleviated some of the detrimental effects of oxidative stress. The heat-tolerant cultivar L-93 maintained a higher ability to scavenge active O2 and was better able to curtail lipid peroxidation and cell membrane damage at high temperatures.


   ACKNOWLEDGMENTS
 
Research was supported by the United States Golf Association, and Kansas Turfgrass Foundation. This is contribution No. 00-268-J from the Kansas Agricultural Experiment Station.

Received for publication May 23, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 




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