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TURFGRASS SCIENCE

Effects of Differential Air and Soil Temperature on Carbohydrate Metabolism in Creeping Bentgrass

Dep. of Horticulture, Forestry, and Recreation Resources, Kansas State Univ., Manhattan, KS 66506-5506 USA

bhuang{at}oz.oznet.ksu.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Bentgrass quality often declines under high temperature conditions. The physiological mechanisms of heat stress injury in creeping bentgrass are not well understood. The objective of this study was to determine the relative importance of air vs. soil temperature in the regulation of carbohydrate metabolism in two cultivars of creeping bentgrass (Agrostis palustris Huds.), `L-93' and `Penncross'. Shoots and roots of both cultivars were exposed to four differential air/soil temperatures: 20/20 (control), 20/35, 35/20, and 35/35°C in growth chambers and water baths. Under high soil (20/35) and high air/soil (35/35°C) temperature conditions, canopy net photosynthetic rate (P_n) of L-93 and Penncross decreased dramatically; however, respiration rates of whole plants (R_plant) and roots (R_root) increased to levels above those at 20/20 and 35/20°C within 8 d of treatment and then decreased to lower levels by 21 d after treatment. At 35/35°C, daily carbon consumption was 2 to 5 times carbon production for L-93 and 3.5 to 12 times for Penncross. At 20/35°C, carbon consumption exceeded production within 10 d of treatment for both cultivars. Total nonstructural carbohydrate (TNC) contents in shoots and roots were reduced at 20/35, 35/20, and 35/35°C, compared to that at 20/20°C. Reducing soil temperature while exposing shoots to high temperature (35/20°C) increased P_n and carbohydrate content and reduced the carbon consumption to production ratio. The results suggested that roots play more important role than shoots in the mediation of carbohydrate responses to high air temperatures or high soil temperatures. High soil temperature alone or combined with high air temperature caused imbalance between photosynthesis and respiration and decreases in carbohydrate availability, which could contribute to the decline in shoot and root growth under high temperature conditions.

Abbreviations: LSD, least significance difference • P_n, photosynthetic rate • R_plant, Whole-plant respiration rate • R_root, root respiration rate • TNC, total nonstructural carbohydrate

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
HIGH TEMPERATURE is a major factor limiting shoot and root growth of creeping bentgrass during summer in warm climate and the transitional regions. In these areas, roots often are exposed to supraoptimal soil temperatures, which may reach injuriously high levels and profoundly affect shoot growth and even survival of creeping bentgrass. Soil temperature strongly influences growth of shoots in various species (Aldous and Kaufmann, 1979; Kuryanagi and Paulsen, 1988; Martin et al., 1989; Ruter and Ingram, 1990; McMichael and Burke, 1994; Udomprasert et al., 1995a,b; Ziska, 1998; Xu and Huang, 2000) and appears to be more critical than air temperature in controlling plant growth (Aldous and Kaufmann, 1979; Kuryanagi and Paulsen, 1988; Xu and Huang, 2000). In creeping bentgrass, Xu and Huang (2000) reported that exposing roots to high temperature (35°C) while maintaining shoots at the optimum level (20°C) caused severe damage to both shoot and root growth. In contrast, maintaining roots at the optimum temperature while exposing shoots to high temperatures improved shoot and root growth to the level close to those plants which both shoots and roots were grown at the optimum temperature. There is limited understanding of the physiological mechanisms underlying the effects of soil temperature on plant growth and tolerance to heat stress. Soil temperature may regulate plant growth response to heat stress by altering carbohydrate metabolism.

Photosynthesis is extremely sensitive to supraoptimal temperature and is often the first metabolic process that is damaged (Paulsen, 1994). Severe reduction in photosynthetic rate under supraoptimal temperature conditions has been observed in many plant species (Pearcy, 1977; Grover et al., 1986; Harding et al., 1990a, b; Wolf et al., 1990; Midmore and Prange, 1992; Stamps, 1994; Schwarz et al., 1997; Madsen and Brix, 1997; Huang et al., 1998a; Huang and Gao, 2000). Dark respiration rate often increases initially with increasing temperatures (Hansen and Jensen, 1977; Deal et al., 1990; Wolf et al., 1990; Ruter and Ingram, 1991; Huang et al., 1998a; Huang and Gao, 2000). However, the optimum temperature for photosynthesis is lower than that for respiration (Nilsen and Orcutt, 1996). Therefore, high temperatures may cause an imbalance between photosynthesis and respiration processes and carbohydrate depletion, particularly for creeping bentgrass that is mowed daily at low mowing height. Low mowing when temperature is high during summer imposes additional stress on the turf by removing large amounts of leaf area that are used for photosynthesis, while respiration continues (Huang et al., 1998a).

The present study was designed (i) to compare the differential effects of air vs. soil temperature on photosynthesis, respiration, and carbohydrate allocation and accumulation; and (ii) to determine whether heat stress injury to shoots from high air temperature or to roots from high soil temperature is related to alteration in carbohydrate metabolism in two cultivars of creeping bentgrass differing in heat tolerance. Previous studies (Huang et al., 1998a,b; Liu and Huang, 2000) demonstrated that L-93 is more heat tolerant than Penncross.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Sod pieces of Penncross and L-93 were collected from the Rocky Ford Turfgrass Research Center, Manhattan, KS and transplanted to a mixture (9:1, v/v) of sand and fritted clay (Profile, AILMOR, Deerfield, IL) in clear polyethylene bags (5 cm in diameter and 40 cm in length, with holes pierced at the bottom for drainage). The soil mix contained no organic matter and was sterilized before filling the bags to minimize soil microbial respiration. The polyethylene bags were placed in polyvinylchloride (PVC) tubes of the same diameter and length, which were installed vertically in water baths. These were designed in a way that enabled plant to grow in well-drained soil , while soil temperature was controlled at a constant, predetermined level. Two water baths were placed in each growth chamber. Plants were grown in growth chambers at 20/15°C (day/night), 400 µmol m^-2 s^-1 photosynthetic photon flux density, and a 13-h photoperiod for 40 d before differential air/soil temperature treatments were imposed. Before and during temperature treatments, turf in each container was mowed daily at 3- to 4-mm height with an electric hair clipper, watered daily until soil moisture reached field capacity, and fertilized weekly with 100 mL full-strength Hoagland's nutrient solution (Hoagland and Arnon, 1950). Polyethylene bags containing the soil mix without grasses were placed in each treatment and received the same amounts of water and fertilizers as the grassed bags.

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

Air temperatures at various distances from the canopy and soil temperatures at different depths from the soil surface were measured with thermocouples connected to a thermometer (Xu and Huang, 2000). In the 20/20°C treatment, both shoots and roots were maintained around 20°C; in the 20/35°C treatment, air temperature ranged from 23 to 25°C, and root-zone temperature was about 35°C; in the 35/20°C treatment, air temperature ranged from 32 to 35°C, while root-zone temperature ranged from 18 to 21°C; and in the 35/35°C treatment, air and root-zone temperatures were maintained at 33 to 36°C. Each temperature treatment was repeated in four water baths and growth chambers.

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

Canopy net photosynthetic rate (P_n) was measured from 1000 to 1400 h at various days of treatment using an LI-6400 portable gas exchange system (LI-COR Inc., Lincoln, NE). Dark respiration rates of the whole plant (shoots and roots) and soil (R_plant+soil), bare soil without grasses growing (R_soil), and roots and soil (R_root+soil) after detopping the shoots were measured during the night from 2000 to 2400 h with the LI-6400. The differences between R_plant+soil and R_root+soil vs. R_soil were used to estimate R_plant and R_root as described in Biscoe et al. (1975) and Huang and Gao (2000). The P_n was expressed as CO₂ uptake, and R_plant, and R_root were expressed as CO₂ evolution per unit canopy area, respectively. The amount of carbon consumed in respiration as a proportion of that produced in photosynthesis per day was calculated using the data of P_n and R_plant integrated over a 13-h photoperiod and an 11-h dark period, respectively. Daily carbon consumption to production ratio = (R_plant x 11)/(P_n x 13).

Total nonstructural carbohydrate (TNC) was determined using the method described by Ting (1959). Briefly, 20 to 50 mg oven-dried samples were transferred to 0.5 mL 0.1% clarase solutions and incubated at 38°C for 24 h. One milliters of hydrochloric acid (50%, v/v) then was added to the incubation solution. After the solution was incubated at room temperature for 18 h, 0.5 mL of 10 M NaOH solution was added. The pH value of the solution was adjusted to between 5 and 7 with 10 M NaOH solution. One milliliter of the solution was transferred to a 100-mL flask, and 5 mL of ferricyanide reagent was added. Then the flasks were placed in a boiling water bath for 10 min. After heating, the flasks were cooled quickly in running water. The solutions were neutralized partially with 10 mL of 1 M H₂SO₄ solution and mixed thoroughly until no more gas was evolved. Four milliliters of arsenomolybdate were added, and solutions were mixed again and then diluted to volume. The absorbance of the solution was measured at 515 nm with a spectrophotometer (Spectronic Instruments, Inc. Rochester, NY).

The carbon allocation pattern was determined using pulse ¹⁴CO₂ labeling technique. Plants were enclosed in a clear plexiglass chamber (5 cm tall and 10 cm in diameter) and exposed to 7 µCi ¹⁴CO₂ for 20 min. Excessive ¹⁴CO₂ in the chamber was absorbed by bubbling the air in the chamber through a saturated NaOH solution for 10 min. Three days after labeling, shoots and roots were harvested, killed by exposure to 105°C for 15 min, and then dried in an oven at 75°C for 48 h. The samples were oxidized with a biological oxidizer (R.J. Harvey Instrument Corp., Hillsdale, NJ). ¹⁴C activities in shoots and roots were measured with a liquid scintillation analyzer (Packard, Deers Grove, IL) and the proportion of carbon allocated to roots was calculated.

	Results

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Canopy Net Photosynthetic Rate (P_n)
Canopy P_n of Penncross and L-93 declined to below the control level (20/20°C) when either roots alone (20/35°C) or both shoots and roots (35/35C) were exposed to high temperatures (Fig. 1) . The P_n at 20/35°C was significantly higher than that at 35/35°C after 8 d of treatment for L-93 and within the first 20 d for Penncross. The P_n at 35/20°C was not different from that at 20/20°C for both cultivars, but was higher than that at 35/35°C after 1 d and than that at 20/35 after 34 d, especially for Penncross.

View larger version (24K): [in this window] [in a new window]   Fig. 1 Canopy photosynthesis (Pn) as affected by differential air/soil temperatures. Vertical bars indicate LSD for treatment comparisons at a given day of treatment

Whole-Plant Respiration Rate (R_plant)
The R_plant at 20/35 and 35/35°C increased to above the control (20/20°C) level at 1 d of treatment and remained until 8 d for both cultivars (Fig. 2) . The increase in R_plant within the first 8 d of treatment at 35/35°C was more dramatic for Penncross than for L-93. The R_plant decreased to below the control level after 35 d at both 20/35 and 35/35°C for Penncross but only at 35/35°C for L-93. The R_plant at 35/20°C was not significantly different from that at 20/20°C for either cultivar during the entire experimental period, but was lower than those at 20/35 and 35/35°C within 8 d of treatment for both cultivars. After 34 d of treatment, it was higher than those at 20/35 and 35/35°C for Penncross and higher than that at 35/35°C for L-93. At 35/35°C, L-93 maintained a lower respiration rate than Penncross during the first 8 d of treatment. At 20/35°C, L-93 had a higher respiration rate than Penncross after 34 d. Both cultivars had similar R_plant at 35/20 and 20/20°C. At 20/20 and 35/20°C, P_n was greater than R_plant; however, at 20/35 and 35/35, R_plant was higher than P_n for both cultivars (Fig. 1 and 2).

View larger version (23K): [in this window] [in a new window]   Fig. 2 Whole-plant respiration rate (Rplant) as affected by differential air/soil temperatures. Vertical bars indicate LSD for treatment comparisons at a given day of treatment

View larger version (20K): [in this window] [in a new window]   Fig. 3 Root respiration rate (Rroot) as affected by differential air/soil temperatures. Vertical bars indicate LSD for treatment comparisons at a given day of treatment

View larger version (25K): [in this window] [in a new window]   Fig. 4 The ratio of daily carbon consumption in respiration to carbon production in photosynthesis as affected by differential air/soil temperatures

View larger version (33K): [in this window] [in a new window]   Fig. 5 Total nonstructural carbohydrate (TNC) content in shoots and roots as affected by differential air/soil temperatures. Columns marked with the same letters are not significantly different based on an LSD test . The lowercase letters indicate cultivar comparisons within a given air/soil temperature. The uppercase letters indicate air/soil temperature comparisons for a given cultivar

Carbon-14 Allocation to Roots
The proportions of newly photosynthesized ¹⁴C allocated to roots of both cultivars were significantly lower than the control at 35/20 and 35/35°C after 23, 36, and 50 d of treatment and at 20/35°C after 23 and 36 d of treatment (Fig. 6) . The proportion of carbon allocation to roots was higher at 35/20 than at 35/35°C for L-93 after 23, 36, and 50 d and for Penncross after 36 and 50 d, but was not different between 20/35 and 35/20°C. Specifically, an average of 25.0% of the total newly fixed ¹⁴C was allocated to roots for L-93 and 22.3% for Penncross at 20/20°C; 13% for L-93 and 12.0% for Penncross at 35/20°C; 13.5% for L-93 and 11.7% for Penncross at 20/35°C; and 3.7% for L-93 and 3.3% for Penncross at 35/35°C.

View larger version (19K): [in this window] [in a new window]   Fig. 6 Carbon allocation to roots as affected by differential air/soil temperatures. Vertical bars indicate LSD for treatment comparisons at a given day of treatment

	Discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

The imbalance between carbon consumption and production and decreases in carbohydrate availability under high temperature conditions were caused mainly by the reduction in photosynthetic rate, because respiration rates were affected to a much lesser extent. Canopy P_n of both cultivars was reduced almost immediately after roots alone or both shoots and roots were exposed to high temperatures and declined rapidly to zero. Decreased P_n in response to supraoptimal soil temperatures also has been reported by others (Gur et al., 1972; Al-Khatib and Paulsen, 1984; Foster, 1986; Ruter and Ingram, 1992; Ziska, 1998). Such decreases in P_n could be due to the interruption of electron transport in photosystem II (Harding et al., 1990a); reduction in the activity of RuBP carboxylase (Grover et al., 1986; Ruter and Ingram, 1992); decreased chlorophyll content (Huang et al., 1998a); and leaf senescence caused by decreased cytokinin activity at elevated root-zone temperatures (Gur et al., 1972).

Respiration rate often increases with increasing temperatures (Ruter and Ingram, 1990, 1991; Huang and Gao, 2000). In our study, both R_plant and R_root increased during the initial 8 d of exposure of roots alone or both roots and shoots to heat stress and then rapidly declined. However, R_plant was higher than P_n under either high soil or air/soil temperatures. Increased root respiration during the initial periods of heat stress may cause more consumption of carbohydrates. Increased soil temperature mainly elevates root maintenance respiration (Szaniawski and Kielkiewicz, 1982), which may result in insufficient carbohydrate levels needed for growth respiration and, thus, decreased growth (Gent and Enoch, 1983). The decreases in R_plant or R_root after prolonged periods of heat stress may be due to limited carbohydrate availability and to the progressive degradation of enzymatic processes (Hurewitz and Janes, 1983).

Supraoptimal soil temperature alone or combined air/soil temperature inhibited ¹⁴C allocation to roots in both cultivars, as found in other species (Ruter and Ingram, 1990; Sattelmacher et al., 1990). The reduction in TNC content under high temperatures was also more severe for roots than for shoots. These results indicated that roots had lower priority than shoots when carbohydrates become limited during heat stress. Foster (1986) proposed that decreases in the amount of carbon allocated to roots when exposed to high soil temperatures was due to a physical blockage of the vascular system or to the loss of carbon as a result of increased root respiration rate. Less carbon allocated to roots and less carbohydrate in roots may result in the limited growth and death of roots that occur under high soil or air/soil temperature conditions in these two cultivars of creeping bentgrass (Xu and Huang, 2000). Schmidt and Snyder (1984) also reported TNC decreased as ambient temperatures were elevated in creeping bentgrass. However, Duff and Beard (1974) reported increased photosynthetic rate and increased level of ethanol and water-soluble sugars in creeping bentgrass with increasing temperatures. Both studies did not distinguish the effects of high soil temperature from high air temperatures.

Maintaining soil temperature at the optimum level while shoots were exposed to supraoptimal temperatures improved canopy P_n, reduced carbon consumption to production ratio, enhanced carbohydrate accumulation in roots, and increased carbon allocation to roots in both cultivars. Improved photosynthesis (Martin et al., 1989; Udomprasert et al., 1995b), more carbon allocation to roots (Ruter and Ingram, 1990), and delayed leaf senescence (Kuryanagi and Paulsen, 1988) in response to reduced soil temperature have been reported in several other species. In contrast, reducing air temperature while exposing roots to high temperatures had detrimental effects on carbohydrate metabolism. These results suggested that soil temperature was more important than air temperature in the regulation of photosynthesis, whole-plant or root respiration, and carbohydrate accumulation and partitioning.

In summary, this study clearly demonstrated that negative carbon balance and decreases in carbohydrate availability, especially decline in photosynthesis, contributed to the damage to shoots from high air temperatures or to roots from high soil temperatures. Moreover, roots played more important role than shoots in regulating carbohydrate metabolic responses to heat stress. Reducing soil temperature improved growth of creeping bentgrass under supraoptimal ambient temperatures (Xu and Huang, 2000), which could at least partially by maintaining a positive carbon balance.

	ACKNOWLEDGMENTS

 
Funds were provided by the United States Golf Association and Kansas Turfgrass Foundation. Contribution No. 00-78-J from Kansas Agricultural Experiment Station.

Received for publication November 15, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 

• Aldous D.E., Kaufmann J.E. Role of root temperature on shoot growth of two Kentucky bluegrass cultivars. Agron. J. 1979;71:545-547.[Abstract/Free Full Text]
• Al-Khatib K., Paulsen G.M. High-temperature effects on photosythetic processes in temperate and tropical cereals. Crop Sci. 1984;39:119-125.[Abstract/Free Full Text]
• Biscoe P.V., Scott R.K., Monteith J.L. Barley and its environment. III. Carbon budget of the stand. J. Appl. Ecol. 1975;12:269-293.
• Deal D.L., Raulston J.C., Hinesley L.E. High temperature effects on apical bud morphology, dark respiration, and fixed growth of blue spruce. Can. J. For. Res. 1990;20:1871-1877.
• Duff D.T., Beard J.B. Supraoptimal temperature effects upon Agrostis palustris. Part II. Influence on carbohydrate levels, photosynthetic rate, and respiration rate. Physiol. Plant. 1974;32:18-22.
• Foster, T.A. 1986. Photosynthesis, respiration, and carbohydrate partitioning in IIex crenata `rotundifolia' in response to supraoptimal root-zone temperatures. M.S. Thesis, Univ. of Florida, Gainsville, FL.
• Gent M.P.N., Enoch H.Z. Temperature dependence of vegetative growth and dark respiration: A mathematical model. Plant Physiol. 1983;71:562-567.[Abstract/Free Full Text]
• Grover A., Sabat S.C., Gepstein P. Effect of temperature on photosynthetic activities of senescing detached wheat leaves. Plant Cell Physiol. 1986;27:117-126.[Abstract/Free Full Text]
• Gur A., Bravado B., Mizirahi Y. Physiological response of apple trees to supraoptimal root temperatures. Physiol. Plant 1972;27:130-138.
• Hansen G.K., Jensen C.R. Growth and maintenance in whole plants, tops, and roots of Lolium multiflorum. Physiol. Plant. 1977;39:155-164.
• Harding S.A., Guikema J.A., Paulsen G.M. Photosynthetic decline from high temperature stress during maturation of wheat. II. Interaction with source and sink processes. Plant Physiol. 1990;92:654-658 a.[Abstract/Free Full Text]
• Harding S.A., Guikema J.A., Paulsen G.M. Photosynthetic decline from high temperature stress during maturation of wheat. I. Interaction with senescence processes. Plant Physiol. 1990;92:648-653 b.[Abstract/Free Full Text]
• Hoagland D.R., Arnon D.I. The water-culture method for growing plants without soil. Davis: Circular 347. California Agric. Exp. Stn, 1950.
• Huang B., Liu X., Fry J.D. Shoot physiological responses of two bentgrass cultivars to high temperature and poor soil aeration. Crop Sci. 1998;38:1219-1224 a.[Abstract/Free Full Text]
• Huang B., Liu X., Fry J.D. Effects of high temperature and poor soil aeration on root growth and viability of creeping bentgrass. Crop Sci. 1998;38:1618-1622 b.[Abstract/Free Full Text]
• Huang B., Gao H. Growth and carbohydrate metabolism of creeping bentgrass in response to increasing temperatures. Crop Sci. 2000;40:1119-1124.
• Hurewitz J., Janes H.W. Effect of altering the root-zone temperature on growth, translocation, carbon exchange rate, and leaf starch accumulation in the tomato. Plant Physiol. 1983;73:46-50.[Abstract/Free Full Text]
• Kempthorne O. The design and analysis of experiments. New York: John Wiley and Sons, 1952.
• Kuryanagi T., Paulsen G.M. Mediation of high-temperature injury by roots and shoots during reproductive growth of wheat. Plant Cell Environ. 1988;11:517-523.
• Liu X., Huang B. Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 2000;40:503-510.[Abstract/Free Full Text]
• Madsen T.V., Brix H. Growth, photosynthesis and acclimation by two submerged macrophytes in relation to temperature. Oecologia 1997;110:320-327.
• Martin C.A., Ingram D.L., Nell T.A. Supraoptimal root-zone temperature alters growth and photosynthesis of holly and elm. J. Arboric. 1989;15:272-276.
• McMichael B.L., Burke J.J. Metabolic activity of cotton roots in response to temperature. Environ. Exp. Bot. 1994;34:201-206.
• Midmore D.J., Prange R.K. Growth responses of two Solanum species to contrasting temperatures and irradiance levels: Relations to photosynthesis, dark respiration and chlorophyll fluorescence. Ann. Bot. (London) 1992;69:13-30.[Abstract/Free Full Text]
• Nilsen, E.T., and D.M. Orcutt. 1996. Physiology of Plants under Stress: Abiotic Factors. p. 463. John Wiley & Sons, Inc., New York.
• Paulsen G.M. High temperature responses of crop plants. In: Boote K.J., Bennett J.M., Sinclair T.R., Paulsen G.M., eds. Physiology and determination of crop yield. Madison WI: ASA, CSSA, SSSA, 1994:365-389.
• Pearcy R.W. Effects of growth temperature on the thermal stability of the photosynthetic apparatus of Atriplex lentiformis (Torr.) Wats. Plant Physiol. 1977;59:873-878.[Abstract/Free Full Text]
• Ruter J.M., Ingram D.L. <sup>14</sup>Carbon-labeled photosynthate paritioning in Ilex crenata `rotundifolia' at supraoptimal root-zone temperatures. J. Am. Soc. Hort. Sci. 1990;115:1008-1013.[Abstract/Free Full Text]
• Ruter J.M., Ingram D.L. Root respiratory characteristics of `rotundifolia' holly under supraoptimal temperatures. J. Am. Soc. Hort. Sci. 1991;116:560-564.[Abstract/Free Full Text]
• Ruter J.M., Ingram D.L. High root-zone temperatures influence Rubisco activity and pigment accumulation in leaves of `rotundifolia' holly. J. Am. Soc. Hort. Sci. 1992;117:154-157.[Abstract/Free Full Text]
• Sattelmacher B., Marschner H., Kuhne R. Effects of root zone temperature on root activity of two potato (Solanum tuberosum L.) clones with different adaptation to high temperature. J. Agron. Crop Sci. 1990;165:131-137.
• Schmidt R.E., Snyder V. Effects of N, temperature, and moisture stress on the growth and physiology of creeping bentgrass and response to chelated iron. Agron. J. 1984;76:590-594.[Abstract/Free Full Text]
• Schwarz P.A., Fahey T.J., Dawson T.E. Seasonal air and soil temperature effects on photosynthesis in red spruce (Picea rubens) saplings. Tree Physiol. 1997;17:187-194.
• Stamps R.H. Production temperatures influence growth and physiology of leather leaf fern. HortScience. 1994;29:67-70.
• Szaniawski R., Kielkiewicz M. Maintenance and growth respiration in shoots and roots of sunflower plants grown at different root temperatures. Physiol. Plant. 1982;54:500-504.
• Ting S.V. Rapid colorimetric methods for simultaneous determination of total reducing sugars and fructose in citrus juices. Fruit Juice Assoc. 1959;4:263-266.
• Udomprasert N., Li P.H., Davis D.W., Markhart A.M., III. Root cytokinin level in relation to heat tolerance of Phaseolus acutifolius and Phaseolus vulgaris. Crop Sci. 1995;35:486-490 a.[Abstract/Free Full Text]
• Udomprasert N., Li P.H., Davis D.W., Markhart A.M., III. Effects of root temperature on leaf gas exchange and growth at high air temperature in Phaseolus acutifolius and Phaseolus vulgaris. Crop Sci. 1995;35:486-490 b.
• Wolf S., Olesinski A.A., Rudich J., Marani Effect of high temperature on photosynthesis in potatoes. Ann. Bot. (London) 1990;65:179-185.[Abstract/Free Full Text]
• Xu Q., Huang B. Growth and physiological responses of creeping bentgrass to changes in shoot and root temperatures. Crop Sci. 2000;40:1363-1368.[Abstract/Free Full Text]
• Ziska L.A. The influence of root zone temperature on photosynthetic acclimation to elevated carbon dioxide concentrations. Ann. Bot. (London) 1998;81:717-721.[Abstract/Free Full Text]

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				B. Huang, X. Liu, and Q. Xu Supraoptimal Soil Temperatures Induced Oxidative Stress in Leaves of Creeping Bentgrass Cultivars Differing in Heat Tolerance Crop Sci., March 1, 2001; 41(2): 430 - 435. [Abstract] [Full Text] [PDF]

				Q. Xu and B. Huang Morphological and Physiological Characteristics Associated with Heat Tolerance in Creeping Bentgrass Crop Sci., January 1, 2001; 41(1): 127 - 133. [Abstract] [Full Text] [PDF]

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