Scientia Horticulturae 113 (2007) 120128

www.elsevier.com/locate/scihorti

Impact of exogenous salicylic acid on the growth, antioxidant activity

and physiology of carrot plants subjected to combined salinity
and boron toxicity
Figen Eraslan 1, Ali Inal *, Aydin Gunes, Mehmet Alpaslan
Ankara University, Faculty of Agriculture, Department of Soil Sci. & Plant Nutr., 06110 Diskapi-Ankara, Turkey
Received 14 November 2006; received in revised form 23 February 2007; accepted 21 March 2007

Abstract
Previous studies have shown that salicylic acid (SA) plays a role in the response of plants to salt and osmotic stresses. Therefore, an experiment
was conducted to investigate the impact of exogenous salicylic acid on the growth, physiology and antioxidant activity of carrot (Daucus carota L.
cv. Nantes) grown under combined stress of salinity and boron toxicity. The treatments consisted of salt (control, NaCl, and Na2SO4), boron ( B: 0
and +B: 25 mg B kg 1) and salicylic acid ( SA: 0 and +SA: 0.5 mmol SA kg 1). The diameter of the storage root was increased by NaCl salinity
in the absence of B toxicity, however, it was increased by Na2SO4 salinity under B toxicity. For the storage root yield, NaCl salinity was more toxic
than Na2SO4 salinity. With its role in plant growth regulation, SA application positively affected the storage root dry weight, S concentration,
carotenoids and anthocyanin content and increased the total antioxidant activity (AA) of the shoot and storage root. SA application regulated
proline and toxic ion (B, Cl) accumulation in the storage root and shoot. This study reports the long term effects of SA under stress conditions and
reveals that SA was not as effective as in alleviating abiotic stress as reported in the literature conducted with short-term studies. That means longterm effects of SA would be significantly different from its short-term effects.
# 2007 Elsevier B.V. All rights reserved.
Keywords: Antioxidants; Ascorbate peroxidase; B toxicity; Catalase; Salicylic acid; Salinity

1. Introduction
Salinity and sodicity can reduce plant growth and alter ionic
relations by ionic and osmotic effects (Tarakcioglu and Inal,
2002), and oxidative stress (Borsani et al., 2001). There is an
abundance of information concerning the effects of NaCl,
however, relatively little is known about the responses of plants
to Na2SO4, although there are indications that NaCl is more
phytotoxic than Na2SO4 (Rogers et al., 1998). Boron is
frequently associated with other salts and generally found in
high concentrations in irrigation water of arid regions where
saline soils and saline irrigation water can be prevalent (BenGal and Shani, 2002). Reductions in boron accumulation in the
presence of high sulfate-salinity have been reported in the stems

* Corresponding author. Tel.: +90 312 5961392; fax: +90 312 3178465.
E-mail address: inal@agri.ankara.edu.tr (A. Inal).
1
Future address: Suleyman Demirel University, Faculty of Agriculture,
Department of Soil Sci. & Plant Nutr., Isparta, Turkey.
0304-4238/$ see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.scienta.2007.03.012

of several rootstocks of Prunus (El-Motaium et al., 1994) and in

Eucalyptus tree (Poss et al., 1999). According to Grieve and
Poss (2000) excess external B and salinity interact to limit
growth, yield and yield components of wheat. In a study,
Grattan et al. (2005) have reported that both Cl and SO4 based
salts showed a significant salinityboron interaction and
tolerance of plant to boron increased with increasing salinity
showing no significant difference between salt types. According to Yadav et al. (1989), B concentration of chickpea was
reduced when salinizing salts were 80% chloride and 20%
sulphate.
When plants are subjected to saline conditions, such
biochemical changes occur as production of reactive oxygen
species (ROS) like superoxide, hydrogen peroxide and
hydroxyl radicals (Dat et al., 2000). In order to avoid the
harmful effects of these ROS, plants evolved an effective
scavenging system composed of non-enzymatic antioxidants
(carotenoids, ascorbate, tocopherol), and enzymatic antioxidants, such as catalase (CAT; EC 1.11.1.6) and ascorbate
peroxidase (APX; EC 1.11.1.11). The results of most studies

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

suggest that the resistance to salt stress is usually correlated

with a more efficient antioxidative system (Gossett et al., 1996;
Gueta-Dahan et al., 1997). The enzymatic action of APX
reduces H2O2 using the ascorbate as an electron donor. CAT is
also implicated in removal of H2O2. Salinity induced
production of ROS disturbs the cellular redox system in favor
of oxidized forms, and thereby creating an oxidative stress that
can damage DNA, inactivate enzymes and cause lipid
peroxidation (Smirnoff, 1993).
Under the toxic B conditions, ROS accumulations are
common (Molassiotis et al., 2006). Excess B induced oxidative
damage was reported in apple rootstock (Molassiotis et al.,
2006), in citrus leaves (Keles et al., 2004), and in barley
(Karabal et al., 2003) plants. The decreasing effect of SA on Na,
Cl and B concentrations in plants under saline and toxic B
conditions explains the ameliorating effect of SA (Gunes et al.,
2005). These ameliorating effects of SA may probably arise
from its role in increased antioxidant activity and its protective
role on the deterioration of membranes that regulate the ion
uptake.
Salicylic acid (SA) is considered as a hormone-like
substance, which plays an important role in the regulation of
plant growth and development, seed germination, fruit yield,
glycolysis, flowering and heat production in thermogenic plants
(Klessig and Malamy, 1994). Ion uptake and transport (Harper
and Balke, 1981), photosynthetic rate, stomatal conductance
and transpiration (Khan et al., 2003) could also be affected by
SA application. The role of the SA in defense mechanisms
under both biotic and abiotic stresses suggests that it also
alleviates the salt stress in plants (Tissa et al., 2000; Al-Hakimi
and Hamada, 2001). According to Borsani et al. (2001), SA
multiplies the ROS generation under stress. A direct
physiological effect of SA is the alteration of antioxidant
enzyme activities in vivo. Exogenous SA could regulate the
activities of antioxidant enzymes and increase plant tolerance
to the abiotic stress (He et al., 2002).
However, in contrast to the interaction between NaCl
salinity and B toxicity, a limited number of investigations have
been carried out regarding the interaction between Na2SO4 and
B toxicity, and there is no report on the long-term effects of
salicylic acid on those interaction in carrot. Therefore, the
objective of this work was to investigate the long-term impact
of salicylic acid on the growth, physiology and antioxidative
enzyme activity of carrot plants grown under a combined
salinity (NaCl and Na2SO4 salinity) and B toxicity treatments.
2. Materials and methods
2.1. Growth conditions and treatments
Carrot (Daucus carota L. cv. Nantes) was grown from
October 2004 to May 2005 in a naturally lighted (approximately 70% relative humidity, and 1820/1416 8C day/night
temperature, and heated between November and March)
greenhouse at Faculty of Agriculture, Ankara University.
The soil used in the experiment was clay loam in texture (34%
clay and 39% sand), consisting of 7.76% CaCO3, and has a pH

121

(1:2.5 water extract) of 7.91, 0.39 dS m 1 EC (saturation

extract), 18 mg kg 1 NaHCO3-available P, and 60, 479, 2656
and 143 mg kg 1 NH4OAc-extractable Na, K, Ca and Mg,
respectively, 0.18% total-N (Kjeldahl), and 0.76% OM
(Walkley-Black). Experimental soil also contained DTPAextractable micronutrients (mg kg 1) of 7.12 Fe, 1.40 Zn, 16.53
Mn, 1.90 Cu and 2.67 B. All soil analyses were carried out
according to Page et al. (1982). PVC pots (25 cm in length and
diameter) lined with a polyethylene bag were filled with 8 kg
air-dried soil. Gibberd et al. (2002) conducted an experiment
with carrot by using the salinity rates of 080 mM from a NaCl
and CaCl2 mixture. Apostol et al. (2002) used 60 mM salinity
rate either achieved by NaCl or Na2SO4, and 2 mM B to create
B toxicity in jack pine seedlings. Based on these two and also
our previous studies, the following treatments were chosen. A
three factorial experiment was conducted. Treatments, with
four replicates, consisted of: three salts (control, 50 mmol
NaCl kg 1 and 25 mmol Na2SO4 kg 1), two boron (0 and
25 mg B kg 1 as H3BO3) and two salicylic acid (0 and
0.5 mmol kg 1 soil). The rate of SA used in the experiment was
based on our previous study (Gunes et al., 2005). All these
treatments were applied and incorporated into the soil before
seed sowing. Seeds were sown on October 18, 2004. For the
basal fertilization, 200 mg N kg 1 soil (half before seed sowing
and half in March) from NH4NO3 (33% N) and 100 and
125 mg P and K kg 1 soil from KH2PO4 (before seed sowing)
were applied. Carrot seeds were sown at the rates of 20 seeds to
each pot. After a good stands of plants was established in
November, they were thinned to seven plants per pot. During
the experiment, soil was kept at approximately 70% of the field
capacity by watering with tap water. Plants were irrigated with
boron free tap water 23 times per week when needed. Any
pesticide-like substance was used.
2.2. Sampling and harvest procedure
For fresh matter used in assay, samples were taken from
shoots by choosing youngest fully matured leaflets. All the
measurements with fresh matter were conducted on April 19
29, 2005. At the end of the experiment, plants were harvested
on May 30, 2005 and separated into shoot and storage root.
After weighing biomasses, the shoots were washed once with
tap water and twice in deionized water. After the storage roots
were washed, by the same manner as in shoots, their length and
diameter were measured with a ruler and a digital caliper,
respectively. And, their fresh weights were recorded. The
storage roots were sliced first horizontally into two equal parts,
then, for the electrolyte leakage (EC) measurements, 3 mmthick storage root discs were taken from the hypocotyl side of
the storage root with a vegetable peeler. Then, the storage root
was re-sliced vertically into two equal parts. For the
determination of lipid peroxidation (MDA), ascorbic acid
(Asc), anthocyanin (Acy) and total antioxidant activity (AA)
half disc samples from the storage root were taken individually
and kept in frozen ( 20 8C) until analysis. The rest of the
storage root was shredded into 12 mm pieces. Sub-samples
from the shoots and shredded storage root were dried in a forced

122

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

air oven at 65 8C until a constant mass was reached. They were

then weighed for dry weight determination, and subsequently
ground (40 mesh sieve) for elemental analysis.
2.3. Enzyme extraction and assay
Enzyme extraction was carried out at 04 8C. Samples from
the youngest fully matured leaflet of 0.5 g fresh shoot tissue
homogenized by a Heidolph, Diax 900 homogenizer in 5 mL
100 mM potassium phosphate buffer (pH 7.6) containing 1 mM
EDTA-Na2 and 0.5 mM ascorbate. The homogenized samples
were centrifuged at 10,000  g for 5 min. The supernatant was
used as crude enzyme extract for CAT and APX enzyme
analyses. All colorimetric measurements (including enzyme
activities) were conducted at 25 8C using a spectrophotometer
(Shimadzu UV/VIS 1201). Ascorbate peroxidase (APX)
activity was determined by following the decrease of ascorbate
and measuring the change in absorbance at 290 nm for 1 min
(Nakano and Asada, 1981). The activity was calculated using
the extinction coefficient (2.8 mM 1 cm 1) for ascorbate.
Catalase (CAT) activity (EC 1. 11.1.6) was determined as a
decrease in absorbance at 240 nm for 1 min following the
decomposition of H2O2 (Change and Maehly, 1955). The
activity was calculated using the extinction coefficient
(40 mM 1 cm 1) for H2O2.
2.4. Determination of membrane damage and nonenzymatic antioxidants (stress markers)
Lipid peroxidation (MDA) and electrolyte leakage (EC)
percentage in the storage root disc and shoot samples was
measured (Hodges et al., 1999) to assess the membrane
damage. The amount of MDATBA complex (red pigment)
was
calculated
from
the
extinction
coefficient
155 mM 1 cm 1. The electrolyte leakage percentage (EC%)
was measured by using electrical conductivity method for the
shoot and 3 mm-thick storage root disc samples as described by
Yan et al. (1996).
The H2O2 content of shoot was colorimetrically measured as
described by Mukherjee and Choudhuri (1983). Free proline
content was extracted from 0.5 g of fresh shoot samples in 3%
(w:v) aqueous sulphosalicylic acid and estimated by ninhydrin
reagent (Bates et al., 1973). The non-enzymatic total
antioxidant activity was estimated by the method of Prieto
et al. (1999). Ascorbic acid content was estimated as described
by Mukherjee and Choudhuri (1983).
2.5. Stomatal resistance measurements and photosynthetic
pigments determinations
Chlorophyll and carotenoids were extracted from shoot
tissue with aqueous acetone (80%, v:v). The absorption of the
extracts was measured at 665, 645 and 470 nm. Chlorophyll
and carotenoids were calculated according to Lichtenthaler and
Wellburn (1983). Anthocyanin (Acy) was estimated as
described by Reay et al. (1998). Total carotenoids content of
storage root was estimated by dimethyl sulphoxide containing

acetone extraction method as described by Alalsavar et al.

(2005). Stomatal resistance (s cm 1) of the experimental plants
was measured using the DT Porometer AP4 (DELTA-T
DEVICES, UK). The youngest fully developed intact leaflets
were used in the stomatal resistance measurements. Measurements were conducted on three plants in each pot and
performed in the morning (9.3011.30 a.m.) at the steady light
intensity (>400 mmol m 2 s 1), while leaf temperature varied
between 23 and 26 8C.
2.6. Mineral element determination
In the shoot and storage root samples, Cl concentration was
determined by the method of Johnson and Ulrich (1959). For
the B concentration measurement, 0.5 g of each of the shoot
and storage root sample was dry-ashed in a muffle furnace at
500 8C for 6 h. The ash was then dissolved in 0.1N HCl and B
was determined colorimetrically (420 nm) using the azomethine-H method (Wolf, 1971). In the same extract
solutions, sodium (Na) was determined by flame photometry
(Jenway PFP7, ELE Instrumet Co. Ltd.). Sulphur was
determined by using C-S determinator (Eltra CS 500). Values
were expressed as mg kg 1 DW for B and g kg 1 DW for the
other minerals.
Table 1
Dry (DW) weights (g) of shoots and storage roots, and length (L, cm) and
diameter (D, mm) of storage roots of carrot plants
Salicylic
acid

Boron
(B)

Salt
(S)

Shoot
DW

Storage root
DW

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO
Control
Nacl
Na2SO4

14.3
12.0
14.1
12.7
11.5
12.8
15.9
12.3
41.4
12.9
10.6
14.5

25.8
20.5
25.6
22.6
18.4
30.4
28.2
21.6
27.9
27.9
20.9
30.9

10.0
6.35
9.78
8.95
5.93
9.98
10.2
6.13
10.6
9.18
6.38
9.80

22.2
24.5
22.2
22.6
23.9
23.5
22.0
24.4
22.0
21.9
21.6
23.4

ns

ns

ns

ns

12.9
13.4

23.9
26.2

8.50
8.71

23.2
22.6

ns

**

ns

ns

15.1
12.1
14.3
12.8
11.0
13.7

26.9B
21.0C
26.8B
25.2B
19.6C
30.6A

10.1
6.24
10.2
9.06
6.15
9.89

22.1C
24.5A
22.1C
22.3C
22.7BC
23.5B

ns

**

ns

**

F-test signicance
Mean for SA
SA
+SA
F-test signicance
Mean for B  S
B

+B

F-test signicance

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

Values in columns followed by different letters, where available according to Ftest significance, are significantly different at p < 0.05. ns: Non-significant and
**
p < 0.01.

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

2.7. Statistical analysis

123

anion, dry weight decreases caused by NaCl could be

attributable to Cl toxicity (Table 4). The dry weight of
storage root was increased from 23.9 to 26.2 g by SA
application. This means that SA alleviates the imbalances
caused by salinity and B toxicity. Neither salt nor SA
affected the length of the storage root. Without B toxicity,
NaCl salinity caused an increase in the diameter of storage
root but with B toxicity Na2SO4 salinity caused a decrease in
the diameter of the storage root (Table 1). Under saline
conditions, plants may tend to produce shallow root system
could be an explanation to this result.

A three factorial (salicylic acid, boron and salt) experiment

was set up in a completely randomized design. Each pot
contained seven plants, and each treatment contained four
replicate pots. Analysis of variance was performed on the data,
and significant differences among treatment means were
calculated by the use of Duncans multiple range test
( p < 0.05).
3. Results
3.1. Yield responses

3.2. Photosynthetic pigments, physiological and

antioxidative responses

In contrast to shoot dry weight, storage root dry weight

was influenced by boron and salt interaction. Regardless of B
toxicity, NaCl salinity decreased the dry weights of the
storage root (Table 1). However, Na2SO4 salinity gave
similar yield to that of control under normal B conditions it
increased dry weights of the storage root under toxic B
conditions. Because only difference is the accompanying

Lipid peroxidation (MDA) of carrot shoot was affected by

boron  salt interaction. As compared with control, Na2SO4
increased the shoot MDA content and that was more
pronounced under toxic B conditions (Table 2). This result
indicated that Na2SO4 salinity might have caused more serious
injury on membranes and toxic amount of B accumulation

Table 2
MDA (nmol g 1 FW) content, membrane permeability (EC,%), ascorbic acid (Asc, mmol kg 1 FW) contents, total antioxidant activity (AA, mmol kg 1 FW) of
shoots and storage roots, and proline (mmol kg 1 FW) content, APX and CAT enzyme activity (mmol g 1 DW min 1), and H2O2 content (mmol kg 1 FW) of carrots
shoots
Salicylic
acid

Boron
(B)

F-test
cance

Salt
(S)

MDA
Shoot

Storage root

Shoot

Storage root

Shoot

Storage root

Shoot

Storage root

Proline

APX

CAT

H2O2

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

8.74
8.89
9.65
9.58
8.26
10.8
8.58
9.81
10.1
9.97
9.03
10.8

6.52
6.71
7.49
7.00
6.90
6.70
6.90
6.84
7.32
8.06
7.10
7.30

6.02
6.17
6.08
6.14
6.32
6.38
5.72
6.90
5.78
6.27
6.57
6.92

26.2
26.6
27.2
25.1
25.6
25.9
26.2.
26.4
27.1
25.4
25.7
25.2

20.6
21.4
25.9
22.9
25.9
27.8
23.7
25.1
25.3
25.8
28.2
28.7

13.8A
11.5B
11.9AB
11.0B
12.1AB
12.2AB
12.0AB
12.0AB
11.5B
12.9AB
11.8AB
12.2AB

39.0
34.5
43.1
35.7
35.2
48.5
39.2
36.9
43.5
39.2
35.7
48.3

33.3
32.7
35.7
31.3
34.4
35.8
34.6
37.7
34.0
34.0
40.8
36.2

0.17
0.21
0.32
0.21
0.29
0.33
0.23
0.22
0.38
0.26
0.34
0.32

0.59
1.18
1.03
1.26
1.43
1.37
0.77
1.13
1.01
1.39
1.43
0.98

0.82
1.08
1.15
0.89
1.32
1.22
0.92
1.44
1.03
1.10
1.07
1.11

9.48
12.0
12.2
9.95
11.6
11.5
10.3
11.4
12.7
10.7
10.4
9.33

ns

ns

ns

ns

ns

ns

ns

ns

ns

ns

ns

9.33
9.71

6.88
7.25

6.19
6.36

26.1
26.0

24.1
26.1

12.1
12.1

39.3
40.5

33.8
36.2

0.25
0.29

1.14
1.12

1.08
1.11

11.1
10.8

ns

ns

ns

ns

ns

ns

**

**

ns

ns

ns

8.66B
9.35B
9.86AB
9.77AB
8.64B
10.8A

6.71
6.77
7.40
7.53
7.00
7.00

5.87
6.53
5.93
6.21
6.44
6.65

26.2
26.5
27.1
25.2
25.7
25.5

22.2
23.2
25.6
24.4
27.1
28.2

12.9
11.7
11.7
11.9
12.0
12.2

39.1C
35.7DE
43.3B
37.5CD
35.4E
48.4A

33.9
35.2
34.8
32.6
37.6
36.0

0.20B
0.21B
0.35A
0.24B
0.31A
0.32A

0.68
1.16
1.02
1.33
1.43
1.17

0.87
1.26
1.09
0.99
1.19
1.16

9.91
11.7
12.4
10.3
11.0
10.4

ns

ns

ns

ns

ns

**

ns

**

ns

ns

ns

signifi-

EC

Asc

AA

Shoot

Mean for SA
SA
+SA
F-test
cance

signifi-

Mean for B  S
B

+B

F-test
cance

signifi-

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

Values in columns followed by different letters, where available according to F-test significance, are significantly different at p < 0.05. ns: Non-significant.
*
p < 0.05.
**
p < 0.01.

124

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

under Na2SO4 salinity might also be responsible for this

increase (Table 4). MDA content of the storage root and
membrane permeability (EC) of the shoot and storage root were
not affected by B x S interaction. Shoot Asc content remained
unchanged. However, there was a significant SA  B  salt
interaction on the Asc content of storage root. Storage root Asc
content showed decreases under normal conditions in NaCl
treatment, under toxic B conditions in control treatment and SA
applied conditions under Na2SO4 salinity.
Irrespective of B toxicity, the AA content of carrot shoot was
decreased by NaCl salinity, however, it was increased by Na2SO4
salinity. This shows that NaCl salinity was more toxic than
Na2SO4 salinity. SA application increased the non-enzymatic
total antioxidant activity (AA) of carrot shoot and storage root
from 39.3 to 40.5 mmol kg 1 and from 33.8 to 36.2 mmol kg 1,
respectively (Table 2). The decrease in shoot AA content caused
by NaCl could be explained by specific anion effect and the
ameliorative effect of SA on specific anion toxicity.
Shoot proline content was significantly increased by NaCl
salinity only under toxic B conditions (Table 2), however,
Na2SO4 salinity increased the proline content of carrot shoot
regardless of B toxicity. This shows that the dual effect of NaCl
salinity and B toxicity creates an extra stress conditions. On the
other hand, accumulation of organic solutes, such as proline is
generally one of the main physiological responses of plants to

salinity stress. The activities of APX and CAT enzymes and

H2O2 content of the carrot shoot were not influenced by
salt  boron interaction and SA application (Table 2). There
should be transient changes in enzyme activity and H2O2
accumulation but at the end these parameters remained
unchanged.
Storage root total carotenoids content was influenced by B
toxicity and salt interaction. Boron toxicity decreased the storage
root total carotenoids content under Na2SO4 salinity. This means
that salt type under toxic B conditions exerts its importance on
carotenoids metabolism. Total carotenoids content of the storage
root was affected significantly ( p < 0.01) by the SA application
(Table 3). Approximately, 15% higher storage root total
carotenoids accumulated in SA treated plants. By amending B
toxicity, SA could relieve the effect of stress on plants. Carrot
shoot anthocyanin (Acy) content remained unchanged (Table 3).
SA application led to an increase in Acy content of storage root
from 12.4 to 18.0 mg 100 g 1 FW.
Boron  salt interactive effect on chlorophyll and carotenoids content of shoot was significant. In the absence of B
toxicity, NaCl and Na2SO4 salinity decreased the chlorophyll
content in a similar manner (Table 3). In the presence of B
toxicity, NaCl salinity caused less chlorophyll content as
compared to Na2SO4 salinity. Salinity achieved by Na2SO4
decreased the carotenoids content of the shoot under the

Table 3
Storage root total carotenoids (mg 100 g 1 FW) content, shoot and storage root anthocyanin (Acy, mg 100 g
and carotenoids, mg g 1 FW), and stomatal resistance (s cm 1) of carrot shoots
Salicylic
acid

Boron
(B)

FW) contents, photosynthetic pigments (chlorophyll

Salt
(S)

Storage roots
total carotenoids

Acy
Shoot

Storage root

Chlorophyll

Carotenoids

Stomatal resistance

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

13.8
14.7
15.3
16.1
16.7
14.7
16.5
16.3
20.1
18.8
17.8
15.5

179
207
221
210
185
196
228
189
217
2.5
175
195

13.0
11.8
14.5
9.44
12.5
13.4
16.1
21.4
17.1
14.5
20.7
18.4

1.81
1.63
1.40
1.72
1.57
1.79
2.02
1.75
1.78
1.38
1.47
1.70

0.36
0.32
0.28
0.35
0.32
0.39
0.40
0.36
0.39
0.30
0.29
0.36

3.96
5.11
5.90
3.77
6.95
5.70
4.75
7.55
6.15
3.82
7.40
6.83

ns

ns

ns

ns

ns

ns

15.2
17.5

200
202
ns

12.4
18.0

1.65
1.68
ns

0.34
0.35
ns

5.23
6.08

15.1B
15.5AB
17.7A
17.5AB
17.3AB
15.1B

204
198
219
207
180
195

1.46
16.6
15.8
12.0
16.6
15.9

1.92A
1.69BC
1.59BC
1.55BC
1.52C
1.74AB

0.38A
0.34ABC
0.33BC
0.32C
0.30C
0.37AB

4.35
6.33
6.02
3.79
7.18
6.27

**

ns

ns

**

**

ns

F-test significance

Shoot

Mean for SA
SA
+SA

**

F-test significance

**

Mean for B  S
B

+B

F-test significance

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

Values in columns followed by different letters, where available according to F-test significance, are significantly different at p < 0.05. ns: Non-significant.
*
p < 0.05.
**
p < 0.01.

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

absence of toxic B but increased it under toxic B conditions. On

the aspects of chlorophyll and carotenoids content of carrot
shoot, combined effects of NaCl salinity and B toxicity seems
to more deleterious than that of Na2SO4 salinity and B toxicity.
Shoot stomatal resistance, as another physiological parameter,
was significantly affected by SA ( p < 0.05) application.
Stomatal resistance was increased from 5.23 to 6.08 s cm 1
by SA application (Table 3).
3.3. Mineral nutrient responses
Mineral nutrient responses of the carrot plants are presented
in Table 4. In the absence of B, toxicity shoot and storage root B
concentrations were similar to that of control regardless of salt
type. However, when compared to control, NaCl salinity
decreased shoot and storage root B concentration under toxic B
conditions. In contrast to NaCl salinity, Na2SO4 salinity gave
similar shoot but higher storage root B concentration to that of
control plants (Table 4). Storage root B concentration was
significantly decreased from 48.8 to 43.0 mg kg 1 by the SA
application.
Regardless of salt type shoot and storage root Na
concentrations were significantly increased. But, the increases
in Na contents were more pronounced under Na2SO4 salinity.
Under toxic B conditions the increases in Na contents were less
Table 4
Boron (B, mg kg

Salicylic
acid

DW), sodium (Na, g kg

Boron
(B)

DW), chloride (Cl, g kg

125

than that of normal B conditions (Table 4). This seems to

suggest that there was a significant interaction between salinity
and B toxicity. The interaction between NaCl salinity and B
toxicity was much strong than the interaction between Na2SO4
and B toxicity.
Interaction between B and salt was significant on Cl
concentrations of shoot and storage root of carrot. While NaCl
salinity increased the shoot and storage root Cl concentrations
both in the absence or presence of B toxicity, the increases in Cl
concentrations were less under toxic B conditions. Regardless
of B toxicity, a general decrease in the Cl content was caused by
Na2SO4 salinity. Chloride (Cl) concentrations of the shoot and
storage root of carrot plants were significantly decreased by SA
application (Table 4).
While Na2SO4 salinity increased the shoot and storage root S
concentrations both in the absence or presence of B toxicity, the
increases in S concentration was less under toxic B conditions.
Regardless of B toxicity, a general decrease in the S content was
caused by NaCl salinity (Table 4). Storage root S concentration
was increased from 0.54 to 0.61 g kg 1 by SA.
4. Discussion
When compared with Na2SO4 salinity, dry weights of
storage root were decreased sharply by NaCl salinity either in

DW), and sulphur (S, g kg

DW), concentrations of shoots and storage roots of carrots

Salt
(S)

B
Shoot

Storage root

Shoot

Storage root

Shoot

Storage root

Shoot

Storage root

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

50.0
40.7
51.0
303
161
293
52.7
45.3
50.2
289
148
303

14.3
11.1
17.0
88.8
66.3
95.3
13.9
10.2
19.3
71.9
53.7
89.0

1.46
6.37
7.86
1.44
4.88
6.34
1.56
6.50
7.78
2.03
5.15
6.68

0.75
2.39
3.47
0.83
1.97
2.09
0.73
2.20
3.46
0.81
1.71
2.08

12.3
49.7
10.1
12.4
44.5
11.6
9.90
49.4
9.90
12.0
44.5
8.80

2.40
12.4
1.50
2.50
9.50
1.60
1.70
10.7
0.70
2.30
10.2
1.70

2.46
2.46
4.09
2.88
2.47
3.27
2.69
2.42
3.85
2.85
2.47
3.16

0.36
0.44
0.87
0.50
0.30
0.75
0.39
0.68
0.88
0.49
0.42
0.80

ns

ns

ns

ns

ns

ns

ns

ns

150
148

48.8
43.0

4.72
4.95

1.92
1.83

23.4
22.4

4.98
4.55

2.94
2.91

0.54
0.61

ns

**

ns

ns

ns

**

51.4C
43.0C
50.6C
296A
155B
298A

14.1D
10.7D
18.1D
80.4B
60.0C
92.2A

1.51D
6.43B
7.82A
1.73D
5.01C
6.51B

0.74D
2.30B
3.47A
0.82D
1.84C
2.08BC

11.1CD
49.6A
10.0D
12.2C
44.5B
10.2D

2.05C
11.6A
1.10D
2.40C
9.85B
1.65CD

2.58CD
2.44D
3.97A
2.86C
2.47D
3.21B

0.38D
0.56C
0.88A
0.49C
0.36D
0.77B

**

**

**

**

**

**

**

**

F-test significance

Na

Cl

Mean for SA
SA
+SA
F-test significance
Mean for B  S
B

+B

F-test Significance

Control
NaCl
Na2SO4
Control
NaCl
Na2SO4

Values in columns followed by different letters, where available according to F-test significance, are significantly different at p < 0.05. ns: Non-significant.
*
p < 0.05.
**
p < 0.01.

126

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

the presence or absence of B toxicity. Similar findings on the

comparisons of SO4 and Cl salinity were reported for the dry
mass and root growth rate of rice (Abdelgadir et al., 2005) and
maize plant (Turan and Aydin, 2005). Under toxic B conditions,
Na2SO4 salinity increased storage root dry weight. Yield
reduction induced by NaCl salinity is probably associated with
the higher rate of toxic Cl ion accumulation (Table 4). In a
study, Lucerne genotypes were found more tolerant to salinity
where Na2SO4 predominates than the situation where NaCl is
the dominant salt (Rogers et al., 1998). Storage root diameter
was increased by NaCl salinity under normal B conditions, but
under B toxic conditions it was increased by Na2SO4 salinity.
According to Apostol et al. (2002), low injury and lesser
reduction of growth in Na2SO4 salinity, compared with NaCl
salinity, could be partly due to the ability of jack pine of
preferentially accumulating S, Na and B in roots rather than in
shoots. It is also possible that S could help alleviate Na toxicity
(Harborne, 1977). An increase in storage root dry weight with
the effect of SA could be attributable to its growth stimulating
effects. Similar to this, yield improvements in wheat as the
result of SA application has been reported by Shakirova et al.
(2003).
The MDA content of the shoot, as an index of the membrane
integrity and lipid peroxidation, was increased by Na2SO4
salinity especially under toxic B conditions. It was reported
that, membrane permeability in maize and sorghum (Ismail,
2003/2004) and in jack pine seedling (Apostol et al., 2002)
increased under the saline conditions (NaCl and Na2SO4) with
the increasing levels of B.
Boron  salt  SA interactions decreased the storage root
Asc content as compared to control. Sairam et al. (2005)
reported the decreases in Asc content of wheat genotypes under
salinity. Ascorbic acid, as an antioxidant, could scavenge ROS
and H2O2 non-enzymatically, and also take part in ascorbate
peroxidase (APX) mediated scavenging of H2O2 (Asada, 1992).
While Na2SO4 salinity increased the total antioxidant
activity (AA) of carrot shoot, NaCl salinity decreased it
significantly. Exogenous SA application increased the AA of
both shoot and storage root. This may increase the stress
tolerance of carrot plants resulting in higher storage root yield.
There are suggestions that SA also acts as an antioxidant
(Cheng et al., 1996). Prevention of oxidative damage to cells
during stress was suggested as one of the mechanisms of stress
tolerance (Kraus and Fletcher, 1994) and this level of protection
was attributed to the increased antioxidant activity (Senaratna
et al., 1988; Dat et al., 1998).
In the present study, salt  boron interaction caused
significant increases in shoot proline content. Similarly, Turan
and Aydin (2005) found increases in proline contents of maize
under NaCl and Na2SO4 salinity. Exogenous SA increased the
accumulation of proline in carrot shoot significantly. This result
is consistent with those of Shakirova et al. (2003) who reported
that SA increased the proline content of wheat seedlings grown
under both normal and salt stress. Since proline is one of the
important components of the adaptation of plants to salinity, SA
would contribute to the accumulation of this amino acid under
stress.

APX and CAT detoxify the H2O2 in peroxisomes, cytosol

and chloroplasts. CAT is known to dismutate H2O2 into H2O
and O2. In the present study, APX and CAT activity remained
unchanged. According to Fadzilla et al. (1996), NaCl had no
effect on CAT activity in rice shoots. In the present study, H2O2
content of shoot remained unchanged. Lin and Kao (2000)
reported similar results for rice under the stress of 200 mM
NaCl and Cheng et al. (1996) stated that because of the
dismutation by enzymes a transient increase could occur in
H2O2 accumulation.
SA application caused significant increases in the storage
root total carotenoids content. Similar to total carotenoids, SA
application increased the Acy content of storage root. Brosche
and Strid (2003) stated that the anthocyanin accumulation in
many plants could be induced by biotic and abiotic stresses,
UVB radiation, drought and high or low temperature.
Recently, by concluding the accumulation of anthocyanin
inducible by a wide range of environmental stimuli, Asrar et al.
(2005) reported that the excess Mn in rooting medium increased
the anthocyanin content of spearmint plant. Similarly, Edreva
et al. (2002) reported that reddening of cotton leaves induced by
anthocyanin in the field of Aegean Region was provoked by
high soil salinity resulting in osmotic stress in plants and
Kennedy and De Filippis (1999) found that anthocyanin
pigments increased with NaCl stress in both salt tolerant and
salt sensitive Grevillea species. Under the effects of boron  salt interaction, photosynthetic pigments showed significant decreases. This suggests that there was an antagonistic
relation between photosynthetic pigments, especially for
chlorophyll, and B application.
Leaf stomatal resistance provides sensitive comparisons or
indicates the degree of stress in plants under adverse conditions.
At medium saline conditions, it was reported that both stomatal
and non-stomatal limitations accounted for a reduction of
photosynthesis (Brugnoli and Bjorkman, 1992), and that nonstomatal limitations at the biochemical level due to toxic ions in
leaf cells prevailed under more severe salinity conditions
(Everard et al., 1994). In our experiment, an increase in
stomatal resistance has been detected under the effects of SA.
However, Khan et al. (2003) reported that the stomatal
conductance did not differ from control in SA treated corn and
soybean.
NaCl salinity decreased the shoot and storage root B and
shoot S concentrations. Similarly, salinity caused decreases in
B concentrations in sorghum (Ismail, 2003/2004) and tomato
(Alpaslan and Gunes, 2001) salinized with NaCl was also
reported. The decreases in B concentration of salt-treated plants
were likely responsible for the reduced B toxicity symptoms
(El-Motaium et al., 1994). In contrast to our results, reduced B
accumulation in the presence of high-sulphate or mixed salt
salinity has been reported (Yadav et al., 1989; Poss et al., 1999).
However, Apostol et al. (2002) found decreases in shoot B but
increases in root B concentration in B + NaCl and B + Na2SO4
treatments versus B alone. An interaction between salinity
(NaCl and Na2SO4) and B was reported by Grattan et al. (2005).
Concentration of Na in the shoot and storage root was increased
by both NaCl and Na2SO4 salinity. In pepper plants, again

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

Navarro et al. (2003) also found higher Na in Na2SO4 treated

than that of NaCl treated plants. Salinity achieved by Na2SO4
decreased Cl concentrations, but increased S concentrations of
shoot and storage root. Interactive effects of boron and salt
increased B but decreased Na, Cl and S concentrations of shoot
and storage root. SA decreased storage root B, and shoot and
storage root Cl concentrations but increased the S concentration
of storage root. Also, Metwally et al. (2003) reported that SA
application caused increases in S content of barley roots. NaCl
salinity increased the shoot and storage root Cl concentrations.
Significant increases in Cl and SO4 under saline conditions
were also reported in a study conducted with pepper plants by
Navarro et al. (2003).
5. Conclusion
Results of our study demonstrated that interactive effects of
Na2SO4 and NaCl salinity either in the presence or absence of B
toxicity had different effects on carrot plant growth suggesting
specific anion effects. With respect to the yield, NaCl salinity
was generally more toxic than the Na2SO4 salinity either in the
presence or absence of B toxicity. A strong salt  B interaction,
being greater between NaCl and B toxicity, was established.
With the effects of this strong interaction, generally salt tend to
decrease B accumulation and B toxicity tend to decrease toxic
ion (Na and Cl) accumulation. The positive effect of the SA
application was more pronounced on the data of increased
storage root dry weight, carotenoids, anthocyanin and S content
of storage root, and increased total AA of shoot and storage
root. SA application caused the regulation of proline
accumulation and decreased the toxic ion (Cl) accumulation
both in storage root and shoot. SA diminished the toxic effects
of boron in storage root. However, our experiment studied the
long-term effects of exogenous SA application, those effects
rooted from exogenous SA could be attributable to the
secondary effects of SA application. These beneficial effects
of the SA application could be attributable to its role in plant
growth regulation being a hormone-like substance, and to its
inhibitory effect of abiotic stresses including salt stress. This
study reports the long-term effects of SA under stress
conditions and reveals that SA was not as effective as in
alleviating abiotic stress as reported in the literature conducted
with short-term studies
Acknowledgements
We gratefully thank to Dr. Darrell Norton (Purdue
University, USDA-ARS-NSERL, IN) for critical reading of
the manuscript and help with the English. We are thankful to
Ankara University Scientific Research Fund (BAP) for
supporting the project (Project No: 20030711084).
References
Abdelgadir, E.M., Oka, M., Fujiyama, H., 2005. Nitrogen nutrition of rice plants
under salinity. Biol. Plant. 49, 99104.

127

Alalsavar, C., Al-Farsi, M., Quantick, P.C., Shahidi, F., Wiktorowicz, R., 2005.
Effect of chill storage and modified atmosphere packaging (MAP) on
antioxidant activity, anthocyanins, carotenoids, phenolics and sensory
quality of ready-to-eat shredded orange and purple carrots. Food Chem.
89, 6976.
Al-Hakimi, A.M.A., Hamada, A.M., 2001. Counteraction of salinity stress on
wheat plants by grain soaking in ascorbic acid, thiamin or sodium salicylate.
Biol. Plant. 44, 253261.
Alpaslan, M., Gunes, A., 2001. Interactive effects of boron and salinity stress on
the growth, membrane permeability and mineral composition of tomato and
cucumber plants. Plant Soil 236, 123128.
Apostol, K.G., Zwiazek, J.J., MacKinnon, M.D., 2002. NaCl and Na2SO4 alter
responses of jack pine (Pinus banksiana) seedlings to boron. Plant Soil 240,
321329.
Asada, K., 1992. Ascorbate peroxidase-a hydrogen peroxide scavenging
enzyme in plants. Physiol. Plant. 55, 235241.
Asrar, Z.A., Khavari-Nejad, R.A., Heidari, H., 2005. Excess manganese effects
on pigments of Menta spicata at flowering stage. Arch. Agron. Soil Sci. 51,
101107.
Bates, L.S., Waldren, R.P., Teare, J.D., 1973. Rapid determination of proline for
water stress studies. Plant Soil 39, 205207.
Ben-Gal, A., Shani, U., 2002. Yield, transpiration and growth of tomatoes under
combined excess boron and salinity stress. Plant Soil 247, 211221.
Borsani, O., Valpuesta, V., Botella, M.A., 2001. Evidence for a role of salicylic
acid in the oxidative damage generated by NaCl and osmotic stress in
Arabidopsis seedlings. Plant Physiol. 126, 10241030.
., 2003. Molecular events following perception of ultraBrosche, M., Strid, A
violetB radiation by plants. Physiol. Plant. 117, 110.
Brugnoli, E., Bjorkman, O., 1992. Growth of cotton under continuous salinity:
influence on allocation pattern, stomatal and light energy. Planta 187, 335
347.
Change, B., Maehly, A.C., 1955. Assay of catalases and peroxidase. Meth.
Enzymol. 2, 764775.
Cheng, I.F., Zhao, C.P., Amolins, A., Galazka, M., Doneski, L., 1996. A
hypothesis for the in vivo antioxidant activity of salicylic acid. Biometals
9, 285290.
Dat, J.F., Lopez-Delgado, H., Foyer, C.H., Scott, I.M., 1998. Parallel changes in
H2O2 and catalase during thermotolerance induced by salicylic acid or heat
acclimation in mustard seedlings. Plant Physiol. 116, 13511357.
Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D., Van
Breusegem, F., 2000. Dual action of the active oxygen species during plant
stress responses. Cell Mol. Life Sci. 57, 779795.
Edreva, A., Gurel, A., Gesheva, E., Hakerlerler, E., 2002. Reddening of cotton
(Gosspiyum hirsutum L ). Leaves Biol. Plant. 45, 303306.
El-Motaium, R., Hu, H., Brown, P., 1994. The relative tolerance of six Prunus
rootstocks to boron and salinity. J. Am. Soc. Hort. Sci. 119, 1169
1175.
Everard, J.D., Gucci, R., Kann, S.C., Flore, J.A., Loescher, W.H., 1994. Gas
exchange and carbon partitioning in the leaves of celery (Apium graveolens)
at various levels of root zone salinity. Plant Physiol. 106, 281292.
Fadzilla, N.M., Gill, V., Finch, R.P., Burdon, R.H., 1996. Chilling, oxidative
stress and antioxidant responses in shoot cultures of rice. Planta 199, 552
556.
Gibberd, M.R., Turner, N.C., Storey, R., 2002. Influence of saline irrigation on
growth, ion accumulation and partitioning, and leaf gas exchange of carrot
(Daucus carota L.). Ann. Bot. 90, 715724.
Gossett, D.R., Banks, S.W., Millhollon, E.P., Cran Lucas, M., 1996. Antioxidant
response to NaCl stress in a control and a NaCl-tolerant cotton cell line
grown in the presence of paraquat, buthionine sulfoximine and exogenous
glutathione. Plant Physiol. 112, 803809.
Grattan, S.R., Grieve, C.M., Poss, J.A., 2005. Does salinity reduce borons toxic
effect in broccoli? [Abstract]. Am. Soc. Hort. Sci. 40,1075. American
Society of Horticulture Science Meeting.
Grieve, C.M., Poss, J.A., 2000. Wheat response to interactive effects of boron
and salinity. J. Plant Nutr. 23, 12171226.
Gueta-Dahan, Y., Yaniv, Z., Zilinskas, B.A., Ben-Hayyim, G., 1997. Salt and
oxidative stress: similar and specific responses and their relation to salt
tolerance in Citrus. Planta 203, 460469.

128

F. Eraslan et al. / Scientia Horticulturae 113 (2007) 120128

Gunes, A., Inal, A., Alpaslan, M., Cicek, N., Guneri, E., Eraslan, F., Guzelordu,
T., 2005. Effects of exogenously applied salicylic acid on the induction of
multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Arch.
Agron. Soil Sci. 51, 687695.
Harborne, J.B., 1977. Flavonoid sulphates: a new class of natural product of
ecological significance in plants. In: Reinhold, L., Harborne, J.B., Swain, T.
(Eds.), Progress in Phytochemistry, vol. 4. Pergamon, New York, USA, pp.
189208.
Harper, J.R., Balke, N.E., 1981. Characterization of the inhibition of K+
absorption in oats roots by salicylic acid. Plant Physiol. 68, 13491353.
He, Y.L., Liu, Y.L., Chen, Q., Bian, A.H., 2002. Thermotolerance related to
antioxidation induced by salicylic acid and heat hardening in tall fescue
seedlings. J. Plant Physiol. Mol. Biol. 28, 8995.
Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K., 1999. Improving the
thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604611.
Ismail, A.M., 2003/2004. Response of maize and sorghum to excess boron and
salinity. Biol. Plant. 47, 313316.
Johnson, J.M., Ulrich, A., 1959. Analytical methods for use in plant analysis. II,
Bull. No. 766, California Agric. Exp. Sta. Berkeley, CA.
ktem, H.A., 2003. Antioxidant responses of tolerant
Karabal, E., Yucel, M., O
and sensitive barley cultivars to boron toxicity. Plant Sci. 164, 925933.
Keles, Y., Oncel, I., Yenice, N., 2004. Relationship between boron content and
antioxidant compounds in Citrus leaves taken from field with different
water source. Plant Soil 265, 345353.
Kennedy, B.F., De Filippis, L.F., 1999. Physiological and antioxidative
responses to NaCl of the salt tolerant Grevillea ilicifolia and salt sensitive
Grevillea arenaria. J. Plant Physiol. 155, 746754.
Khan, W., Prithiviraj, B., Smith, D.L., 2003. Photosynthetic responses of corn
and soybean to foliar application of salicylates. J. Plant Physiol. 160, 485
492.
Klessig, D.F., Malamy, J., 1994. The salicylic acid signal in plants. Plant Mol.
Biol. 26, 14391458.
Kraus, T.E., Fletcher, R.A., 1994. Paclobutrazol protects wheat seedlings from
heat and paraquat injury. Is detoxification of active oxygen species
involved? Plant Cell Physiol. 35, 4552.
Lichtenthaler, H.K., Wellburn, W.R., 1983. Determination of total carotenoids
and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc.
Trans. 11, 591592.
Lin, C.C., Kao, C.H., 2000. Effect of NaCl stress on H2O2 metabolsim in rice
leaves. Plant Growth Reg. 30, 151155.
Metwally, A., Finkemeier, I., Georgi, M., Dietz, K.-J., 2003. Salicylic acid
alleviates the cadmium toxicity in barley seedlings. Plant Physiol. 132, 272
281.
Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I., 2006.
Boron-induced oxidative damage and antioxidant and nucleolytic responses
in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh).
Environ. Exp. Bot. 56, 5462.
Mukherjee, S.P., Choudhuri, M.A., 1983. Implications of water stress-induced
changes in the levels of endogenous ascorbic acid and hydrogen peroxide in
Vigna seedlings. Physiol. Plant. 58, 166170.

Nakano, Y., Asada, K., 1981. Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22, 867880.
Navarro, J.M., Garrido, C., Martinez, V., Carvajal, M., 2003. Water relations
and xylem transport of nutrients in pepper plants grown under two different
salts stress regimes. Plant Growth Reg. 41, 237245.
Page, A.L., Miller, R.H., Keeney, D.R., 1982. Methods of Soil Analysis. Part 2:
Chemical and Microbiological Properties, second ed. SSSA, Madison,
Wisconsin, USA.
Poss, J.A., Grattan, S.R., Grieve, C.M., Shannon, M.C., 1999. Characterization
of leaf boron injury in salt-stressed Eucalyptus by image analysis. Plant Soil
206, 237245.
Prieto, P., Pineda, M., Aguilar, M., 1999. Spectrophotometric quantitation of
antioxidant capacity through the formation of a phosphomolybdenum
complex: specific application to the determination of vitamin E. Anal.
Biochem. 269, 337341.
Reay, F.P., Fletcher, R.H., Thomas, V.J.G., 1998. Chlorophylls, carotenoids and
anthocyanin concentrations in the skin of Gala apples during maturation
and the influence of foliar applications of nitrogen and magnesium. J. Sci.
Food Agric. 76, 6371.
Rogers, M.E., Grieve, C.M., Shannon, M.C., 1998. The response of lucerne
(Medicago sativa L.) to sodium sulphate and chloride salinity. Plant Soil
202, 271280.
Sairam, R.K., Srivastava, G.C., Agarwal, S., Meena, R.C., 2005. Differences in
antioxidant activity in response to salinity stress in tolerant and susceptible
wheat genotypes. Biol. Plant. 49, 8591.
Senaratna, T., McKay, C.E., McKersie, B.D., Fletcher, R.A., 1988. Uniconazole
induced chilling tolerance in tomato and its relationship to antioxidant
content. J. Plant Physiol. 133, 5661.
Shakirova, F.M., Sakhabutdinova, A.R., Bezrukova, M.R., Fatkhutdinova, R.A.,
Fatkhutdinova, D.R., 2003. Changes in the hormonal status of wheat
seedlings induced by salicylic acid and salinity. Plant Sci. 164, 317322.
Smirnoff, N., 1993. The role of active oxygen in the response of plants to water
deficit and desiccation. New Phytol. 125, 2758.
Tarakcioglu, C., Inal, A., 2002. Changes induced by salinity, demarcating
specific ion ratio (Na/Cl) and osmolality on ion and proline accumulation,
nitrate reductase activity, and growth performance of lettuce. J. Plant Nutr.
25, 2741.
Tissa, S., Darren, D., Eric, B., Kinsley, D., 2000. Acetyl salicylic acid (aspirin)
and salicylic acid induce multiple stress tolerance in bean and tomato plants.
Plant Growth Reg. 30, 157161.
Turan, M., Aydin, A., 2005. Effects of different salt sources on growth,
inorganic ions and proline accumulation in corn (Zea mays L.). Eur. J.
Hort. Sci. 70, 149155.
Wolf, B., 1971. The determination of boron in soil extracts, plant materials,
composts, manures, water and nutrient solutions. Commun. Soil Sci. Plant
Anal. 2, 363374.
Yadav, H.D., Yadav, O.P., Dhankar, O.P., Oswal, M.C., 1989. Effect of chloride
salinity and boron on germination, growth, and mineral composition of
chickpea (Cicer arietinum L.). Annals Arid Zone 28, 6367.
Yan, B., Dai, Q., Liu, X., Huang, S., Wang, Z., 1996. Flooding-induced
membrane damage, lipid oxidation and activated oxygen generation in
corn leaves. Plant Soil 179, 261268.