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Effects of abscisic acid on antioxidant systems of Stylosanthes guianensis (Aublet) Sw. under chilling stress.

REACTIVE OXYGEN SPECIES (ROS), including [O.sup.-.sub.2], hydrogen peroxide ([H.sub.2][O.sub.2]), hydroxyl free radical (*OH) and singlet oxygen ([sup.1][O.sup.2]), are normal metabolites of plants (Pastori et al., 2000; Scandalios, 1993; Iannelli et al., 1999). The plant antioxidant apparatus includes enzymatic scavenging and nonenzymatic scavenging systems. The former includes SOD, CAT, peroxidase (POD), APX, and glutathione reductase (GR). Nonenzymatic scavenging system includes ascorbic acid, reduced GSH, carotenoids, and vitamin E. The balance of ROS production and scavenging is destroyed under stress conditions such as chilling, which leads to accumulation of ROS and resulting in lipid peroxidation of cell membranes (Thompson et al., 1987; Hodgson and Raison, 1991).

Abscisic acid plays an important role in the response to low temperature and is correlated with the enhancement of chilling resistance in some plant species (Bravo et al., 1998; Machackova et al., 1989). A mutant of Arabidopsis deficient in ABA was unable to cold-acclimate unless treated with exogenous ABA (Heino et al., 1990). Exogenous ABA treatment enhances the chilling resistance of maize (Zea mays L.) seedlings (Anderson et al., 1994; Prasad et al., 1994a). A chilling resistant banana (Musa spp.) cultivar accumulated higher levels of ABA than the chilling sensitive one under chilling conditions (Zhou et al., 1995). ABA is involved in the expression of numerous stress-induced genes and in the production of stress-induced proteins; it also induces gene expression independent of stress (Chandler and Robertson, 1994). Following exposure of plants to various water-deficit-related stresses, including desiccation, water stress, high osmolarity, and low temperature, a group of proteins named dehydrins are induced in castor bean (Ricinus communis L.) (Han and Kermode, 1996). ABA induces dehydrin gene expression (Han et al., 1997) and helps to maintain a favorable water balance in cotton (Gossypium L.) (Rikin et al., 1979) by induction of stomatal closure and by regulating the contents of soluble sugars, soluble protein, and proline (Bravo et al., 1998). ABA also induces antioxidant systems (Prasad et al., 1994b). Application of ABA in maize had greater biomass accumulation than an untreated control under NaCl stress (Khan and Srivastava, 1998). However, ABA has not been used practically because it is expensive. In recent years, a low prices (S)-ABA was biosynthetically produced in China, which allows its potential application for protection of crops against abiotic stresses.

Stylosanthes guianensis originated in the tropics and is an important pasture legume with high yield and quality, acidity-tolerance, and adaptation to low fertility soil in tropical and subtropical countries (Guodao et al., 1997; Meijer and Broughton, 1981; Miles and Grof, 1997; Miles and Lascano, 1997). It is also an important intercrop in orchards and rubber plantations (Jiang et al., 1999). Chilling injury of S. guianensis is a serious problem in subtropical cultivated areas. Chilling injury and its regulation in S. guianensis has not been studied. In a preliminary experiment, ABA was found to improve the chilling resistance of S. guianensis. It is thus hypothesized that the cold tolerance of S. guianensis could be improved by ABA treatment.

An experiment was conducted under controlled condition with the objective to determine the chilling injury and antioxidant systems in S. guianensis. Specifically, we determined the relative water content; electrolyte leakage; activities of SOD, CAT, and APX; and contents of AsA and GSH in S. guianensis leaves subjected to chilling stress after treated with ABA.

MATERIALS AND METHODS

Plant Material

Seeds of S. guianensis cv. CIAT184 were soaked in hot (80[degrees]C) water for 5 rain, then rapidly cooled to room temperature and soaked again in cold water overnight. The seeds were sown in 15-cm diam plastic pots containing mixture of peat and perlite (3:1, v/v) for germination. Seedlings were grown under natural light in a greenhouse with temperature from 25 to 30[degrees]C and irrigated daily. Stylosanthes guianensis grows very slowly during its seedling stage. Fifteen plants of similar size were reserved in a single pot, and fertilization was applied by irrigating 0.3% of N-P-K fertilizer (15-15-15) solution once a week after plants were 4 wk old and used for the study when they were 8 wk old.

Experiment Procedures

In the preliminary experiment for selection of the effective concentration of ABA for increasing chilling resistance of S. guianensis, seedlings were sprayed uniformly with 0, 2, 5, 10, 15, 20, 30 mg [L.sup.-1] of (S)-ABA (90% powder, Lomon Bio Technology Co, Ltd., Sichuan Province, China) containing 0.01% (v/v) Tween-20 (polysorbate 20), until the canopy was completely wetted. One day later, plants were transferred to a 10[degrees]C growth chamber with a 12-h photoperiod at 160 [micro]mol [m.sup.-2] [s.sup.-1] photosynthetic photon flux density. The seedlings sprayed with water remained in a 28[degrees]C growth chamber as an unchilled control with a 12-h photoperiod at 160 [micro]mol [m.sup.-2] [s.sup.-1] photosynthetic photon flux density. The plant pots were placed in a completely randomized design in growth chamber and grown for 4 d. Leaflet samples were taken from each pot of plants and used for the measurement of electrolyte leakage after chilling treatment. The experiment consisted of seven treatments under chilling plus an unchilled control and four replications. The experiment was repeated twice over time.

To investigate the effect of ABA on antioxidant system and its relation to chilling resistance, an experiment involving two levels of ABA and two levels of temperature (10 and 28[degrees]C) was arranged in a split-plot design with three replications. Each treatment x temperature combinations consisted of three pots, which were later on used for sampling and analysis. Plants were sprayed uniformly with 10 mg L-] of (S)-ABA or water as control. The plants were moved to growth chambers with a 12-h photoperiod at 160 [micro]mol [m.sup.-2] [s.sup.-1] photosynthetic photon flux density at 28[degrees]C or 10[degrees]C. The chilled plants were rewarmed to 28[degrees]C for 2 d after 7 d of chilling treatment. At 9 d after treatment, leaflet samples were taken from each pot of ABA x temperature treatment combinations for the following measurements. The experiment was also repeated twice within an 8-too period.

Electrolyte Leakage

Electrolyte leakage was determined according to the method of Blum and Ebercon (1981). Samples of six leaflets were rinsed with distilled water and immersed in 6 mL of distilled water for 12 h. The conductivity of the solution (R1) was measured with a conductivity meter (Model DDS-11A, Shanghai Leici Instrument Inc., Shanghai, China). Samples were then heated in boiling water for 20 min and then cooled to room temperature. The conductivity of killed tissues (R2) was again measured. Electrolyte leakage was calculated as the ratio of R1 to R2.

Relative Water Content

Fresh leaves (0.5 g; [W.sub.f]) were rinsed in water for several hours until the weight of the leaves was constant. The saturated leaves were weighed ([W.sub.s]) and then dried for 24 h at 80[degrees]C for determinations of the dry weigh ([W.sub.d]). Relative water content (RWC) was calculated by the following formula: RWC = ([W.sub.f] - [W.sub.d])/([W.sub.s] - [W.sub.d]) x 100%.

Superoxide Dismutase and Catalase Activity

Fresh leaves (0.5 g) were ground in a mortar and pestle in 5 mL of 50 mM cool phosphate buffer (pH 7.8) containing 2% (w/v) polyvinylpolypyrrolidone (PVP). The homogenates were centrifuged at 13 000 x g for 20 min at 4[degrees]C. The supernatants were used for assays of enzyme activity.

Superoxide dismutase activity was determined according to the method of Giannoplitis and Ries (1977). The 3-mL reaction solution contained 13 [micro]M methionine, 63 [micro]M p-nitro blue tetrazolium chloride (NBT), 1.3 [micro]M riboflavin, 50 mM phosphate buffer (pH 7.8), and enzyme extract. The reaction solution was incubated for 10 min under fluorescent light with 80 [micro]mol [m.sup.-2] [s.sup.-1]. Absorbance was determined at 560 nm with a spectrophotometer (Model UV-2010, Hitachi, Japan). One unit of SOD activity was defined as the amount of enzyme required for inhibition of photochemical reduction of NBT by 50%.

Catalase activity was determined spectrophotometerically by following the decrease of absorbance of [H.sub.2][O.sub.2] (extinction coefficient 39.4 m[M.sup.-1] [cm.sup.-1]) within 1 min at 240 nm according to the method of Chance and Maehly (1955). The 3-mL reaction solution contained 15 mM [H.sub.2][O.sub.2], 50 mM phosphate buffer (pH 7.0), and 50 [micro]L of enzyme extract. The reaction was initiated by adding enzyme extract.

Protein content in enzyme extracts was determined according to the method of Bradford (1976). Twenty-five microliters of enzyme extract was added to 3 mL of 0.01% (w/v) Coomassie Brilliant Blue G-250 solution [4.7% (w/v) ethanol, 8.5% (w/v) phosphoric acid]. The absorbance at 595 nm was spectrophotometerically recorded after protein-dye binding for 5 min. Protein content was calculated by comparison to a standard curve made with bovine serum albumin as a standard.

Ascorbate Peroxidase Activity

Ascorbate peroxidase activity was determined spectrophotometrically according to the method of Nakano and Asada (1981). Leaves (0.3 g) were ground in a mortar and pestle in 3 mL of 50 mM cool phosphate buffer (pH 7.0, containing 1 mM AsA, 1 mM EDTA). The homogenates were centrifuged at 13 000 x g for 20 min at 4[degrees]C. The supernatants were used for assays of enzyme activity. The 3-mL reaction solution contained 50 mM phosphate buffer (pH 7.0), 0.5 mM AsA, 0.1 mM H202, and 0.1 mL enzyme extract. APX activity was calculated by following the decrease in absorbance of AsA (extinction coefficient 2.8 m[M.sup.-1] [cm.sup.-1]) within 1 min at 290 nm.

Ascorbic Acid and Reduced Glutathione Contents

Fresh leaves (0.3 g) were ground in a mortar and pestle in 3 mL of 5% (v/v) trichloroacetic acid. The homogenates were centrifuged at 10 000 x g for 15 min at 4[degrees]C. The supernatants were used for assays of AsA and GSH contents.

Ascorbic acid content was determined according to the method of Law et al. (1983). Supernatant (0.4 mL) was combined with 0.2 mL of 150 mM Na[H.sub.2]P[O.sub.4] (pH 7.7). To this mixture 0.4 mL of 10% (v/v) TCA, 0.4 mL of 44% (v/v) [H.sub.3]P[O.sub.4], 0.4 mL of 4% (w/v) bipyridyl (in 70% alcohol), and 0.2 mL of 3% Fe[Cl.sub.3] (w/v) was successively added. The mixture was incubated at 37[degrees]C for 1 h. Absorbance was determined at 525 nm. AsA concentration was calculated by comparison to a standard curve.

Reduced glutathione content was measured according to the method of Ellman (1959). Supernatant (0.2 mL) was added to 2.6 mL of 150 mM Na[H.sub.2]P[O.sub.4] (pH 7.4). Two hundred microliters of 5,5'-dithio-bis(2-nitrobenzoic) (DTNB) (75.3 mg of DTNB was dissolved in 30 mL of 100 mM phosphate buffer, pH 6.8) was then added. The mixture was incubated at 30[degrees]C for 5 min. Absorbance was determined at 412 nm and the GSH concentration was calculated by comparison to a standard curve.

Experimental Design and Statistical Analysis

All data were subjected to analysis of variances according to the model for completely randomized or a split plot design using a SPSS program (SPSS Inc.). Differences among treatment means were evaluated by the least significant difference (LSD) test at 0.05 probability level when the F test showed a significant (P [less than or equal to] 0.05) effect.

RESULTS

In the preliminary experiment (Fig. 1), electrolyte leakage was used to screen the effective concentration of ABA for increased chilling resistance of S. guianensis. Among the six concentrations of ABA tested, spraying ABA at 10 mg [L.sup.-1] was most effective in decreasing electrolyte leakage of S. guianensis under chilling conditions (Fig. 1). Therefore, 10 mg [L.sup.-1] ABA was used for further experiments to study its effect on chilling resistance and antioxidant systems.

[FIGURE 1 OMITTED]

The control plants grown at 28[degrees]C had a low level of electrolyte leakage. Electrolyte leakage of water-treated plants increased by 17% after chilling for 5 d, indicating that S. guianensis was only slightly damaged by the chilling treatment. It increased to over 30% after chilling for 7 d (Fig. 2A). Electrolyte leakage of ABA-treated plants increased under chilling conditions, but was lower than that of water-treated plants. When plants were rewarmed, electrolyte leakage decreased, indicating that the plants recovered (Fig. 2).

[FIGURE 2 OMITTED]

Relative water content in control plants remained high during the experimental period. Under chilling conditions, RWC decreased rapidly in water-treated plants and wilting occurred at Day 3 after chilling treatment, while ABA-treated plants retained much higher RWCs. RWC increased to control levels after the water- and ABA-treated plants were rewarmed for 2 d (Fig. 3).

[FIGURE 3 OMITTED]

Superoxide dismutase activity showed little change in control plants during the experimental period. Under chilling conditions, SOD activity in water-treated plants remained unchanged for 5 d, but decreased at Day 7. ABA treatment increased SOD activity for 5 and 7 d, respectively, under chilling and normal conditions. SOD activity increased to the control level after the plants were rewarmed for 2 d (Fig. 4).

[FIGURE 4 OMITTED]

Catalase activity showed a transient increase by ABA treatment before the plants were subject to chilling (Fig. 5), indicating induction of CAT activity by ABA. Under chilling conditions, both water-treated and ABA-treated plants had higher CAT activity than control plants for the first 5 d, indicating chilling induced CAT activity. CAT activity decreased at Day 7, but increased after the plants were rewarmed (Fig. 5).

[FIGURE 5 OMITTED]

Ascorbate peroxidase activity was transiently induced by ABA before the plants were subjected to chilling and then decreased to the level of control plants for 9 d (Fig. 6). Water-treated plants showed decreased APX activity during chilling conditions, while APX activity of ABA-treated plants remained at higher levels than in water-treated plants (Fig. 6).

[FIGURE 6 OMITTED]

Reduced GSH content in ABA-treated plants was transiently induced before the plants were subjected to chilling and decreased to the level of control plants. GSH content in water-treated plants was not significantly affected by chilling, but GSH content in ABA-treated plants remained at higher level under chilling conditions (Fig. 7).

[FIGURE 7 OMITTED]

ABA-treated plants showed a transient increase of AsA content before the plants were subject to chilling and then decreased to the level of water-treated plants under normal conditions. AsA content was not affected significantly by chilling treatment, but ABA-treated plants had higher AsA contents than water-treated plants under chilling conditions (Fig. 8).

[FIGURE 8 OMITTED]

DISCUSSION

Relative water content is a good and simple index of plant water status. Low temperature stress indirectly induces water stress (Eze et ah, 1983); hence, the level of water stress induced by chilling can be measured by RWC. Chilling treatment decreased the RWC of S. guianensis, indicating that water stress occurred at low temperature. Membrane permeability is closely related to the cell membrane injury (Blum and Ebercon, 1981). Electrolyte leakage increased under chilling conditions, suggesting that the membrane system of S. guianensis was damaged under chilling stress. Environmental stress induced oxidative damage is related to the imbalance of ROS production (Bowler et al., 1992). After plants were subjected to chilling for 5 d, CAT activity was induced; SOD activity and AsA and GSH contents were not significantly affected, and therefore, S. guianensis plants were only slightly damaged by chilling treatment. APX activity decreased gradually, indicating that it was somewhat sensitive to chilling. The early accumulation of [H.sub.2][O.sub.2] in plants under chilling signals production of antioxidant enzymes, such as CAT (Prasad et ah, 1994a). SOD and CAT activities decreased while the plants were severely damaged by chilling treatment for 7 d. The results indicated that the declined antioxidant enzymes activity was related to chilling injury in S. guianensis.

ABA maintained membrane stability in cotton (Rikin et ah, 1979) and increased chilling tolerance of treated maize (Prasad et al., 1994b; Anderson et al., 1994). Our study showed that ABA treatment increased RWC and lowered electrolyte leakage under chilling conditions, indicating that ABA increased the chilling resistance of S. guianensis. Chilling resistance induced by chemicals such as ABA and uniconazole [(E)-(RS)-l-(4-chlorophenyl) -4,4-dimethyl-2-(1H-1,2,4-triazol-l-yl)pent-1-en-3-ol] increased the scavenging system in plants and protected the membranes from oxidative stress (Prasad et al., 1994a; Senaratna et al., 1988). SOD and APX activities in maize were induced by ABA (Gong et al., 1998). ABA pretreatment increased activities of antioxidant enzymes and the contents of nonenzymatic antioxidants in maize seedlings and reduced the degrees of oxidative damage under stressful conditions. The induction on antioxidant enzymes was suppressed by ABA biosynthesis inhibitor, tungstate (Jiang and Zhang, 2002a). ABA triggered the increased generation of ROS, which, in turn, led to the induction of the antioxidant system (Jiang and Zhang, 2002b). Our investigation of S. guigensis is consistent with the previous reports. ABA induced the antioxidant systems in S. guianensis. ABA induced SOD activity under both normal and chilling conditions. APX and CAT activities and GSH and AsA content were transiently induced in ABA-treated plants before the plants were subject to chilling. APX activity and GSH and AsA content remained higher in ABA-treated plants than those in water-treated plants during chilling treatment. ABA-induced antioxidant system in S. guianensis is possibly involved in the gene expression. Transcription of Sod4, encoding Cu/Zn cytosolic SOD gene, in maize was increased within 4 h of ABA treatment (Guan and Scandalios, 1998). The Fe-SOD gene of rice (Oryza sativa L.) was also induced by ABA (Kaminaka et al., 1999). However, ABA induced antioxidant systems is not as effective as it is in decreasing chilling injury in S. guianensis. ABA induced expression of numerous genes and proteins in stressed plants (Chandler and Robertson, 1994). It is suggested that higher levels of antioxidant enzyme activity and AsA and GSH contents in ABA-treated plants were partially associated with the increased chilling resistance in S. guianensis.

ABA-treated S. guianensis had high levels of RWC under chilling conditions, suggesting ABA improved water balance in S. guianensis at low temperature. It has been observed that ABA treatment maintained a favorable water balance in plants (Rikin et al., 1979; Ristic and Cass, 1993). ABA reduces water stress at low temperature by decreasing the transpiration rate and increasing the water potential in litchi (Litchi chinensis Sonn.) (Zhou et al., 2002). However, the mechanism by which ABA maintained water balance through regulating stomatal closure, transpiration, and endogenous hormone levels needs further investigation.

Although ABA is effective in increasing resistance to abiotic stress in plants, it has not been practically used because of its cost. The S-ABA we used was produced biosynthetically, and its price is relatively low, which make it possible to be applied to protecting crops, including S. guianensis, from abiotic stress. The field traits and the economical benefit of ABA application are going to be evaluated. In summary, ABA improved water status and increased chilling tolerance of S. guianensis. ABA induced antioxidant systems were partially associated with increased chilling tolerance of S. guianensis.

Abbreviations: ABA, abscisic acid; AsA, ascorbic acid; APX, ascorbate peroxidase; CAT, catalase; GR, Glutathione reductase; GSH, reduced glutathione; POD, peroxidase; ROS, reactive oxygen species; RWC, relative water content; SOD, superoxide dismutase.

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Biyan Zhou, Zhenfei Guo, * and Zhiling Liu

Biyan Zhou and Zhenfei Guo, College of Life Science, South China Agricultural Univ., Guangzhou 510642, China; Biyan Zhou and Zhiling Liu, College of Horticulture, South China Agricultural Univ., Guangzhou 510642, China. Received 10 May 2003. Crop Ecology, Management & Quality. * Corresponding author (zhfguo@scau.edu.cn).
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Title Annotation:Crop Ecology, Management & Quality
Author:Zhou, Biyan; Guo, Zhenfei; Liu, Zhiling
Publication:Crop Science
Date:Mar 1, 2005
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