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Scientia Horticulturae 115 (2008) 190–195

Effects of simultaneous drought and heat stress on Kentucky bluegrass

Jinrong Liu a,b,1, Xiaorong Xie a,1, Jianxiong Du b,c, Jixiong Sun b,*, Xiaomin Bai b

a Department of Biology, Key Laboratory of Resources, Environment and Chemistry of West China, Hexi University, Gansu, Zhangye 734000, Chinab College of Grassland, Gansu Agricultural University, Gansu, Lanzhou 730070, China

c School of Resources and Environmental Management, Guizhou College of Finance and Economics, Guizhou, Guiyang 550004, China

Received 25 November 2006; received in revised form 7 June 2007; accepted 14 August 2007

Abstract

Growth of Kentucky bluegrass (Poa pratensis L.) is limited by drought and heat stress during summer. Understanding the factors associated with

performance under drought and heat stress is important for identifying drought and heat stress tolerant germplasm. The objective of this study was

to study morphological and physiological responses of five Kentucky bluegrass cultivars subjected to drought and high temperature stress

conditions in northwestern arid region of China. Award, Conni, Nuglade, Impact, and Bluechip were grown in three containers (replicates) and

exposed to day/night temperatures of 26–37/20–26 8C by withholding irrigation for 21 d until complete leaf wilting of most plants. During the

stress period, all measurements were made 3 d intervals in this experiment. Relative water content (RWC), electrolyte leakage (EL), leaf wilting

(LW), turf quality (TQ), superoxide dismutase (SOD), catalase (CAT), and malondialdehyde (MDA) were determined. Simultaneous drought and

heat stresses induced oxidative injury in all cultivars, as demonstrated by the reduction in antioxidant enzymes and increase in lipid peroxidation.

Meanwhile it caused turf quality and relative water content to decline, while electrolyte leakage and leaf wilting increased with prolonged stress

treatments. All the physiological index under combined drought and heat stress were significantly correlated each other except SOD. This result

indicated that when Kentucky bluegrass was stressed by drought and heat, increasing of SOD activity cannot inhibit formation and accumulation of

free radicals, and only delay accumulation of free radicals to a certain extent, in order to alleviate active oxygen damage to cells.

# 2007 Elsevier B.V. All rights reserved.

Keywords: Turfgrass; Leaf water content; Leaf wilting; Turf quality; Antioxidant enzymes; Lipid peroxidation

1. Introduction

Kentucky bluegrass is a cool-season grass, which is

considered by many to be a stress premier lawn grass that

can form an attractive, durable, persistent turf (Meyer and Funk,

1989). The optimum temperature for shoot growth of cool-

season grasses is 15–23 8C (Beard, 1973). However, tempera-

tures in northwestern arid region of China often approach 38 8Cor higher during summer months. At the same time, water

deficit is a very serious problem. Drought often lasts for long

time. Therefore, drought and heat stresses are two major factors

limiting the growth of cool-season grasses. An understanding of

the growth responses involved in summer stress tolerance may

enable plant breeders to enhance selection and screening

strategies used to identify improved cultivars.

* Corresponding author.

E-mail addresses: ljr2197@163.com (J. Liu), sunjixiong.725@163.com

(J. Sun).1 These authors contributed equally to this research.

0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved.

doi:10.1016/j.scienta.2007.08.003

The deleterious effects of combined drought and heat stress

are associated with damage to cell membrane and antioxidant

system in perennial ryegrass (Lolium perenne L.) and tall fescue

(Festuca arundinacea Shreb.) (Chen et al., 1988; Jiang and

Huang, 2001a), which reduced leaf water content in wheat

(Triticum aestivum L.) (Shah, 1992); led to severe decline in

turf quality under field conditions (Jiang and Huang, 2001a).

Drought and heat stress can cause oxidative stress through

the production of reactive oxygen species such as superoxide

radicals and hydrogen peroxide. Reactive oxygen species can

cause lipid peroxidation, in turn damage cell membranes

(Smirnoff, 1993; Foyer et al., 1994). It is well documented that

a critical component of the dehydration tolerance for grasses is

cell membrane stability (Crowe et al., 1987; Volaire and

Lelievre, 2001). In fact, the resistant cultivars exhibited better

membrane stability than susceptible ones under simultaneous

drought and heat stress, as demonstrated by the lower EL.

Drought or heat-induced oxidative damage is related to the

suppression of activities of antioxidant enzymes, such as SOD

and CAT (Smirnoff, 1993; Foyer et al., 1994; Zhang and

J. Liu et al. / Scientia Horticulturae 115 (2008) 190–195 191

Kirkham, 1996; Fu and Huang, 2001). These are two key

enzymes plants evolved to quench reactive oxygen species and

protect plants from oxidative damage (Bowler et al., 1992).

However, how drought and heat stresses interact and

influence growth of cool-season turfgrasses is not well

understood. Knowledge of this interaction would help to

identify physiological factors involved in drought and heat

tolerances to improve summer performance of cool-season

turfgrasses. This research will provide documentation for

breeding/selection of higher drought and heat resistance cool-

season turfgrass in arid and hot temperature region.

The experiment was conducted to investigate the response to

simultaneous drought and heat stresses in five Kentucky

bluegrass cultivars. The objectives of the experiment were (i) to

evaluate the effects of the combined stresses on growth and

physiological activities of Kentucky bluegrass and (ii) to

identify the drought and heat tolerance of Kentucky bluegrass

cultivars in northwestern arid region of China and similar arid

regions of the world.

2. Materials and methods

2.1. Plant materials and growth conditions

The experiment was conducted at the Gansu Agricultural

University Research Field, China (latitude, 368030N; longitude,

1038530E) from May to August 2005 and the same time in 2006

the study was repeated again. Five cultivars (Bluechip, Conni,

Nuglade, Impact, and Award) were provided by China National

Seed Group Corporation implored from USA. Each Kentucky

bluegrass was grown in brick-built containers 0.7 m � 1.5 m

� 0.6 m deep, filled with 5 cm gravel for drainage, 45 cm

sterilized topsoil and 5 cm organic compost in the greenhouse for

about 2 months and fertilized twice with controlled-release

fertilizer (N–P–K, 16–4–8) before the drying treatment was

imposed. The soil texture was clay-loam (37% clay, 27% silt and

36% sand) with 0.87% organic matter and a pH of 7.4. Absor-

bable N, P, and K were 114, 72, and 220 ppm, respectively. Each

container was watered once weekly. Turf was clipped weekly at a

5-cm height. The clippings after each mowing were removed.

The experiments were design in a randomized complete block

design with six replicates in July 2005 and 2006, respectively.

Plants in six containers (replicates) for each cultivars was

exposed to simultaneous drought and heat stress by withholding

irrigation for 21 d until complete leaf wilting of most plants.

Mean day/night air temperatures of greenhouse ranged from

26–37/20–26 8C during the experiment. Relative humidity was

averaged (24 h) 65%. Photoperiod was averaged 13 h in the

greenhouse in the experiment, photosynthetically active

radiation of 600 mmol m�2 s�1. By 21 d of combined stress,

most plants turned to brown color.

3. Measurements

During the stress period, all measurements were made 3 d

intervals in the experiment. RWC, EL, LW, TQ, SOD, CAT, and

MDA were determined.

TQ was rated on a 0-to-9 scale, where 0 brown, dead turf; 6

acceptable quality for a home lawn; 9 optimum color, density,

and uniformity (Turgeon, 2002).

Leaf water status was determined by measuring relative

water content (RWC, %) calculated as follows (Barrs and

Weatherley, 1962): RWC = (FW–DW)/(SW–DW) � 100,

where FW is the leaf fresh weight, DW the dry weight of

leaves after drying at 85 8C for 2 d, and SW is the turgid weight

of leaves after being soaked in water for 4 h at room

temperature (approximately 20 8C).

Cell membrane stability was estimated by measuring EL

from leaf tissues. Samples of fresh leaves (0.1 g) were rinsed

with deionized water, immersed in 20 mL of deionized water,

and subjected to a vacuum of 48 kPa for 15 min. The

conductivity of the solution (Cinitial) was measured after the

leaves were shaken for 24 h using a conductivity meter (YSI-

3100, Guangzhou, China). Leaves then were killed by

autoclaving at 140 8C for 20 min. The conductivity of killed

tissues (Cmax) was measured after samples were cooled down to

room temperature. Relative EL was calculated as the

percentage of Cinitial over Cmax.

Leaf wilting percentage was determined by visually

estimating the total percentage of wilting leaf area. LW was

evaluated on 0-to-9 scale, where 0 no observable leaf wilting

and 9 completely wilted.

The activity of SOD was determined by measuring its ability

to inhibit the photoreduction of nitro blue tetrazolium (NBT)

following the method (Giannopolitis and Ries, 1977). The

reaction solution (3 mL) contained 50 mM NBT, 1.3 mM

riboflavin, 13 mM methionine, 75 mM EDTA, 50 mM phos-

phate buffer (pH 7.8), and 20–50 mL enzyme extract. Test tubes

containing the reaction solution and leaves were irradiated

under a light bank (15 fluorescent lamps) at 78 mmol m�2 s�1

for 15 min. The absorbance of the irradiated and nonirradiated

solution at 560 nm was determined with a spectrophotometer

(721/721-100, Shanghai, China). One unit of SOD activity was

defined as the amount of enzyme that would inhibit 50% of

NBT photoreduction.

Activity of CAT was measured using the following method

(Chance and Maehly, 1955) with modification. The CAT

reaction solution (3 mL) contained 50 mM phosphate buffer

(pH 7.0), 15 mM H2O2, and 0.1 mL enzyme extract. Reaction

was initiated by adding enzyme extract. Changes in absorbance

of the reaction solution at 240 nm were read every 20 s. One

unit CAT activity was defined as an absorbance change of

0.01 unit min�1.

The activity of each enzyme was expressed on a protein

basis. Protein concentration of the crude extract was measured

by the method (Bradford, 1976).

Lipid peroxidation was measured in terms of malondialde-

hyde(MDA) content (Dhindsa et al., 1981). About 1 mL MDA

extract was added to 4 mL of trichloroacetic acid containing

0.5% thiobarbituric acid [4,6(1H,5H)-pyrimidinedione]. The

solution was heated at 95 8C for 30 min and then quickly

cooled in running water. The solution was centrifuged at

10,000 � g for 10 min. The absorbance of the supernatant was

measured at 532 and 600 nm. The concentration of MDA was

J. Liu et al. / Scientia Horticulturae 115 (2008) 190–195192

calculated by subtraction of 600 from 532 and an extinction

coefficient of 155 mm�1 cm�1 for MDA (Heath and Packer,

1968).

3.1. Data collection

The RWC, EL, LW, TQ, SOD, CAT, and MDA at 0, 3, 6, 9,

12, 15, 18, and 21 d of combined drought and heat stress were

measured in 2005 and 2006.

Cultivar difference during combined stress, duration of

stress treatment, and the interaction of cultivar with stress

Fig. 1. Variation in (A) relative water content (RWC), (B) electrolyte leakage (EL), (

catalase (CAT), and (G) malondialdehyde (MDA) among five Kentucky bluegrass du

given day of treatment represents one cultivar. Vertical bars at the top or bottom of th

the given day of treatment.

treatment were determined by ANOVA according to the general

linear model procedure of SAS (SAS Institute, 1992). Means of

stress durations, and cultivars were tested with LSD at a

probability level of 0.05.

Correlation analysis at 21 d of combined stress was

conducted to determine relationships among RWC, EL, LW,

SOD, CAT, MDA, and TQ.

Data collection and statistical analysis come from six

containers (replicates) for each cultivar (three replicates

come from 2005, and another three replicates come from

2006).

C) leaf wilting (LW), (D) turf quality (TQ), (E) superoxide dismutase (SOD), (F)

ring the experiment of simultaneous drought and heat stress. Each data point at a

e figure indicate LSD values (P = 0.05) for the comparison between cultivars at

J. Liu et al. / Scientia Horticulturae 115 (2008) 190–195 193

4. Results

RWC started to decrease below the 0 d level at 6 d under

simultaneous drought and heat stress for five Kentucky

bluegrass cultivars (Fig. 1A). A more rapid and greater

decrease in RWC was observed for Award and Conni than

Nuglade, Impact, and Bluechip.

EL increased at 3 d of stress for Award, Conni, Nuglade and

Impact, and for Bluechip increased until 9 d (Fig. 1B). EL for

Award and Conni was significantly higher than that for

Nuglade, Impact, and Bluechip from 6 to 21 d of treatment.

LW rate began to increase under combined stress for Award

and Conni at 6 d, and for Nuglade, Impact, and Bluechip at 9 d

(Fig. 1C). However, LW for Award was dramatically higher

than that for the others from 9 to 21 d of stress.

TQ declined gradually with the combined stress to below the

0 d level at 6 d of stress for five cultivars. Bluechip and Impact

had higher turf quality than Award, Conni, and Nuglade

throughout most of the stress period, including the end of the

stress period (Fig. 1D).

The activity of two enzymes exhibited significant changes

under stress conditions. A slightly declined in SOD activity was

observed at 0–3 d of the combined stresses for five cultivars,

and then increased from 3 to 6 d. The activity of SOD decreased

rapidly to a level from 6 to 21 d of the combined stress for five

cultivars (Fig. 1E).

The response of CATactivity to the stresses was different from

that of SOD. A continuous decline in CAT activity was observed

in five cultivars during the entire experimental period under

combined stresses, starting at 3 d (Fig. 1F). Combined stresses

induced lipid peroxidation in five cultivars. MDA content exhi-

bited significant increases during the stress period (Fig. 1G).

Through correlation analysis at 21 d of combined stress, we

observed that RWC, TQ, and CAT had significant negative

correlation with EL, LW, and MDA under combined drought

and heat stress. However, SOD had significant positive

correlation with RWC and CAT at the 0.05 level, and had

negative correlation with MDA, EL, and LW without

significance (Table 1).

5. Discussion

Drought and heat tolerant turfgrasses are commonly able to

maintain high turf quality, leaf water status (or less leaf

wilting), but also low levels of EL (an indicator of cell

Table 1

Correlation analysis at 21 d of combined stress was conducted to determine relatio

RWC EL LW

RWC 1 �0.997** �0.960**

EL �0.997** 1 0.968**

LW �0.960** 0.968** 1

TQ 0.879* �0.857 �0.909*

SOD 0.881* �0.876 �0.860

CAT 0.952* �0.956* �0.980**

MDA �0.971** 0.976** 0.993**

** Correlation is significant at the 0.01 level (two-tailed).* Correlation is significant at the 0.05 level (two-tailed).

membrane stability) during drought stress (Huang and Gao,

1999; Qian and Fry, 1997). These physiological parameters

have been widely used as physiological indicators for the

selection of drought tolerant plant materials in turfgrasses and

other species (Blum and Pnuel, 1990; Bonos and Murphy, 1999;

Jiang and Huang, 2001).

RWC of five cultivars decreased to different extent. RWC of

Award reduced sharplier than the other cultivars, which reached

20.17% (Fig. 1A). Optimum leaf RWC is about 85–95% for

most species when water uptake by roots equals the leaf

transpirational water loss (Taiz and Zeiger, 1998). At the same

treatment level, RWC of Conni, Nuglade, Impact, and Bluechip

was from 28.08 to 47.61%, the highest RWC of cultivars was

47.61%, which was probably the result of their better ability for

water uptake at low soil water potential (Volaire et al., 1998),

along with better dehydration tolerance of their tissue (Volaire

and Lelievre, 2001).

Five cultivars of Kentucky bluegrass declined in their TQ

and increased in their LW from 3 to 21 d under both stresses, it

suggested that the drought stress period is the main factor that

affects the TQ and LW in the northwestern arid region of China.

The study also revealed that positive correlation existed

between RWC and TQ, negative correlation between LW and

TQ. That is, the higher RWC, the lower LW, and the better TQ

are highly associated each other. This finding suggests that

RWC can be used as an important physiological indicator for

the evaluation of adaptability to environment conditions. The

higher RWC is correlated with the higher water uptake ability in

turfgrasses, and hence the better TQ is normally observed.

SOD is the key enzyme in the antioxygen scavenger system

because it catalyzes superoxide free radical dismutation into

H2O2 and O2 (Elstner, 1982; Bowler et al., 1992; Scandalios,

1993). In this study the SOD activity slightly declined at 0–3 d

and then increased at 6 d of stress, subsequently decreased in

leaves of all cultivars (Fig. 1E). Some researchers also found the

increase in SOD activity during the first 7 d of heat stress and

dramatic decline in SOD activity after 14–21 d of heat stress

under controlled environmental conditions (Liu and Huang,

2000; Huang et al., 2001).Transient increases in antioxidant

activities with increasing temperatures have been reported in

other species (Guo et al., 1998; Jiang and Huang, 2001).

CAT catalyzes the oxidation of substrates by H2O2, break

down and detoxifies H2O2 (Asada, 1992). Thus, decrease in CAT

activity would result in H2O2 accumulation, which can react with

(O2�) to produce hydroxyl-free radicals via the Herbert–Weiss

nships among RWC, EL, LW, SOD, CAT, MDA and TQ

TQ SOD CAT MDA

0.879* 0.881* 0.952* �0.971**

�0.857 �0.876 �0.956* 0.976**

�0.909* �0.860 �0.980** 0.993**

1 0.816 0.909* �0.905*

0.816 1 0.943* �0.819

0.909* 0.943* 1 �0.956*

�0.905* �0.819 �0.956* 1

J. Liu et al. / Scientia Horticulturae 115 (2008) 190–195194

reaction (Elstner, 1982; Bowler et al., 1992). The hydroxyl-free

radicals can directly damage the membrane by attacking

unsaturated fatty acids of lipid to induce lipid peroxidation

(Okuda et al., 1991). In this study, activities of CAT declined with

prolonged stress period (Fig. 1F), then higher MDA and EL could

be the result (Fig. 1G,B). Previous study has found that the

decline in CAT relative activity (Feierabend and Engel, 1986;

Polle, 1997), which may lead to the accumulation of H2O2 and

causes damage to cell membranes (Dhindsa et al., 1981). But

change of CATactivity has different from that in Fu and Huang’s

paper (Fu and Huang, 2001).

An increase in EL suggests membrane in the jury has

occurred (Blum and Ebercon, 1981). Furthermore, the extent of

lipid peroxidation has been used to assess the level of free

radical damage to cell membranes under stress conditions

(Scandalios, 1993). MDA is the final product of peroxidation of

unsaturated fatty acids in phospholipids and is responsible for

cell membrane damage, this assay has often been used as an

indicator of the level of lipid peroxidation (Halliwell and

Gutteridge, 1989; Scandalios, 1993). The result also indicated

that EL value and MDA content always went together and

increased in the leaves of five cultivars under combined stress,

performing significantly positive correlation between increas-

ing rate of EL and that of MDA content.

All the physiological indexes under combined drought and

heat stress were significantly correlated each other except SOD.

This result indicates that when Kentucky bluegrass was stressed

by drought and heat, increased of SOD activity can not inhibit

formation and accumulation of free radicals, but may delay

accumulation of free radicals to a certain degree to alleviate

active oxygen damage to cell membrane.

In summary, the results suggested that simultaneous drought

and heat stress was detrimental for turfgrass, particularly for the

drought and heat susceptible cultivar. The combined stresses

induced oxidative injury in five cultivars, as demonstrated by the

reduction in antioxidant enzymes and increase in lipid

peroxidation. Five cultivars exhibited a defensive mechanism

to protect against free radicals in the early periods of stress

treatments, as shown by the transient increases in SOD activities.

Clearly, decline of TQ, RWC, and increase of LW, and EL in

drought and heat environment was associated closely with leaf

water deficit, as well as a decline in antioxidant enzyme activity

and an increase in lipid peroxidation. These physiological

parameters could be used to select Kentucky bluegrass

germplasm for the improvement of summer stress survival.

Acknowledgements

This research was financed by the special project ‘‘Study of

turf-grass drought resistance in Arid Desert Oasis Region’’

from Key Laboratory of Resources, Environment and

Chemistry of West China.

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