Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass.
Various cultural practices such as irrigation, fertilization, and soil cultivation have been extensively investigated to improve turf performance in cool-season turfgrass during summer stress. However, limited information is available on the use of hormones or plant growth regulators in heat stress management for cool-season turfgrasses and results vary with chemistry types. Kentucky bluegrass plants treated with trinexapac-ethyl, a synthetic gibberellic acid inhibitor, were less heat tolerant than untreated plants (Heckman et al., 2002). Humic substances and seaweed extracts that contain phytohormones were reported to improve turfgrass stress tolerance in various turfgrass species (Zhang et al., 2003a, 2003b). Other organic compounds such as ascorbic acid were used as free radical scavengers to alleviate oxidative stress in various species (Zhang and Kirkham, 1996). Salicylic acid has been defined as a new potential plant hormone (Raskin, 1992a) and found to play an important role in disease resistance (Raskin, 1992b) and abiotic stress tolerance. Exogenous application of SA improved plant tolerance to heat (Dat et al., 1998), chilling (Janda et al., 1999), and salt stress (Borsani et al., 2001) in dicotyledons. Application of SA has recently been reported to increase heat tolerance in creeping bentgrass (Agrostis palustris Huds.) (Larkindale and Huang, 2004) and tall fescue (Festuca arundinacea Schreb.) seedlings (He et al., 2002). Improved heat tolerance in creeping bentgrass by application of SA was associated with its protection against oxidative damages (Larkindale and Huang, 2004).
Kentucky bluegrass is the most widely used cool-season turfgrass in temperate climates. Turf quality of Kentucky bluegrass often declines during summer. Previous studies in other plant species found that the effects of SA on heat tolerance were dose dependent. The potential benefits of exogenous SA in alleviating heat stress injury in Kentucky bluegrass have not been determined.
This study was designed to determine whether exogenous application of SA could improve heat tolerance in Kentucky bluegrass and whether SA-induced heat tolerance was related to oxidative protection by affecting [O.sup.*-.sub.2] generating rate, [H.sub.2][O.sub.2] content, and activities of antioxidant enzymes such as CAT and SOD.
MATERIALS AND METHODS
Sods of 3-yr-old 'Wabash' Kentucky bluegrass were collected from field plots on the farm of the College of Agriculture and Biology of Shanghai Jiaotong University in November 2001, and transplanted into plastic containers (7.6 cm in diam. and 20 cm in height, with holes pierced at the bottom for drainage, 90-100 plants per container) filled with clayey loamy soil (hydric haplaquent) (Soil Survey Staff, 1990) from the field plot. The containers of grass were first kept in a greenhouse under natural conditions for about 1 mo between November and December 2001 in Shanghai, China. The containers were then moved to a growth chamber (RXZ artificial chamber, Jiannan Equipment Factory, Ningbo, China) for 0.5 to 2 mo at a relative humidity of 50 to 70%, a 12-h photoperiod, a 25[degrees]C (day/night) temperature regime, and 400 [micro]mol [m.sup.-2] [s.sup.-1] of photosynthetically active radiation (PAR) at the canopy level under fluorescent and incandescent lights. Plants received a weekly application of 100 mL full-strength Hoagland's nutrient solution (Hoagland and Arnon, 1950) to maintain adequate nutrient levels. Turf was mowed once a week at a 6-cm height with a hand clipper.
Salicylic Acid and Heat Stress Treatment
Three independent experiments were conducted between January and March 2002. Experiment 1 was conducted to determine a suitable SA concentration for enhancing heat tolerance. Plants were sprayed with 100 mL of distilled water (control) or a range (0.1, 0.25, 0.5, 1.0, and 1.5 mmol) of SA dissolved in distilled water. All spray solutions, including distilled water controls, were adjusted to pH 7.0 with NaOH. Solutions were sprayed to the shoots uniformly using a hand-pump sprayer, which was sufficient to drench the soil in each container. Immediately after SA application, plants were exposed to 46 [+ or -] 0.5[degrees]C for 72 h in a growth chamber (ZYX-350B model, Qianjian Equipment Factory, Hangzhou, China) under 400 [micro]mol [m.sup.-2] [s.sup.-1] PAR for a 12-h photoperiod under fluorescent and incandescent lights. The treatments were arranged in a completely randomized plot design, with three replicates for each treatment (total of 18 containers of grass). After heat stress, plants were then returned to a day/night temperature of 15/10[degrees]C for recovery under natural lighting in a greenhouse in Shanghai, China, in February 2002. During heat stress, plants were watered daily to prevent leaf wilting due to high water demand under high temperature conditions. During the recovery in the greenhouse, plants were watered every 3 d and no clipping was performed. Plant survival ability was assessed by the recovery potential of plants 20 d following heat treatment. Heat tolerance was evaluated as plant height (length from the plant base to the tip) and green leaf index (leaf area ratio of green leaves to yellow leaves in each plant). Leaf area was estimated using the leaf length from base to tip multiplied by the width in the middle of the leaf blades. Five individual plants were randomly sampled from 90 to 100 plants in each container, and means of the five subsamples were used to represent a single replication in ANOVA.
Experiment 2 examined the effects of 0 and 0.25 mmol SA (the optimum concentration in Exp. 1) on [H.sub.2][O.sub.2] metabolism. Plants were treated, as in Exp. 1, with 0.25 mmol SA or water (control) and then exposed to 46 [+ or -] 0.5[degrees]C for 0, 0.5, 1, 2, and 12 h in two chambers regulated to 25 [+ or -] 0.5[degrees]C (for 0-h treatments, RXZ artificial chamber, Jiannan Equipment Factory, Ningbo, China) and 46 [+ or -] 0.5[degrees]C (for heat stress treatments, ZYX-350B model, Qianjian Equipment Factory, Hangzhou, China), respectively, under 400 [micro]mol [m.sup.-2] [s.sup.-1] of PAR with a 12-h photoperiod under fluorescent and incandescent lights as described in the section on plant culture. Each treatment was replicated four times with two subsamples for [H.sub.2][O.sub.2] content measurement and three subsamples for CAT activity measurement in a completely randomized design. Each mean of the subsamples was used as a single replication in ANOVA. Shoots were sampled at 0, 0.5, 1, 2, and 12 h of heat stress. One 0.5-g sample of fresh shoots (containing sheath and leaf blades) was used immediately after heat stress for [H.sub.2][O.sub.2] content determination, and another 0.5-g fresh shoot sample was frozen in liquid N2 and stored under -20[degrees]C until analysis for CAT activities. A third sample of 0.7 to 1.9 g was collected from each container to determine water content and tissue dry weight (DW).
In Exp. 3, leaves were only sampled at 0, 2, and 6 h before leaf wilting occurred to avoid the confounding effects of water deficit from heat stress on oxidative damage, because in Exp. 2 leaves started to show signs of water deficit or wilting 12 h after exposed to heat stress. This experiment was designed to investigate whether the effects of SA on heat tolerance were related to changes in [O.sup.*-.sub.2] metabolism. Treatments were the same as in Exp. 2. Each treatment was replicated four times in a completely randomized design with two subsamples for measurement of [O.sup.*-.sub.2] generation rate and four subsamples for SOD activity. Means of subsamples were used as a single replication in ANOVA. Two grams of fresh shoots were sampled at 0, 2, and 6 h of heat stress for measuring the [O.sub.2] generation rate and SOD activities. Water content and tissue DW was determined in remaining shoots as in Exp. 2.
Water Content Measurement
After fresh weight (FW) measurement, shoots were dried at 110[degrees]C for 1 h to kill tissues quickly to prevent respiratory weight loss and then dried at 70[degrees]C for 24 h in a forced-air oven. Dry shoots were weighed after being cooled to room temperature in a desiccator for 0.5 h. Water content was calculated using the formula
Water content (% FW) = (FW - DW) x 100/FW
Extraction of Enzymes, Superoxide Anion and Hydrogen Peroxide
For measurement of [O.sup.*-.sub.2] generation rate and CAT and SOD activities, shoots were ground in liquid N2 and extracted in 3 mL of ice-cold 50 mmol sodium phosphate buffer (PBS) (pH 7.0) (Sambrook et al., 1989), in an ice-water bath. The homogenate was centrifuged at 12 000 x g for 16 min at 4[degrees]C. Supernatant was stored at 4[degrees]C before measurement and in an ice-water bath during measurement of SOD or CAT activities and [O.sup.*-.sub.2] generation rate.
For [H.sub.2][O.sub.2] extraction, shoots were ground in liquid N2 and extracted in 5 mL of ice-cold acetone in an ice-water bath. The homogenate was centrifuged at 3 000 x g for 20 min. Supernatant was used for [H.sub.2][O.sub.2] measurement.
Antioxidant Enzyme Assays
Superoxide dismutase activity was determined by measuring its ability to inhibit the photochemical reduction of nitro blue tetrazolium chloride (NBT, 2,2'-di-p-nitrophenyl-5,5'-diphenyl-[3,3-dimethoxy-4,4'-diphenylene] ditetrazolium chloride) according to the method of Giannopolitis and Ries (1977), with slight modifications. The reaction solution (3 mL) contained 37 mmol PBS (pH 7.8), 4 x [10.sup.-3] mmol riboflavin (7,8-dimethyl-10-ribitylisoalloxazine), 13 mmol methionine [2-amino-4-(methylthio)-butyric acid], 1 x [10.sup.-4] mmol EDTA (ethylenedinitrilotetraacetic acid), 0.075 mmol NBT, and 50 [micro]L enzyme extract. Reaction solution was irradiated under incandescent lights at 1000 [micro]mol [m.sup.-2] [s.sup.-1] for 40 min. Absorbance of reaction solution at 560 nm was determined with a spectrophotometer (7230G, Shanghai Analytical Equipment Factory, Shanghai, China). One unit of enzyme activity was defined as the amount of the enzyme bringing 50% inhibition of the photochemical reduction of NBT.
Catalase activity was assayed by measuring the rate of decomposition of [H.sub.2][O.sub.2] at 240 nm in a reaction mixture consisting of 33.33 mmol PBS (pH 7.4) (He et al., 2001) and 15 mmol [H.sub.2][O.sub.2] (modified method of Aebi, 1984). One unit of enzyme was defined as a decrease in absorbance by 0.1 at 240 nm as [H.sub.2][O.sub.2] was decomposed. Spectrophotometric measurements were done using a spectrophotometer (UV751GD, Shanghai Analytical Equipment Factory, Shanghai, China).
[O.sup.*-.sub.2] and [H.sub.2][O.sub.2] Measurement
The [O.sup.*-.sub.2] level was determined by monitoring the [A.sub.530] of the product of the hydroxylamine reaction following the modified method of Elstner and Heupel (1976) as described by Wang and Luo (1990). One-milliliter supernatant of fresh shoot extraction was added to 0.9 mL 65 mmol PBS (pH 7.8) and 0.1 mL 10 mmol hydroxylammoniumchloride. The reaction was conducted at 25[degrees]C for 35 min. A 0.5-mL solution from the above reaction mixture was then added in 0.5 mL 17 mmol sulfanic acid and 0.5 mL 7.8 mmol a-naphthylamine solution. After 20 min of reaction, 2 mL of ether was added into the above solution, and then mixed well. The solution was centrifuged at 1500 x g at 4[degrees]C for 5 min. The absorbance of the pink supernatant was measured at 530 nm with the spectrophotometer (7230G model, Shanghai Analytical Equipment Factory, Shanghai, China). Absorbance values were calibrated to a standard curve generated with known concentrations of HN[O.sub.b2]. The 02 concentration was calculated as two times the concentration of HN[O.sub.b2] using the following formula [[O.sup.*-.sub.2]] = 2 x [HN[O.sub.b2]].
Hydrogen peroxide levels were measured by monitoring the A410 of the titanium-peroxide complex following some modifications of the method described by Patterson et al. (1984). One milliliter of cold acetone extracted supernatant was added to 0.1 mL 20% titanium reagent (20% w/v Ti[Cl.sub.4] in 12.1 mol HCl) and 0.2 mL 17 mol ammonia solution. The solution was centrifuged at 3000 x g at 4[degrees]C for 10 min and the supernatant was discarded. The pellet was dissolved in 3 mL 1 mol sulfuric acid. The absorbance of the solution was measured at 410 nm. Absorbance values were calibrated to a standard curve generated with known concentrations of [H.sub.2][O.sub.2]. Spectrophotometric measurements were done using a spectrophotometer (7230G, Shanghai Analytical Equipment Factory, Shanghai, China).
For each test, data were analyzed with an ANOVA using Microsoft Excel 2000 (Microsoft Corporation, Redmond, WA) (Levine et al., 2001), and mean separations were performed with the Fisher's protected LSD test at P = 0.05 (Steel and Torrie, 1980).
RESULTS AND DISCUSSION
Effects of Salicylic Acid on Turf Quality and Leaf Water Content
The regrowth potential following heat stress was significantly different among the treatments. Plant height and green leaf index treated with 0.25 mmol SA were significantly higher than those for other SA treatments or water control (Table 1). Plants treated with 0.25 mmol SA exhibited slightly less wilting than the plants treated with any other concentrations of SA (0.1, 0.5, 1.0 and 1.5 mmol) or water (control) after exposed to 46[degrees]C for 72 h (personal observation, data not shown). As observed in mustard (Sinapis alba L.) seedlings, beneficial effects of SA on enhancing heat tolerance were less at both lower and higher concentrations compared with the most effective concentrations (Dat et al., 1998, 2000).
Heat treatment at 46[degrees]C for 12 h reduced leaf water content significantly by 3.4% compared with plants at 25[degrees]C (Fig. 1). Plants treated with 0.25 mmol SA had 3.6% higher water content than SA-untreated plants under heat stress and maintained the water level similar to that of the plants (77%) at 25[degrees]C (Fig. 1).
[FIGURE 1 OMITTED]
These results demonstrated that application of the 0.25 mmol SA solution was the most effective concentration for improving heat tolerance in Kentucky bluegrass plants (Table 1, Fig. 1). Previous studies with other cool-season turfgrasses found that 0.5 mmol SA significantly increased heat tolerance in tall fescue seedlings (He et al., 2002), and 0.01 mmol SA was effective in increasing turf quality, leaf net photosynthetic rate, and suppressing lipid peroxidation in creeping bentgrass (Larkindale and Huang, 2004). The SA-enhanced heat tolerance has also been reported in dicotyledon species. For example, mustard seedlings sprayed with SA solutions between 0.01 and 0.5 mmol significantly improved their tolerance to a subsequent heat shock at 55[degrees]C (Dat et al., 1998). Low concentrations ([10.sup.-6] to [10.sup.-5] mol) of acetylsalicylic acid (ASA, derivative of SA) in the culture medium improved tolerance of potato (Solanum tuberosum L.) microplants to a 5-wk high temperature (35[degrees]C) treatment by 3.7-fold (Lopez-Delgado et al., 1998). Seed imbibitions or soil drenches with SA or ASA enhanced tolerance to heat, chilling, and drought stress in bean (Phaseolus vulgaris L.) and tomato (Lycopersicon esculentum Mill.) (Senaratna et al., 2000). Tobacco (Nicotiana tabacum L.) cv. Samsun grown in vitro for 4 wk on medium containing 0.01 mmol SA exhibited enhanced tolerance to a 4.5-h heat shock at 49[degrees]C (Dat et al., 2000). However, 0.1 mmol SA did not enhance thermotolerance, and caused reduction in shoot growth and leaf epidermal cell size (Dat et al., 2000). Our results, combined with others, suggest that foliar application of SA could be beneficial in improving heat tolerance in turfgrass management. The effects of SA on heat tolerance were dependent on specific concentrations, and may vary with plant species.
Effects of SA on AOS Production and Antioxidant Enzyme Activity
Superoxide anion generation in shoots of SA-treated and SA-untreated plants as a function of heat stress duration is shown in Fig. 2. Heat stress increased the [O.sup.*-.sub.2] generation rate significantly at 6 h compared with 0 h of heat stress. A significantly lower [O.sup.*-.sub.2] production rate was observed in SA-treated plants compared with that of SA-untreated plants during heat stress.
[FIGURE 2 OMITTED]
Superoxide dismutase activity increased significantly at 2 h of heat stress, but decreased to the control level at 6 h in SA-untreated plants (Fig. 3). The SA-treated plants maintained significantly higher SOD activity than SA-untreated plants at 6 h of heat stress. Salicylic acid has been found to increase SOD activity in Arabidopsis thaliana L. (Rao et al., 1997). In our study, the increases in SOD activity with SA application were accompanied by the decline in [O.sup.*-.sub.2] generation (Fig. 2), indicating that SA could reduce oxidative damage by maintaining SOD activity to remove the [O.sup.*-.sub.2].
[FIGURE 3 OMITTED]
Heat stress and SA influenced [H.sub.2][O.sub.2] accumulation in a time-dependent manner (Fig. 4). The [H.sub.2][O.sub.2] level in SA-untreated plants increased to the maximum level at 0.5 h of heat stress and then decreased to the control level at 1, 2, and 12 h of heat stress compared with that at 0 h of heat stress. The [H.sub.2][O.sub.2] level in SA-treated plants fluctuated before 2 h of heat stress. It significantly decreased at 0.5 h but increased to the maximum level at 1 h of heat stress and declined afterward. No significant difference was observed between the two maximum levels of [H.sub.2][O.sub.2] in SA-treated and SA-untreated plants. However, after 2 h of heat stress, a significantly lower [H.sub.2][O.sub.2] level was detected in SA-treated plants compared with SA-untreated plants.
[FIGURE 4 OMITTED]
Increases in AOS are typical plant responses to biotic and abiotic stress (Foyer et al., 1997), and [O.sup.*-.sub.2] and [H.sub.2][O.sub.2] levels have been shown to increase during heat stress in plant tissues (Foyer et al., 1997; Dat et al., 1998). In our study, the [H.sub.2][O.sub.2] level declined across time for both SA-untreated and SA-treated plants rather than continuing to rise or else rising to a steady state after the burst of [H.sub.2][O.sub.2] at 0.5 and 1 h of heat stress, respectively. Similar patterns of change in [H.sub.2][O.sub.2] level have been reported in other species. The mechanisms of such changes are not yet understood. For example, a peak in [H.sub.2][O.sub.2] content was observed within 5 min of 0.1 mmol SA solution applied at 24[degrees]C, but between 2 and 3 h after the SA treatment, [H.sub.2][O.sub.2] significantly decreased below control level in mustard seedlings (Dat et al., 1998). The [H.sub.2][O.sub.2] content increased markedly during the first 3 h of heat stress (42[degrees]C) treatment, and then decreased markedly to close to the control level in the following 3 h of the heat stress in maize (Zea mays L.) seedlings for two cultivars (Gong et al., 2001). Anderson and Padhye (2004) suggested that [H.sub.2][O.sub.2] did not play a direct role in acute heat stress injury in vinca [Catharanthus roseus (L.) G. Don] and sweet pea (Lathyrus odoratus L.). The fact that the lack of significant difference in the [H.sub.2][O.sub.2] peak value between SA-untreated and SA-treated plants (Fig. 4) indicates that the increase in [H.sub.2][O.sub.2] level at 0.5 and 1 h of heat stress was a stress response and not due to the effect of SA. Similar results were also reported in other species. Salicylic acid at < 1.0 mmol did not significantly increase the [H.sub.2][O.sub.2] level in Arabidopsis thaliana (Rao et al., 1997). It is reasonable to conclude that the influence of SA on [H.sub.2][O.sub.2] level under heat stress is also dose dependent. The burst of [H.sub.2][O.sub.2] at an early stage of heat stress might be a signal of heat stress, but was not significantly increased by 0.25 mmol SA that was the most effective concentration for heat tolerance induction in Kentucky bluegrass.
The CAT activity increased to the maximum at 0.5 and 1 h of heat stress and decreased thereafter in both SA-untreated and SA-treated plants, respectively (Fig. 5). The SA-treated plants had higher CAT activity than untreated plants during the entire stress period. The results differed from the general responses in disease defense studies (Chen et al., 1993; Conrath et al., 1995; Scandalios, 1993). However, the influence of SA on CAT was also dose-dependent and varied with plant species. Salicylic acid < 0.25 mmol in tobacco (Bi et al., 1995), < 2 mmol in barley (Hordeum vulgare L.) (Song et al., 1998), and = 1.0 mmol in rice (Oryza sativa L.) (Sanchez-Casas and. Klessig, 1994) did not inhibit CAT activities. In the present study, increased CAT activities induced by 0.25 mmol SA application were consistent with previous studies. During late embryogenesis in maize, total CAT activity in scutella increased dramatically with 1 mmol SA treatment, which was contributed to the accumulation of CA[T.sub.2] transcript (Guan and Scandalios, 1995). Salicylic acid at 0.5 mmol resulted in an increase in CAT activity under normal temperature (25[degrees]C) and suppression of decrease in CAT activities under heat stress (42[degrees]C) in tall fescue seedlings (He et al., 2002).
[FIGURE 5 OMITTED]
Catalase is important for maintenance of normal cellular processes under stress conditions (Guan and Scandalios, 1995). In our study, the temporary reduction of [H.sub.2][O.sub.2] (Fig. 4) corresponded to the increase in CAT activities (Fig. 5) in SA-treated plants, compared with plants at 0 h of heat stress. This result implied that the increase in CAT activity induced by SA under heat stress was greater than the increase of [H.sub.2][O.sub.2] caused by heat stress, which means that the [H.sub.2][O.sub.2] generation caused by heat stress was less than the [H.sub.2][O.sub.2] scavenging at 0.5 h of heat stress in SA-treated plants. The suppression of decreases in CAT activity with SA treatment (Fig. 5) corresponded to the significantly lower [H.sub.2][O.sub.2] level at 2 and 12 h of heat stress (Fig. 4) compared with SA-untreated plants, which suggests that SA may help protect plants from excessive [H.sub.2][O.sub.2] production by promoting CAT activity.
Taken together with the effects of SA on [O.sup.*-.sub.2] (Fig. 2) and [H.sub.2][O.sub.2] production (Fig. 4), SOD (Fig. 3) and CAT (Fig. 5) activities, our results suggest that SA-induced heat tolerance could be related to higher [O.sup.*-.sub.2] and [H.sub.2][O.sub.2] scavenge potential due to higher SOD and CAT activities under heat stress. Our results in Kentucky bluegrass agree with the reports in Arabidopsis and creeping bentgrass that SA is involved in protection against heat stress-induced oxidative damage (Larkindale and Knight, 2002; Larkindale and Huang, 2004).
In summary, the present study demonstrated that application of 0.25 mmol SA improved heat tolerance of Kentucky bluegrass in controlled environmental conditions and SA-induced heat tolerance was related to AOS scavenging by increasing SOD and CAT activities in Kentucky bluegrass. Further tests are needed to determine the efficacy of SA in improving heat tolerance of cool-season turfgrasses under field conditions.
Abbreviations: AOS, active oxygen species; ASA, acetylsalicylic acid; CAT, catalase; DW, dry weight; FW, fresh weight; [H.sub.2][O.sub.2], hydrogen peroxide; NBT, nitro blue tetrazolium chloride; [O.sup.*-.sub.2], superoxide anion; PAR, photosynthetically active radiation; PBS, sodium phosphate buffer; SA, salicylic acid; SOD, superoxide dismutase.
Table 1. Plant height and green leaf index of Kentucky bluegrass at 20 d recovery from heat stress (46[degrees]C) as influenced by salicylic acid (SA). Green leaf SA treatment Plant height ([dagger]) index ([double dagger]) mmol cm 0 11.0d ([section]) 0.79b 0.1 12.6bc 1.07b 0.25 15.2a 3.76a 0.5 12.8bc 1.42b 1 13.4b 1.18b 1.5 12.0cd 1.47b LSD (0.05) 1.12 1.781 ([dagger]) Length from the plant base to the tip. ([double dagger]) Leaf area ratio of green leaves to yellow leaves in each plant. ([section]) Values followed by the same letter within each column are not significantly different at P = 0.05.
Aebi, H. 1984. Catalase in vitro. Methods Enzymol. 105:121-126. Anderson, J.A., and S.R. Padhye. 2004. Protein aggregation, radical scavenging capacity, and stability of hydrogen peroxide defense systems in heat-stressed vinca and sweet pea leaves. J. Am. Soc. Hortic. Sci. 129:54-59.
Bi, Y.M., P. Kenton, L. Murr, R. Darby, and J. Draper. 1995. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 8:234-245.
Borsani, O., V. Valpuesta, and M.A. Botella. 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126:1024-1030.
Bowler, C., M.V. Montagu, and D. Inze. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:83-116.
Chen, Z., H. Silva, and D.F. Klessig. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science (Washington, DC) 262:1883-1886.
Conrath, U., Z. Chen, J.R. Ricigliano, and D.F. Klessig. 1995. Two inducers of plant defense responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. USA 92:7143-7147.
Dat, J.F., H. Lopez-Delgado, C.H. Foyer, and I.M. Scott. 1998. Parallel changes in [H.sub.2][O.sub.2] and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116:1351-1357.
Dat, J.F., H. Lopez-Delgado, C.H. Foyer, and I.M. Scott. 2000. Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J. Plant Physiol. 156:659-565.
Elstner, E.F., and A. Heupel. 1976. Inhibition of nitrite formation from hydroxylammonium-chloride: A simple assay for superoxide dismutase. Anal. Biochem. 70:616-620.
Foyer, C.H., P. Descourvieres, and K.J. Kunert. 1994. Protection against oxygen radicals: An important defense mechanism studied in transgenic plants. Plant Cell Environ. 17:507-523.
Foyer, C.H., H. Lopez-Delgado, J.F. Dat, and I.M. Scott. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol. Plant. 100:241-254.
Giannopolitis, C.N., and S.K. Ries. 1977. Superoxide dismutases. I. Occcurrence in higher plants. Plant Physiol. 59:309-314.
Gong, M., B. Chen, Z.G. Li, and L.H. Guo. 2001. Heat-shock-induced cross adaptation to heat, chilling, drought and salt stress in maize seedlings and involvement of [H.sub.2][O.sub.2]. J. Plant Physiol. 158:1125-1130.
Guan, L., and J.G. Scandalios. 1995. Developmentally related responses of maize catalase genes to salicylic acid. Proc. Natl. Acad. Sci. USA 92(13):5930-5934.
He, Y.L., Y.L. Liu, Q. Chen, and A.H. Bian. 2002. Thermotolerance related to antioxidation induced by salicylic acid and heat acclimation in tall rescue seedlings. (In Chinese, with English abstract.) J. Plant Physiol. Mol. Biol. 28:89-95.
He, Y.L., Y.L. Liu, Q. Chen, A.H. Bian, and W. Chen. 2001. Optimal pH for four antioxidant enzymes in the seedlings of tall fescue and Kentucky Bluegrass. (In Chinese, with English abstract.) J. Nanjing Agric. Univ. 24:1-4.
Heckman, N.L., G.L. Horst, R.E. Gaussoin, and B.T. Tavener. 2002. Trinexapac-ethyl influence on cell membrane thermostability of Kentucky bluegrass leaf tissue. Sci. Hortic. (Canterbury, Engl.) 92: 183-186.
Hoagland, C.R., and D.I. Arnon. 1950. The solution-culture method for growing plants without soil. Circ. 347. California Agric. Exp. Stn., Tulare.
Janda, T., G. Szalai, I. Tari, and E. Paldi. 1999. Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175-180.
Kraus, T.E., and A. Fletcher. 1994. Palclobutrazol protects wheat seedlings from heat and paraquat injury. Is detoxification of active oxygen species involved? Plant Cell Physiol. 35:45-52.
Larkindale, J., and B. Huang. 2004. Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethyelene. J. Plant Physiol. 161:405-413.
Larkindale, J., and M.R. Knight. 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128:682-95.
Levine, D.M., P.P. Ramsey, and R.K. Smidt. 2001. Applied statistics for engineers and scientists: Using Microsoft Excel and MINI-TABLE. Prentice Hall, Upper Saddle River, NJ.
Liu, X., and B. Huang. 2000. Heat stress injury of creeping bentgrass in relation to membrane lipid peroxidation. Crop Sci. 40:503-510.
Lopez-Delgado, H., J.F. Dat, C.H. Foyer, and I.M. Scott. 1998. Induction of thermotolerance in potato microplants by acetylsalicylic acid and [H.sub.2] [O.sub.2]. J. Exp. Bot. 49:713-720.
Patterson, B.D., E.A. MacRae, and I.B. Ferguson. 1984. Estimation Of hydrogen peroxide in plant extracts using titanium (IV). Anal. Biochem. 139:487-492.
Rao, M.V., G. Paliyath, D.P. Ormrod, D.P. Murr, and C.B. Watkins. 1997. Influence of salicylic acid on [H.sub.2][O.sub.2] production, oxidative stress, and [H.sub.2] [O.sub.2]--metabolizing enzymes. Plant Physiol. 115:137-149.
Raskin, I. 1992a. Salicylate, a new plant hormone. Plant Physiol. 99: 799-803.
Raskin, I. 1992b. Role of salicylic acid in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:439-463.
Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning. Cold Spring Harbor Laboratory Press, Woodbury, NY.
Sanchez-Casas, P., and D. Klessig. 1994. A salicylic acid-binding activity and a salicylic acid inhibitable catalase activity are present in variety of plant species. Plant Physiol. 106:1675-1679.
Scandalios, J.G. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101:7-12.
Senaratna, T., C.E. McKay, B.D. McKersie, and R.A. Fletcher. 1988. Uniconazole induced chilling tolerance in tomato and its relationship to antioxidant content. J. Plant Physiol. 133:56-61.
Senaratna, T., D. Touchell, E. Bunn, and K. Dixon. 2000. Acetyl Salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Reg. 30:157-161.
Soil Survey Staff. 1990. Key to soil taxonomy. Virginia Polytechnic Inst. and State Univ., Blacksburg.
Song, Z.S., G.Y. Jiang, Y.C. Lu, and Y.X. Zhu. 1998. Decrease of mRNA content of CAT gene induced by salicylic acid. (In Chinese.) Sci. Rep. Sin. 43:422-425.
Steel, R.G.D., and J.H. Torrie. 1980. Principles and procedures of statistics. 2nd ed. McGraw-Hill, New York.
Wang, A.G., and G.H. Luo. 1990. Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. (In Chinese.) Plant Physiol. Comm. 6:55-57.
Zhang, X., E.H. Ervin, and R.E. Schmidt. 2003a. Physiological effects of liquid applications of a seaweed extract and humic acid on creeping bentgrass. J. Am. Soc. Hortic. Sci. 128:402-406.
Zhang, X., E.H. Ervin, and R.E. Schmidt. 2003b. Plant growth regulators can enhance the recovery of Kentucky bluegrass sod from heat injury. Crop Sci. 43:952-956.
Zhang, J., and M.B. Kirkham. 1996. Lipid peroxidation in sorghum and sunflower seedlings as affected by ascorbic acid, benzoic acid, and propyl gallate. J. Plant Physiol. 149:489-493.
Yali He, Youliang Liu, Weixing Cao, Mingfang Huai, Baogang Xu, Bingru Huang *
Y. He, M. Huai, and B. Xu, College of Agriculture and Biology, Shanghai Jiaotong Univ., Shanghai 201101, China; Y. He, Y. Liu, and W. Cao, Agricultural College, Nanjing Agricultural Univ., Nanjing 210095; B. Huang, Dep. of Plant Science, Cook College, Rutgers Univ., New Brunswick, NJ 08901-8520. Received 17 Dec. 2003. Turfgrass Science. * Corresponding author (firstname.lastname@example.org).
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|Author:||He, Yali; Liu, Youliang; Cao, Weixing; Huai, Mingfang; Xu, Baogang; Huang, Bingru|
|Date:||May 1, 2005|
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