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Combined effects of salinity and phosphorus


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nutrient status of Catapodium rigidum

Article in Arid Land Research and Management · February 2018


DOI: 10.1080/15324982.2018.1427640

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Arid Land Research and Management

ISSN: 1532-4982 (Print) 1532-4990 (Online) Journal homepage: http://www.tandfonline.com/loi/uasr20

Combined effects of salinity and phosphorus


availability on growth, gas exchange, and nutrient
status of Catapodium rigidum

Ons Talbi Zribi, Ines Slama, Najla Trabelsi, Abdelwahed Hamdi, Abderrazak
Smaoui & Chedly Abdelly

To cite this article: Ons Talbi Zribi, Ines Slama, Najla Trabelsi, Abdelwahed Hamdi, Abderrazak
Smaoui & Chedly Abdelly (2018): Combined effects of salinity and phosphorus availability on
growth, gas exchange, and nutrient status of Catapodium rigidum, Arid Land Research and
Management, DOI: 10.1080/15324982.2018.1427640

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ARID LAND RESEARCH AND MANAGEMENT
https://doi.org/10.1080/15324982.2018.1427640

none defined

Combined effects of salinity and phosphorus availability on


growth, gas exchange, and nutrient status of Catapodium
rigidum
Ons Talbi Zribia, Ines Slamaa, Najla Trabelsib, Abdelwahed Hamdia, Abderrazak Smaouia,
and Chedly Abdellya
a
Laboratory of Extremophile Plants, Center of Biotechnology of Borj Cédria, Tunisia; bLaboratory of Olive
Biotechnology, Center of Biotechnology of Borj Cédria, Tunisia

ABSTRACT ARTICLE HISTORY


The combined effects of NaCl-salinity and phosphorus deficiency on Received 23 June 2017
biomass production, nutritional status, and photosynthetic activity Accepted 10 January 2018
were studied in Catapodium rigidum: an annual Poacea with fodder KEYWORDS
potential. Plants were grown in hydroponic conditions for 55 days Catapodium rigidum;
under two phosphorus (P) supply: 5 (low) or 180 µmol KH2PO4 phosphorus deficiency;
(sufficient), in the absence or presence of 100 mM NaCl. Obtained photosynthesis; salinity
results demonstrated that both salinity and P deficiency treatments
applied separately reduced substantially plant growth and CO2
assimilation rate with a more marked impact of salt stress. Salinity
has no substantial effect on both shoot P concentrations and
phosphorus acquisition efficiency independently of P availability.
The highest decrease in plant growth (−91%) was observed in plants
simultaneously submitted to both stresses suggesting an
additive effect of the two stresses and that P deficiency increased
the susceptibility of C. rigidum to salinity. This may be linked to a
significant decrease in potassium acquisition (−95%), K/Na selectivity
ratio (−73%), stomatal conductance (−66%), CO2 assimilation rate
(−64%), and shoot water content (66%). Furthermore, plants cultivated
under combined salinity and sufficient P supply displayed higher
stomatal conductance, CO2 assimilation rate, K/Na selectivity ratio, and
plant growth than plants cultivated under combined effects of salinity
and P deficiency. These results suggest that adding P to saline soils
could be an alternative for alleviating the negative effects of salinity
and may ameliorate salinity tolerance.

Introduction
Salinity and phosphorus (P) deficiency are two major abiotic stresses that impose serious
limitation on plant production and pasture development worldwide (Chaves, Flexas, and
Pinheiro 2009; Shen et al. 2011).
Salinity generally affects plants in two main ways. First, the presence of salt in the soil
solution decreases the capacity of roots to extract water. This is referred as the
osmotic effect of salinity. Second, high concentrations of salts within the plant can be toxic,

CONTACT Ons Talbi Zribi onstalbi_zribi@yahoo.fr Laboratoire des Plantes Extrêmophiles, Centre de Biotechnologie
de Borj Cédria, BP 901,Hammam-Lif 2050, Tunisie.
Ines Slama and Najla Trabelsi contributed equally to this work.
© 2018 Taylor & Francis
2 O. T. ZRIBI ET AL.

resulting in an inhibition of many physiological and biochemical processes such as nutrient


uptake and assimilation (Munns and Tester 2008; Parihar et al. 2015).
Phosphorus deficiency induces also a wide array of metabolic effects that limit plant
growth. Plants have evolved sophisticated developmental and metabolic adaptations to
conserve P and to maximize its acquisition from the rhizosphere in P limiting media
(Vance, Uhde-Stone, and Allan 2003; Veneklaas et al. 2012). Such adaptations include
remodeling of root system architecture (Lynch 2011), increased production and
secretion of hydrolytic enzymes such as phosphatases, phytases, and ribonucleases
(Talbi Zribi et al. 2014; Secco et al. 2017), exudation of protons and organic acids
(Hinsinger 2001) and effective mobilization of phosphorus within the plant from
mature plant parts to actively growing tissue (Van de Wiel, der Linden, and
Scholten 2016).
While the individual effects of salinity and P deficiency have been widely studied and are
well described in the literature, information about the physiological behavior of plants to
the combined effects of salinity and P shortage is still scarce. Furthermore, there is no
consensus about the relationships between these two stresses (Grattan and Grieve 1999;
Talbi Zribi et al. 2015). However, plants are often subjected to the combined effects of these
two constraints mainly in calcareous salt-affected soils characterized by high pH and low
P solubility (Naidu and Rengasamy 1993, Clark and Baligar 2000).
According to Rizhsky et al. (2004), plants subjected to a mixture of stresses activate a
particular and unique stress response which is not always additive. Indeed, the stress
combinations may have negative as well as positive effects on plants (Pandey et al. 2017).
Catapodium rigidum (L.) C.E. Hubb. (Poacea) is an annual facultative halophyte with
fodder potential. The study of its behavior in a wide range of salinity demonstrates its
ability to preserve its growth potential up to 300 mM NaCl (Barhoumi 2007). According
to Böcük and Türe (2014), this species shows resistance to boron toxicity. Nevertheless,
data related to its physiological responses to salt-P deficiency mixed stress are unknown.
Thus, in this study, we investigate the effect of phosphorus deficiency and/or salinity on
C. rigidum growth, nutrition status and photosynthetic activity.
We hypothesize that the combined effects of the two constraints may be additive on the
above-mentioned parameters and that the combined treatment will decease shoot water
content, phosphorus and potassium acquisition efficiencies, Kþ/Naþ selectivity ratio and
photosynthetic activity (CO2 assimilation rate, stomatal conductance, and chlorophyll
content) in C. rigidum plants. We hypothesize also that increasing P supply will increase
plant growth under saline conditions.

Materials and methods


Plant material and treatments
Seeds of C. rigidum (harvested at Soliman Sebkha) were germinated in Petri dishes with
moistened filter paper. At day 5, the germinated seeds were transferred to 5 L-pots filled
with a 10-fold-modified Hewitt’s nutrient solution (pH 6.0) for 30 days (Hewitt 1966).
Arnon and Hoagland 1940; Jacobson 1951. Phosphorus (added as KH2PO4) concentration
was adjusted to 5 µM. After this pretreatment period, a first harvest was made and four
treatments were imposed: C=Control (180 µM KH2PO4 and 0 mM NaCl), D ¼ P deficiency
treatment (5 µM KH2PO4 and 0 mM NaCl), C þ S ¼ salt treatment (180 µM KH2PO4 and
ARID LAND RESEARCH AND MANAGEMENT 3

100 mM NaCl), and D þ S ¼ combined treatment (5 µM KH2PO4 and 100 mM NaCl). The
choice of P concentrations was based on another experiment demonstrating that
C. rigidum reached its maximum growth at 180 µMP and that 5 µM P provoked clear P
shortage symptoms (Talbi-Zribi et al. 2017a).
The study was conducted in a glasshouse under controlled conditions with a day/night
temperatures of 24°C /16°C, a 14 h photoperiod and 70–75% relative humidity). The
nutrient solution was continuously aerated and changed once a week.
Plants were harvested 55 days after the initiation of treatment. Plants were separated
into shoots, roots, and ears. The fresh weight (FW) was directly determined after the
harvest whereas the dry weight (DW) was determined after oven drying for 72 h at 65°C.

Water status
Shoot water content (WC) was determined according to the following equation
WC (m L g−1 DW) ¼ (FW−DW)/DW.

Nutrient extraction and analysis


Sodium and potassium were analyzed using flame spectrophotometry (Corning 410, UK)
after extraction of the finely grounded dry matter in a mixture of nitric and perchloric acids
4/1 (v/v), Cl− content was measured by a chloridometer (Haake Buchler), and phosphorus
was determined by the nitro-vanado-molybdate method (Fleury and Leclerc 1943).

Chlorophyll determination and gas exchange measurements


Leaf chlorophyll concentrations were determined in 80% acetone extract of approximately
100 mg of fresh young leaves according to Lichtenthaler and Welburn (1983).
Gas exchange parameters (CO2 net assimilation rate, transpiration rate, and stomatal
conductance) were measured at the final harvest. Measurements were conducted between
10:00 and 13:00 on young fully expanded leaves using a portable infrared gas analyzer
system (LCA4) (Bio-Scientific, Great Amwell, Herts, UK).
During gas exchange measurements, the photosynthetically active radiation (PAR) was
about 1250 µmol mm−2 s−1 � 349, the leaf temperature was 29 � 2°C and the ambient
CO2 concentration was 380 µmol mol−1. Data were automatically recorded after the
photosynthesis rate was stabilized.

Calculated parameters
. Phosphorus acquisition efficiency (PAE) designates the capability of roots to absorb
P from the soil solution. It is calculated as follows: PAE (µmol P, mg−1 root DW) ¼
(Q2 − Q1)/[(R2 − R1)/(ln R2 −ln R1)] (Talbi Zribi et al. 2014); Q is the amount of P
absorbed throughout the experiment and R is the mean root biomass. The subscripts
1 and 2 refer to initial and final harvests, respectively.
. Phosphorus use efficiency (PUE) is estimated as the ratio of plant biomass (mg) to its P
content (µmol).
. The K/Na selectivity ratio was estimated using the ratio Kþ/(Kþ þNaþ) of the ions
quantities (mM) of C. rigidum shoots. (Talbi Zribi et al., 2011).
4 O. T. ZRIBI ET AL.

Statistical analysis
The experimental design was factorial. Statistical analyses were performed with
STATISTICA 5.0. A Duncan test was performed to test any significant difference between
treatments at P < 0.05. Values were the means of four replicate plants.

Results
Growth
The effects of P level (P), salinity (S), and their interaction (P * S) on parameters describing
plant growth, gas exchanges, water relations, and nutrition status in C. rigidum plants are
summarized in Table 1. A two-way ANOVA indicated significant effects of the interaction
between salinity and P level for all dependent variables studied except for root DW, water
use efficiency (WUE), shoot P content, and phosphorus acquisition efficiency (PAE)
(Table 1).
Phosphorus deficiency and salinity significantly decreased whole plant DW by 65 and
76%, respectively, compared to the control (Figure 1). A significant reduction in whole
plant biomass (−91%) was observed when the two stresses are applied at the same time.
Shoot biomass decreased by approximately 79% under both P deficiency and salt
treatments (Figure 2A). As for whole plant biomass, the highest reduction in shoot biomass
(−94%) was observed when both stresses are combined.
Root biomass was not significantly affected by P deficiency treatment. Nevertheless,
salinity applied only or combined with P deficiency significantly reduced root biomass
by approximately 83%. (Figure 2B).
Phosphorus shortage (D) reduced both leaf and tiller number by 49 and 42% (Table 2).
C þ S treatment decreased these parameters by 75 and 53%, respectively. The more severe

Table 1. Results of a two-way analysis of variance of the effect of P level (P), salinity (S) and their inter-
action (P*S) on parameters describing plant growth, gas exchanges, water relations, and nutrition status
in Catapodium rigidum plants.
Parameter Phosphorus (P) Salinity (S) P*S
Whole plant DW (g) 161.74*** 260.47*** 61.53***
Shoot DW (g) 21.88*** 258.95*** 15.38***
Root DW (g) 1.28ns 55.84*** 0.25ns
Leaf number 23.6** 48.40*** 10.48*
Tiller number 45.29*** 73.85*** 1.08*
Leaf area (cm2) 40.67*** 77.65*** 33.00***
Shoot length (cm) 8.01* 24.86** 6.42*
A (µmol CO2 m−2 s−1) 86.87*** 371.77*** 6.99*
gs (m mol m−2 s−1) 242.41*** 2516.06*** 19.032**
WUE (µmol mmol−1) 19.04** 40.81*** 2.40ns
Shoot water content (ml/g- DW) 29.81*** 18.68** 6.88*
Chlorophyll (a þ b) (mg/g FW) 156.62*** 59.63*** 38.47***
Shoot P (µmol/g DW) 292.8*** 11.35* 0.32ns
PAE (µmol P. mg−1 root DW) 301.62*** 2.96ns 0.26ns
PUE (mg DW µmol−1) 160.30*** 37.16*** 11.77*
Shoot Kþ (µmol/g DW) 31.58*** 171.04*** 4.89*
Whole plant Kþ quantity (µmol) 1493.21*** 1722.58*** 653.99***
Shoot Naþ (µmol/g DW) 27.89*** 96.70*** 19.26**
Soot Cl− (µmol/g DW) 7.84* 82.08*** 10.49**
KAE (µmol g−1 DW) 632.47*** 134.04*** 35.67***
Kþ/(Kþ þNaþ) 53.83*** 211.89*** 4.60*
***
Numbers represent F-values: P < 0.0001; **P < 0.001; *P < 0.05; nsnonsignificant.
ARID LAND RESEARCH AND MANAGEMENT 5

Figure 1. Whole plant biomass. The plants were harvested after 55 days of treatment in a control
nutrient solution (C), containing only 5 µM P (D), with 100 mM NaCl (C þ S), or under combined effects
of salinity and P deficiency (D þ S). Means followed by the same letters are not significantly different at
5% according to the Duncan’s test.

reduction in these parameters was observed when the two stresses are applied at the same
time. The total leaf surface area decreased by 65, 89%, and 97% in D, C þ S, and D þ S
treatments, respectively, compared to the control (Table 2). This latter parameter was much
more reduced than the leaf number, showing a significant reduction of the single leaf
surface area in all treated plants.

Gas exchange and water content


Control plants exhibited the highest values of net photosynthetic rate, stomatal conduc-
tance, chlorophyll content, shoot water content and water use efficiency (A/E) (Table 3).
P deficiency significantly decreased CO2 assimilation rate and stomatal conductance by
21 and 22%, respectively. However, salinity (C þ S treatment) decreased these parameters
by 48 and 52%, respectively. The effects of the two stresses combined were additive. Indeed,
the highest decrease in CO2 assimilation rate and stomatal conductance (−65%) was
observed in plants simultaneously submitted to both constraints. Water use efficiency
calculated as A (photosynthetic rate)/E (transpiration rate) decreased by 12, 22, and 41%
under D, C þ S, and D þ S treatments, respectively. Chlorophyll (a þ b) content
diminished by 45% under salt stress and by approximately 65% under both P deficiency
treatments with and without salt.

Nutrient status
Phosphorus
P shortage decreased shoot P concentrations by 74%. Contrarily to our hypothesis, salinity
has no substantial impact on shoot P concentrations (Table 4). The reduction in shoot P
concentrations was linked with a decline in phosphorus acquisition efficiency in P deficient
plants. Furthermore, salinity has no significant effect on phosphorus acquisition efficiency
(PAE) independently of phosphorus supply. Nevertheless, salinity decreased the quantity of
6 O. T. ZRIBI ET AL.

Figure 2. Biomass of shoots (A) and roots (B). The plants were harvested after 55 days of treatment
in a control nutrient solution (C), containing only 5 µM P (D), with 100 mM NaCl (C þ S), or under
combined effects of salinity and P deficiency (D þ S). Means followed by the same letters are not
significantly different at 5% according to the Duncan’s test.

Table 2. Effect of P availability, salinity, and their combination on leaf number, tiller number, shoot
length and leaf area in C. rigidum plants grown in a control nutrient solution (C), containing only
5 µM P (D), with 100 mM NaCl and 180 µM KH2PO4 (C þ S), or under combined effects of salinity and
P deficiency (D þ S). Means followed by the same letters are not significantly different at 5% according
to the Duncan’s test.
Variable C D C þS D þS
Leaf number 141 � 42a 71 � 9b 34 � 8c 13 � 6c
Tiller number 26 � 6a 15 � 1b 12 � 1b 3.6 � 1c
Shoot length (cm) 19 � 2a 17 � 2a 14 � 2a 9.5 � 1b
Leaf area (cm2) 250 � 53a 86 � 18b 27 � 4c 7 � 3d

biomass produced by unit of absorbed P (phosphorus use efficiency) by 38% when


combined with a low P supply (D þ S plants) and it has no significant effect on PUE
when combined with a sufficient P supply (C þ S plants).

Potassium
Shoot potassium concentrations decreased by 11, 42, and 71% under P deficiency, salinity,
and combined treatments, respectively, compared to the control (Figure 3A). Both salinity
ARID LAND RESEARCH AND MANAGEMENT 7

Table 3. Effect of P availability, salinity, and their combination on photosynthetic rate (A), stomatal
conductance (gs), water use efficiency (WUE, given as A⁄E), shoot water content and leaf chlorophyll con-
tent (Chl) in C. rigidum plants grown in a control nutrient solution (C), containing only 5 µM P (D), with
100 mM NaCl and 180 µM KH2PO4 (C þ S), or under combined effects of salinity and P deficiency (D þ S).
Means followed by the same letters are not significantly different at 5% according to the Duncan’s test.
Variable C D C þS D þS
A (µmol CO2 m−2 s−1) 6.4 � 0.6a 5.0 � 0.6b 3.3 � 0.2c 2.3 � 0.4d
gs (mmol−2 s−1) 270.2 � 9a 208.4 � 43b 128 � 7c 90.1 � 3.2d
WUE (µmol mmol−1) 11.73 � 0.9a 10.32 � 1.6ab 9.10 � 1.2b 6.91 � 0.6c
Shoot water content (ml/g DW) 7.28 � 1.15a 4.31 � 0.12 bc 4.87 � 1.16b 2.48 � 0.17c
Chl (a þ b) (mg/ g FW) 3.34 � 0.3a 1.07 � 0.2c 1.82 � 0.3b 1.24 � 0.3bc
Water use efficiency (WUE) was calculated as A (photosynthetic rate)⁄E (transpiration rate).

Table 4. Effect of P availability, salinity, and their combination on shoot P concentrations, P acquisition
(PAE) and use (PUE) efficiency in C. rigidum plants grown in a control nutrient solution (C), containing
only 5 µM P (D), with 100 mM NaCl and 180 µM KH2PO4 (C þ S), or under combined effects of salinity
and P deficiency (D þ S). Means followed by the same letters are not significantly different at 5% accord-
ing to the Duncan’s test.
Variable C D C þS D þS
Shoot P (µmol g−1 DW) 239 � 28a 61 � 11b 249 � 50a 89 � 25b
PAE (µmol P. mg−1 root DW) 11.11 � 1.1a 1.25 � 0.1b 13.03 � 2.4a 1.98 � 0.2b
PUE (mg DW. µmol−1) 4.06 � 0.1c 12.59 � 0.9a 2.71 � 0.12c 7.72 � 1.3b

and P deficiency treatments restricted potassium uptake as estimated by the whole plant
Kþ amount (Figure 3B). The highest diminution in whole plant Kþ amount was observed
when the two stresses are applied at the same time (−97%). This reduction was associated
with a decline in potassium absorption efficiency in all stressed plants and notably in D þ S
plants (Table 5).

Sodium and chloride


As expected, plants subjected to salt stress accumulated significantly higher shoot Naþ
(Figure 4A) and Cl− concentrations than plants cultivated in the absence of 100 mM NaCl
(Figure 4B). Moreover, plants simultaneously submitted to both constraints exhibited
lower shoot Naþ concentration and conversely higher shoot Cl− concentrations as com-
pared to plants cultivated under salt stress only.
Furthermore, when applied individually, P deficiency and salinity decreased Kþ/Naþ
ratio by 19 and 41%, respectively (Table 5). The highest reduction in Kþ/Naþ ratio
(−73%) was observed in plants simultaneously submitted to both constraints.

Discussion
In this study, we investigate the physiological response of C. rigidum plants to the
combined effects of salinity and phosphorus availability. Our findings showed that both
salinity and phosphorus deficiency treatments applied separately reduced considerably
whole plant growth with a more marked impact of salt stress. As expected, the
highest decrease in whole plant biomass was observed when the two stresses are applied
at the same time. This is likely linked to the severe reduction in shoot potassium content,
Kþ/Naþ selectivity ratio, shoot water content, photosynthetic activities and mainly
potassium acquisition (Figure 5). Indeed, potassium is an essential nutrient that
8 O. T. ZRIBI ET AL.

Figure 3. Shoot Kþ concentrations (A) and whole plant Kþ amount (B) in C. Rigidum plants grown in a
control nutrient solution (C), containing only 5 µM P (D), with 100 mM NaCl (C þ S), or under combined
effects of salinity and P deficiency (D þ S). Means followed by the same letters are not significantly
different at 5% according to the Duncan’s test.

Table 5. Effect of P availability, salinity, and their combination on potassium acquisition efficiency
(KAE) and Kþ/(Kþ þNaþ) ratio in C. rigidum plants grown in a control nutrient solution (C), containing
only 5 µM P (D), with 100 mM NaCl and 180 µM KH2PO4 (C þ S), or under combined effects of salinity
and P deficiency (D þ S). Means followed by the same letters are not significantly different at 5% accord-
ing to the Duncan’s test. Potassium acquisition efficiency is calculated by rationing the amount of Kþ
taken up during the experiment to the mean root biomass.
Variable C D C þS D þS
KAE (µmol g−1 DW) 78.1a 15.5c 43.1b 4.0d
Kþ/(Kþ þNaþ) 0.82a 0.66b 0.48c 0.22d

accomplishes important functions in plants such as photosynthesis, stomatal regulation,


osmoregulation, water uptake, cell elongation, cell membrane stability, and detoxification
of reactive oxygen species (Hafsi et al., 2014). Our results are in accord with those of
Rabhi et al. (2007) who showed that Medicago ciliaris L. growth was more affected by
the combined treatment than by iron deficiency or the salt treatment. However, our
findings contrasted with the response of Hordeum maritimum With., for which salt
exposure might partly alleviate the negative effects of P deficiency on the plant growth
(Talbi Zribi et al. 2012).
ARID LAND RESEARCH AND MANAGEMENT 9

Figure 4. Shoot Naþ (A) and Cl− (B) concentrations in C. rigidum plants grown in a control nutrient
solution (C), containing only 5 µM P (D), with 100 mM NaCl (C þ S), or under combined effects of salinity
and P deficiency (D þ S). Means followed by the same letters are not significantly different at 5%
according to the Duncan’s test.

Literature documenting the combined effects of salinity and P deficiency suggest that
this interaction is very dependent on the plant species, plant developmental stage, the com-
position and level of salinity as well as the P concentration in the substrate (Grattan and
Grieve 1999). In the present study, we showed that plant response to the combined stresses
is also organ dependent. Indeed D þ S plants exhibited root growth that was similar to that
of plants grown under the more severe stress (salt stress). These findings are similar to
those of Van der Ploe, Bohm, and Kirkham (1999) who demonstrated that when plants
are simultaneously submitted to salinity and nutrient deficiency stresses, growth is
controlled by the most growth-limiting factor. However, in shoots, the more severe
reduction in biomass was observed in D þ S plants. Similar results were observed in barley
plants cultivated simultaneously under combined effects of salinity and waterlogging (Zeng
et al. 2013).
The greatest reduction in whole plant biomass of D þ S plants could be partly attributed
to a considerable decrease in both shoot growth and CO2 assimilation rate. Indeed,
our results indicate that the plant growth may be controlled by its photosynthetic perfor-
mance since CO2 net assimilation rate correlated significantly with whole plant biomass
(Figure 6a). Furthermore, a high correlation was found between net photosynthetic rate
and both stomatal conductance (Figure 6b) and shoot water content (Figure 6c) suggesting
10 O. T. ZRIBI ET AL.

Figure 5. Graph showing relationship between treatments and parameters in growth reduction of
C. rigidum plants cultivated under P deficiency, salinity, and combined salinity and P deficiency.

Figure 6. Relationships between CO2 assimilation rate and dry matter production (A), stomatal
conductance (B) and leaf water content (C) in C. rigidum plants grown in a control nutrient solution
(C), containing only 5 µM P (D), with 100 mM NaCl (C þ S), or under combined effects of salinity and
P deficiency (D þ S).

that the reduction in growth in C. rigidum plants under various treatments was highly
linked to the decrease in leaf gas exchange parameters, which are known to be highly
dependent on the water status (Figure 5). Stomatal closure led to a decrease in photosyn-
thetic activity by limiting the CO2 entry into leaves (Chaves, Flexas, and Pinheiro 2009). A
similar relationship between net photosynthetic rate and both DW and gs has also been
reported in many other species. However, Gorai et al. 2010 and Talbi Zribi et al.
(2017b) did not found a correlation between growth and photosynthetic activity in
Phragmites australis (Cav.) Trin. ex. Steud. and Aeluropus littoralis Parl. Plants, respectively.
ARID LAND RESEARCH AND MANAGEMENT 11

In this experiment, the decrease in CO2 net assimilation rate under P deficiency and/ or
salt stress could be due mainly to lowered gs, while non stomatal limitation such as
mesophyll resistance might have also occurred in leaves under stressful conditions.
Furthermore, the reduction in leaf chlorophyll content under D, D þ S, and C þ S treat-
ments also suggested that metabolic inhibition of photosynthesis had occurred under these
conditions. Similar findings are observed in H. maritimum and wheat plants cultivated
respectively under P deficiency and salt conditions (Talbi Zribi et al. 2012; Kiani-Pouya
and Rasouli 2014). Nevertheless, recently we found that both P shortage and salt stresses
applied individually or combined increase leaf chlorophyll content in A. littoralis plants.
The decrease in chlorophyll content may be due to a reduction in synthesis and/or an
increase of chlorophyll degradation, and to chlorophyllase activity stimulation (Santos
2004).
Our findings demonstrated also that shoot water content was similarly reduced by both
P deficiency and salt stress. However, the greatest reduction in shoot water content was
observed when plants are subjected to both stresses simultaneously. Furthermore, D þ S
plants exhibited the lowest value of water use efficiency which suggests that osmotic
adjustment is not efficient in C. rigidum plants cultivated under combined effects of salinity
and P deficiency. This trend was associated with a low accumulation of Naþ and Kþ in
shoots of D þ S plants suggesting the involvement of these solutes in osmotic adjustment.
In the present study, we found that both salinity and P deficiency treatments applied
individually have significant reducing effect on shoot Kþ concentrations. The greatest
reductions in shoot Kþ concentrations were observed when plants are simultaneously sub-
mitted to both constraints. These results are not in accord with our findings in H. mariti-
mum plants where we found that when both constraints are applied simultaneously, the
effects on leaf Kþ concentrations were less harmful than when each constraint was applied
individually. The reduction in Kþ concentration caused by salinity might be related to the
competition between sodium and potassium ions which cause an increase in the uptake of
Naþ at the cost of Kþ (Munns and Tester 2008). Furthermore, at the whole plant level,
P deficiency and salinity, applied separately, similarly decreased the whole plant Kþ
quantity. Thus, our findings suggest that both constraints affected Kþ transport systems.
It is interesting to note that the larger decrease in shoot Kþ concentration in C. rigidum
plants simultaneously submitted to both stresses was linked with the more severe
reduction of growth and shoot water content (Figures 3 and 5) which suggests that the
observed restriction in Kþ uptake in plants cultivated simultaneously under salinity and
P deficiency stresses was the consequence of some harmful effect of the osmotic stress
on plants.
Furthermore, the severe growth reduction in C. rigidum plants submitted to combined
effects of salinity and P deficiency could be related also to the lower Kþ/(Kþ þNaþ) ratio in
D þ S plants (Table 5). Indeed, Chen et al. (2007) pointed out that Kþ/Naþ ratio is a
reliable parameter for screening salt-tolerant genotypes.
Our results showed also that, contrary to our hypothesis, salinity has no significant
effect on both shoot P concentrations and phosphorus acquisition efficiency (PAE)
independently of P availability. Literature data regarding the interaction between salt stress
and phosphorus status in plants are contradictory. In most cases, salinity diminishes the P
concentration in plant tissues (Kaya et al., 2001; Bybordi and Ebrahimian 2011), but the
results of several studies showed that salinity either increased or had no substantial effect
12 O. T. ZRIBI ET AL.

on P acquisition depending on the plant species and growing conditions (Grattan and
Grieve 1999; Talbi Zribi et al. 2015).
Furthermore, in this study, we showed that salinity, combined with a low P supply,
decreased the quantity of biomass produced per unit of absorbed P. These results
contrasted with our results in cultivated barley where we found that salinity has no
significant effect on PUE independently of P availability (Talbi Zribi et al. 2014).
Finally, in reclamation approaches of salinized land, it was reported that crop yield can be
improved through P fertilization (Naheed, Shahbaz, and Akram 2008). In this study, as
expected, we showed that plants cultivated under combined salinity and sufficient P supply
displayed higher Kþ/Naþ selectivity ratio, stomatal conductance, CO2 assimilation rate and
plant growth than plants cultivated simultaneously under salinity and P deficiency treat-
ments. These findings are in accord with those of Kaya, Kirnak, and Higgs (2001) who
demonstrated that supplementary P can reduce the adverse effects of salinity on plant growth
and physiological development of spinach plants. It is suggested that phosphorus plays a role
in osmotic adjustment, possibly explaining the beneficial role of additional P under saline
conditions (Treeby and Van Steveninck 1988). However, Naheed, Shahbaz, and Akram
(2008) showed that increasing soil phosphorus concentration could not improve the adverse
effects of salinity on rice in terms of growth and gas exchange characteristics.

Conclusion
Our results indicate that P deficiency increased the susceptibility of C. rigidum to salinity,
as indicated by the large decrease in leaf expansion and shoot growth. This effect was
induced by the substantial reduction in potassium acquisition, K/Na ratio, stomatal
conductance, CO2 assimilation rate, and shoot water content. Furthermore, in this
experiment, it appears that phosphorus supply has a beneficial effect on C. rigidum growth
under saline conditions. Thus, adding P to saline soil could be an alternative for alleviating
the negative effects of salinity and may ameliorate salinity tolerance.

Funding
This research was supported by the Tunisian Ministry of Higher Education and Scientific Research
(LR10CBBC02).

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