AGRICULTURAL COMMUNICATIONS, 2014, 2(3): 8-14.
Anatomical Changes Induced by NaCl Stress in Root and Stem of
Gazania harlequin L.
ADNAN YOUNIS1,2, ATIF RIAZ1, IFTIKHAR AHMED1, MUHAMMAD IRFAN SIDDIQUE1, USMAN TARIQ1,
MANSOOR HAMEED3 AND MUHAMMAD NADEEM1
1Institute
of Horticultural Sciences, University of Agriculture, Faisalabad, Pakistan.
of Horticultural Science, Kyungpook National University, Daegu, Korea.
3Department of Botany, University of Agriculture, Faisalabad, Pakistan.
*Corresponding Author: [email protected]
2Department
(Accepted: 28 Jun. 2014)
ABSTRACT
NaCl induces the stress that results in plant reduced growth due to changes in internal mechanism of
the plant. The present study was designed to investigate the performance of Gazania harlequin grown
under different salinity levels (25, 50, 75 and 100 mgl-1 of NaCl). The experiment was laid out in the
completely randomized design (CRD) with four replications. Microscopic studies for root and stem
anatomical attributes showed that salinity plays an important role in growth inhibition of plants.
Xylem and phloem areas of root and stem were observed in decreasing trend under salt stress
condition and the cortex also. While minimum cortex and epidermis area was observed in plants
treated with 100 mgl-1. The study revealed that control (T0) exhibited better results as compared to
other treatments under saline conditions. Visual observations showed that the reduction of water
uptake by the plants under high saline condition created osmotic conditions and ion toxicity which
results in smaller cell size and cell injury.
Keywords: Cortex, epidermis, phloem, salinity, stress, xylem.
INTRODUCTION
Ornamental plants provide aesthetic pleasure,
soothing effect; improve the environment and
quality of life (Younis et al., 2002). Ornamental
flowering species tend to have a greater demand
worldwide, depending on people’s preferences for
a particular flowering species (Younis et al., 2010;
Tariq et al., 2012). Gazania harlequin is an
ornamental and flowering plant which is cultivated
in parks and these annuals are usually used for
decorative purpose. It starts blooming in early or
mid and in some varieties in late summer.
Environmental conditions affect the phonological
characters, composition, growth and development
of individual plant species (Younis et al., 2014a).
Whenever the environmental features exceed from
the optimum tolerance level of any plant species,
it brings the plant under stress, and it
adversely affects structural, developmental,
biochemical and physiological processes in plants
(Riaz et al., 2010).
Soil salinity and drought hindered plant
production round the world (Pill et al., 1991; Tanji,
2002; Nadeem et al., 2012). A total of 880 million
hectares of the global soils are salt-affected in
Pakistan, about 6.7 million hectares of soils are
salt-contaminated and of which 1.89 million
hectares are saline, 1.85 million hectares are
permeable saline-sodic, 1.39 million hectares are
impermeable saline-sodic while 0.028 million
hectares is acidic (Riaz et al., 2013). High salinity
levels affect all phases of plant growth and
development, forcing the plants to adapt a complex
regulatory network to survive under stress
conditions. The negative effects of stress on
growth, morphology, anatomy, ultra-structure and
metabolism were reported by different researchers
on different plant species (Shae et al., 2008; Riaz et
al., 2013). Among various abiotic stresses, NaCl
induced salinity is the major factor that hampers
the plant growth and development, decreases
germination and ultimately reduces plant
establishment and yield. Growth, yield and quality
reduction under saline conditions occurred due to
a decrease in the ability of plants to uptake water
from the soil solution and the destruction of soil
structure (Barret-Lennard, 2003).
Salts in soil can result in modifications of plant
metabolic processes, culminating in stunted
growth,
reducing
enzyme
activities
and
YOUNIS ET AL.
biochemical constituents (Muthukumarasamy and
Panneerselvam, 1997). Salinity leads to anatomical
modifications in plant body and make them
capable of minimizing the detrimental effects of
salt stress. The effect of salinity on anatomical
structure was discussed by Gadalla (2009)
and Younis et al. (2014c). The negative effect of
salinity on growth was reported by Hussein et al.
(2009), Abdel-Monem et al. (2010) and
Saffan (2008).
Most of the researches about salt stress were
carried out in food crops, but less in ornamental
plants. Therefore, it is the need of time to explore
ornamental plants that are tolerant to salt stress;
this will help landscape designers to select
resistant plants in their designs in saline areas.
Keeping in view the potential of plants to salt
tolerance, the present study was carried out to
assess the effect of salinity on the anatomy of
Gazania harlequin L., to check the response of the
plant cells and their tolerance level under salt
stress conditions.
and examined under microscope and consequently
microphotography was done. Double staining
dehydration procedure (safranin and fast green)
was used for the preparation of permanent slides
(Ruzin, 1999) to study various cells and tissues of
root and stem. Measurements and micrographs
were made using a digital camera (Nikon FDX-35)
equipped with a Nikon stereo-microscope (Nikon
104, Japan). The anatomical parameters observed
in this present study were: xylem area, phloem
area, cortex area, epidermis area within the stem
and root with a precision of μm2.
Statistical Analysis:
Statistical analysis was carried out by using
Fishers’ analysis of variance (ANOVA) techniques.
The mean values were compared with least
significance difference test (LSD) following Steel et
al. (1997).
RESULTS
It was noticed that salinity brings about adverse
effects on stem anatomy of Gazania. The statistical
analysis confirmed that with the increase in
salinity level, significant changes were noticed in
different anatomical characteristics of stem. Stem
area decreased consistently, but at the same time it
increased remarkably by the increment of NaCl
level. Xylem and phloem area of stem showed a
decreasing trend under salt stress condition
(Table 1) which indicates that with the increase in
salinity level there was noticeably decrease in the
xylem and phloem cell growth. Xylem area was
maximum under normal soil (control) and phloem
area was also at the highest level under normal soil
(control). The phloem area was not significantly
different in control, 25 mgl-1, 50 mgl-1 and
75 mgl-1 treatments. The lowest xylem and phloem
area of 21091.56 and 30558.00 µm2, respectively
was found at 100 mgl-1 NaCl. This indicates
that salinity induces structural changes in xylem
and
phloem
of
stems.
The
increasing
salinity reduces the stems vascular area while cell
thickness increased with salinity level compared
to control treatment (Fig. 1). Cortical cell
length and width also gradually reduced under
salinity and therefore, it decreased its cell
area (Fig. 1) and the significant results are shown
in Table 1.
Epidermis cell area of Gazania rapidly increased
by the induction of salt in the growing medium,
but in the present experiment, it gradually
decreased with further increase in salt
content (Table 1). Minimum stem epidermis
area of 39937.27, 23911.55 and 23494.84 μm2
were observed at 50 mgl-1, 75 mgl-1 and
100 mgl-1 NaCl respectively with no significance
difference, whereas control and 25 mgl-1
of NaCl were noticed with maximum stem
epidermis area.
MATERIALS AND METHODS
Experimental Site and Design:
A pot experiment was conducted in the green
house, University of Agriculture, Faisalabad,
Pakistan, in order to investigate the effects of
different salinity levels on possible anatomical
changes in Gazania. The experiment was laid out in
the completely randomized design (CRD) with four
replications.
Experiment Material and Imposition of Salinity
Stress in the Pots:
After one month of sowing the seedlings of
G. harlequin were transplanted in the pots (20 cm
diameter and 22 cm depth) having a mixture of silt
and leaf manure in the ratio of 1:1 as a growth
medium. These transplanted seedlings were kept
for 20 days to get settled before applying different
salinity levels (25, 50, 75, 100 mgl-1 of NaCl
solution). The experiment was comprised of
weighing the soil that was 1500 g (growth
medium) in each pot and the salinity levels
were developed artificially by adding the solution
of 25, 50, 75, and 100 mgl-1 NaCl salt along
with the control. The EC of garden soil
was determined as 2.5 dSm-1 and taken as control.
Data were collected after 90 days of
transplantation.
Anatomical Parameter:
Plants were removed from the soil, their shoots
and roots were separated. Root parts with length of
3 cm were cut and washed with distilled water to
remove soil dust and other contaminations. The
stem were prepared according to the method as
adopted by Johansen (1940). Briefly, stem were
dipped into 70 percent ethanol solution for 15 days
after that the sections were fixed in Canada balsam
9
AGRICULTURAL COMMUNICATIONS.
Table 1. Effect of different salinity levels on stem anatomy of Gazania harlequin.
Parameters
Treatment
Stem xylem area
(μm2)
Stem phloem area
(μm2)
Stem cortex area
(μm2)
Stem epidermis area
(μm2)
91199.2a†
177751.1a
369793.7a
142770.0a
NaCl
88234.8ab
163079.5a
358203.2ab
76216.5b
50 mgl-1 NaCl
42283.7bc
126144.7a
301063.7ab
39937.3c
30925.80c
112835.5a
210061.1bc
23911.5c
21091.56c
30558.0b
82472.2c
23494.8c
73783.1
149256.2
35368.9
Control
25
75
mgl-1
mgl-1
NaCl
100 mgl-1 NaCl
LSD Value
47181.1
† Means
with the same letter are not significantly different at P<0.05.
Fig. 1. Transverse section of stem of Gazania harlequin plant grown (A) in the absence of NaCl, (B) in presence of 25 mgl-1 NaCl, (C) in
presence of 50 mgl-1 NaCl, (D) in presence of 75 mgl-1 NaCl and (E) in presence of 100 mgl-1 NaCl.
10
YOUNIS ET AL.
and epidermis area of 925428.03 μm2,
1210745.2
μm2
and
347859.68
μm2,
536741.01 μm2, respectively while the minimum
xylem (227003.19 μm2), phloem (69318.95 μm2),
cortex (81182.52 μm2) and epidermis area
(75168.874 μm2) were observed in plants treated
with 100 mgl-1 Nacl. It was also clear that root
xylem, phloem, cortex and epidermis area
significantly decreased as compared to control
(Fig. 2). Results indicate that lower salinity doses
have a lower effect as compared to higher
concentrations on root anatomy of Gazania.
It was also clear from the figure that by
increasing salinity levels, there was a significant
decrease in the stem epidermis cell area (Fig. 1).
Mean values of treatment revealed that control
have higher cortex and epidermis cell area as
compared to other salt treatments.
Salinity showed a subtractive effect on root
anatomy of Gazania. The statistical data indicate
that with the increase in salinity level, there was a
significant decrease in root xylem, phloem, cortex
and epidermis area (Table 2). The mean values of
control have maximum root xylem phloem, cortex
Table 2. Effect of different salinity levels on root anatomy of Gazania harlequin.
Parameter
Treatment
Root xylem area
(μm2)
Root phloem area
(μm2)
Root cortex area
(μm2)
Root epidermis area
(μm2)
536741.0a
925428.1a†
347859.7a
1210745.2a
mgl-1NaCl
751500.5ab
275939.9ab
894623.9ab
516734.8a
50 mgl-1 NaCl
577491.2abc
107448.4bc
570961.4bc
369151.2ab
75 mgl-1 NaCl
100 mgl-1
NaCl
LSD value
368853.3bc
104051.8bc
314562.4c
210343.4bc
227003.2c
69319.0c
81182.5c
75168.9c
190187.0
571541.7
255597.5
Control
25
468039.0
† Means
with the same letter are not significantly different at P<0.05.
area of stem decreased due to a reduction in xylem
width and length. Salinity reduced both its phloem
area and sieve area at higher levels, and such
findings were correlated with less tolerant species
(Goncharova and Dobrenkova， 1981). Salinity
caused the gradual changes in plant internal
structure which reduces the xylem and the phloem
area (Hameed et al., 2010). Xylem vessels also
reduced under salt stress, as reported by Ling An et
al. (2002). These studies are in contrary to the
findings of Akram et al. (2002) and Hu et al. (2005)
who reported decreased meta xylem area and
cortical area, but there was no definite
response of cortical thickness and its cell area of
the stem.
Cortex area of root and stem was also
significantly decreased under high level of salinity.
Microscopic studies showed visual cell injury at
100 mgl-1 of NaCl in stem while the root cells injury
were observed at 50, 75 and 100 mgl-1 of NaCl. The
root cortex cells were injured as these cells
controlled the salt transport into root. In stem
cortex cells, 50 and 75 mgl-1 of NaCl showed no
injuries as the root cortex serves to reduce the
transport to the stem. These cell injuries reduced
the growth and area of cortex tissue in roots and
stem. These results are supported by Casenave et
al. (1999) findings, in which they observed smaller
cortex in cotton seedlings at high salinity level.
Walsh (1990) suggested that the thickness of
DISCUSSION
In the present study, anatomical changes in root
and stem of Gazania under different salinity levels
were studied. The results of this study revealed
that increasing the salinity level adversely affects
the cell growth. Plants growing under saline
conditions undergo different anatomical and
cytological changes (Winter, 1988; Huang and Van
Steveninck, 1990). These modifications are
different in organ to organ at different levels of
organization (Mills, 1989).
It is clear from above results that salinity
elevation in soil has contrary effects on xylem and
phloem area of the stem and root as their area
tended to decrease under salt stress condition. It
was due to the reduction of water uptake by the
plants under high saline conditions and this
reduction in water intake by the cells created
osmotic condition. Salinity affects plant growth
through osmotic effects and ion toxicity (Hampson
and Simpson, 1990). In ornamental plants, salinity
causes reduction in cell turgor and reduces the rate
of root and stem elongation (Fricke et al., 2006;
Younis et al., 2014b) and this results in reduction
of stem and root area. In saline conditions, reduced
xylem and phloem area of stem and roots was
earlier observed by Datta and Som (1973) and
Reinoso et al. (2004) in Prosopis strombulifera.
These results are in agreement with Nadia (1998),
Soha (2006) and Baum et al. (2000) that xylem
11
AGRICULTURAL COMMUNICATIONS.
cortical area increases up to a certain level, but
under severe condition it turns to decrease. So,
cortical cell area decreased at higher salinity levels,
as reported by Akram et al. (2002), but increased
cortical area under salt stress in the salt tolerant
species may be critical under physiological drought
for its better storage capacity (Baloch et al., 1998).
As salt level increased, root diameter of Gazania
decreased, as reported by De Villiers et al. (1995).
In 1999, a botanist, Degano, relates succulence in
root with the mechanisms of adaptation to saline
conditions. Thicker meta phloem area of root was
obtained under higher salinity levels which
indicated its better adaptation to high salinity
(Awasthi and Pathak, 1999). The less affected root
area in the salt tolerant species may be for their
better adaptation. These results of cortex match
with the findings of Akram et al. (2002) who
reported that cortical area of root decreased with
increase of salinity levels.
Fig. 2. Transverse section of root of Gazania harlequin plant (A) in the absence of NaCl, (B) in presence of 25 mgl-1 NaCl, (C) in
presence of 50 mgl-1 NaCl, (D) in presence of 75 mgl-1 NaCl and (E) in presence of 100 mgl-1 NaCl.
Salinity generally reduces epidermal cell area in
stem by reducing water uptake and induces
osmotic condition (Akram et al., 2002). Increasing
salt levels in roots caused reduction in epidermal
area due to cell injuries. Halophytic or salt tolerant
species generally possess thick epidermis and this
12
YOUNIS ET AL.
development. Increasing levels of salts in soil has a
negative impact on cell growth that it is expressed
as anatomical and cytological changes. Salts in the
root zone are responsible for the reduction of
water uptake by the plants roots and this reduction
in water intake by the cells creates osmotic
condition in roots as well as in the stem. Reduced
cell turgor and depressed rates caused by salt
stress in root and stem resulted in the elongation
of root and stem. Therefore, xylem, phloem, cortex
and epidermis area of root and stem showed a
decreasing trend with increasing salt stress
condition. Despite from osmotic effects induced by
salt stress the ion toxicity was also main obstacle in
cell growth, as it was resulted in cell injuries. From
the obtained results it is proved and clear that
Gazania is a fairly tolerant plant species to salt
stress and it can be recommended for the
landscaping of moderately saline soils.
serves as an effective mechanism against water
loss during limited moisture availability, but at
high salinity levels thickness of epidermis
decreased (Botti et al., 1998) however, in the salt
tolerant species, epidermis thickness greatly
increased, which showed its better adaptability
because thick epidermis is a specific character of
the salt tolerant species (Awasthi and Pathak,
1999). This characteristic is critical under limited
moisture availability as thick epidermis is capable
of checking water loss through stems (Nawaz et al.,
2006, 2012a,b; Kanwal et al., 2012). Curtis and
Lauchli (1987) observed that salt stress condition
reduced the epidermis cell width and length due to
that area of epidermal cell in the root of the plant.
CONCLUSION
In conclusion, it is clear that salt stress
conditions affect all aspects of plant growth and
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