American Journal of Plant Sciences, 2011, 2, 808-815
doi:10.4236/ajps.2011.26095 Published Online December 2011 (
Copyright © 2011 SciRes. AJPS
Physiological Responses of Tamarix ramosissima to
Extreme NaCl Concentrations
Jacob M. Carter1,2*, Jesse B. Nippert1,3
1Division of Biology, Kansas State University, Manhattan, USA; 2Department of Ecology and Evolutionary Biology, University of
Kansas, Lawrence, USA; 3Division of Biology, Kansas State University, Manhattan, USA.
Email: *,
Received July 21st, 2011; revised September 19th, 2011; accepted October 21st, 2011.
Hydrologic alterations of river systems in western North America over the past century have increased soil salinity,
contributing to the establishment and spread of an introduced halophytic species, Tamarix ramosissima (Ledeb.). The
physiological responses of Tamarix ramosissima to salinity stress are incompletely known. To assess the salinity toler-
ance of this species, we measured several whole plant and leaf-level physiological responses of Tamarix ramosissima
cuttings grown in a controlled environment over three NaCl concentrations (0, 15 and 40
·l–1). Tamarix ramosissima
photosynthesis (A2000), stomatal conductance to water (gs), water potential (Ψw), and the maximum quantum yield of
photosystem II (Fv/Fm) decreased at 15 and 40 g·l–1 NaCl compared to control treatments. However, after approxi-
mately 35 days, Tamarix ramosissima had increased photosynthetic rates, maximum quantum yield of photosystem II,
and stomatal conductance to water. These data suggests that physiological functioning of Tamarix ramosissima accli-
mated to extremely high NaCl concentrations over a relatively short period of time. Additionally, we present prelimi-
nary evidence that suggests proline synthesis may be the mechanism by which this species adjusts osmotically to in-
creasing salinity.
Keywords: Chlorophyll Fluorescence, Gas Exchange, Proline, Saltcedar, Salt Stress, Tamarisk
1. Introduction
Many adaptations have been hypothesized as mecha-
nisms facilitating the spread of the invasive, exotic tree
species, Tamarix ramosissima Ledeb., along disturbed ri-
parian corridors in western North America. These in-
clude high seed production, high growth rates [1], drought
tolerance [2], ability to resprout after fire [3] or grazing,
and the facultative phreatophytic nature of the species [4].
In western North America, riparian soils are naturally
saline from low annual precipitation, but salinization has
been exacerbated by river flow regulation, groundwater
pumping, and river channel changes that decrease the
frequency of overbank flooding [5-7]. The halophytic
nature of the species is also commonly hypothesized as a
primary factor contributing to the spread and establish-
ment of Tamarix ramosissima [8-11].
Although salinity adversely affects the production and
growth of most species, halophytes are adapted to toler-
ate highly saline environments. One mechanism to toler-
ate high salinities is to regulate Na transport to shoots
and leaves [12,13]. Salts can be excluded from leaves by
selective uptake by root cells, although it is unclear
which cell types control this selectivity [14]. Some ha-
lophytic species have specialized salt glands or salt
bladders that exude salt from the plant via apoplastic path-
ways [15,16]. Additionally, compartmentalization and
the synthesis of compatible solutes are also important
salt tolerating mechanisms. Many halophytes compart-
mentalize Na+ in cell vacuoles to limit toxicity in the
cytoplasm [14,17-19]. Compartmentalization of Na+ dis-
rupts the osmotic balance in cells between the vacuole
and cytoplasm. Plants may synthesize compatible solutes
(e.g., proline, glycine betaine) in the cytoplasm to rees-
tablish osmotic balance. These low-molecular-mass com-
pounds do not interfere with normal biochemical reac-
tions [20]. However, compatible solutes are energetically
expensive, requiring as much as 52 ATP per mol for
synthesis [21].
Tamarix ramosissima has various salinity tolerance
mechanisms. Most notably, Tamarix ramosissima deve-
lops salt glands that secrete excess salts that would be
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations809
accumulated by non salt-tolerant species [22]. Salt is
excreted in solution through specialized salt glands via
an apoplastic pathway to alleviate metabolic stress caused
by Na+ [23]. Tamarix ramosissima also accumulates
compatible solutes during periods of salinity stress. Stu-
dies conducted along the Tarim River, China [24,25] and
the Yellow River, China [26] suggest Tamarix ramosis-
sima accumulates compatible solutes (proline and solu-
ble sugars) during salinity stress to maintain internal os-
motic balance. Solomon et al. [27] also showed that
Tamarix jordanis Boiss. synthesizes N-methyl-L-proline
(MP) and N-methyl-trans-4-hydroxy-L-proline (MHP) in
the presence of high NaCl content. Both solutes are ef-
fective at maintaining the carboxylating activity of Rubi-
Although Tamarix ramosissima has salt-tolerating me-
chanisms, physiological responses of Tamarix ramosis-
sima to salinity stress are incompletely known and few
studies have reported how increasing salinity impacts
these responses. Kleinkopf and Wallace [11] reported
increased salt concentrations had a marginal effect on the
net exchange rates of carbon and water in Tamarix ra-
mosissima. Kleinkopf and Wallace [11] also measured a
decrease in Tamarix ramosissima growth as salinity in-
creased, which they attributed to the increased energy
required for pumping salts from leaf glands. Glenn et al.
[8] grew a mix of shrubs and trees, including Tamarix
ramosissima, in a greenhouse and subjected plants to a
salinity gradient from 0 to 32 g·l–1 NaCl. Tamarix ramo-
sissima transpiration decreased markedly between 16 and
32 g·l–1 NaCl, but growth rate showed only a minor re-
duction (2%).
To address this gap in our understanding of the phy-
siological responses of Tamarix ramosissima to soil sa-
linity, we measured several whole plant and leaf-level
physiological responses of cuttings grown at three NaCl
concentrations in a controlled environment. Using these
results, we address the effects of the NaCl concentrations
tested (0, 15 and 40 g·l–1) in reducing gas exchange rates,
leaf water potentials, and chlorophyll fluorescence.
2. Materials and Methods
2.1. Experimental Design and Procedures
Branch tip cuttings of Tamarix ramosissima were col-
lected from trees growing at two sites: the Ashland Re-
search Site (ARS) adjacent to the Cimarron River near
Ashland, Kansas, USA (37˚11'N and 99˚46'W) and the
Cedar Bluff Reservoir (CBR) near Ellis, Kansas, USA
(38˚48'N and 99˚43'W). Cuttings were kept moist, cut at
the stem base (approximately 0.6 cm in diameter) and
auxin was applied to promote root development. Cuttings
were propagated in a Conviron (Pembina, North Dakota,
USA) growth chamber at Kansas State University (Man-
hattan, Kansas, USA) in plastic nursery pots (19.3 cm
diameter, 17.8 cm deep). Prior to transplanting cuttings
to pots, soils were soaked in a nutrient solution made up
of 20% nitrogen 20% phosphoric acid, 20% soluble pot-
ash, 0.02% boron, 0.05% chelated copper, 0.15% che-
lated iron, 0.05% chelated manganese, 0.0009% molyb-
denum, and 0.05% chelated zinc. Pots contained 550 g of
a mixture of potting soil and native soil (1:1 v/v). Native
soils were collected from both the Ashland research site
and Cedar Bluffs Reservoir. Controlled environment con-
ditions were set on a 12-hour photoperiod.
NaCl was added to distilled water to make solutions of
0, 15, and 40 g·l–1 NaCl. Salinity trials were initiated by
irrigating pots with 400 ml of NaCl solution over a four
day period (100 ml per day) to reduce salinity shock on
the cuttings. Physiological responses were measured bi-
weekly on each cutting, after the total solution was added.
Measurements continued until all plants within the 40
g·l–1 treatment were dead, which varied between 65 - 75
days. A total of 48 cuttings were used in the experiment.
The control treatment contained 12 cuttings, whereas the
15 and 40 g·l–1 treatments contained 18 cuttings each.
Tamarix ramosissima cuttings collected from both sites
were assigned to treatments at random.
2.2. Plant Physiology
Gas exchange measurements were taken using a Licor-
6400 infra-red gas analyzer with a red/blue light source
and a CO2 injector (Licor Inc., Lincoln, Nebraska, USA).
Irradiance inside the cuvette was 2000 µmol·m–2·s–1, CO2
concentration was 400 ppm and the relative humidity
was maintained at ambient. Measurements reported in-
clude photosynthetic rate at 2000 µmol·m–2·s–1 (A2000),
stomatal conductance to water vapor (gs), and intercellu-
lar CO2 concentration (Ci). Projected leaf area within the
gas exchange cuvette was estimated using a Licor 3100
leaf area meter. Water potentials were measured using a
Scholander pressure bomb (PMS Instruments, Albany,
Oregon, USA) and the maximum quantum yield of pho-
tosystem II (Fv/Fm) was measured using a chlorophyll
fluorometer (Walz Instruments, Germany). The last bi-
weekly measurements before death were analyzed for
each cutting using a mixed-effects model ANOVA in
SAS 9.1. (Cary, North Carolina, USA). NaCl concentra-
tion was treated as a fixed effect in the model whereas
date of sampling was considered a random effect to ac-
count for repeated measures in the experimental design.
2.3. Stable Isotope Analysis
On each sampling date, approximately 1g of leaf sample
was collected from each cutting. Each sample was dried
for 48 hours at 60˚C. Samples were ground with liquid
Copyright © 2011 SciRes. AJPS
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations
nitrogen and then analyzed for their stable carbon iso-
topic signature (δ13C) using a Finnigan Delta-plus con-
tinuous flow isotope ratio mass spectrometer connected
to an elemental analyzer. Within run precision was <0.04‰
for δ13C, while between run variation was <0.12‰ for δ13C.
2.4. Proline Determination
Free proline was determined spectrophotometrically fol-
lowing methods from Bates et al. [28]. A standard curve
was generated using L-Proline. Approximately 0.5 g of
plant material was homogenized in 10 ml of 3% sul-
fosalicylic acid. The homogenate was filtered through
Whatman #2 filter paper and then reacted with 2 ml
acid-ninhydrin and 2 ml of glacial acetic acid for 1 hour
at 100˚C in a test tube. The reaction was stopped by
placing test tubes in an ice water bath and then mixing
vigorously with toluene. The chromophore containing
toluene was separated and absorbance read at 520 nm
using toluene as a blank. To react at least 0.5 g of plant
material with 3% sulfosalicylic acid required us to use all
leaf tissues from all samples per salinity treatment by
sampling date.
3. Results
Leaf-level gas exchange measurements suggest Tamarix
ramosissima physiological functioning varied as a func-
tion of salinity (Figure 1). Photosynthetic rates ranged
from 0.2 to 37 µmol CO2 m
–2·s–1 among all treatments.
Photosynthesis declined by 50% between control and the
40 g·l–1 NaCl treatment, but did not vary significantly by
salinity treatment (p = 0.30, Figure 1(a)). Stomatal con-
ductance to water vapor ranged from 0.01 to 0.48 mol
H2O m–2·s–1 among treatments. Stomatal conductance
values significantly declined nearly 75% from 0 g·l–1
NaCl concentration to 40 g·l–1 NaCl concentration (p <
0.05; Figure 1(b)). Leaf-level stomatal conductance and
photosynthetic rates were lower at the 15 g·l–1 NaCl con-
centration compared to the control, but did not vary sig-
nificantly (Figures 1(a), (b)).
Decreases in the maximum quantum yield of photo-
system II (Fv/Fm) suggest Tamarix ramosissima meta-
bolic functioning significantly declined as salinity in-
creased from 15 to 40 g·l–1 NaCl (p < 0.05; Figure 1(c)).
Mean maximum quantum yield of photosystem II for the
40 g·l–1 treatment was 0.76 ± 0.015, whereas mean maxi-
mum quantum yield of photosystem II for control plants
was 0.81 ± 0.007. The maximum quantum yield of pho-
tosystem II ranged from 0.59 to 0.84. Ψw varied signifi-
cantly as salinity increased (p < 0.001; Figure 1(d)). Ψw
ranged from –0.3 to –4.0 among treatments. Mean Ψw
values were nearly two times lower in 40 g·l–1 NaCl
treatments compared to controls. Neither above-ground
nor below-ground biomass were significantly affected by
salinity concentrations tested (p > 0.05; Figures 1(e), (f)).
Leaf δ13C significantly varied as salinity increased (p <
0.05; Figure 1(g)). Leaf δ13C was most enriched in 40
g·l–1 NaCl concentration and the most depleted in control
treatments. δ13C values ranged from –28.1 to –36.9 among
Tamarix ramosissima physiological functioning accli-
mated to salinity over time (Figure 2). Photosynthetic
rates declined immediately after initial NaCl additions,
but began to increase after approximately 35 days (Fig-
ure 2(a)). However, of the 3 treatments, Tamarix ramo-
sissima cuttings in the 40 g·l–1 NaCl treatment consis-
tently exhibited lower photosynthesis, stomatal conduc-
tance to water, maximum quantum yield of photosystem
II, and the highest proline concentrations compared to
the 0 and 15 g·l–1 NaCl treatments (Figure 2). All plants
subjected to the 40 g·l–1 NaCl concentration treatment died
between 60 - 75 days after induction of the treatment.
4. Discussion
The salt tolerance of Tamarix ramosissima is likely one
mechanism by which this species persists and expands its
range in western North America compared to native ri-
parian species [29-32]. Increasing salinity is known to
cause physiological stress in most species [19,33,34], but
few studies have examined the physiological responses
of Tamarix ramosissima to salinity [8,11]. Our results
are consistent with Glenn et al. [8], suggesting that Ta-
marix ramosissima leaf-level physiological responses
decrease at extremely high NaCl concentrations. Our
results also show short term acclimation to both high
salinity treatments, however, growth in extreme salt con-
centrations (40 g·l–1) eventually resulted in death regard-
less of an acclimation response.
Previous work has shown that salinity imparts both
ionic and osmotic stress [18,19]; our results suggest Ta-
marix ramosissima was impacted by both at high Sali-
nity. Osmotic stress had the greatest impact on Tamarix
ramosissima individuals. High NaCl concentration re-
duced stomatal conductance and Ψw (Figures 1(b), (d)).
Ψw is highly sensitive to saline soils such that reduced
water availability can be a dominant factor determining
plant responses to stress [35,36]. Even low-level salt ex-
posure can impact plant-water relations [37,38]. It is dif-
ficult to partition alterations in physiological functioning
to water stress or salt-specific effects, as these changes
can be co-dependent over time. After minutes to hours,
growth rates and physiological responses instantaneously
decline as salinity concentrations increase. Typically
there is a partial recovery after initial declines, but growth
rates and physiological functioning still remain low when
under salt stress [14,18,19]. These quick declines also
occur in plants where KCl, mannitol, or polyethylene
Copyright © 2011 SciRes. AJPS
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations
Copyright © 2011 SciRes. AJPS
Figure 1. Tamarix ramosissima mean (±1 SE) (a) photosynthetic rate at 2000 µmol m2·s1 (Aat 2000), (b) stomatal conductance
to water vapor (gs), (c) the maximum quantum yield of photosystem II (Fv/Fm), (d) water potential (Ψw), (e) above-ground
and (f) below-ground biomass, and (g) δ13C among three NaCl concentrations.
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations
Figure 2. Tamarix ramosissima (a) photosynthetic rate at 2000 µmol m–2·s–1 (Aat2000), (b) maximum quantum yield of photo-
system II (Fv/Fm), (c) stomatal conductance to water vapor (gs), and (d) proline concentration over time across three NaCl
concentrations (closed circles = 0 g·l–1 [NaCl], opened circles = 15 g·l–1 [NaCl], closed triangles = 40 g·l–1 [NaCl]).
glycol (PEG) have been added, suggesting these re-
sponses are not solely salt-specific [20,39].
In the present study, Tamarix ramosissima plants sub-
jected to 40 g·l–1 NaCl showed marked physiological
declines after 14 days (Figure 2). Declines in the maxi-
mum quantum yield of photosystem II, photosynthesis,
and stomatal conductance were consistent after 28 days.
However, these parameters increased after 40 days. Cor-
responding to these increases, free proline concentration
also increased in all treatments after 28 days. An increase
in free proline concentration is an indicator of water
stress [28,40,41]. It is possible that Tamarix ramosissima
was able to maintain physiological functioning, including
water status, by accumulating proline. Similar results
have been shown for Tamarix jordanis [27]. It is also
important to note that our high salinity treatment (40 g·l–1
or 40,000 ppm NaCl) constitutes an extreme salinity end-
point. Tamarix ramosissima was able to acclimate to this
extreme salinity over ~35 days. The highest documented
soil salinity reported for Tamarix ramosissima in the US
is approximately 20,000 ppm in the delta of the Colorado
River where the species gives way to obligate halophytes
such as Distichlis palmeri (Vasey) Fassett ex I.M. Johnst.
[42]. The ability to acclimate to extreme salinities could
provide a competitive advantage for Tamarix ramosis-
sima over native glycophytes.
Proline accumulation is not the only tolerance strategy
that halophytic species may utilize to maintain osmotic
balance. Guard cells may be triggered to close around
stomatal pores to conserve water when under osmotic
stress [43,44]. The integrated stomatal behavior of leaves
is commonly inferred by measuring the δ13C stable iso-
topic signature as an estimate of water use efficiency
[45]. Our results suggest high salinity reduces stomatal
aperture in Tamarix ramosissima. Values of leaf δ13C
were, on average, heaviest in 40 g·l–1 treatments sug-
gesting greatest stomatal regulation compared to 0 and
15 g·l–1 NaCl treatments. Similarly, our gas exchange
data show reduced stomatal conductance at 40 g·l–1 NaCl.
In controlled outdoor experiments Tamarix ramosissima
Copyright © 2011 SciRes. AJPS
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations813
maintains high leaf stomatal conductance when under
water or salt stress [9,46-48].
The overall objective of this study was to assess whole
plant and leaf-level physiological responses of Tamarix
ramosissima to extreme NaCl concentrations. Previous
results suggested that Tamarix ramosissima maintained
physiological functioning in the field from 0 to 14 g·l–1
NaCl [47]. In this study, Tamarix ramosissima had de-
creased gas exchange, maximum quantum yield of pho-
tosystem II, and Ψw at 15 and 40 g·l–1 NaCl, compared to
the control. Physiological functioning changed over time
as salinity stress was induced, suggesting short-term ac-
climation. Results from this study suggest that NaCl
concentrations of 15 g·l–1 or higher impact Tamarix
ramosissima physiological functioning, but physiological
responses may acclimate over time, even at extremely
high salinities. Long-term physiological acclimation to
high salinities by this species will require further as-
5. Acknowledgements
We would like to thank the anonymous reviewers whose
comments improved this manuscript. We would also like
to thank Dave Arnold and Cedar Bluffs State Park for
allowing us to collect cuttings from their land. We also
thank the following people who contributed to this work:
John Blair, Brian Maricle, Jeff Hartman, Sally Tucker,
Gracie Orozco, Teall Culbertson, and Kristen Polacik.
We acknowledge support from NSF DGE-0841414 and
the Kansas State University GK-12 program, the Divi-
sion of Biology at Kansas State University, and the Kon-
za Prairie Long-Term Ecological Research program.
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