International Journal of Agriculture and Crop Sciences.
Available online at www.ijagcs.com
IJACS/2013/5-8/838-844
ISSN 2227-670X ©2013 IJACS Journal
Changes in root traits and some physiological
characteristics of four wheat genotypes under salt
stress
ElaheAkbari Ghogdi1, Azam Borzouei2*, Sepideh Jamali3, NafisehHashem pour3
1. Department of Agronomy and Plant Breeding, College of Abouraihan, University of Tehran, Tehran, Iran.
2. Agricultural and Industrial Research School, Nuclear Science and Technology Research Institute, Karaj, Iran.
P.O.Box:31485-498.
3. Department of Agronomy, Islamic Azad University, Karaj Branch.
*Corresponding author email: [email protected], aborzouei@ nrcam.org,
Telephone number: +982634464060
ABSTRACT: The effects of salt stress on some root features and biochemical traits in wheat
(Trticumaestivum L.) were carried out in a factorial experiment based on completely randomized design,
under greenhouse condition. Four Salinity treatment levels were established: S =1.3dS.m-1 (control), 5,
10, 15 dS.m-1 that combined calcium chloride and sodium chloride sources with 1:10 (Ca:Na ratio) and
wheat genotypes involved 4 cultivars: Sistani and Neishabour (tolerant) ,Tajan and Bahar (sensitive).
Various roottraits as volume androot area shoot and root dry weight and root/shoot ratio wererecorded at
10 days after pollination. In addition, membrane stability index (MSI), malondialdehyde (MDA) and
superoxide dismutase (SOD) activity as some biochemical traits were measured at the tillering stage (45
days after sowing) and flowering stage (75 days after sowing). Salinity stress reduced MSI and all root
traits. Nonetheless, the superoxide dismutase (SOD) activity and MDA accumulation were increased in all
genotypes and in both growth stage. Sistani and Neishabour showed more amounts of MSI and SOD
activity and all root traits under salt conditions, compared to Bahar and Tajan that exhibited higher value
of MDA accumulation (at both growth stage). Results suggested that the salinity tolerance of tolerant
cultivars as manifested by higher value in root features is associated with higher antioxidant activity of
SOD, lower MDA accumulation relative to the sensitive cultivars.
Key words: Superoxide dismutase, Membrane stability Index, Malondialdehyde, Salinity
INTRODUCTION
Salt stress could inhibit plant growth and reduce plant productivity through water deficit, ionic toxicity and
nutritional imbalance. Water deficit is the primary effect of salt stress due to lowered water potential of the soil
solution and restricting root water uptake (Munns, 2002). Salinity can affect growth, dry matter accumulation and
yield. It is well known that dry mass of plants is reduced in proportion to the increase in salinity (Asish Kumar et al.,
2005). Inhibition of plant growth by salinity may be due to the inhibitory effect of ions. Neumann (1995) indicated
that salinity can rapidly inhibit root growth and hence capacity of water uptake and essential mineral nutrition from
soil. It has been reported that the plants had the reduction in their fresh weights because of the proportional
increase in Na+ concentration, which could imply that an ionic effect was being manifested (Maas, 1986). Unlike
drought, salinity stress is an intricate stress which includes osmotic stress, specific ion effect and nutrient
deficiency, etc., thereby affecting various physiological and biochemical mechanisms associated with plant growth
and development. Salinity has a pronounced effect on plasma membrane lipid peroxidation, thereby affecting its
permeability which in turn modulates the pattern of ion leakage (Sairam et al., 2002; Kukreja et al., 2005). Evidence
suggests that membranes are the primary sites of salinity injury to cells and organelles (Candan and Tarhan, 2003)
because ROS can react with unsaturated fatty acids to cause peroxidation of essential membrane lipids in
plasmalemma or intracellular organelles (Karabalet al., 2003; Stewart and Bewley, 1980). Peroxidation of
plasmalemma leads to the leakage of cellular contents, rapid desiccation and cell death. Stability of biological
Intl J Agri Crop Sci. Vol., 5 (8), 838-844, 2013
membranes has been taken as an effective screening tool to assess the salinity stress effects (Kukreja et al.,
2005). For example, Sairam et al. (2002) have used membrane stability index (MSI) as one of the parameters to
differentiate two wheat genotypes growing at salinity levels between electrical conductivity (EC) of 5.4 and 10.6
dS.m-1 (app. 50–100 mM). They reported salinity-induced reduction in MSI and relative water content (RWC) in
both genotypes. When a plant faces harsh conditions, ROS production will overcome scavenging systems and
oxidative stress will burst. In these conditions, ROS attack vital biomolecules and disturb the cell metabolism and
ultimately the cell causes its own death (Sakihama et al., 2002). Fortunately, plants have developed various
protective mechanisms to eliminate or reduce ROS, which are effective at different levels of stress-induced
deterioration (Beak and Skinner, 2003). The enzymatic antioxidant system is one of the protective mechanisms
including superoxide dismutase (SOD: EC 1.15.1.1), which can be found in various cell compartments and it
catalyses the disproportion of two O2·-radicals to H2O2 and O2 (Scandalios, 1993). In plant cells, the cooperation
from antioxidant enzymes is essential for the scavenging of ROS(Esfandiari et al., 2007). Role of cellular
antioxidant system in relation to water and/or temperature stress tolerance has been reported by many workers
(Sairam et al., 1998). These antioxidant enzymes are reported to increase under various environmental stresses
(Hernandez et al., 1993; Yu and Rengel, 1999) as well as comparatively higher activity has been reported in
tolerant cultivars than the susceptible ones (Sreenivasulu et al., 2000; Sairam et al., 2000), suggesting that higher
antioxidant enzymes activity have a role in imparting tolerance to these cultivars against environmental stresses.
Salinity has the most important role in decreasing wheat growth and performance in Iran. On the other hand, wheat
has a significant role in food security in our country. Thus, the present study was conducted to elucidate the
difference in salt tolerant and sensitive cultivars of wheat crop in relation to some root features and biochemical
traits including of lipid peroxidation and superoxide dismutase activity as one of antioxidant enzymes in salt stress
condition.
MATERIALS AND METHODS
Plant growth and treatment
In order to investigate the effects of salt stress on some of root features and biochemical traits in wheat,
this study carried out in a greenhouse (14 h light/10 h dark and natural light with of 250 mol m-2 s-1 irradiance,
25±2°C/15±2°C day/night temperature and 60±5% relative humidity) and consisted of four wheat (Triticumaestivum
L.) cultivars, known as Neishabour and Sistani (salt stress tolerant), and also Bahar and Tajan (salt stress
susceptible). Plants were grown in uniformed pots (23×30 cm) filled with 4 kg loamy soil. These cultivars were
received from Iranian Seed and Plant Improvement Institute, Karaj, Iran. The experimental plan was a completely
randomized design in factorial arrangement that was replicated three times. This experiment consisted of four
salinity treatment levels including: 1.3 dS.m-1(control), 5, 10 and 15 dS.m-1 with calcium chloride and sodium
chloride in 1:10 ratio (Ca2+: Na+). Before experimentation, seeds were decontaminated by 10% sodium hypochlorite
solution within 8 min, washed thoroughly, and then imbibed in distilled water. After that, five seeds were planted in
each pot but in 4-6 leaf stage, just three plants were retained in each pot. To avoid any osmotic shock while seeds
were emerging, salt enforcing was initiated in 4-6 leaf stage and continued until maturity stage. Observations for
various root traits were recorded at 10 days after pollination. The plants were harvested and the roots and shoots
were separated and washed with deionized distilled water.Various root traits as volume and root area, shoot and
root dry weight and root/shoot ratio were measured. For the estimation of plant dry matter, the plants were dried at
70 C for 48 h. In addition, membrane stability index (MSI), malondialdehyde (MDA) and superoxide dismutase
(SOD) activity as some biochemical traits were estimated at the tillering stage (45 days after sowing) and flowering
stage (75 days after sowing). Samples of each treatment were immediately transferred to liquid nitrogen and
maintained at -70°.
Lipid peroxidation
Lipid peroxidation in leaf tissue was determined by measuring malondialdehyde (MDA), a major
thiobarbituric acid reactive species (TBARS) and product of lipid peroxidation (Stewart and Bewley 1980). The
amount of MDA was calculated using the extinction coefficient of 155mM−1 cm−1 and expressed as nmol g−1 FW.
Membrane stability index
Membrane stability index was determined by recording the electrical conductivity of leaf leakages in double
distilled water at 40 and 1000C (Sairam, 1994).
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Intl J Agri Crop Sci. Vol., 5 (8), 838-844, 2013
Assay of SOD activity
SOD activity was estimated by recording the decrease in absorbance of superoxide-nitro blue tetrazolium
complex by the enzyme (Dhindsaet al. 1981).
Statistical analysis
The present data are the mean values of three independent experiments with five replicates. Statistical
calculations were performed with SPSS-16 statistical software. Mean difference comparison among different
treatments was done by ANOVA and Duncan’s multiple range tests at a 0.05 probability level.
RESULTS AND DISCUSSION
Root area and root volume decreased with the increase in salinity levels in all of cultivars and showed
significant difference in different salinity levels as compared with the control. This difference was also observed
between susceptible and tolerant cultivars (Table1). Sistani and Neishabourcvs indicated the highest mentioned
traits at all salinity levels and exhibited significant difference as compared with other two cultivars (Table 2). Root
and shoot dry weight decreased with the increase in salinity levels. Percentage reduction of root and shoot dry
weight at 15 dS.m-1in comparison with the control was 57.31% and 46.95%, respectively. In both traits, Bahar and
Sistani maintained the lowest and the highest, respectively (Table1). Besides ,Bahardisplayed the lowest root dry
weight at all salinity levels. However, this cultivar did not show significant difference as compared at all salinity
levels with control (Table 2).Root to shoot ratio decreased along with an increase in salinity levels. Bahar and
Sistani showed the lowest and the highest value, respectively (Table 1). In addition, it was higher in salt tolerance
cultivars at all salinity levels (Table 2). When the salinity levels increased, the membrane stability index showed a
decrease (Fig. 1A). At two stages, MSI was lower in Tajan and Bahar cultivars and there was significant different at
the highest salinity level (15dS.m-1) in these cultivars in comparison with two other cultivars. Although, MSI
changes in Sistani and Neishabour at all salt stress levels were not so different, but in two other cultivars amount of
MSI reduced consecutively by increasing the salinity levels and these showed significant differences at salinity
levels of 10 and 15 dS.m-1 compared with control, as the mean of percentage reduction in MSI at 15 dS.m-1 over
control were 57.07% (Bahar) and 54.09% (Tajan), however these values were 24.17% in Sistani and 20.32% in
Neishabour cultivars.MDA rose by the increasing of salt stress levels at both stages (Fig.2B). The trends of MDA
content were completely disparate in tolerant and sensitive cultivars of wheat. The amount of MDA rose with the
increasing of salt stress level in four cultivars for both stages (Fig.2B). However the increasing rate of MDA content
was higher in Tajan and Bahar than another two cultivars. Moreover, the increasing of MDA content in Bahar was
more than Tajan (Fig.2B).Sistani and Neishabour showed more SOD activity at both stages for all salinity levels
(Fig. 1C). In first stage, enzyme activity in these cultivars significantly increased at salt level of 15dS.m-1 as
compared tothe control. This increasing was 46.49% and 117.77% in Sistani and Neishabour, respectively. Salt
sensitive cultivars had no significant variation in this case. At flowering stage, SOD activity augmented under
salinity stress in salt tolerance cultivars, too. In Tajan and Bahar the most enzyme activity observed at the first
salinity level (5dS.m-1) and then decreased with increase in salinity levels (Fig. 1C).
The limitation of water absorption as one of the results of salt stress can clear root role as the most
important organ involving in this field. So, it seems that considering its features plays the key role in studying plants
reaction to salt stress. The diversitybetween different plant varieties in root traits such as root volume and area is
associated with their differences in stress resistance including salt stress. Consequently, the selection based on
these, as one of selection criteria, can be useful to screen genotypes and varietiesfor salinity tolerance (Gregory,
1988).High value of root traits in salt tolerant cultivars (Sistani and Neishabour) indicates more ability in their water
absorption and maintains turgor which is necessary for better growth under salinity. Similarly, a significant and
positive correlation between root volume and weight with seed function has also been found in wheat genotypes
(Bangalet al, 1988). Accordingly, considering root volume and area as useful traits in better growth and function
and superiority of Sistani and Neishabour cultivars in these two cases, better function of these cultivars under
stress condition could be predicted.High root/shoot ratio may actually enhance the salt tolerance of plants. So, it
has been suggested as a reliable indicator in screening salt tolerance (LalKhajanchiet al, 2007). The mentioned
results did not conformto related reports, because Duncan grouping of cultivars did not match well with rankings in
terms of their salt tolerance and based on this, Tajan as salt sensitive cultivar, was ranked the same as
Neishabour, as salt tolerance cultivar (Table1).This was also perceived at different salinity levels. However,
root/shoot ratio was higher in salt tolerance cultivars at all salinity levels (Table2). It seems that the same ranking of
cultivars with different salt tolerance degree can be solved by using of more sampling records.Insignificant changes
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Intl J Agri Crop Sci. Vol., 5 (8), 838-844, 2013
of values for root dry weight in Bahar at all salinity levels (Table2) indicates that this cultivar has allocated less
assimilate to root and then this is an important feature for salt sensitive cultivars. It can verify the disadvantages of
this cultivar in comparison to Tajan in some traits like shoot dry weight, root volume and root area (Table2).Munns
(2002) reported that salt-tolerant plants show greater ability to survive and maintain continued growth under
salinity. As mentioned above, superiority of Sistani and Neishabour as salt tolerant cultivars of this study was
observed in terms of some root traits. Besides, the differential growth response of the tested cultivars to salinity
was accompanied by distinct cellular parameters such as cell membrane stability and lipid peroxidation.
Interestingly, from this finding, it is very clear that in salt-tolerant cultivars Sistani and Neishabour relatively higher
membrane stability was found. However, the reverse was true in salt-sensitive cultivars Tajan and Bahar. These
results are substantially in accordance with those of Sairam et al. (2005) who reported a lower decrease in
membrane stability index in tolerant genotypes of wheat than in salt-sensitive ones under salt stress.Various works
have examined the generation of ROS and lipid peroxidation in plants in response to salinity stress and have
demonstrated that there is an increase in lipid peroxidation and a decrease of MSI by increasing senescence and
salinity (Sairam et al., 2002; Wang and Jian-guo, 2009).MSI and extent of lipid peroxidation have been used as
indices of salt injury and salt tolerance in crop.The membrane stability decrease reflects the amount of lipid
peroxidation caused by reactive oxygen species (Dhindsaet al., 1981). In this regardFarooq and Azam (2006)
suggested this index is not as suitable for screening wheat under high salinity levels. They reported more injury to
the cell membrane in salt sensitive line as well. So, it seems that more malondialdehyde accumulation and lipid
peroxidation can cause presence of the lowest values of MSI in Tajan and Bahar (Fig.1A). Furthermore, more
membrane stability in salt tolerant cultivars is justified with respect to more increase in antioxidant enzymes
activities in salt tolerant cultivars (including of SOD in this study) and thereby more ability of these cultivars in
destruction of ROS and so less oxidative damage.
Table1.Mean values of shoot and root dry weight, root/shoot ratio and root area and volume for fourwheat cultivars and different
salinity levels
Root
3
volume(cm )
Root
2
area(cm )
Root/shoot
ratio
Shoot dry
-1
weight(g.plant )
Root dry
weight(g/plant)
-1
Salinity levels(dS.m )
control
5
10
15
Cultivar
Bahar
Tajan
Sistani
Neishabour
a
3.5
b
2.32
c
1.62
c
1.51
b
0.85
b
0.98
a
3.63
a
3.48
a
0.83
ab
0.32
c
0.29
c
0.32
a
2.24
b
1.87
c
1.36
c
1.19
a
0.89
b
0.64
c
0.42
c
0.38
26.77
b
29.99
a
135.32
a
134.64
0.25
b
0.30
a
0.41
b
0.35
d
0.89
b
1.54
a
2.13
a
2.09
c
0.22
c
0.48
b
0.75
a
0.88
129.87
b
79.80
cd
61.43
c
55.62
b
a
d
Within columns means followed by the same letter are not significantly different at the 0.05 level according to Duncan’s multiple
range test.
Table2.Comparison of in four wheat cultivars under control and salt stress conditions
Salinity levels (dS.m
)
1
control
5
10
15
-
Cultivars
Bahar
Tajan
Sistani
Neishabour
Bahar
Tajan
Sistani
Neishabour
Bahar
Tajan
Sistani
Neishabour
Bahar
Tajan
Sistani
Neishabour
Root
3
volume(cm )
fgh
1.58
efg
1.68
a
5.52
a
5.21
ghi
1.04
hi
0.88
c
3.22
b
4.13
i
0.44
i
0.71
c
3.11
def
2.22
i
0.35
i
0.67
cd
2.67
de
2.34
Root
2
area(cm )
de
45.09
d
52.69
a
212.77
a
208.91
def
29.68
def
28.26
c
115.45
b
145.18
ef
19.23
ef
21.48
c
110.76
c
94.25
f
13.09
ef
17.54
c
102.27
c
89.59
Root/shoot
ratio
c
0.25
abc
0.36
a
0.46
a
0.44
c
0.24
bc
0.30
abc
0.36
ab
0.4
c
0.26
bc
0.28
abc
0.35
bc
0.3
c
0.25
bc
0.28
a
0.47
bc
0.28
Shoot dry
weight(g/plant)
fg
1.13
bc
1.27
a
2.85
b
2.44
fgi
1.00
def
1.68
b
2.41
b
2.40
hi
0.71
gh
1.12
cd
1.84
cde
1.80
i
0.56
gh
1.12
defg
1.53
def
1.73
Root dry
weight(g/plant)
efg
0.34
bc
0.81
a
1.39
b
1.07
fg
0.23
de
0.51
bc
0.88
b
0.94
g
0.17
efg
0.32
cd
0.64
de
0.54
g
0.14
efg
0.31
cd
0.62
def
0.47
Within columns means followed by the same letter are not significantly different at the 0.05 level according to Duncan’s multiple
range test.
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A
B
C
Figure1. Effect of salinity levels on (A) Membrane stability index (MSI), (B) Malondialdehyde(MDA), (C) Superoxide dismutase
activity (SOD), in wheat genotypes. Data is significant at P 0.05 for treatments and varieties
MDA is regarded as a marker for evaluation of lipid peroxidation or damage to plasmalemma and organelle
membranes that increases with environmental stresses (Esfandiariet al., 2007). MDA content at 15 dS.m-1
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Intl J Agri Crop Sci. Vol., 5 (8), 838-844, 2013
compared with control in Bahar and Tajan in both stages indicates an increase in their membrane permeability,
lipid peroxidation, injury to the cell membrane and finally a decrease in MSI (Fig.1B). Similarly, finding of DionisioSese and Tobita (1998) showed lower MDA accumulation and lipid peroxidation in salt tolerant cultivar of rice. The
same amount of MDA in Sistani and Neishabour can be due to higher activity of antioxidant enzymes at salinity
conditions resulted to scavenge detoxify ROS (specially hydrogen peroxide) and decrease in injury to the cell
membranes (Ashraf and Ali, 2007). An increase in enzyme activity in salt stress conditionas compared to control
was different among cultivars. It can be indicator of their ability to detoxify ROS and oxidative stress tolerance.
Having been studied earlier researches it becomes evident that improvement in the salt tolerance in different plant
species is possible through the genetically engineered overexpression of specific enzymes for scavenging reactive
oxygen species (Van Camp et al., 1994; Ashraf, 2009). More enzyme activity in salt tolerant cultivars demonstrate
more ability of these cultivars in converting of superoxide (O2-)to peroxide hydrogen (H2O2) and increase of
tolerance to oxidative damage. Furthermore, in some other reports comparatively higher activity has been reported
in tolerant cultivars than the susceptible ones (Sairam et al.,1998; Hernandez et al., 2001), suggesting that higher
antioxidant enzymes activity has a role in imparting tolerance to these cultivars against environmental stresses.
During the studying of membrane permeability and activities of some antioxidant enzymesin four lines of canola
(Brassica napusL.), Ashraf and Ali (2007) found that salt tolerant cultivar had more SOD and CAT activity along
with less relative membrane permeability. They proved that overall relative cell membrane permeability and
activities of antioxidant enzymes (SOD, CAT and POX) can be very effective in discriminating the canola cultivars
for salt tolerance. Similarly, in the present study, according to more MSI and less lipid peroxidation by increasing of
SOD activity in Sistani and Neishabour, the higher salt tolerance of these cultivars is suggested. In accordance with
Ashraf’s report (2009), salt sensitive cultivars are not able to enhance enough antioxidant enzymes’ activity in
stress conditions. So, the accumulation of ROS in Bahar and Tajan and thereby, decrease in SOD activity can be
atributad their salt stress sensitivity. However, this should be noted that more activity of this enzyme could not be
the only reason of tolerance of tolerant cultivars. Therefore, it seems that exploration of some other antioxidant
enzymes involved in salt tolerance can be beneficial in detection of the efficiency of salinity-induced tolerance in
studied wheat cultivars.
CONCLUSION
This review provides information on some morphological and biochemical bases of salt tolerance. The
assessment of the effect of salinity on some root parameters in four wheat varieties can be concluded that all of the
considered parameters were affected by salinity with a varietal difference. Indeed, the Sistani cultivar was the more
tolerant one, and Bahar was intermediate the less tolerant.The salt treatments affected negatively on the
membrane permeability and SOD. Considering data obtained on explorated indices of salinity stress tolerance, it is
possible that better salinity resistance of tolerant cultivars was associated with their ability to maintain higher
activity of antioxidant enzymes viz., SOD resulting in lower lipid peroxidation and higher membrane stability. In
conclusion, in the present work, we propose the use of certain root and biochemical indicators for salt tolerance in
wheat, such as exploration of root area and volume, increasing antioxidant enzymes activity (for example, SOD
and some other related enzymes) as well as the reduction fundamentally of lipid peroxidation.
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