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Effects of High Salinity on Physiological and Anatomical Indices in the Early

Stages of Populus euphratica Growth

Article  in  Russian Journal of Plant Physiology · February 2015

DOI: 10.1134/S1021443715020168

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ISSN 10214437, Russian Journal of Plant Physiology, 2015, Vol. 62, No. 2, pp. 229–236. © Pleiades Publishing, Ltd., 2015.

RESEARCH PAPERS

Effects of High Salinity on Physiological and Anatomical Indices

in the Early Stages of Populus euphratica Growth1
V. D. Rajputa, b, Y. Chena, and M. Ayupa
a
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences,
Urumqi, China
b University of Chinese Academy of Sciences, Beijing, China

email: chenyn@ms.xjb.ac.cn
Received June 3, 2014

Abstract—The effects of salinity stress on stomatal aperture and density, xylem vessels, the activities of anti
oxidant enzymes, such as superoxide dismutase (SOD) and peroxidase (POD), and xylem embolism
(PLC values) in Populus euphratica in the arid ecosystem of China. Pot experiment was conducted at different
concentrations of salt (50, 100, 150, and 200 mM NaCl) contained in the irrigation water used for 3 months
The POD activity increased with the increase in the severity of NaCl stress, but SOD activity was varied at
different levels of salt. Results indicated that salt treatment reduced stomatal aperture and leaf photosynthetic
capacity. However, the significant reduction in the stomatal area, in the length of stomata openings and an
increase in stomata density were noticed. Salinity stress affected water transport, which reduced native
PLC value, whereas xylem vessel area was also decreased. Presented results open the possibility of genetic
improvement for selecting the high salttolerant of Populus spp.to reclaim salinized lands.
Keywords: Populus euphratica, PLC value, salinity, POD, SOD, xylem anatomy

DOI: 10.1134/S1021443715020168

1
INTRODUCTION
The Tarim River and the Heihe River are two most
important and largest inland rivers in Western China.
Their downstream areas are known as a green corridor
covered with lush riparian forests several miles wide.
World’s 54% area of Populus euphratica vegetation is
spread in this basin [1] and mainly distributed on river
banks or areas with deep water tables [2]. Salinity is
one of the major abiotic stresses limiting plant growth
and productivity, particularly in arid land. Researchers
showed that salinity caused several anatomical and
physiological modifications in plants viz. changes in
tracheary element density, lumen area, vessels diame
ter [3–5], stomatal density, shape, and size [6], plant
growth and activities of antioxidant enzymes [7–9].
The effect of abiotic stress on hydraulic traits in ripar
ian plants is highly correlated with plant anatomy viz.
fibers, pith membrane [10, 11]. Vessels of halophytic
trees are more numerous and narrower than those in
mesophytic ones.
Plants protect themselves from ROSinduced oxi
dative damage through both enzymatic and nonenzy
matic defense mechanisms [12], including the activa
1 This text was submitted by the authors in English.
Abbreviations: POD—peroxidase; SOD—superoxide dismutase.
tion of antioxidant enzymes, such as superoxide dis
mutase (SOD) and peroxidase (POD) [7–9]. The
degree of oxidative stress experienced by the cell is
determined by the levels of superoxide, H2O2, and
hydroxyl radicals generated. The antioxidant activities
are crucial for suppressing toxic ROS levels within
cells [13]. SOD and POD have been considered as two
key enzymes in ROS elimination [14]. The estimation
of antioxidants is necessary to know the adaptability of
P. euphratica under salinity stress conditions.
Plants adjust their xylem hydraulic traits under var
ious stress conditions through developing more resis
tant xylem to droughtinduced cavitation [15], reduc
ing root hydraulic conductance [16], maintaining the
high hydraulic efficiency in stems and roots [17], and
also by increasing whole plant leaf specific conductiv
ity [18] and changes in the xylem sap. Hydraulic con
ductivity and embolism are the important factors con
straining plant survival and its productivity. These fac
tors are correlated with the xylem structure and
functions [19].
Various studies have been made to understand the
variations in xylem anatomical structures and hydraulic
functions at the interspecific, intraspecific and intra
plant level [20]. According to Zwieniecki et al. [21], the
ionic content of the xylem sap has a significant effect on
the hydraulic conductivity of plants. The hydraulic

229
230 RAJPUT et al.
stress adaptation of P. euphratica involves cell wall mod
ifications and suppresses xylem development [22].
Many researchers performed their study in hydroponics
and controlled conditions. There are hardly any reports
about physiological and anatomical effects of salinity in
early stage of P. euphratica life under under natural con
ditions.
Therefore, it is important to further understand
the salinity effect on P. euphratica especially on sto
matal aperture, xylem state and their relation with to
hydraulic conductivity and antioxidants. Present
study deals with the effects of salinity stress on xylem
vessels, antioxidant enzyme activities, stomatal aper
ture and hydraulic conductivity (PLC %) at early
stage of P. euphratica growth to gain more informa
tion for assessing its capacity to adapt to high saline
environment.
MATERIALS AND METHODS
Plant source and maintenance. Oneyearold
P. euphratica seedlings have been selected from nurs
ery located at downstream of Tarim River (41.68° N,
86.06° E), Xinjiang Uygur Autonomous Region,
Northwest China. The average height of seedlings
above the soil was 60 ± 2.68 cm. There were no leaves
on seedlings at a time of planting. Plants were planted
into pots containing grey desert soils (organic matter
6.26 ± 1.56 g/kg, total nitrogen 0.11 ± 0.04 g/kg, phos
phorous 0.17 ± 0.07 g/kg, potassium 21.18 ± 0.19 g/kg,
and total salts 4.73 ± 0.05 mg/g, the pH and electrical
conductivity of soils were 7.8 and 0.93 (mS/cm),
respectively) for experimentation at research station
situated at Urumqi, Xinjiang, China (43.46° N,
87.36° E). Each pot contains 23.48 ± 0.17 kg soil on
dry weight basis. Pots were immediately irrigated with
tap water and seedlings sprouted within a month and
well survived in 45 days. Thereafter, well survived
plants were treated with NaCl with the irrigation
water. After three months of salt water irrigation of
plants, soils were analyzed and salt accumulations
were calculated. Salt concentrations were increased
due to the accumulation of NaCl from 4.73 (0 mM) to
59.88 mg/g (200 mM).
Salt treatment. Saline treatment was imposed with
1 L of tap water with 50, 100, 150, and 200 mM con
centrations of NaCl once in a week for three months.
We irrigated control plants with 1 L of water contain
ing no salt. Each treatment was performed in 10 repli
cates. Experimental pots were kept in natural condi
tions facing low precipitation.
Sample collection. Samples were collected after
three months of salt treatments along with control
ones and immediately transported in the laboratory for
analysis. Healthy leaves were collected for the observa
tion of stomatal aperture (density, area, and size) and
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
antioxidant enzyme activities (SOD, POD), whereas
stems of similar diameter were collected for anatomi
cal and hydraulic trait measurements.
Measurement of stomatal aperture. Fresh leaf sam
ples were obtained and prepared for scanning electron
microscopy (SEM) to observe stomatal aperture. Leaf
samples were recut into 5−10 mm length segments,
kept in increasing order of ethanol (50, 70, 90, and
100%) for 30 min each for dehydration and airdried
for 12 h at room temperature. Sample segments were
fixed to aluminum stubs with electron conductive car
bon cement (“Neubauer Chemikalien”, Germany),
and stomatal aperture and density were observed by
SEM. Ten images were obtained from different sites of
each sample. Images from SEM were processed by
ImageJ software and the observation of stomatal den
sity was performed by circling 1 mm2 area.
Anatomical measurements. Cross sections were
obtained from P. euphratica stems 5.50–6.50 mm in
diameterand immediately fixed in a FAA solution con
sisting of formalin, acetic acid, and ethanol (5 : 5 : 90,
v/v/v). Samples were immediately dehydrated with
alcohol for better slices and paraffin section method
was used for making theses sections [23]. Thin cross
sections (7–9 µm) were cut by slide microtome, dou
blestained with 1% safranin and 1% fast green dye,
and observed under a light Olympus, BX51 microscope
(Olympus, Japan) equipped with a digital camera
(Olympus UTV0.5XC3). Images were analyzed by
ImageJ software. We mainly focused on the vessel area
in this context. The average of vessel area was calcu
lated on the basis of 50 vessels for each treatment.
Extraction and assay of antioxidant enzymes.
Leaves were harvested, quickly frozen in liquid nitro
gen, and further stored at −80°C until assays of anti
oxidant enzyme activities. For enzyme extraction
and assays, 0.20 g of leaves were frozen in liquid
nitrogen and then ground with a mortar and pestle in
4 mL of the solution containing 50 mM phosphate
buffer (pH 7.0), 1% (w/v) polyvinylpyrrolidone
(PVP) under low temperature maintained by icetray
and centrifuged at 15 000 rpm for 15 min at 4°C, and
the supernatant was collected for enzyme assays
[24].The activity of SOD (EC 1.15.1.1) was mea
sured as described by Giannopolities and Ries [25].
The assay medium contained 50 mM phosphate
buffer (pH 7.8), 13 mM methionine, 75 µM pnitro
blue tetrazolium chloride (NBT), 1.30 mM ribofla
vin, 0.10 mM EDTANa, and 100 mL of the enzyme
extract. Riboflavin was added last, the test tubes were
placed in the reaction chamber with fluorescent light
(4000 lx), and the reaction was terminated after one
minute by turning off the light. The absorbance was
read at 560 nm. A nonirradiated reaction mixture,
which was covered with foil and did not develop
color, served as control. The reaction mixture lacking
Vol. 62 No. 2 2015
 EFFECTS OF HIGH SALINITY ON PHYSIOLOGICAL AND ANATOMICAL INDICES
20 µm
(а) (b)
20 µm
(d) (e)
Fig. 1. Effect of NaCl on stomatal density (circled area, 62500 µm2).
(a) 0 mM; (b) 50 mM; (c) 100 mM; (d) 150 mM; (e) 200 mM.
enzyme developed maximum color as a result of
maximum reduction of NBT. One unit of enzyme
activity was determined as the amount of the enzyme
to reach an inhibition of 50% NBT reduction rate.
The activity of POD (EC 1.11.1.7) was determined
by the oxidation of guaiacol in the presence of H2O2.
The assay medium contained 2.30 mL of 50 mM
sodium phosphate buffer (pH 6.5), 0.30 mL of
200 mM guaiacol, 0.30 mL of 2% H2O2, and 0.10 mL
of the sample in a total volume of 3.0 mL. Testtube
were stirred well, kept in the 34°C water bath for
1 min, and the absorbance was read at 470 nm.
Five measurements were done after 30s intervals.
Blanks were used as a control [26].
Hydraulic trait analysis. Native PLC% and hydrau
lic conductivity were measured from 3–5cmlong
and 5.50–6.50 mm in diameter of P. euphratica stem
by using XYL’EM, a xylem embolism meter
(Bronkhorst, Montignylescormeilles, France) fol
lowing Sperry and Tyree [27]. Fresh stem samples
were collected, kept under distilled water. and covered
by black plastic bags. Samples were processed in labo
ratory to recut under water with a sharp razor blade
from both ends and immediately inserted to the
hydraulic apparatus filled with double distilled water.
Samples were flushed at high pressure (at 150–
180 kPa) and maximum conductivity (Kmax, kg/MPa)
was measured. Specific conductivity was calculated as
Ks = k (kg/(s MPa)) × segment length (m)/segment
surface area (m2). Finally, native PLC% value in the
form of percentage loss of hydraulic conductivity was
calculated as PLC = 100(1 – Ks(init)/Ks(max)).
Analysis of data. Statistical analyses were per
formed by using IBM SPSS Statistics 22. A compari
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
231
20 µm 30 µm
(c)
20 µm
son of treatment was done by oneway ANOVA. Cor
relations were considered significant at P ≤ 0.05.
RESULTS
After three months of weekly NaCl treatments with
irrigation water, we collected samples for laboratory
observation. Results showed that the number of leaves
decreased relative to control treatment, also the diam
eter of stem increased slightly under stress conditions.
Salinity affected anatomical and morphological char
acters alongwith physiological parameters.
Effect of Salinity on Stomatal Aperture
The analysis revealed that stomatal density, area,
and size of stomata opening were highly affected by
different salt concentrations. The area of stomata
reduced with the increase of salinity up to the concen
tration of 100 mM, whereas it increased at 150 and
200 mM of NaCl relative to 100 mM; however, it was
less than control (0 mM) (Figs. 1, 2, 3a). Stomatal
aperture area were 327.70 ± 21.75, 238.51 ± 12.71,
205.83 ± 25.30, 233.69 ± 13.53, and 242.93 ±
24.80 µm2 for treatments at 0, 50, 100, 150, and
200 mM NaCl, respectively. The density of stomata
kept increasing up to 150 mM and suddenly decreased
at 200 mM of salt (Figs. 1, 3b). The stomatal density
was enhanced from 35 ± 3.67 (0 mM) to the maximum
of 49.72 ± 5.13 (150 mM) per mm2 of area. The results
showed that salinity also affected the length of stomatal
opening. It decreased from 29.03 ± 3.10 (0 mM) to the
minimum of 16.89 ± 2.12 µm (150 mM) (Figs. 2, 3c).
Although the stomatal density was increased however,
Vol. 62 No. 2 2015
232 RAJPUT et al.
1 µm
(а) (b)
1 µm
(d) (e)
Fig. 2. Effect of NaCl on stomata and on its openness.
(a) 0 mM; (b) 50 mM; (c) 100 mM; (d) 150 mM; (e) 200 mM.
the area of stomata shrunk significantly but did not
qualify the significant test (P > 0.05).
Effect of Salinity on Xylem Anatomy
The effect of salinity on the vessel section area in
the early stage of P. euphratica growth (Figs. 4, 5) was
only slight and insignificant (P > 0.05) at 0, 50, 100,
150, and 200 mM NaCl treatments; The values were
2258.50 ± 55.83, 1911.52 ± 62.75, 2030.30 ± 77.78,
1879.38 ± 63.17, and 2063.22 ± 54.73 µm2, respectively.
The reason for such slight reduction of vessel section
area may be a shortterm exposure to NaCl.
Effect of Salinity on Antioxidants
POD activity increased with the increase in the
concentration of NaCl (Fig. 6a). The values were
118.35 ± 3.12 (0 mM), 142.66 ± 2.30 (50 mM),
172.15 ± 1.65 (100 mM), 161.29 ± 3.54 (150 mM),
and 191.44 ± 3.82 (200 mM) U/(g min). SOD activ
ity increased with the increase in the salinity level rel
ative to control treatment; however, it was followed by
some reduction at 200 mM of NaCl (Fig. 6b). SOD
activity was increased from 1333.59 ± 25.68 (0 mM)
to 1453.87 ± 10.35 (150 mM) U/g.
Effect of Salt on Xylem Native Embolism
The mean PLC values of the stem xylem in P. euph
ratica under 0, 50, 100, 150, and 200 mM NaCl treat
ments were 33.80 ± 0.40, 47.74 ± 3.79, 48.70 ± 1.12,
49.32 ± 2.15, and 53.56 ± 4.77 in percentage, respec
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
1 µm 1 µm
(c)
2 µm
tively (Fig. 7). PLC value observed was 159% at
200 mM NaCl as compared to control (0 mM). Dif
ferences were insignificant (P > 0.05).
DISCUSSION
Salinity is one of the most important factors limiting
plant growth and yield. Previous studies have shown
that salinity affects plant physiology as well as anatomy.
In our experiments three months of enhanced salinity
resulted in increased stomatal density at 50, 100, and
150 mM NaCl, whereas at 200 mM salt concentration
it decreased in comparison with other salt treatments,
the area of stomata was declined as well. Salinity also
affected the length of stomata openings, it decreased in
salttreated plants to reduce evaporation. Similar results
were also found by Abbruzzese et al. [6] and Meloni et
al. [7]. According to Fichot et al. [20] the vessel diame
ter and hydraulic conductivity were correlated posi
tively with stomatal conductance.
The xylem anatomy is optimized to ensure a con
tinuous transport of water from roots to leaves. A gen
eral decrease in the cell size and an important rise in
the vessel density were observed by Fichot et al. [20]
under water deficit condition, also which seemed to be
common to salinity stress [3, 4]. Salt concentration
affected vessel section area of P. euphratica irrigated by
different doses of saline water for three months,
slightly decreasing it relative to control plants. Variable
concentration of salts and nature of plants demon
strated variable response of wood anatomy. Junghans
et al. [3] observed that salinity reduced vessel diameter
Vol. 62 No. 2 2015
 EFFECTS OF HIGH SALINITY ON PHYSIOLOGICAL AND ANATOMICAL INDICES 233

400 (a)

350

Stomatal area, µm2

300

250

200

150
0 50 100 150 200
NaCl concentration, mM
60 (b)
Stomatal density, number/mm2

50

40

30

20
0 50 100 150 200
NaCl concentration, mM
40 (c)
Length of stomatal openness, µm

30

20

10

0
0 50 100 150 200
NaCl concentration, mM

Fig. 3. Effect of NaCl on (a) stomatal area (µm2); (b) stomatal density (number of stomata per mm2); (c) length of stomatal
openings (µm).

in saltsensitive plants after exposure to much lower
salt concentration than in saltresistant plants,
whereas the high salt concentration (150 mM) showed
the higher reduction of cambial activity in P. euphrat
ica, which was reflected in the lower number of xylem
cells formed under salt stress and significantly reduced
vessel diameters. We observed similar trends: the vessel
section area reduced up to 150 mM salt, whereas at
200 mM there was no such respond. Similar finding
were found by EscalantePérez et al. [4]: xylem differ

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 62 No. 2 2015

234 RAJPUT et al.

100 µm 100 µm 100 µm

(a) (b) (c)

(d) 100 µm (e) 100 µm

Fig. 4. Effect of NaCl on P. euphratica xylem anatomy. Changes in vessel number and area are seen.
(a) 0 mM; (b) 50; (c) 100 mM; (d) 150 mM; (e) 200 mM.

entiation zone and lumina were reduced under high
salt conditions.
Antioxidants play a key role in reducing salinity
effects on plants survivability. The balance between
ROS and antioxidant ability is important for plants to
overcome various stresses [28]. Mechanisms of sus
taining the balance existed in all plants are activities of
such enzymes as SOD, POD, and others [29]. Accord
ing to Hishida et al. [8] and Ediga et al. [9] activities of
antioxidant enzymes were increased under salinity
stress. Our experiment showed that POD activity
increased with increasing rate of salt concentration at
3000
2500
Vessel area, µm2
all levels. SOD activity showed variable results at dif
ferent concentration of salt (50, 100, and 150 mM): it
increased as compare to control, whereas SOD activ
ity was less at 200 mM level as compared to 150 mM.
Similar activities were observed at different levels of
canopy in P. euphratica, the activities of POD declined
from the lower to the upper canopy, while the activity
of SOD increased [30].
Native embolism rate of P. euphratica xylem was
affected by salinity: the PLC values in stem were neg
atively affected from 33.80 ± 0.40 in 0 mM to 53.56 ±
4.77 in 200 mM salt. Salinity reduced hydraulic con
ductivity up to 54%. Decreasing vessel section area
and increasing wood density reduce hydraulic vulner
ability plant to cavitation and contribute to continue
water transport [4]. It was reported that salt stress
caused a general reduction (40–80%) in root hydrau

2000
lic conductivity. Comparing the mean PLC data of all
treatment groups, PLC values increased from 50 to
1500 200 mM salt treatment.
Above results and discussion showed salinity toler
1000 ance capacity of P. euphratica in arid ecosystem; we cal
culated the accumulation of sodium chloride in pots
500 containing grey desert soil. The accumulated salts
increased the concentration of NaCl in pots, which may
0 increase the threshold level of resistance of P. euphratica
0 50 100 150 200
NaCl concentration, mM more than 200 mM NaCl. Plants treated with 200 mM
salt for three months showed toxic effect on leaves. Due
to threshold level, the rates of leaf shedding were
Fig. 5. Effect of NaCl on vessel section area (µm2). increased in comparison to new leaf formation.

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 62 No. 2 2015

 EFFECTS OF HIGH SALINITY ON PHYSIOLOGICAL AND ANATOMICAL INDICES 235

250 (a) control evaporation because changes in stomatal area

has a direct effect on transpiration. PLC value showed
POD activity, U/(g min)

200 the effect on water transport, whereas vessels, which

are major components for plant water supply, also were
affected by salinity. The increase of antioxidant
150 showed tolerance capacity of P. euphratica under stress
conditions. Salt stress induced antioxidant enzyme
100 activity, which is directly correlated with stress toler
ance. This result makes the possibility of genetic
50 improvement by selecting high salt tolerant P. spp. to
reclaim salinized lands. Longterm salinity experi
0 ment in field condition will provide better information
0 50 100 150 200 for changes in wood anatomy, relation with hydraulic
NaCl concentration, mM conductivity.
1500 (b)
ACKNOWLEDGMENTS
1450
SOD activity, U/g

This research was supported by the National Natural

Science Foundation of China (grant no. 91025025),
1400
State Key Laboratory of Desert and Oasis Ecology, Xin
jiang Institute of Ecology and Geography, Chinese
1350 Academy of Sciences, Urumqi 830011, China.
1300
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