Metabolic Responses to Heat Stress under Elevated Atmospheric CO2 Concentration in a Cool-season Grass Species

in Journal of the American Society for Horticultural Science
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  • 1 Horticulture College of Nanjing Agricultural University, Nanjing 210095, P.R. China; and the Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ 08901
  • | 2 School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 201101, P.R. China
  • | 3 Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ 08901; and Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources, Chinese Academy of Sciences, Beijing 100101, P.R. China
  • | 4 Department of Plant Biology and Pathology, Rutgers University, 59 Dudley Road, New Brunswick, NJ 08901

Heat is a major factor limiting growth of C3 grass species. Elevated CO2 may mitigate the adverse effects of heat stress or enhance heat tolerance. The objective of this study was to determine metabolic changes associated with improvement of heat tolerance by elevated atmospheric CO2 concentration in tall fescue (Festuca arundinacea). Plants (cv. Rembrandt) were exposed to ambient day/night temperature (25/20 °C) or heat stress (35/30 °C) and ambient CO2 concentration (400 ± 10 μmol·mol−1) or double ambient CO2 concentration (800 ± 10 μmol·mol−1) in growth chambers. Turf quality (TQ), shoot growth rate, and leaf electrolyte leakage results demonstrated that heat stress at ambient CO2 concentration inhibits turf growth and reduces cell membrane stability, whereas heat-stressed plants under elevated CO2 concentration exhibit improved TQ, shoot growth rate, and membrane stability. Plants exposed to heat stress under elevated CO2 exhibited a significantly greater amount of several organic acids (shikimic acid, malonic acid, threonic acid, glyceric acid, galactaric acid, and citric acid), amino acids (serine, valine, and 5-oxoproline), and carbohydrates (sucrose and maltose) compared with heat-stressed plants at ambient CO2. The increased production or maintenance of metabolites with important biological functions such as those involved in photosynthesis, respiration, and protein metabolism could play a role in elevated CO2 mitigation of heat stress damage. Therefore, elevated CO2 conditions may contribute to improved heat stress tolerance as exhibited by better TQ and shoot growth of heat-stressed plants. Practices to harness the power of CO2 may be incorporated into turfgrass management for plant adaptation to increasing temperatures, particularly during summer months.

Abstract

Heat is a major factor limiting growth of C3 grass species. Elevated CO2 may mitigate the adverse effects of heat stress or enhance heat tolerance. The objective of this study was to determine metabolic changes associated with improvement of heat tolerance by elevated atmospheric CO2 concentration in tall fescue (Festuca arundinacea). Plants (cv. Rembrandt) were exposed to ambient day/night temperature (25/20 °C) or heat stress (35/30 °C) and ambient CO2 concentration (400 ± 10 μmol·mol−1) or double ambient CO2 concentration (800 ± 10 μmol·mol−1) in growth chambers. Turf quality (TQ), shoot growth rate, and leaf electrolyte leakage results demonstrated that heat stress at ambient CO2 concentration inhibits turf growth and reduces cell membrane stability, whereas heat-stressed plants under elevated CO2 concentration exhibit improved TQ, shoot growth rate, and membrane stability. Plants exposed to heat stress under elevated CO2 exhibited a significantly greater amount of several organic acids (shikimic acid, malonic acid, threonic acid, glyceric acid, galactaric acid, and citric acid), amino acids (serine, valine, and 5-oxoproline), and carbohydrates (sucrose and maltose) compared with heat-stressed plants at ambient CO2. The increased production or maintenance of metabolites with important biological functions such as those involved in photosynthesis, respiration, and protein metabolism could play a role in elevated CO2 mitigation of heat stress damage. Therefore, elevated CO2 conditions may contribute to improved heat stress tolerance as exhibited by better TQ and shoot growth of heat-stressed plants. Practices to harness the power of CO2 may be incorporated into turfgrass management for plant adaptation to increasing temperatures, particularly during summer months.

Heat stress is a major abiotic factor limiting growth of temperate plant species in many areas during summer months and may become a threat as global warming occurs [Fry and Huang, 2004; Intergovernmental Panel on Climate Change (IPCC), 2007]. Heat stress induces changes in various metabolites such as organic acids, amino acids, and carbohydrates, which have important functions involved in photosynthesis and respiration (Merewitz et al., 2012). These compounds are involved in vital metabolic functions within the plant such as regulating plant water relations, signaling, protein synthesis as well as stress defense (Sairam et al., 2000; Zobayed et al., 2005). CO2 concentrations in the atmosphere are more than 100 μmol·mol−1 higher since the beginning of the industrialization era and the concentration is predicted to rise at a rate of ≈2 μmol·mol−1 per year (IPCC, 2007). Increasing evidence has shown that elevated CO2 may promote plant growth and mitigate heat stress damage in various plant species, particularly C3 species (Hamerlynck et al., 2000; Kirkham, 2011; Qaderi et al., 2006) including perennial turfgrass species such as tall fescue (Yu et al., 2012). Various studies report elevated CO2 promotes shoot growth, root growth, and photosynthesis but inhibits dark respiration and photorespiration rates (Gonzàlez-Meler et al., 1996; Leakey et al., 2006; Reddy et al., 2010). However, the metabolites associated with the improvement in plant growth and changes in photosynthesis and respiration metabolic processes resulting from elevated CO2, particularly under heat stress, are not well documented.

Metabolic profiling is an effective and quantitative method to elucidate mechanisms of abiotic stress tolerance, including heat stress (Kaplan et al., 2004; Mayer et al., 1990). Mayer et al. (1990) reported an increase in the abundance of γ-aminobutyric acid (GABA), β-alanine, alanine, and proline in cowpea (Vigna unguiculata) as a result of heat shock under ambient CO2 conditions. Du et al. (2011) reported that heat stress at ambient CO2 induced significant accumulation of multiple metabolites, including threonic acid, galacturonic acid, gluconic acid, succinic acid, proline, aspartic acid, serine, valine, methylmaleic acid, fructose, galactose, xylose, glucose, mannose, and sucrose in kentucky bluegrass (Poa pratensis). Most of the previous studies examined metabolic changes in response to heat stress without consideration of the interaction with CO2. Very few studies investigated changes in metabolite accumulation in response to heat stress under elevated CO2 conditions despite some studies that reported the positive effects of elevated CO2 on plant growth under detrimental environments such as water dehydration and fertilizer deficiency (Kirkham, 2011; Lavola and Julkunen-Tiitto, 1994).

Tall fescue is a widely used cool-season, C3 turfgrass species. This species exhibits good drought avoidance traits such as deep rooting characteristics but has limited high temperature tolerance (Fry and Huang, 2004). Doubling ambient CO2 concentration improved tall fescue tolerance to the combined stress of heat and drought by enhancing plant water status, cellular membrane stability, and photosynthesis capacity and by suppressing carbon consumption through lowering respiration rate (Yu et al., 2012). Understanding metabolic changes associated with mitigation of heat stress injury by increasing CO2 will provide further insight into the interactive effects of heat stress and elevated CO2 in plant species. In addition, it has great potential for future use in the development of novel management practices. For instance, products aimed to enhance the CO2 in the gas layers surrounding plants or CO2 fertilization could be used as management strategies of turfgrasses or other plant species. Therefore, the objective of this study was to examine differential changes in metabolite accumulation of tall fescue in response to heat stress under elevated CO2 with an aim to further understand metabolic mechanisms for elevated CO2 enhancement of heat tolerance in C3 perennial grass species.

Materials and Methods

Plant materials and growth conditions.

Sod pieces of tall fescue (cv. Rembrandt) plants were collected from the research farm at Rutgers University in Adelphia, NJ, and transplanted into plastic tubes (10 cm diameter and 60 cm long) filled with a mixture of fine sand and soil (fine-loamy-mixed mesic typic Hapludult) (1:1, v/v). Plants were maintained in a greenhouse with an average temperature regime of 21/16 °C (day/night) and 810 μmol·m−2·s−1 photosynthetically active radiation (PAR) in natural sun light and 65% relative humidity for 70 d (May to June 2011) to establish canopy and roots. During this establishment period, plants were watered every other day and fertilized once weekly with half-strength Hoagland’s solution (Hoagland and Arnon, 1950). Plants were cut once a week to maintain a copy height of 5 to 6 cm. After establishment, plants were moved to growth chambers with the temperature set at 25/18 °C (day/night), 70% relative humidity, PAR of 650 μmol·m−2·s−1, and a 12-h photoperiod.

Experimental design and treatments.

The experiment consisted of two factors (two CO2 concentrations and two temperatures), which were arranged in a complete, randomized block design with four replicates for each treatment. The CO2 treatments included ambient CO2 (400 ± 10 μmol·mol−1) and elevated CO2 (800 ± 10 μmol·mol−1). Temperature was controlled at two levels: 25/20 °C (day/night, optimal temperature control) and 35/30 °C (day/night, heat stress). Plants were well watered to maintain soil water content at the field capacity (through irrigating plants until drainage ceased). Plants were grown at two CO2 levels in the growth chambers for 70 d before imposition of temperature treatments.

The treatment set-up and assignment in growth chambers followed the same designed as described in Yu et al. (2012). Four chambers were maintained at the ambient CO2 level with two of them set to elevated temperature (35/30 °C) and the other two set at the optimal temperatures (25/20 °C). Following the ambient CO2 treatment, the same four growth chambers were set to the elevated CO2 level with two at elevated temperature and two at the optimal temperature. Plants were relocated among the different chambers once per week to minimize confounding effects of environmental variation between different chambers. The concentration of CO2 inside each growth chamber was maintained with an automated, open-chamber CO2 control system connected to a gas tank containing 100% CO2 (Airgas, Radnor, PA) (Yu et al., 2012). The CO2 levels were continuously monitored through an infrared gas analyzer (LI-820; LI-COR, Lincoln, NE) and controlled using an automatic system consisting of a programmable logic controller unit, solenoid valves, and a laptop computer with monitoring software accurate to within 10 μmol·mol−1 of the target levels (400 and 800 μmol·mol−1).

Growth and cell membrane stability analysis.

Plant growth was evaluated by rating of TQ and shoot vertical growth rate. TQ is a widely used parameter evaluating overall plant performance (Turgeon, 1996). TQ was visually rated on a scale from 1 (completely dead plants) to 9 (green and dense canopy). Shoot vertical growth rate (expressed as millimeters per day) was calculated as the difference in average canopy height at 3-d intervals and in which canopy height was measured with a floating disk ruler method as the vertical distance from a paper disk placed on the turf canopy and the base of the shoot (Ervin and Zhang, 2007; Sharrow, 1984).

Cellular level of heat damage or tolerance was evaluated as cell membrane stability of leaves, which was determined by measuring electrolyte leakage (EL) (Blum and Ebercon, 1981). For EL analysis, 0.2 g of fresh leaves was placed in test tubes containing 20 mL deionized water and then shaken for 24 h under room temperature to measure the initial conductivity of the solution (Cinitial) with a conductivity meter (YSI Instrument, Yellow Springs, OH). Leaves were then killed by autoclaving at 140 °C for ≈20 min and to measure the conductivity of killed tissues (Cmax) after which samples were shaken for another 24 h. The percent EL was calculated as the ratio of Cinitial to Cmax × 100 (Blum and Ebercon, 1981).

Extraction and derivatization of metabolites and gas chromatography–mass spectrometry analysis.

The procedure was conducted following the method used by Du et al. (2011). Leaf tissue samples of 28-d treatment were harvested and immediately frozen in liquid nitrogen and stored at –80 °C for metabolic profiling. The extraction protocol was modified from Rizhsky et al. (2004) and Roessner et al. (2000) . For each sample, frozen leaves were ground to a fine powder with liquid nitrogen, and then 25 mg leaf tissue powders were transferred into 10-mL microcentrifuge tubes, and they were extracted in 1.4 mL of 80% (v/v) aqueous methanol for 2 h at 23 °C. Ribitol solution of 10 μL (2 mg·mL−1 water) was added as an internal standard before incubation. Then, extraction was done in a water bath at 70 °C for 15 min. Tubes were centrifuged for 30 min at 9660 gn and the supernatant was decanted to new culture tubes, and 1.4 mL of water and 0.75 mL of chloroform were added. The mixture was vortexed thoroughly and centrifuged for 5 min at 5025 gn and then 2 mL of the polar phase (methanol/water) was decanted into 1.5-mL high-performance liquid chromatography vials and dried in a benchtop centrifugal concentrator (Centrivap; Labconco Corp., Kansas City, MO). The dried polar phase was methoximated with 80 μL of 20 mg·mL−1 methoxyamine hydrochloride at 30 °C for 90 min and was trimethylsilylated with 80 μL N-methy-N-(trimethylsilyl) trifluoroacetamide (with 1% trimethylchlorosilane) for 60 min at 70 °C.

The gas chromatography–mass spectrometry (GC-MS) analysis was modified from Qiu et al. (2007). The derivatized extracts were analyzed with a gas chromatograph coupled with a mass spectrometer (TurboMass-Autosystem XL; PerkinElmer, Waltham, MA). A 1-μL extract aliquot of the extracts was injected into a capillary column (30 m × 0.25 mm × 0.25 μm, DB-5MS; Agilent J&W Scientific, Folsom, CA). The inlet temperature was set at 260 °C. After a 6.5-min solvent delay, initial GC oven temperature was set at 60 °C; 1 min after injection, the GC oven temperature was raised to 280 °C with 5 °C·min−1 and finally held at 280 °C for 15 min. The injection temperature was set to 280 °C and the ion source temperature was adjusted to 200 °C. Helium was used as the carrier gas with a constant flow rate set at 1 mL·min−1. The measurements were made with electron impact ionization (70 eV) in the full scan mode [with a mass to charge ration (m/z) of 30 to 550]. The metabolites detected were identified by Turbomass 4.1.1 software (PerkinElmer) coupled with commercially available compound libraries (NIST 2005; PerkinElmer) and Wiley 7.0 (John Wiley & Sons, Hoboken, NJ). For GC-MS results, compounds were identified based on retention time and comparison with reference spectra in mass spectral libraries. Peaks areas of compounds were integrated with the Genesis Algorithm program (New Light Industries, Spokane, WA).

Statistical analysis.

Data were analyzed using SAS (Version 9.0; SAS Institute, Cary, NC). The analysis of variance with a fixed model was used to determine treatments effects. When a particular F test was significant, the means were tested with a least significance difference test at a confidence level of 0.05.

Results and Discussion

Physiological responses to heat stress and elevated CO2 concentration.

TQ (Fig. 1A) and shoot vertical growth rate (Fig. 1B) declined under heat stress and under ambient CO2 conditions, but plants exposed to the high CO2 concentration had significantly higher TQ and shoot growth rate under heat stress than those plants at ambient CO2 concentration. Leaf EL increased with heat stress at ambient CO2 conditions, but the increase was to a significantly less extent under elevated CO2 conditions (Fig. 1C). These results demonstrate that elevated CO2 suppresses heat inhibition of turf growth and damage to cellular membranes. These results are consistent with the positive effects of elevated CO2 on tall fescue tolerance to the combined stress of heat and drought observed in our previous study (Yu et al., 2012). It was noted that elevated CO2 concentration decreased TQ and increased EL significantly after 14 d of treatment compared with plants grown at ambient CO2 conditions, indicating that higher CO2 under unstressed conditions for a long time was an additional stress to plants (Yu et al., 2012).

Fig. 1.
Fig. 1.

Changes in turf quality (TQ) (A), shoot growth rate (mm·d−1) (B), and electrolyte leakage of leaves (EL) (C) of tall fescue in response to heat stress and elevated CO2 concentrations. TQ was visually rated on a scale from 1 (completely dead plants) to 9 (green and dense canopy). The treatment symbols are 25 to 800 for optimal temperature, and elevated CO2, 25 to 400 for optimal temperature, and ambient CO2, 35 to 800 for heat stress, and elevated CO2, 35 to 400 for heat stress, and ambient CO2. Vertical bars indicate least significant difference values for the comparison between treatments at a given day of treatment based on P ≤ 0.05.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 137, 4; 10.21273/JASHS.137.4.221

Metabolic responses to heat stress and elevated CO2.

A total of 41 metabolites responding to elevated CO2 and heat stress were identified by GC-MS (Table 1). Among the 41 metabolites, organic acids, amino acids, and carbohydrates accounted for 37%, 27%, and 17% of the total amount of metabolites, respectively (Table 1).

Table 1.

List of 41 identified metabolites in leaves of tall fescue exposed to elevated CO2 and heat stress for 28 d.

Table 1.

Organic acid accumulation.

A total of 15 organic acids is identified and the data for those acids responsive to CO2 or heat stress are presented in Figure 2. Significant interactive effects between CO2 concentration and temperature were detected and different organic acids exhibited differential responses to elevated CO2 or heat stress. Biological functions of metabolites responsive to heat stress under either ambient CO2 or elevated CO2 conditions are discussed in the context of CO2 mitigation of heat stress damages in tall fescue.

Fig. 2.
Fig. 2.

Changes in organic acid accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 137, 4; 10.21273/JASHS.137.4.221

Under ambient CO2 concentration, heat stress caused a significant decline in the abundance of a majority of the organic acids identified in this study, including oxalic acid (68%), shikimic acid (71%), malonic acid (68%), threonic acid (55%), glyceric acid (71%), and galactaric acid (85%), whereas the abundance of citric acid increased; other organic acids such as pyruvic acid and malic acid did not change under heat stress (data not shown) (Fig. 2). Under elevated CO2 concentration, heat-stressed plants exhibited a significantly higher abundance of shikimic acid (2.9-fold), malonic acid (2.8-fold), threonic acid (90%), glyceric acid (1.5-fold), galactaric acid (1.3-fold), and citric acid (1.7-fold) than plants exposed to the control temperature (Fig. 2).

Citric acid is a key metabolite in the respiration pathway for energy production (Benkeblia et al., 2007). Increases in citric acid content during heat stress under either ambient or elevated CO2 indicate that heat stress could stimulate respiration rates leading to more citric acid production or maintenance. Heat-induced accumulation of citric acid was also found in other turfgrass species [hybrid bermudagrass (Cynodon transvaalensis × C. dactylon) and kentucky bluegrass (Du et al., 2011)]. Elevated CO2 may suppress heat-enhanced respiration, because plants exposed to elevated CO2 had a lower abundance of citric acid than plants with ambient CO2 under heat stress. Previous studies suggest that increasing atmospheric CO2 concentration inhibited dark respiration in some plant species (Gonzàlez-Meler et al., 1996; Hamilton et al., 2001). Ziska and Bunce (1993) separated total respiration required for growth and maintenance and found a significant effect of elevated CO2 on both components, causing a significant reduction in growth respiration at 20, 25, and 30 °C in alfalfa (Medicago sativa) and at 15 and 25 °C in Dactylus glomerata.

The majority of the organic acids (oxalic acid, shikimic acid, malonic acid, threonic acid, glyceric acid, and galactaric acid) responsive to heat or elevated CO2 found in this study are involved in several metabolic pathways, in particular stress defense pathways. Oxalic acid is known to be involved in antioxidant stress defense (Ding et al., 2007; Jiang et al., 2008; Zhang et al., 2001). Exogenous application of oxalic acid improved heat tolerance of pepper (Capsicum annuum) (Zhang et al., 2001) and alfalfa by enhancing chlorophyll accumulation and increasing antioxidant enzyme activities that was inhibited by heat stress (Jiang et al., 2008). Its accumulation has also been associated with drought tolerance in creeping bentgrass [Agrostis stolonifera (Merewitz et al., 2012)] and cold tolerance in arabidopsis [Arabidopsis thaliana (Korn et al., 2010)]. Shikimic acid is involved in the production of polyphenol flavonoid compounds such as anthocyanins, which have antioxidant properties to suppress heat-induced oxidative damage (Shao et al., 2007). Xu and Huang (2012) reported a decrease in shikimic acid resulting from drought stress in kentucky bluegrass. Little is known about the direct effects of elevated CO2 on shikimic acid, but studies have shown an increase in secondary metabolites derived from the shikimic acid pathway such as tannins in response to enriched CO2 (Lindroth et al., 2001; Peñuelas and Estiarte, 1998). Malonic acid is a dicarboxylic acid and malonate is its ionized form. Malonate acts as a major competitive inhibitor of succinate dehydrogenase involved in the tricarboxylic acid cycle of respiration (Li and Copeland, 2000). Malonate also has been associated with osmotic adjustment and stress defensive system (Lecoeur et al., 1992; Li and Copeland, 2000). Threonic acid is a metabolic product of ascorbic acid and also correlated with glyceric acid synthesis (Helsper and Loewus, 1982). Threonic acid and glyceric acid have been reported to be sensitive to heat stress in many species, including arabidopsis (Kaplan et al., 2004), hybrid bermudagrass, and kentucky bluegrass (Du et al., 2011). Galactaric acid is derived from galacturonic acid by galacturonic acid oxidase, which has been found to stimulate the oxidation of indole acetic acid by peroxidase (Pressey, 1991) and acts as a substrate for galacturonic acid reductase leading to the synthesis of ascorbic acid. Sanchez et al. (2008) reported that galactaric acid was decreased by salinity in arabidopsis. The decline in the abundance of these organic acids under heat stress suggested that heat stress mainly weakened the stress defense mechanisms, whereas the increases or maintenance of the abundance of those organic acids in plants exposed to elevated CO2 under heat stress could contribute to the improvement in heat tolerance by enhancing or maintaining more active oxidative defense mechanisms. However, direct mechanisms of CO2 mitigation of heat damage involving these organic acids are yet to be determined.

Amino acid accumulation.

A total of 11 amino acids was identified and the data for those amino acids responsive to CO2 or heat stress are presented in Figure 3. Amino acids exhibited differential responses to elevated CO2 or heat stress and significant interactive effects between CO2 concentration and temperature were detected.

Fig. 3.
Fig. 3.

Changes in amino acid accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. GABA = γ-aminobutyric acid. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 137, 4; 10.21273/JASHS.137.4.221

Under ambient CO2 concentration, the abundance of alanine and serine was 48% and 58% lower, respectively, at heat stress than at the control temperature condition, but GABA abundance increased 2.3-fold under heat stress; valine and 5-oxoproline did not change in response to heat stress (Fig. 3). Under elevated CO2 concentration, the abundance of serine (3.8-fold), valine (96%), and 5-oxoproline (1.5 fold) of heat-stressed plants were significantly higher than that of the control plants, whereas GABA abundance was lower (70%) in heat-stressed plants than in the control plants; alanine maintained the abundance at the equivalent level under heat stress and the control temperature (Fig. 3).

Alanine and serine are constituents of many proteins and involved in various metabolic processes (Bourguignon et al., 1999). The decline in alanine and serine abundance under heat stress at ambient CO2 and the accumulation of serine and maintenance of alanine under elevated CO2 for plants exposed to heat stress could be reflective of CO2 mitigation of the heat inhibitory effects on protein synthesis and metabolisms involving these two important amino acids. Valine is also used for synthesizing proteins and secondary metabolites (Singh, 1999). Tschaplinski et al. (1995) reported significant increases in valine accumulation under elevated CO2 concentration in drought-stressed plants. Valine accumulation was reported to be associated with improved drought stress tolerance (Merewitz et al., 2012) and with heat shock (Kaplan et al., 2004). The increased accumulation of valine in heat-stressed plants under elevated CO2 in tall fescue in this study could be associated with the CO2-induced improvement in heat tolerance, although the specific mechanisms are not clear.

Pyroglutamic acid or 5-oxoproline is a precursor to the synthesis of glutamate (Ohkama-Ohtsu et al., 2008). Conversion of 5-oxoproline to glutamate is required in the regeneration of glutathione, which is known as an effective antioxidant. Increased 5-oxoproline production may be involved in a strengthened antioxidant system (Marrs, 1996). The accumulation of 5-oxoproline that resulted from elevated CO2 under heat stress indicated the positive CO2 effects on promoting antioxidant metabolism in tall fescue under heat stress.

GABA is a non-protein amino acid, serving as a signaling molecule and regulating numerous stress response mechanisms such as the carbon/nitrogen balance, osmotic potential, free radical scavenging, and pH regulation (Bouche and Fromm, 2004; Kinnersley and Turano, 2000). In the present study, the level of GABA significantly increased under heat stress for tall fescue exposed to ambient CO2, but under elevated CO2, heat-stressed plants had lower GABA abundance than the control plants. Studies conducted under ambient CO2 conditions reported rapid accumulation of GABA after heat shock in arabidopis (Rizhsky et al., 2004) or heat stress in cowpea (Mayer et al., 1990) as well as drought stress (Bor et al., 2009; Raggi, 1994). Tschaplinski et al. (1995) reported an increase in GABA caused by elevated CO2 in sugar maple (Acer saccharum) under ambient temperature. Studies comparing GABA content in plants differing in drought tolerance reported a negative relationship of GABA with drought tolerance (Kinnersley and Turano, 2000). However, little is known about the interactive effects of CO2 and temperature on GABA production.

Carbohydrate accumulation.

A total of seven carbohydrates is identified and the data for five carbohydrates responsive to CO2 or heat stress are presented in Figure 4. Significant interactive effects between CO2 concentration and temperature on different carbohydrates were detected.

Fig. 4.
Fig. 4.

Changes in carbohydrate accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 137, 4; 10.21273/JASHS.137.4.221

Under ambient CO2 concentration, heat-stressed plants had significantly greater abundance of sucrose than the control plants, but under elevated CO2, sucrose abundance did not change with temperature (Fig. 4). Heat caused reduction in the abundance of maltose under ambient CO2 but did not have effects under elevated CO2. The abundance of three monosaccharaides (fructose, glucose, and galactose) was unaffected by heat stress under ambient CO2, but under elevated CO2, heat-stressed plants had significantly lower contents of each sugar than the control plants. The abundance of fructose, glucose, and galactose increased with elevated CO2 under the control temperature but not under heat stress (Fig. 4).

Monosaccharides such as glucose, fructose, and galactose have important functions such as serving as energy sources and osmoregulants, whereas disaccharides such as sucrose and maltose are the main forms of carbohydrates for transport and storage in plants (Kaplan et al., 2004; Merewitz et al., 2012; Urbonaviciute et al., 2006). Previous studies with CO2 effects on carbohydrates examined plants exposed to elevated CO2 under normal temperature and found unchanged sucrose content but increased content of fructose and glucose by doubling ambient CO2 concentration such as in radish [Raphanus sativus (Urbonaviciute et al., 2006)], scots pine [Pinus sylvestris (Jach and Ceulemans, 1999)], and silver birch [Betula pendula (Lavola and Julkunen-Tiitto, 1994)]. Those results were similar to the results with sucrose, fructose, and glucose in tall fescue in this study. The increased accumulation of fructose and glucose as primary assimilates from photosynthesis is consistent with the enhanced photosynthetic rate by elevated CO2 in tall fescue, as reported in a previous study (Yu et al., 2012). Little is known of the interactive effects of CO2 and heat stress on carbohydrate accumulation. In this study, tall fescue plants exposed to heat stress had significantly lower contents of fructose, glucose, and galactose under elevated CO2 than plants exposed to normal temperature, whereas the abundance of sucrose and maltose was not responsive to heat stress under elevated CO2. The maintenance of disaccharides (sucrose and maltose) under heat stress in plants with elevated CO2 may help to maintain carbohydrate storage and supply for continued plant growth. However, how the decline in the monosaccharides (fructose, glucose, and galactose) may be involved in the interactive effects of heat and elevated CO2 is not clear, and they may be reflective of more active metabolic activities that are needed for continued consumption of soluble sugars under heat stress in plants exposed to elevated CO2.

Conclusions

Exposure of plants to elevated CO2 improved growth and physiological activities of tall fescue under heat stress and altered responses of various metabolites to heat stress. Elevated CO2 led to increased production of several organic acids (shikimic acid, malonic acid, threonic acid, glyceric acid, galactaric acid, and citric acid) and amino acids (serine, valine, and 5-oxoproline) as well as the maintenance of production of two disaccharide (sucrose and maltose) under heat stress. Those metabolites could play roles in elevated CO2 mitigation of heat stress damage in tall fescue and thus could contribute to improved heat tolerance.

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  • Helsper, J.P. & Loewus, F.A. 1982 Metabolism of l-threonic acid in Rumex × acutus L. and Pelargonium crispum (L.) L'Hér Plant Physiol. 69 1365 1368

    • Search Google Scholar
    • Export Citation
  • Hoagland, D.R. & Arnon, D.I. 1950 The water-culture method for growing plans without soil California Agr. Expt. Sta. Circ. 347 1 32

  • Intergovernmental Panel on Climate Change 2007 Climate change: Fourth assessment report. Cambridge University Press, London, UK

  • Jach, M.E. & Ceulemans, R. 1999 Effects of elevated atmospheric CO2 on phenology, growth and crown structure of scots pine (Pinus sylvestris) seedlings after two years of exposure in the field Tree Physiol. 19 289 300

    • Search Google Scholar
    • Export Citation
  • Jiang, Y., Wang, C. & Li, D. 2008 Effect of oxalic acid on chlorophyll content and antioxidant system of alfalfa under high temperature stress Pratacultural Sci. 25 55 59

    • Search Google Scholar
    • Export Citation
  • Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y. & Guy, C.L. 2004 Exploring the temperature-stress metabolome of arabidopsis Plant Physiol. 136 4159 4168

    • Search Google Scholar
    • Export Citation
  • Kinnersley, A.M. & Turano, F.J. 2000 Gamma aminobutyric acid (GABA) and plant responses to stress Crit. Rev. Plant Sci. 19 479 509

  • Kirkham, M.B. 2011 Elevated carbon dioxide: Impact on soil and plant water relations. CRC Press, Boca Raton, FL

  • Korn, M., Gärtner, T., Erban, A., Kopka, J., Selbig, J. & Hincha, D.K. 2010 Predicting arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition Mol. Plant 3 224 235

    • Search Google Scholar
    • Export Citation
  • Lavola, A. & Julkunen-Tiitto, R. 1994 The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendula (Roth) Oecologia 99 315 321

    • Search Google Scholar
    • Export Citation
  • Leakey, A.D.B., Uribelarrea, M., Ainsworth, E.A., Naidu, S.L., Rogers, A., Ort, D.R. & Long, S.P. 2006 Photosynthesis, productivity, and yield of maize are not affected by open-air elevation of CO2 concentration in the absence of drought Plant Physiol. 140 779 790

    • Search Google Scholar
    • Export Citation
  • Lecoeur, J., Wery, J. & Turc, O. 1992 Osmotic adjustment as a mechanism of dehydration postponement in chickpea (Cicer arietinum L.) leaves Plant Soil 144 177 189

    • Search Google Scholar
    • Export Citation
  • Li, J. & Copeland, L. 2000 Role of malonate in chickpeas Phytochemistry 54 585 589

  • Lindroth, R.L., Kopper, B.J., Parsons, W.F.J., Bockheim, J.G., Karnosky, D.F., Hendrey, G.R., Pregitzer, K.S., Isebrands, J.G. & Sober, J. 2001 Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) Environ. Pollut. 115 395 404

    • Search Google Scholar
    • Export Citation
  • Marrs, K.A. 1996 The functions and regulation of glutathione S-transferases in plants Annu. Rev. Plant Biol. 47 127 158

  • Mayer, R.R., Cherry, J.H. & Rhodes, D. 1990 Effects of heat shock on amino acid metabolism of cowpea cells Plant Physiol. 94 796 810

  • Merewitz, E.B., Du, H., Yu, W., Liu, Y., Gianfagna, T. & Huang, B. 2012 Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation J. Expt. Bot. 63 1315 1328

    • Search Google Scholar
    • Export Citation
  • Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K. & Oliver, D.J. 2008 A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in arabidopsis Plant Physiol. 148 1603 1613

    • Search Google Scholar
    • Export Citation
  • Peñuelas, J. & Estiarte, M. 1998 Can elevated CO2 affect secondary metabolism and ecosystem function? Trends Ecol. Evol. 13 20 24

  • Pressey, R. 1991 Oxidized oligogalacturonides activate the oxidation of indoleacetic acid by peroxidase Plant Physiol. 96 1167 1170

  • Qaderi, M.M., Kurepin, L.V. & Reid, D.M. 2006 Growth and physiological responses of canola (Brassica napus) to three components of global climate change: Temperature, carbon dioxide and drought Physiol. Plant. 128 710 721

    • Search Google Scholar
    • Export Citation
  • Qiu, Y., Su, M., Liu, Y., Chen, M., Gu, J., Zhang, J. & Jia, W. 2007 Application of ethyl chloroformate derivatization for gas chromatography–mass spectrometry based metabonomic profiling Anal. Chim. Acta 583 277 283

    • Search Google Scholar
    • Export Citation
  • Raggi, V. 1994 Changes in free amino acids and osmotic adjustment in leaves of water-stressed bean Physiol. Plant. 91 427 434

  • Reddy, A.R., Rasineni, G.K. & Raghavendra, A.S. 2010 The impact of global elevated CO2 concentration on photosynthesis and plant productivity Curr. Sci. 99 46 57

    • Search Google Scholar
    • Export Citation
  • Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. & Mittler, R. 2004 When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress Plant Physiol. 134 1683 1696

    • Search Google Scholar
    • Export Citation
  • Roessner, U., Wagner, C., Kopka, J., Trethewey, R.N. & Willmitzer, L. 2000 Simultaneous analysis of metabolites in potato tuber by gas chromatography–mass spectrometry J. Plant 23 131 142

    • Search Google Scholar
    • Export Citation
  • Sairam, R.K., Srivastava, G.C. & Saxena, D.C. 2000 Increased antioxidant activity under elevated temperatures: A mechanism of heat stress tolerance in wheat genotypes Biol. Plant. 43 245 251

    • Search Google Scholar
    • Export Citation
  • Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M. & Kopka, J. 2008 Plant metabolomics reveals conserved and divergent metabolic responses to salinity Physiol. Plant. 132 209 219

    • Search Google Scholar
    • Export Citation
  • Shao, L., Shu, Z., Sun, S.L., Peng, C.L., Wang, X.J. & Lin, Z.F. 2007 Antioxidation of anthocyanins in photosynthesis under high temperature stress J. Integr. Plant Biol. 49 1341 1351

    • Search Google Scholar
    • Export Citation
  • Sharrow, S.H. 1984 A simple disk meter for measurement of pasture height and forage bulk J. Range Manage. 37 94 95

  • Singh, B. 1999 Plant amino acids: Biochemistry and biotechnology. CRC Press, Boca Raton, FL

  • Tschaplinski, T.J., Stewart, D.B. & Norby, R.J. 1995 Interactions between drought and elevated CO2 on osmotic adjustment and solute concentrations of tree seedlings New Phytol. 131 169 177

    • Search Google Scholar
    • Export Citation
  • Turgeon, A.J. 1996 Turfgrass management. 4th Ed. Prentice-Hall, Upper Saddle River, NJ

  • Urbonaviciute, A., Samuoliene, G., Sakalauskaite, J., Duchovskis, P., Brazaityte, A., Siksnianiene, J.B., Ulinskaite, R., Sabajeviene, G. & Baranauskis, K. 2006 The effect of elevated CO2 concentrations on leaf carbohydrate, chlorophyll contents and photosynthesis in radish Pol. J. Environ. Stud. 15 921 925

    • Search Google Scholar
    • Export Citation
  • Xu, C. & Huang, B. 2012 Proteins and metabolites regulated by trinexapac-ethyl in relation to drought tolerance in kentucky bluegrass J. Plant Growth Regul. 31 25 37

    • Search Google Scholar
    • Export Citation
  • Yu, J., Chen, L., Xu, M. & Huang, B. 2012 Effects of elevated CO2 on physiological responses of tall fescue (Festuca arundinacea) to elevated temperature, drought stress, and the combined stresses Crop Sci. (in press)

    • Search Google Scholar
    • Export Citation
  • Zhang, Z.S., Li, R.Q. & Wang, J.B. 2001 Effects of oxalate treatment on the membrane permeability and calcium distribution in pepper leaves under heat stress Acta Phytophysiol. Sinica 27 109 113

    • Search Google Scholar
    • Export Citation
  • Ziska, L.H. & Bunce, J.A. 1993 Inhibition of whole plant respiration by elevated CO2 as modified by growth temperature Physiol. Plant. 87 459 466

  • Zobayed, S.M.A., Afreen, F. & Kozai, T. 2005 Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in st. john's wort Plant Physiol. Biochem. 43 977 984

    • Search Google Scholar
    • Export Citation

Contributor Notes

We thank the Chinese Scholarship Council and Rutgers Center of Turfgrass Science for funding support. We also thank Dr. Emily Merewitz, Patrick Burgess, and David Jespersen for critical review of the manuscript.

Corresponding author. E-mail: huang@aesop.rutgers.edu, mingxu@crssa.Rutgers.edu.

  • View in gallery

    Changes in turf quality (TQ) (A), shoot growth rate (mm·d−1) (B), and electrolyte leakage of leaves (EL) (C) of tall fescue in response to heat stress and elevated CO2 concentrations. TQ was visually rated on a scale from 1 (completely dead plants) to 9 (green and dense canopy). The treatment symbols are 25 to 800 for optimal temperature, and elevated CO2, 25 to 400 for optimal temperature, and ambient CO2, 35 to 800 for heat stress, and elevated CO2, 35 to 400 for heat stress, and ambient CO2. Vertical bars indicate least significant difference values for the comparison between treatments at a given day of treatment based on P ≤ 0.05.

  • View in gallery

    Changes in organic acid accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

  • View in gallery

    Changes in amino acid accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. GABA = γ-aminobutyric acid. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

  • View in gallery

    Changes in carbohydrate accumulation of tall fescue leaves in response to 28 d of heat stress under ambient or elevated CO2 concentrations. The treatment symbols are 25 and 35 °C for optimal temperature and heat stress and 400 and 800 for ambient and elevated CO2 concentrations, respectively. Bars with the same lowercase letter are not significantly different based on least significant difference test at P ≤ 0.05.

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  • Ervin, E.H. & Zhang, X. 2007 Influence of sequential trinexapac-ethyl applications on cytokinin content in creeping bentgrass, kentucky bluegrass, and hybrid bermudagrass Crop Sci. 47 2145 2151

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  • Fry, J. & Huang, B. 2004 Applied turfgrass science and physiology. Wiley, Hoboken, NJ

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  • Helsper, J.P. & Loewus, F.A. 1982 Metabolism of l-threonic acid in Rumex × acutus L. and Pelargonium crispum (L.) L'Hér Plant Physiol. 69 1365 1368

    • Search Google Scholar
    • Export Citation
  • Hoagland, D.R. & Arnon, D.I. 1950 The water-culture method for growing plans without soil California Agr. Expt. Sta. Circ. 347 1 32

  • Intergovernmental Panel on Climate Change 2007 Climate change: Fourth assessment report. Cambridge University Press, London, UK

  • Jach, M.E. & Ceulemans, R. 1999 Effects of elevated atmospheric CO2 on phenology, growth and crown structure of scots pine (Pinus sylvestris) seedlings after two years of exposure in the field Tree Physiol. 19 289 300

    • Search Google Scholar
    • Export Citation
  • Jiang, Y., Wang, C. & Li, D. 2008 Effect of oxalic acid on chlorophyll content and antioxidant system of alfalfa under high temperature stress Pratacultural Sci. 25 55 59

    • Search Google Scholar
    • Export Citation
  • Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y. & Guy, C.L. 2004 Exploring the temperature-stress metabolome of arabidopsis Plant Physiol. 136 4159 4168

    • Search Google Scholar
    • Export Citation
  • Kinnersley, A.M. & Turano, F.J. 2000 Gamma aminobutyric acid (GABA) and plant responses to stress Crit. Rev. Plant Sci. 19 479 509

  • Kirkham, M.B. 2011 Elevated carbon dioxide: Impact on soil and plant water relations. CRC Press, Boca Raton, FL

  • Korn, M., Gärtner, T., Erban, A., Kopka, J., Selbig, J. & Hincha, D.K. 2010 Predicting arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition Mol. Plant 3 224 235

    • Search Google Scholar
    • Export Citation
  • Lavola, A. & Julkunen-Tiitto, R. 1994 The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendula (Roth) Oecologia 99 315 321

    • Search Google Scholar
    • Export Citation
  • Leakey, A.D.B., Uribelarrea, M., Ainsworth, E.A., Naidu, S.L., Rogers, A., Ort, D.R. & Long, S.P. 2006 Photosynthesis, productivity, and yield of maize are not affected by open-air elevation of CO2 concentration in the absence of drought Plant Physiol. 140 779 790

    • Search Google Scholar
    • Export Citation
  • Lecoeur, J., Wery, J. & Turc, O. 1992 Osmotic adjustment as a mechanism of dehydration postponement in chickpea (Cicer arietinum L.) leaves Plant Soil 144 177 189

    • Search Google Scholar
    • Export Citation
  • Li, J. & Copeland, L. 2000 Role of malonate in chickpeas Phytochemistry 54 585 589

  • Lindroth, R.L., Kopper, B.J., Parsons, W.F.J., Bockheim, J.G., Karnosky, D.F., Hendrey, G.R., Pregitzer, K.S., Isebrands, J.G. & Sober, J. 2001 Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) Environ. Pollut. 115 395 404

    • Search Google Scholar
    • Export Citation
  • Marrs, K.A. 1996 The functions and regulation of glutathione S-transferases in plants Annu. Rev. Plant Biol. 47 127 158

  • Mayer, R.R., Cherry, J.H. & Rhodes, D. 1990 Effects of heat shock on amino acid metabolism of cowpea cells Plant Physiol. 94 796 810

  • Merewitz, E.B., Du, H., Yu, W., Liu, Y., Gianfagna, T. & Huang, B. 2012 Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation J. Expt. Bot. 63 1315 1328

    • Search Google Scholar
    • Export Citation
  • Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K. & Oliver, D.J. 2008 A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in arabidopsis Plant Physiol. 148 1603 1613

    • Search Google Scholar
    • Export Citation
  • Peñuelas, J. & Estiarte, M. 1998 Can elevated CO2 affect secondary metabolism and ecosystem function? Trends Ecol. Evol. 13 20 24

  • Pressey, R. 1991 Oxidized oligogalacturonides activate the oxidation of indoleacetic acid by peroxidase Plant Physiol. 96 1167 1170

  • Qaderi, M.M., Kurepin, L.V. & Reid, D.M. 2006 Growth and physiological responses of canola (Brassica napus) to three components of global climate change: Temperature, carbon dioxide and drought Physiol. Plant. 128 710 721

    • Search Google Scholar
    • Export Citation
  • Qiu, Y., Su, M., Liu, Y., Chen, M., Gu, J., Zhang, J. & Jia, W. 2007 Application of ethyl chloroformate derivatization for gas chromatography–mass spectrometry based metabonomic profiling Anal. Chim. Acta 583 277 283

    • Search Google Scholar
    • Export Citation
  • Raggi, V. 1994 Changes in free amino acids and osmotic adjustment in leaves of water-stressed bean Physiol. Plant. 91 427 434

  • Reddy, A.R., Rasineni, G.K. & Raghavendra, A.S. 2010 The impact of global elevated CO2 concentration on photosynthesis and plant productivity Curr. Sci. 99 46 57

    • Search Google Scholar
    • Export Citation
  • Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. & Mittler, R. 2004 When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress Plant Physiol. 134 1683 1696

    • Search Google Scholar
    • Export Citation
  • Roessner, U., Wagner, C., Kopka, J., Trethewey, R.N. & Willmitzer, L. 2000 Simultaneous analysis of metabolites in potato tuber by gas chromatography–mass spectrometry J. Plant 23 131 142

    • Search Google Scholar
    • Export Citation
  • Sairam, R.K., Srivastava, G.C. & Saxena, D.C. 2000 Increased antioxidant activity under elevated temperatures: A mechanism of heat stress tolerance in wheat genotypes Biol. Plant. 43 245 251

    • Search Google Scholar
    • Export Citation
  • Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M. & Kopka, J. 2008 Plant metabolomics reveals conserved and divergent metabolic responses to salinity Physiol. Plant. 132 209 219

    • Search Google Scholar
    • Export Citation
  • Shao, L., Shu, Z., Sun, S.L., Peng, C.L., Wang, X.J. & Lin, Z.F. 2007 Antioxidation of anthocyanins in photosynthesis under high temperature stress J. Integr. Plant Biol. 49 1341 1351

    • Search Google Scholar
    • Export Citation
  • Sharrow, S.H. 1984 A simple disk meter for measurement of pasture height and forage bulk J. Range Manage. 37 94 95

  • Singh, B. 1999 Plant amino acids: Biochemistry and biotechnology. CRC Press, Boca Raton, FL

  • Tschaplinski, T.J., Stewart, D.B. & Norby, R.J. 1995 Interactions between drought and elevated CO2 on osmotic adjustment and solute concentrations of tree seedlings New Phytol. 131 169 177

    • Search Google Scholar
    • Export Citation
  • Turgeon, A.J. 1996 Turfgrass management. 4th Ed. Prentice-Hall, Upper Saddle River, NJ

  • Urbonaviciute, A., Samuoliene, G., Sakalauskaite, J., Duchovskis, P., Brazaityte, A., Siksnianiene, J.B., Ulinskaite, R., Sabajeviene, G. & Baranauskis, K. 2006 The effect of elevated CO2 concentrations on leaf carbohydrate, chlorophyll contents and photosynthesis in radish Pol. J. Environ. Stud. 15 921 925

    • Search Google Scholar
    • Export Citation
  • Xu, C. & Huang, B. 2012 Proteins and metabolites regulated by trinexapac-ethyl in relation to drought tolerance in kentucky bluegrass J. Plant Growth Regul. 31 25 37

    • Search Google Scholar
    • Export Citation
  • Yu, J., Chen, L., Xu, M. & Huang, B. 2012 Effects of elevated CO2 on physiological responses of tall fescue (Festuca arundinacea) to elevated temperature, drought stress, and the combined stresses Crop Sci. (in press)

    • Search Google Scholar
    • Export Citation
  • Zhang, Z.S., Li, R.Q. & Wang, J.B. 2001 Effects of oxalate treatment on the membrane permeability and calcium distribution in pepper leaves under heat stress Acta Phytophysiol. Sinica 27 109 113

    • Search Google Scholar
    • Export Citation
  • Ziska, L.H. & Bunce, J.A. 1993 Inhibition of whole plant respiration by elevated CO2 as modified by growth temperature Physiol. Plant. 87 459 466

  • Zobayed, S.M.A., Afreen, F. & Kozai, T. 2005 Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in st. john's wort Plant Physiol. Biochem. 43 977 984

    • Search Google Scholar
    • Export Citation
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