See

discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/260528934

Changes in some anti-oxidative enzymes and

physiological indices among sesame genotypes
(Sesamum indicum L.) in response to soil water
deficits under field conditions
ARTICLE in ACTA PHYSIOLOGIAE PLANTARUM MARCH 2014
Impact Factor: 1.52 DOI: 10.1007/s11738-013-1442-3

DOWNLOADS

VIEWS

70

73

4 AUTHORS, INCLUDING:
Mohammad Pessarakli
The University of Arizona
138 PUBLICATIONS 1,041 CITATIONS
SEE PROFILE

Available from: Mohammad Pessarakli

Retrieved on: 29 July 2015

Acta Physiol Plant (2014) 36:641650

DOI 10.1007/s11738-013-1442-3

ORIGINAL PAPER

Changes in some anti-oxidative enzymes and physiological indices

among sesame genotypes (Sesamum indicum L.) in response to soil
water deficits under field conditions
Azam Kadkhodaie Morteza Zahedi
Jamshid Razmjoo Mohammad Pessarakli

Received: 25 June 2013 / Revised: 7 November 2013 / Accepted: 12 November 2013 / Published online: 29 November 2013
Franciszek Gorski Institute of Plant Physiology, Polish Academy of Sciences, Krakow 2013

Abstract A field experiment was conducted to evaluate

the response of ten sesame genotypes to different levels of
soil water in terms of contents of proline, soluble carbohydrates, carotenoids, and activities of catalase (CAT),
peroxidase (POX) and ascorbate peroxidase (APX). Plants
were grown under three irrigation levels, including irrigation at 55 % (control), 75, and 85 % depletion of soil
available water. Field test plots were a two-way factorial
arranged in a randomized complete block design with three
replications. Under control level of irrigation, the most and
the least grain yields were achieved for genotypes Ultan
(2,519 kg/ha) and Isfahan1 (1,311 kg/ha), respectively.
Grain yield was decreased in some genotypes under 75 %
and in all genotypes under 85 % depletion of available
water. Based on percentage reduction in grain yield under
both 75 and 85 % depletion of soil available water, Isfahan4, Borazjan, Isfahan1, Ahvaz, Ardestan, and Shiraz
were recognized as relatively tolerant and Ultan, Shahreza,
Kal, and Markazi were identified as relatively sensitive to
water stress. The activities of antioxidant enzymes and the
contents of carotenoids, proline, and soluble carbohydrates
in leaves were increased in most genotypes under stress
conditions, and the magnitudes of the increases were
greater in the tolerant than in the sensitive genotypes. The
results of this experiment showed that the stress-induced

Communicated by G. Bartosz.
A. Kadkhodaie  M. Zahedi  J. Razmjoo
Department of Agronomy and Plant Breeding,
Isfahan University of Technology, Isfahan, Iran
M. Pessarakli (&)
School of Plant Sciences, The University of Arizona,
Tucson, AZ 85721, USA
e-mail: pessarak@email.arizona.edu; pessarak@ag.arizona.edu

increase of antioxidant enzymes and the contents of the

compatible solutes in leaves were related to the tolerance
of sesame genotypes.
Keywords Antioxidant enzymes  Carotenoids 
Proline  Sesame genotypes  Water deficit

Introduction
Water deficit is an important factor limiting crop production and it is becoming an alarming problem in many
regions of the world (Abedi and Pakniyat 2010). The percentage of drought affected areas more than doubled from
the 1970s to the early 2000s in the world (Alizadeh 2004).
The problem has become more serious in recent years due
to increasing population that accompanies global climate
changes (Bartoli et al. 1999). To improve crop productivity
in the areas with limited water, it is necessary to understand
the mechanism of plant responses to water deficit. These
responses are complex and different mechanisms are
employed by plants when they encounter water stress
(Chance and Maehly 1955). However, plant responses
depend on the stage of growth, the intensity, rate and
duration of exposure to stress, and also on plant species and
even cultivar within species (Brar et al. 1990).
The exposure of plants to most unfavorable conditions
causes oxidative stress, which adversely affects plant
growth due to the generation of reactive oxygen species
(ROS) (Parida et al. 2007). They are highly reactive and
cause severe damage to membranes, DNA, and proteins.
There are some mechanisms related to the detoxification of
ROS in plants which include activation of enzymatic
(CAT, POX, and APX) as well as non-enzymatic (flavones,
anthocyanins, carotenoids and ascorbic acid) antioxidants

123

642

(Mitra 2001). In some plant species, a positive correlation

between the tolerance to stress and the enhanced ROS
scavenging capacity has been found (Selote and KhannaChopra 2004; Parida et al. 2007; Ghorbanli et al. 2004;
Karaaslan et al. 2007). In several studies, tolerant genotypes increased their antioxidant enzyme activities in
response to water deficit, whereas sensitive genotypes
failed to do so (Selote and Khanna-Chopra 2004). Increase
in the activity of APX in Maize (Pastori and Trippi 1992),
POX in Ctenanthe setosa (Terzi and Kadioglu 2006), and
CAT in sesame (Fazeli et al. 2007), reduction in CAT
activity in rice (Sharma and Dubey 2005) have been
reported. However, the relationship between the capacity to
tolerate stress and the activity of ROS scavenging mechanisms depends on species, genotype, developmental and
metabolic state of plant, and the duration of stress (Rudoplh et al. 1986).
In addition to antioxidant defense mechanism, some
metabolic changes occur in adaptable crops in response to
water stress, which also contribute towards adaptation to
such adverse environmental constraint (Brar et al. 1990).
Osmotic adjustment in terms of accumulation of compatible solutes such as proline and soluble sugars is also
another possible approach for overcoming stress induced
by water deficit. It is well documented that these compounds accumulate in the plant tissues in response to different environmental stresses (Nakano and Asada 1981). In
some investigations, significant positive correlations have
been reported between the accumulation of proline and
soluble carbohydrates and the tolerance to water deficit
(Pinhero et al. 2000). However, in some cases, the stressinduced increase of these compounds has not been found to
be an adapting mechanism.
Carotenoids are yellow, orange, and red pigments
which are synthesized by all photosynthetic and many
non-photosynthetic organisms (Andrew et al. 2008). They
are divided into the hydrocarbon carotenes, such as
lycopene and b-carotene. Carotenoids have essential
functions in photosynthesis and light protecting mechanism (Havaux and Tardy 1999). They protect photosynthetic apparatus against harmful free radicals (Deng et al.
2003). b-carotene, present in the chloroplasts, is exclusively bound to the core complexes of PSI and PSII
(Havaux and Tardy 1999). Protection against damaging
effects of ROS at this site is essential for chloroplast
functioning. Carotenoids also play a critical role in the
assembly of the light-harvesting complex and in the
radiationless dissipation of excess energy (Munne-Bosch
and Alegre 2000). Besides their antioxidant roles in protection from oxidative damage, they are well known for
inhibiting lipid peroxidation and stabilizing membranes
(Demmig-Adams and Adams 1996). Mild water stress
induces ABA synthesis from carotenoids in the roots and

123

Acta Physiol Plant (2014) 36:641650

root ABA signals to the shoots leading to stomatal closure

to reduce water loss and photosynthesis (Yang et al.
2001). Thus, carotenoids could help plants tolerate
drought stress (Jaleel et al. 2009). Increases in the
carotenoids, soluble sugars and proline contents under
drought stress have been reported in sunflower (Nazarli
et al. 2011). However, decreases in chlorophylls, carotenoids and increases in proline and total sugar contents in
cotton (Parida et al. 2007) have also been reported.
In order to select tolerant genotypes of sesame for crop
improvement in breeding programs, it is necessary to
understand physiological and biochemical mechanisms that
enable this crop to adapt to water stress. The aim of this
study was, therefore, to investigate the effects of water
stress on the carotenoid content, accumulation of proline
and soluble sugars and the activity of three antioxidant
enzymes (CAT, APX, and POX) in ten sesame genotypes
and also to evaluate the relationship between the level of
these osmoregulators and enzymes and the degree of tolerance to stress in these genotypes.

Materials and methods

Plant materials and treatments
Seeds of ten sesame genotypes (Isfahan4, Shahreza, Borazjan, Ahvaz, Kal, Shiraz, Markazi, Ardestan, Ultan and
Isfahan1) were collected from different regions of Iran.
Seeds were planted in the Research Field of College of
Agriculture, Isfahan University of Technology, located in
Isfahan (31420 N, 51410 E and 1,850 m above the mean
sea level), Iran, during 20102012. The soil was a clayloam Typic Haplargids, with a bulk density of 1.34 g/
cm3, pH of 7.5, water-holding capacity at field capacity
point of 24 % (determined gravimetrically), organic
carbon of 0.27 %, total N of 0.03 %, available P and
available K of 14.9 and 250 mg/kg, respectively. Plots
consisted of 6 rows, 4 m in length and 50 cm width.
Seeds were sown at 12 cm depth. Nitrogen (100 kg/ha)
was applied in the form of urea (one-third before planting
and the rest as side-dressed at the beginning of flowering
stage).
Irrigation treatments
Irrigation treatments were scheduled on the maximum
allowable depletion (MAD) percentage of the soil available
water (SAW) (Allen et al. 2000). The plots were irrigated
after 55 % (I1; as control), 75 % (I2) and 85 % (I3) MAD of
SAW. A TDR probe (TDR Trase System, Model 6050X1;
Soil Moisture, Santa Barbara, CA) was used to measure
soil water content 2 days after irrigation and continued up

Acta Physiol Plant (2014) 36:641650

to 1 day prior to the next irrigation. Drought treatment

started at the 30 days after planting. In this period, all
experimental plots were irrigated when 50 % of SAW was
depleted. The experimental plots were irrigated when the
respective MAD threshold values were reached for each
treatment and were calculated using the following equations (Allen et al. 2000):


hirrig hfc  hfc  hpwp  p
where hirrig (%) is the MAD threshold value for each
treatment, hfc and hpwp are the soil water contents at field
capacity (%) and wilting point (%), respectively, and p is
the fraction of SAW (55, 75, and 85 %) that can be
depleted from the root zone.
The depth of irrigation was determined based on the soil
water content and was calculated using the following
equations (Allen et al. 2000):
Dirrig hfc  havg  Ze  qb
where Dirrig (cm) is the depth of irrigation, hfc the soil
water content at field capacity (%) and havg the average
water in root development depth, Ze the depth of development of root and qb is the bulk density. The applied
irrigation water at each irrigation event was measured by
flow meters.
The carotenoids content, soluble sugars and proline,
CAT, POX, and APX activities, and seed yield were
measured in ten genotypes. All of the physiological
parameters were determined at full flowering stage.
Physiological measurements
Total leaf proline contents were extracted by the method of
Bates et al. (1973). Leaf samples (0.5 g fresh weight of the
third fully expanded leaf from the apex of the plant) were
homogenized in 10 ml of 3 % aqueous sulfosalicylic acid
and the homogenates were filtered through filter paper.
Two milliliters of the filtered extracts were made to react
with 2 ml of acid ninhydrin and 2 ml of glacial acetic acid
in a test tube for 1 h under a temperature of 100 C, and the
reaction was terminated by placing the tube on an ice bath.
The reaction mixtures were extracted using 4 ml of toluene
and vortexing. The chromophore containing toluene was
aspirated from the aqueous phase, warmed to room temperature and the absorbances were read at 520 nm using
toluene as a blank. Proline concentrations of leaves were
determined using a standard curve.
The content of soluble sugars in the leaves was determined based on Irigoyen et al. (1992). About 0.1 g dry
weight of leaf tissue was homogenized with deionized
water; the extract was filtered and treated with 1 % phenol
and 98 % sulfuric acid. The mixture remained for 1 h at

643

room temperature and absorbance was determined at

485 nm. Content of soluble sugars was determined using
glucose as standard.
Leaf carotenoid contents were determined based on the
method of Gao (2006). Samples of fresh leaves (1 g) were
extracted with 80 % acetone and centrifuged at 5,0009g
for 10 min. The absorbance of the supernatant was read at
470 nm for carotenoid (Hendry and Price 1993).


Carotenoids mgg1 1;000  Abs470  1:9  663
 63:14  645=214
Enzyme activities
Catalase (CAT), peroxidase (POX) and ascorbate peroxidase (APX) activities of genotypes were measured from the
extracts prepared according to the methods of Chance and
Maehly (1955), Herzog and Fahimi (1973), Nakano and
Asada (1981) with some modifications.
All steps of the extraction were carried out at 4 C.
Fresh sample of leaf (0.2 g) was homogenized in a cold
mortar in 1 ml of 50 mM Na-phosphate buffer (pH 7)
containing 2 mM a-dithiothreitol, 2 mM EDTA, 0.2 %
Triton X-100, 50 mM TrisHCl and 2 % polyvinylpyrrolidone and mixed for 15 min. The extracts were immediately used for the determination of enzyme activities.
CAT (EC 1.11.1.6), the assay of catalase activity was
carried out in a total volume of 3 ml of 50 mM Na-phosphate buffer (pH 7.0), containing 4.51 ll of H2O2 (30 %)
and 50 ll of enzyme extract. The decrease in absorbance at
240 nm because of degradation of H2O2 was monitored
every 30 s for 2 min, using a spectrophotometer U-1800
(Hitachi, Japan). Catalase activity was expressed as nanomoles of decomposed per milligram of protein per minute.
POX (EC 1.11.1.7), peroxidase activity was determined
in 3 ml of 50 mM Na-phosphate buffer (pH 7.8), containing 4.51 ll of H2O2 (30 %), 3.35 ll Guiacol, and 50 ll of
enzyme extract. The decrease in absorbance at 470 nm was
monitored every 30 s for 2 min, using a spectrophotometer
U-1800 (Hitachi, Japan), and the amount of formed tetraguaiacol was calculated. Peroxidase activity was
expressed as nanomoles of decomposed per milligram of
protein per minute.
APX (EC 1.11.1.11), ascorbate peroxidase activity was
determined in 3 ml of 50 mM Na-phosphate buffer (pH
7.8), containing 4.51 ll of H2O2 (30 %), 100 ll of 5 mM
ascorbate and 50 ll of enzyme extract. The decrease in
absorbance at 290 nm was monitored for 1 min, using a
spectrophotometer U-1800 (Hitachi, Japan), and the
amount of ascorbate oxidized was calculated. Ascorbate
peroxidase activity was expressed as nanomoles of
decomposed per milligram of protein per minute.

123

644

Acta Physiol Plant (2014) 36:641650

Table 1 Analysis of variance for the effect of different drought levels on carotenoid, proline, carbohydrate, catalase (CAT), peroxidase (POX),
ascorbate peroxidase (APX) and seed yield at plant traits of sesame genotypes
Source
Block

df

Carotenoid

Proline

Carbohydrate

CAT

POX

APX

Seed yield

0.0010ns

0.746ns

490.0ns

0.0051ns

0.281ns

0.0082ns

313,102.0*

ns

554,146.4**

Genotypes

0.0013

1.53**

3,124.0**

0.499**

60.13**

0.025**

Drought

0.049**

7.42**

10,043.76**

0.568**

20.64**

0.267**

815,401.6**

G9D

18

0.0028*

1.25**

1,664.9*

0.257**

7.59**

0.068**

191,468.8*

Error

58

0.0013

0.451

739.0

0.0030

0.770

0.0060

95,484.3

*, ** Significant at the 5 and 1 % levels of probability, respectively

Stress susceptibility index (SSI)

Table 2 Means comparison of irrigation and genotypes (interaction)

on seed yield of sesame genotypes

Stress susceptibility index (SSI) was calculated according

to Fischer and Maurer (1978):




SSI 1  Ysi =Ypi =SI and SI 1  Ys =Yp

Traits

where Ypi is the genotype yield in non-stress condition, Ysi

the genotype yield in stress conditions, Ys the mean yield of
all genotypes yield in stress conditions and Yp is the mean
yield of all genotypes yield in non-stress conditions. Lower
SSI corresponds to higher drought tolerance (Fischer and
Maurer 1978).
Statistical analysis

Results
Grain yield
Analysis of variance for grain yield of sesame genotypes
showed significant interactions between genotypes and
irrigation levels (Table 1). Under control level of irrigation (I1; 55 % depletion of SAW), the highest and the
lowest yields were observed in genotypes Ultan
(2,519 kg/ha) and Isfahan1 (1,311 kg/ha), respectively
(Table 2). The maximum and the minimum yields
were obtained in Shiraz (2,505 kg/ha) and Ardestan
(1,277 kg/ha) at I2 (75 % depletion of SAW) and in
Borazjan (1,289 kg/ha) and Ultan (759 kg/ha) at I3 (85 %

123

I2

I1

I3

Genotypes
Isfahan4

1,667.0ch
ac

1,754.2cg (?5)
c-h

Shahreza

2,158.1

1,664.0

Borazjan

2,062.6ad

1,957.4bf (-5)

Ahvaz
Kal
Shiraz

cf

1,908.5

ab

2,470.9

ad

2,071.5

1,096.6ik (-43)

(-20)

1,226.1hk (-51)

1,975.3

2,504.7 (?21)
1,466.8

Ardestan

1,522.7ei

1,277.2

Isfahan1

gj

1,310.7

1,289.1gj (-37)

(?8)

2,034.5

2,518.7

906.0j-l (-58)

bf

2,067.8

Markazi

(-23)

1,149.9hl (-31)

ad

ae

Ultan

Field test plots were a two-way factorial (3 9 10) arranged

in a randomized complete block design with three replications. The first factor was three irrigation levels and the
second factor was ten sesame genotypes (Isfahan4, Shahreza, Borazjan, Ahvaz, Kal, Shiraz, Markazi, Ardestan,
Ultan, and Isfahan1). Data of 2 years were combined and
combined of analysis of variance (ANOVA) was performed using GLM procedure of SAS statistical program
(ver. 9.1). Treatment means were separated using the LSD
test (p \ 0.05). Data of main effects were omitted due to
interaction.

Seed yield (kg/ha)

fi

(-28)

gk

(-16)

1,098.8ik (-47)
1,040.7il (-49)
831.5jl (-44)

ae

(-20)

758.9kl (-70)

dh

(?25)

809.3jl (-38)

2,007.6
1,632.3

Means of traits in each column with similar letter(s) are not significant
at 5 % probability level
Values in the parentheses are percent decrease (-) or increase (?) as
compared with the control (I1)

depletion of SAW), respectively. Grain yield decreased

in Borazjan (5 %), Ardestan (16 %), Kal (20 %), Ultan
(20 %), Shahreza (23 %), and Markazi (28 %), but it
increased in Isfahan1 (25 %), Shiraz (21 %), Ahvaz
(8 %), and Isfahan4 (5 %) at I2 as compared to the control. At I3, however, grain yield decreased in all tested
genotypes. The amount of decrease at I3 was minimum
for Isfahan4 (31.0 %) followed by Borazjan (37 %),
Isfahan1 (38 %), Ahvaz (43 %), Ardestan (44 %), Shiraz
(47.0 %), Markazi (49 %), Kal (51 %), Shahreza
(58.0 %), and Ultan (70.0 %), respectively.
Stress susceptibility index (SSI) was calculated to assess
drought susceptibility of sesame genotypes. Based on
percentage reductions in grain yield at I2, the values of
SSI for genotypes were -0.26 (Isfahan1), -0.23 (Shiraz),
-0.09 (Ahvaz), -0.06 (Isfahan4), 0.05 (Borazjan), 0.17
(Ardestan), 0.22 (Ultan), 0.22 (Kal), 0.25 (Shahreza), and
0.30 (Markezi). However, based on yield reductions at I3,
the values were 0.60 (Isfahan4), 0.72 (Borazjan), 0.74
(Isfahan1), 0.82 (Ahvaz), 0.86 (Ardestan), 0.91 (Shiraz),

Acta Physiol Plant (2014) 36:641650

645

Table 3 Means comparison of irrigation and genotypes (interaction) on leaf catalase (CAT) and peroxidase (POX) activities of sesame
genotypes
Traits

CAT (nanomol H2O2 mg/protein/min)

Irrigation

I1

I2

POX (nanomol H2O2 mg/protein/min)

I3

I1

I2

I3

Genotypes
Isfahan4

0.125ln
fg

Shahreza
Borazjan

0.403
0.109n

Ahvaz

0.153

Kal

0.173kl

Shiraz
Markazi
Ardestan

kn

ef

0.445

0.322h (?156)
e

11.37 (?5)
2.22jl (?79)

10.37a (-4)
3.22hj (?159)

0.355gh (?132)

0.550d (?259)

0.875mo

1.89km (?116)

2.32ik (?165)

0.121mn (-30)

0.166km (-4)

4.42cg

5.13c (?16)

4.86cd (?10)

3.78

eh

(?12)

4.82ce (?43)

3.88

dh

(?16)

3.63fh (?8)

4.90

cd

0.995 (?124)

lj

km

0.709 (?60)
0.231 (?26)
jk

0.187 (?49)
b

0.168

(-8)

0.273 (?116)
f

3.36

gi

3.35

hi

3.77

eh
cf

Ultan

0.621

0.738 (?19)

0.423 (-32)

4.63

Isfahan1

0.120mn

0.243i (?103)

0.419f (?250)

0.264o

2.14kl (?136)

10.78
1.24lo

1.33kn (?48)

0.327 (-19)
0.353h (?222)

ln

0.126

0.907mo

0.473 (?17)
0.189jk (?72)

jk

0.183

0.534d (?324)

(?30)

6.80b (?80)

5.12 (?11)

4.75ce (?3)

0.688no (?160)

0.836mo (?216)

Means of traits in each column with similar letter(s) are not significant at 5 % probability level
Values in the parentheses are percent decrease (-) or increase (?) as compared with the control (I1)

0.94 (Markezi), 0.97 (Kal), 1.12 (Shahreza), and 1.35

(Ultan). Lower SSI corresponds to higher drought tolerance
(Fischer and Maurer 1978).
Activity of antioxidant enzymes
Analysis of variance showed significant differences among
irrigation levels, genotypes, and interactions between irrigation levels and genotypes in terms of the activities of
CAT, POX, and APX in the leaves (Table 1).
Catalase (CAT)
Among ten evaluated genotypes, Ultan had the highest
CAT activity at I1 and also I2, followed by Shiraz and
Shahreza. The maximum CAT activity at I3 was observed
for Shiraz, Ahvaz, Isfahan4, and Ultan, respectively
(Table 3). The lowest activity was achieved for Borazjan
at I1 and for Kal at I2 and I3. The activity of CAT
increased in most of the tested genotypes under water
deficit treatments as compared to the control level of
irrigation. However, the activity decreased in Kal at I2
and in Ultan, Shahreza, Markazi, and Kal at I3 compared
to the control. The extent of increase in CAT activity at I2
was highest in Isfahan4 (156 %) followed by Ahvaz
(132 %), Isfahan1 (103 %), Borazjan (72 %), Shiraz
(60 %), Ardestan (49 %), Markazi (26 %), Ultan (19 %),
and Shahreza (17 %), respectively. At I3, the maximum
increase in CAT activity was achieved for Isfahan4
(324 %), followed by Ahvaz (259 %), Isfahan1 (250 %),
Borazjan (222 %), Shiraz (124 %), and Ardestan
(116 %), respectively (Table 3).

Peroxidase (POX)
At I1 irrigation level, the maximum POX activity was
observed for genotype Shahreza followed by Ultan and
Kal. At I2 genotypes of Shahreza, Kal, Ultan, and Ardestan
and at I3 genotypes Shahreza, Ardestan, Kal, and Shiraz
possessed the highest POX activities, respectively
(Table 3). The lowest enzyme activity under all irrigation
levels belonged to Isfahan1. Except for Shahreza at I3, the
activity of POX increased at I2 and I3 compared to the
control level of irrigation. However, the magnitude of
increase in POX activity at I2 was highest in Isfahan1
(161 %), followed by Ahvaz (116 %), Borazjan (79 %),
Isfahan4 (48 %), Ardestan (30 %), Kal (16 %), or Markazi
(16 %), Shiraz (12 %), Ultan (11 %), and Shahreza (6 %),
respectively. At I3, the maximum increase in POX activity
was achieved for Isfahan1 (216 %), followed by Ahvaz
(165 %), Borazjan (160 %), Isfahan4 (136 %), Ardestan
(80 %), Shiraz (43 %), Kal (10 %), Markazi (8 %), and
Ultan (3 %), respectively (Table 3).
Ascorbate peroxidase (APX)
Under control level of irrigation, the highest and the lowest
values for APX activity were observed in genotypes Ultan
and Isfahan4, respectively (Table 4). The maximum and
the minimum enzyme activities were achieved in Ultan and
Borazjan at I2 and in Ahvaz and Shahreza at I3, respectively. The activity of APX increased in most tested
genotypes at I2 and I3 as compared to the control level of
irrigation. The magnitude of increase in APX activity at I2
compared to the control was maximum in Isfahan4

123

646

Acta Physiol Plant (2014) 36:641650

Table 4 Means comparison of irrigation and genotypes (interaction) on leaf ascorbate peroxidase (APX) activities and carotenoid content of
sesame genotypes
Traits

APX (nanomol H2O2 mg/protein/min)

Irrigation

I1

I2

Carotenoid content (mg/g)

I3

I1

I2

I3

Genotypes
Isfahan4

0.117m

0.354gk (?203)

0.2523ac (?116)

jn

0.259 (-28)
0.454dh (?131)

0.1558
0.1081n

0.1536 (-1.5)
0.2114bh (?96)

0.1440kn (-8)
0.2437ad (?126)

Ahvaz

0.267jl

0.546bd (?105)

0.749a (?181)

0.1442kn

0.2143bh (?49)

0.2482ad (?72)

Kal

0.306il

0.323ik (?6)

0.402eh (-5)

0.1691fm

0.1869el (?11)

0.2301be (?36)

di

ce

0.1965

dk

(?47)

0.2156b-h (?61)

0.2361

ae

(?18)

0.2490ad (?24)

0.2281

be

(?41)

0.2553ab (?58)

0.2200

be

(0)

0.2091bi (-5)

Markazi
Ardestan

ei

0.418

jl

0.287

ab

0.428

di

0.428

fj

0.385

bc

(?51)
(?2)
(?34)

Ultan

0.666

0.621

Isfahan1

0.193lm

0.330hk (?71)

(-7)

0.527

gk

0.355

(?86)
(-15)

ce

0.525

(?83)

dg

0.479

(-28)

0.537ce (?178)

in

0.2182bg (?87)

0.341 (-5)
0.239km (?22)

0.283

kl

0.1166mn

0.359
0.196lm

jl

hk

0.496cf (?324)

Shahreza
Borazjan

Shiraz

gk

0.1341

ln

0.2004

cij

0.1620

hn

0.2200

bf

0.1656gm

0.2424ad (?46)

0.2877a (?74)

Means of traits in each column with similar letter(s) are not significant at 5 % probability level
Values in the parentheses are percent decrease (-) or increase (?) as compared with the control (I1)

(203 %), followed by Ahvaz (105 %), Isfahan1 (71 %),

Shiraz (51 %), Ardestan (34 %), Borazjan (22 %), Kal
(6 %), and Markazi (2 %), respectively. At I3, the maximum increase in APX activity was achieved for Isfahan4
(324 %), followed by Ahvaz (181 %), Isfahan1 (178 %),
Borazjan (131 %), Shiraz (86 %), and Ardestan (83 %),
respectively. However, the enzyme activity was instead
decreased in genotypes Shahreza (5 %) and Ultan (7 %) at
I2 and in Ultan (28 %), Shahreza (28 %), Markazi (15 %),
and Kal (5 %) at I3 (Table 4).
Carotenoids
Analysis of variance for carotenoid content in leaves
showed significant interactions between genotypes and
irrigation levels (Table 1). Under control level of irrigation, the highest and the lowest content of leaf
carotenoids were observed in genotypes Ultan and Borazjan1, respectively (Table 4). The maximum and the
minimum contents of carotenoids were obtained in Isfahan1 and Shahreza at both I2 and I3, respectively. The
content of carotenoids significantly increased under water
deficit treatments compared to the control in all genotypes, except Ultan and Shahreza. The magnitude of
increase at I2 compared to optimum condition of irrigation was highest in Borazjan (96 %), followed by Isfahan4 (87 %), Ahvaz (49 %), Shiraz (47 %), Isfahan1
(46 %), Ardestan (41 %), Markazi (18 %), and Kal
(11 %), respectively. At I3, the maximum increase in
carotenoid content was achieved for Borazjan (126 %)
followed by Isfahan4 (116 %), Isfahan1 (74 %), Ahvaz
(72 %), Shiraz (61 %), Ardestan (58 %), Kal (36 %), and
Markazi (24 %), respectively.

123

Proline
Analysis of variance for proline content of leaves showed
significant interactions between genotypes and irrigation
levels (Table 1). Under control level of irrigation, the
maximum and the minimum proline contents were
observed in genotypes Shahreza and Isfahan1, respectively
(Table 5). The maximum and the minimum proline contents were obtained in Shahreza and Kal at I2 and in Isfahan4 and Ultan at I3, respectively. The content of proline
significantly increased in most tested genotypes under
water deficit treatments as compared to the control. The
magnitude of increase at I2 was highest in Isfahan1 (32 %),
followed by Isfahan4 (21 %), Ahvaz (21 %), Borazjan
(16 %), Shiraz (14 %), Ardestan (13 %), Markazi (11 %),
Ultan (10 %), and Shahreza (7 %), respectively. At I3, the
maximum increase in proline content was achieved for
Isfahan4 (69 %) followed by Isfahan1 (48 %), Borazjan
(43 %), Ahvaz (34 %), Ardestan (26 %), Shiraz (24 %),
and Kal (2 %), respectively. However, proline content was
instead decreased in Kal (5 %) at I2 and in Ultan (19 %),
Shahreza (13 %), and Markazi (5 %) at I3.
Soluble carbohydrates
Analysis of variance for the content of soluble carbohydrates in leaves showed significant interactions between
genotypes and irrigation levels (Table 1). Under control
irrigation level, the highest and the lowest content of soluble carbohydrates were observed in Markazi and Isfahan4,
respectively (Table 5). However, the maximum and the
minimum contents of soluble carbohydrates were achieved
for Ardestan and Kal at both I2 and I3, respectively. The

Acta Physiol Plant (2014) 36:641650

647

Table 5 Means comparison of irrigation and genotypes (interaction) on leaf proline and soluble sugars contents of sesame genotypes
Traits

Leaf proline content (lmol/g)

Leaf soluble sugars (mg/g)

Irrigation

I1

I2

I3

I1

I2

I3

Isfahan4

4.25hk

5.17bh (?21)

7.19a (?69)

157.2h

219.4eg (?40)

260.3ad (?66)

Shahreza

5.6be

5.99bc (?7)

4.90ej (-13)

230.8cf

241.2be (?4.5)

228.7dg (-1)

Genotypes

Borazjan
Ahvaz
Kal

hk

4.29

jk

4.04

ej

4.91

4.98

ej

4.89

ej

4.68

gk

(?16)

6.13 (?43)

(?21)

5.43

bg

5.00

dj

(-5)

(?2)

fg

195.8

fg

196.2

277.1ab (?41)

(?16)

261.2ad (?33.5)

eg

(?10)

215.7eg (?10)

226.4
214.8

4.71
4.39hk

5.37 (?14)
4.86fj (?11)

5.85 (?24)
4.15ik (-5)

218.3
257.2ad

228.0 (?4.5)
243.2be (-5.5)

276.4ab (?27)
242.9be (-6)

Ardestan

4.76fk

5.38bg (?13)

5.98bd (?26)

225.0dg

249.4be (?11)

291.7a (?29.5)

Ultan
Isfahan1

4.67

3.85

5.12
5.06

ci

(?10)
(?32)

3.79 (-19)
5.70

bf

(?48)

eg

(?17)

dg

230.8

Shiraz
Markazi

ci

be

196.6

be

gk

gk

bg

(?34)

fg

cf

232.5

gh

191.9

dg

be

(?6)

232.1cf (-0.2)

be

(?29)

267.5ac (?39.5)

246.9
247.7

Means of traits in each column with similar letter(s) are not significant at 5 % probability level
Values in the parentheses are percent decrease (-) or increase (?) as compared with the control (I1)

content of soluble carbohydrates significantly increased in

most genotypes under water deficit treatments in comparison with the control. The magnitude of increase at I2 was
the highest in Isfahan4 (40 %), followed by Isfahan1
(29 %), Borazjan (17 %), Ahvaz (16 %), Ardestan (11 %),
Kal (10 %), Ultan (6 %), Shahreza (4.5 %) and Shiraz
(4.5 %), respectively. At I3, the maximum increase in
soluble carbohydrates was achieved for Isfahan4 (66 %),
followed by Borazjan (41 %), Isfahan1 (39.5 %), Ahvaz
(33.5 %), Ardestan (29.5 %), Shiraz (27 %), and Kal
(10 %), respectively. However, the content of soluble
carbohydrates was instead decreased in Markazi (5.5 %) at
I2 and in Markazi (6 %), Shahreza (1 %), and Ultan
(0.2 %) at I3.

Discussion
In this study, under control irrigation level (irrigation based
on 55 % depletion of available soil water), among ten
tested genotypes, the highest grain yields were achieved for
Ultan (2,519 kg/ha) followed by Kal (2,471 kg/ha), Shahreza (2,158 kg/ha), Shiraz (2,072 kg/ha), Borazjan
(2,063 kg/ha), and Markazi (2,034 kg/ha), respectively.
These genotypes may, therefore, be suitable for cultivation
under conditions where water is not limited for crop production. Sesame grain yield significantly decreased at 75 %
(except, for Isfahan1, Isfahan4, Ahvaz, Shiraz) and at 85 %
depletion of available soil water. A major cause of yield
reduction under water deficit conditions is inadequate
photosynthesis owing to stomatal closure and consequently
limited carbon dioxide uptake (Zhu 2001). Genotypes
varied in their response to water stress, so that the reductions in yield at 75 % ranged from 5 (Borazjan) to 28 %

(Markazi) and at 85 % depletion of available soil water

ranged from 31 (Isfahan4) to 70 % (Ultan). In line with our
results, Mensah et al. (2006), Hassanzadeh et al. (2009),
and Saeidi et al. (2012) also reported that seed yields of
sesame genotypes reduced under drought conditions. Variation among sesame genotypes in response to water stress
has also been reported by other researchers (Tantawy et al.
2007; Boydak et al. 2007; Kim et al. 2006). According to
SSI (values reported in results section under grain yield),
the least susceptible genotype at I2 was Isfahan1, followed
by Shiraz, Ahvaz, Isfahan4, Borazjan, Ardestan, Ultan,
Kal, Shahreza and Markazi, while at I3, the least susceptible genotype was Isfahan4, followed by Borazjan,
Isfahan1, Ahvaz, Ardestan, Shiraz, Markazi, Kal, Shahreza, and Ultan.
Water deficit induces several physiological and biochemical responses in plants. Similar to other environmental stresses, water deficit causes oxidative stress
through which ROS are produced in plant tissues (Mittler
et al. 2004). ROS could damage membrane lipids, proteins,
and nucleic acids (Ramachandra Reddy et al. 2004). The
tolerance mechanism to water deficit involves the activation of complex metabolic, including anti-oxidative, pathways, especially ROS scavenging systems which enable
plants to continue their growth under water stress (Zhu
et al. 2004). CAT, APX, and POD are the key antioxidant
enzymes involved in detoxification of superoxide and
hydrogen peroxide (Zhu 2003; Glombitza et al. 2004;
Kreps et al. 2002; Zhu et al. 2004; Shao et al. 2003). There
have been positive correlations between the rising activity
of these enzymes and plant resistance to stress (Kholova
et al. 2011). In the present study, sesame genotypes
responded differently to water stress in terms of POX,
CAT, and APX activities. This shows that different sesame

123

648

genotypes had distinct water stress thresholds and, therefore, they had diverse adaptive mechanisms to regulate
their redox status. The activities of CAT, POX, and APX in
most cases increased under water stress treatments as
compared to the optimum irrigation condition. However,
there were even significant reductions in the activities of
CAT and APX in Kal, Shahreza, Markazi, and Ultan and
POX in Shahreza under water deficit conditions. These
genotypes were categorized as sensitive to water stress. On
the other hand, the magnitude of increases in the activities
of CAT, POX, and APX under water stress was significantly greater in tolerant genotypes such as Isfahan4, Borazjan, Isfahan1, Ahvaz, Ardestan, and Shiraz as compared
to the other tested genotypes. These findings, therefore,
clearly show that the activation of antioxidant enzymes has
an important role in the tolerance of sesame genotypes to
water deficit. However, the degree of increase in POX
activity in tolerant genotype Shiraz under water stress was
low in comparison with other tolerant genotypes. This
genotype also took advantage of other adapted alternative
salvage pathway such as non-enzymatic antioxidants
(carotenoids) for scavenging the H2O2 (Noctor and Foyer
1998). Similar to our results, Fazeli et al. (2007) reported
that water stress increased CAT, POX, and APX activities
in leaves and roots of sesame. In their study, the magnitude
of increases in the activities of these enzymes was greater
in tolerant cultivar of Yekta compared to the sensitive
cultivar of Darab 14, providing the higher efficiency of
Yekta under drought. Abedi and Pakniyat (2010) reported
that CAT activity decreased in most tested genotypes of
oilseed rape under drought stress, but the activity increased
in Licord which was the most tolerant cultivar in their
study. Increased level of enzymatic antioxidant activity
under water deficit has also been reported in wheat (Shao
et al. 2005), maize and soybean (Vasconcelos et al. 2009).
Accumulation of compatible solutes such as proline and
soluble carbohydrates is well known as a common adapting
mechanism acquired by plants under water deficit stress,
through which plants regulate their osmotic potential and
adjust to low soil water availability. These compounds also
improve plant stress tolerance by protecting and stabilizing
membranes and enzymes during stress conditions (Rudoplh
et al. 1986). However, the extent of their accumulation in
response to water deficit differs widely among plant species and genotypes (Pinhero et al. 2000). In the present
study, the tolerant sesame genotypes (Isfahan4, Borazjan,
Isfahan1, Ahvaz, Ardestan, and Shiraz) accumulated more
proline and soluble carbohydrates in their leaves under
stress conditions than sensitive cultivars. Thus, it appears
that the increase in the content of these compatible solutes
during stress induction is an adaptive mechanism in sesame. Similarly, many workers have reported the increased
accumulation of these osmolytes in tolerant cultivars under

123

Acta Physiol Plant (2014) 36:641650

water deficit conditions and found positive correlations

between rising content of these osmo-protectants and the
tolerance to water deficit (Rudoplh et al. 1986). Parida
et al. (2007) reported that the content of proline and soluble
carbohydrates in cotton plants was significantly higher in
tolerant than in sensitive genotype. However, in some
works, there have been no correlations or even negative
correlations between the accumulation of these compatible
solutes and the tolerance to water stress (Pinhero et al.
2000). In other words, in some situations, the stressinduced raise of these compounds may just be an effect of
stress rather than an adapting mechanism.
The content of carotenoids in leaves increased at both 75
and 85 % depletion of available soil water compared with
the control level of irrigation in all genotypes, except Ultan
and Shahreza, the most sensitive genotypes. The magnitudes of increases were greater in tolerant genotypes
(Isfahan4, Borazjan, Isfahan1, Ahvaz, Ardestan, and Shiraz) suggesting the important role of carotenoids as a nonenzymatic antioxidant in the tolerance of sesame genotypes
to water deficit. However, the role of carotenoids in the
induction of water stress tolerance was more pronounced at
severe than at mild water deficit. For instance, the increase
in the content of carotenoids at severe level of water deficit
for the most tolerant genotype (Isfahan4) was the second
highest (116 %) after Borazjan (126 %), but at mild level
the enhancement of carotenoids in the most tolerant
genotype (Isfahan1) was less (46 %) than those of other
tolerant genotypes, Borazjan (96 %), Isfahan4 (87 %),
Ahvaz (49 %), and Shiraz (47 %). The major role of
carotenoids in direct quenching of triplet chlorophyll prevents the generation of singlet oxygen and protects from
oxidative damage (Deng et al. 2003). Wang et al. (2001)
reported that the content of carotenoids in the leaves of
winter wheat increased under drought stress.
The most-yield productive genotypes at 50, 75, and
85 % depletion of SAW were Ultan, Shiraz, and Borazjan, respectively. The activities of CAT, POX, and APX,
and also the content of carotenoids and soluble carbohydrates in Ultan were highest, suggesting the significant
role of these traits in yield superiority of this genotype at
I1 condition. Proline did not have important contribution
in yield variation at this irrigation level, as the differences between genotypes generally were not significant.
At I2, the high yield of Shiraz was related to greater CAT,
POX, and APX activities, and proline content, while the
role of carotenoids and soluble carbohydrates were
insignificant. At I3, Borazjan took advantage by having
greater levels of proline and soluble carbohydrates. The
role of enzymes in yield performance of this genotype
was not significant at I3. The results indicate that the role
of these physiological attributes in yield productivity of
sesame genotypes is dependent on soil moisture.

Acta Physiol Plant (2014) 36:641650

There might be cases in which the yield performance of

a genotype would not adequately be explained by the
attributes reported in this study. For instance, Kal showed
one of the highest grain yield genotypes in I3 condition, but
most parameters were much less affected in this genotype
compared to the other two with high yield at I3, e.g. Borazjan and Isfahan4. It seems that in this study and the
possible similar cases, the yield performance of a genotype
may be more attributed to the other physiological or biochemical traits that are not evaluated in this study.
Based on the SSI, the least susceptible genotypes at I2
and I3 were Isfahan1 and Isfahan4, respectively. Among
measured parameters, the contribution of POX and proline
was greatest in induction of drought tolerance in Isfahan1
as the extent of increases of these two parameters was
highest in this genotype at I2 compared to normal irrigation. However, all parameters, except POX, had significant
contribution to the drought tolerance of Isfahan4 at I3. The
role of carotenoids in this regard was only significant at I3.
The results may indicate that the stress tolerance induced
by antioxidants and osmolytes was genotype and stress
severity dependent. On the other hand, the highest susceptibility of Markazi at I2 was related to the reduction in
CAT and soluble carbohydrates or the least increase in
APX activity. However, the greatest susceptibility of Ultan
at I3 was attributed to its lowest amount of proline and
carotenoids as compared to the other genotypes at this
stress level.
In conclusion, genotypic differences in water stress
tolerance observed in this study were mainly attributed to
the ability of sesame plants to activate enzymatic antioxidant defense mechanism and/or to accumulate greater
amounts of carotenoids, proline, and soluble carbohydrates
in their leaves in response to water stress. In general,
genotypes with higher activity of antioxidant enzymes
CAT, POX, and APX, and also greater content of carotenoids, proline, and soluble carbohydrates had lower
decrease in grain yield under water deficit stress. In other
words, increase in antioxidants and osmoregulators could
increase the survival ability of sesame genotypes under
stress.
Ability of genotypes to induce the antioxidant response
varied under different stress levels. Among tested genotypes, Isfahan4, Borazjan, Isfahan1, Ahvaz, Ardestan, and
Shiraz were recognized as relatively tolerant and Ultan,
Shahreza, Kal, and Markazi were identified as relatively
sensitive genotypes to water stress. Sesame genotypes with
better water deficit tolerance maintain higher antioxidant
enzyme activities resulting in lower water deficit-induced
oxidative damage. According to the results of this experiment, antioxidant status and the contents of proline and
soluble carbohydrate in leaves can be used as indices of
water deficit tolerance in sesame genotypes.

649

Author contribution Azam Kadkhodaie, Ph.D. student

carried out the field work, collected samples and data,
performed laboratory and chemical analyses of the samples, and prepared the first draft of the manuscript. Morteza
Zahedi, Ph.D., Associate Professor, Co-Adviser and Dissertation Director, helped in designing the experiment,
reviewing and improving the manuscript. Jamshid Razmjoo, Ph.D., Professor, Co-Adviser, helped in designing
the experiment and more vigorously reviewing and
improving the manuscript. Mohammad Pessarakli, Ph.D.,
Professor, helped in designing the experiment and most
critically and vigorously reviewing in improving the English language writing skills of the manuscript.
Acknowledgments This work was supported by the Isfahan University of Technology.

References
Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response
to drought stress in ten cultivars of oilseed rape (Brassica napus
L.). Plant Breed 46:2734
Alizadeh A (2004) Soil, water and plant relationship, 4th edn. Emam
Reza University Press, Mashhad (ISBN. 964-6582-57-50)
Allen RG, Pereira LS, Raes D, Smith M (2000) FAO irrigation and
drainage paper. Crop Evapotranspiration (Guidel Comput Crop
Water Requir) 56:1326
Andrew JS, Moreau H, Kuntz M, Pagny G, Lin C, Tanksley S,
McCarthy J (2008) An investigation of carotenoid biosynthesis in Coffea canephora and Coffea arabica. Plant Physiol
165:10871106
Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E,
Puntarulo S (1999) Drought and watering-dependent oxidative
stress: effect on antioxidant content in Triticum aestivum L.
leaves. J Exp Bot 50:375383
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free
proline for water stress studies. Plant Soil 39(1):205207
Boydak E, Karaaslan D, Simsek M, Gercak S, Kirnak H, Kaspa Y,
Ozturk I (2007) Effect of irrigation methods and irrigation
interval on yield and some yield components of sesame growing
in semi-arid area. J Agron 6(3):439443
Brar GS, Kar S, Singh NT (1990) Photosynthetic response of wheat to
soil water deficits in the tropics. J Agron Crop Sci 164:343348
Chance B, Maehly AC (1955) Assay of catalases and peroxidase.
Method Enzymol 2:764775
Demmig-Adams B, Adams WW (1996) Chlorophyll and carotenoid
composition in leaves of Euonymus kiautschovicus acclimated to
different degrees of light stress in the field. Aust J Plant Physiol
23:649659
Deng X, Hu ZA, Wang HX, Wen XG, Kuang TY (2003) A
comparison of photosynthetic apparatus of the detached leaves
of the resurrection plant Boea hygrometrica with its non-tolerant
relative Chirita heterotricha in response to dehydration and
rehydration. Plant Sci 165:851861
Fazeli F, Ghorbanli M, Niknam V (2007) Effect of drought on
biomass, protein content, lipid peroxidation and anti-oxidant
enzymes in two sesame cultivars. Biol Plant 51:98103
Fischer RA, Maurer R (1978) Drought resistance in spring wheat
cultivars. 1. Grain yields responses. Aust J Agric Res 29:897912
Gao J (2006) Experimental techniques of plant physiology. Higher
Education Press, Beijing (In Chinese)

123

650
Ghorbanli M, Ebrahimzadeh H, Sharifi M (2004) Effects of NaCl and
mycorrhizal fungi on antioxidative enzymes in soybean. Biol
Plant 48:575581
Glombitza C, Dubuis PH, Thulke O (2004) Crosstalk and differential
response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant
Mol Biol 51:119
Hassanzadeh M, Ebadi M, Panahyan-e-Kivi M, Jamaati-e-Somarin
SH, Saeidi M, Zabihi-e-Mahmoodabad R (2009) Evaluation of
drought stress on relative water content and chlorophyll content
of sesame (Sesamum indicum L.) genotypes at early flowering
stage. Res J Environ Sci 3(3):345350
Havaux M, Tardy F (1999) Loss of chlorophyll with limited reduction
of photosynthesis as an adaptive response of Syrian barley
landraces to high-light and heat stress. Aust J Plant Physiol
26:569578
Hendry GAF, Price AH (1993) Stress indications: chlorophylls and
carotenoids. In: Hendry GAF, Grime JP (eds) Methods in
comparative plant ecology, 1st edn. Chapman and Hall, London,
pp 148152
Herzog V, Fahimi H (1973) Determination of the activity of
peroxidase. Anal Biochem 55:554562
Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress
induce changes in concentration of proline and total soluble
sugar in nodulated alfalfa (Medicago sativa) plants. Physiol
Plant 84:5560
Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R,
Panneerselvam R (2009) Drought stress in plants: a review on
morphological characteristics and pigments composition. Int J
Agri Biol 11:100105
Karaaslan D, Boydak E, Gercek S, Simsek M (2007) Influence of
irrigation intervals and row spacing on some yield components
of sesame grown in Harran region. Asian J Plant Sci 6:623662
Kholova J, Hash CT, Kocova M, Vadez V (2011) Does a terminal
drought tolerance QTL contribute to differences in ROS
scavenging enzymes and photosynthetic pigments in pearl millet
exposed to drought? Environ Exp Bot 71:99106
Kim KS, Park SH, Jenks MA (2006) Changes in leaf cuticular waxes
of sesame (Sesamum indicum L.) plants exposed to water deficit.
J Plant Physiol 164:11341143
Kreps JA, Wu YJ, Chang HS (2002) Transcriptome changes for
Arabidopsis in response to salt, osmotic, and cold stress. Plant
Physiol 130:21292141
Mensah JK, Obadoni BO, Eruotor PG, Onome-Irieguna F (2006)
Simulated flooding and drought effects on germination, growth,
and yield parameters of sesame (Sesamum indicum L.). Afr J
Biotech 5(13):12491253
Mitra J (2001) Genetics and genetic improvement of drought
resistance in crop plants. Curr Sci 80:758762
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004)
Reactive oxygen gene network of plants. Trends Plant Sci
9(10):490498
Munne-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the
biological significance of chlorophyll loss in Rosmarinus
officinalis plants. Planta 207:925931
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by
ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell
Physiol 22:867880
Nazarli H, Faraji F, Zardashti MR (2011) Effect of drought stress and
polymer on osmotic adjustment and photosynthetic pigments of

123

Acta Physiol Plant (2014) 36:641650

n
sunflower.
Cercetari
Agronomice
Moldova
XLIV(1(145)):3541
Noctor G, Foyer CH (1998) Ascorbate and glutathione. Keeping
active oxygen under control. Ann Rev Plant Physiol Mol Biol
49:249279
Parida AK, Dagaonkar VS, Phalak MS, Umalkar GV, Aurangabadkar
LP (2007) Alterations in photosynthetic pigments, protein and
osmotic components in cotton genotypes subjected to short-term
drought stress followed by recovery. Plant Biotechnol Rep
1:3748
Pastori GM, Trippi VS (1992) Antioxidative protection in a droughtresistant maize strain during leaf senescence. J Plant Physiol
87:227231
Pinhero RG, Pao MV, Palyath G, Murr DP, Fletcher RA (2000)
Changes in the activities of antioxidant enzymes and their
relationship to genetic and paclobutrazol induced chilling
tolerance of maize seedlings. J Plant Physiol 114:695704
Ramachandra Reddy A, Viswanatha Chaitanya K, Vivekanandan M
(2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:11891202
Rudoplh AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing
agents-proline, betaine, and trehalose on membrane phospholipids. Arch Biochem Biophys 245:134143
Saeidi A, Tohidi-Nejad E, Ebrahimi F, Mohammadi-Nejad G,
Shirzadi MH (2012) Investigation of water stress on yield and
some yield components of sesame genotypes (Sesamum indicum
L.) in Jiroft Region. J Appl Sci Res 8(1):243246
Selote DS, Khanna-Chopra R (2004) Drought-induced spikelet
sterility is associated with an inefficient antioxidant defense in
rice panicles. Plant Physiol 121:462471
Shao HB, Liang ZS, Shao MA (2003) Roles of ABA signal
transduction during higher plant seed maturation and germination. Forestry Stud China 5(4):4251
Shao HB, Liang ZS, Shao MA (2005) Impacts of PEG-6000
pretreatment for barley (Hordeum vulgare L.) seeds on the
effect of their mature embryo in vitro culture and primary
investigation on its physiological mechanism. Colloids Surf B
Biointerfaces 41(23):7377
Sharma P, Dubey RS (2005) Drought induces oxidative stress and
enhances the activities of antioxidant enzymes in growing rice
seedlings. Plant Growth Regul 46:209221
Tantawy MM, Ouda SA, Khalil FA (2007) Irrigation optimization for
different sesame varieties grown under water stress conditions.
J Applied Sci Res 3:712
Terzi R, Kadioglu A (2006) Drought stress tolerance and the
antioxidant enzyme system in Ctenanthe setosa. Acta Biol
Cracov Bot 48(2):8996
Vasconcelos ACF, Zhang XZ, Ervin EH, Kiehl JD (2009) Enzymatic
antioxidant responses to Biostimulants in maize and soybean
subjected to drought. Scientia Agricola 66(3):395402
Wang JR, Li SX, Li KI (2001) Effect of water limited deficit stress
during different growth stages on leaf enzymes of winter wheat.
Acta Bot Borel Occident Sin 21(1):4752
Yang D, Shen X, Zhao T, Ma X (2001) Achievement of droughtinjury physiology in maize. Crops (In Chinese) 5:14
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:6671
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr
Opin Plant Biol 6(5):441445
Zhu JH, Shi HZ, Lee BH (2004) An Arabidopsis homeodomain
transcription factor gene, HOS9, mediates cold tolerance through
a CBF-independent pathway. PNAS 101(26):98739878