Does water salinity affect pepper plant response to nitrogen fertigation?

Agricultural Water Management 191 (2017) 57–66

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Does water salinity affect pepper plant response to nitrogen fertigation? Hagai Yasuor a,∗,1 , Guy Tamir a,2 , Avraham Stein a,d , Shabtai Cohen b , Asher Bar-Tal c , Alon Ben-Gal a , Uri Yermiyahu a,1 a

Gilat Research Center, Agriculture Research Organization, Israel Central-and Northern-Arava Research and Development, Israel c Institute of Soil, Water and Environmental Sciences, Agriculture Research Organization, Israel d The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel b

a r t i c l e

i n f o

Article history: Received 6 April 2017 Received in revised form 28 May 2017 Accepted 30 May 2017 Keywords: Chloride Nitrate Nitrogen uptake Mineral distribution Mineral nutrition

a b s t r a c t Recent increase in demand for agricultural products combined with scarcity of fresh water has motivated increased use of non-conventional water sources for irrigation. Application of water varying in quality dictates adjustment of nitrogen (N) management. The response of bell pepper to a range of different concentrations of N and salinity (NaCl) was evaluated in soilless and field experiments under greenhouse conditions. Pepper plant biomass and yield increased with N and decreased with salinity. Chloride accumulated mainly in the stems and the fraction of Cl in leaves increased as a function of increased exposure to salinity. Increasing N application resulted in reduced Cl uptake and accumulation in pepper organs, including leaves and petioles. Although N significantly reduced Cl content and concentration in leaves and petioles it did not compensate for the negative effects of increasing salinity. This indicates that salinity itself and not Cl − N competition was the limiting factor affecting growth and yield. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Recent increase in demand for agricultural products, combined with scarcity of fresh water has provided incentive for utilization of non-conventional water sources for irrigation (Yeo, 1999). Irrigation managers can alternatively utilize water containing high concentrations of salts (Beltrán, 1999) or desalinated water devoid of dissolved minerals (Yermiyahu et al., 2007). Both extremes are most likely to occur in water-scarce arid and semi-arid regions and both require specific management. Irrigation with water high in salts requires an increase in the irrigation volume in order to reduce the salt concentration from the active root zone (Ben-Gal et al., 2009). Desalinated water, whether used directly or incidentally, requires consideration of return of minerals that may otherwise not have needed to be fertilized (Yermiyahu et al., 2007).

∗ Corresponding author: Hagai Yasuor, Department of Vegetable and Field Crop Research, Gilat Research Center, Agricultural Research Organization, Rural delivery Negev, 85280 Israel E-mail address: [email protected] (H. Yasuor). 1 Authors share equal contribution to the manuscript. 2 Current address: Central Mountain Region Research and Development, Israel. http://dx.doi.org/10.1016/j.agwat.2017.05.012 0378-3774/© 2017 Elsevier B.V. All rights reserved.

Irrigation with desalinated water instead of water containing high concentrations of salts has economic and environmental beneficial aspects. Irrigation with desalinated water was found to increase maximum yields of bell peppers by 50% and allowed a reduction in irrigation water application rate by half compared to irrigation with local brackish groundwater (electrical conductivity (EC = 3.2 dS m−1 ) (Ben-Gal et al., 2009). The reduction in the required leaching fraction with the reduction in water salinity, is anticipated to reduce N leaching and enhance efficiency of N fertilization (Yasuor et al., 2013). Optimal N application strategies are expected to vary according to crop water requirements, water quality and irrigation method. The interaction of N nutrition and salinity on plant development is still unclear. Shenker et al. (2003) reported that in sweet corn plants grown in lysimeters under low salinity (EC = 0.5 dS m−1 ) levels, leaf N concentration, N uptake, and yield increased with increased N fertilization. However, as salinity increased (EC from 2.5 to 7.5 dS m−1 ) the uptake of N and its effect on corn plants decreased. Min et al. (2014) reported that cotton biomass, yield, evapotranspiration and water use efficiency decreased significantly when the salinity of irrigation water increased. This in spite of the fact that, regardless of irrigation salinity, the measured parameters increased as N application rate increased. The relative positive effects of N were reduced when the EC of the irrigation water was

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H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

8.0 dS m−1 (Min et al., 2014). Chen et al. (2010) reported that, under low soil salinity (2.4 dS m−1 in saturated-paste extract), increasing the rate of N application significantly enhanced the N uptake of cotton plants grown in pots. However, under moderate and high soil salinity levels (7.7, 12.5, 17.1 dS m−1 in saturated-paste extract) total N uptake was not correlated with the N application treatment. One of the ways that salinity affects plant response is due to the competition between specific ions resulting in differential uptake and possibly leading to mineral imbalances or deficiencies which might reduce crop growth (Bernstein et al., 1974; Grattan and Grieve 1992). Under conditions of salinity, N concentration in plant leaves has been shown to decrease due to increasing chloride (Cl) concentration in pepper (Cohen et al., 2003; De Pascale et al., 2003; Rubio et al., 2010), tomato (Kafkafi et al., 1982), lettuce and Chinese cabbage (Feigin et al., 1991). The repercussions of this competition are stronger in salt susceptible plants as compared to tolerant plants (Xu et al., 2000). Kafkafi et al. (1982) and Feigin et al. (1991) showed that increasing the nitrate (NO3 ) concentration in the root medium led to a decrease of Cl uptake in tomato, lettuce, and Chinese cabbage plants. Sweet bell pepper (Capsicum annum L.) production is commercially important in various regions of the world including Israel, Southern Europe and North Africa where the crop is grown from autumn to spring in greenhouses and net-houses. Such production in protective structures commonly yields seasonally more than 100 ton·ha−1 of high quality fruit (Bar-Tal et al., 2001; Ben-Gal et al., 2008; Yasuor et al., 2013). Peppers are considered to be sensitive to salinity (Maas, 1990), with a response function described by a threshold of saturated paste soil extract electrical conductivity (ECe) of 1.5 dS m−1 and a 14% decrease in biomass production for every additional 1 dS m−1 increase in ECe (Ben-Gal et al., 2008). Semiz et al. (2014) demonstrated that increasing irrigation water EC reduced pepper yield under both optimal (270 kg ha−1 ) and sub-optimal N application (135 kg ha−1 ). However, when plants were grown under sub-optimal N, pepper fruit was not affected by increased salinity levels up to 3.4 dS m−1 . These observations clearly demonstrate that when pepper plants face more than one stress causing factor, plant response is mainly affected by the most limiting factor (Shani et al., 2005; Yermiyahu et al., 2008). Our driving hypothesis was that low salinity (desalinated) irrigation water would improve N uptake by crops leading to increased and improved yield. Contrarily, irrigation with water high in salts would reduce N uptake and decrease yield relative to low salinity irrigation water. Therefore, under high salinity plant response to N concentration in the irrigation water would be stronger than under low salinity. The objectives of this study were to: 1) evaluate pepper response to different N levels under varied water salinity and 2) study the interactions between N and Cl uptake, accumulation and distribution in pepper plants.

2. Materials and methods 2.1. Description of study sites Experiments on bell peppers (Capsicum annum L.) grown in containers in 2011 (Soilless 1 experiment) and 2012 (Soilless 2 experiment) were conducted in a 50-mesh screen house at the Gilat Research Center (31◦ 20 N, 34◦ 39 E), in Israel. A third experiment (field experiment), in a 25-mesh screen house, also investigating bell peppers, was conducted in soil during 2012 at the Central Arava R&D experimental station (30◦ 46 N, 35◦ 14 E), Israel. Soilless 1 and 2 experiments involved a summer cropping season while the field experiment was conducted in autumn-winter. In all three cases, the experimental design was complete randomized

block, with nine treatments of three salinity levels (low, medium and high) and three N application levels (low, medium and high), replicated 5 times (Table 1). In all three experiments, irrigation water was applied at a rate designed to achieve a leaching fraction (drainage/irrigation) of 0.23. The rate of applied water therefore changed during the growing season according to plant development and weather conditions. 2.2. Description of the soilless experiments Bell pepper plants (Rita, 7199, Zeraim Gedera, Israel) were grown over two seasons in 90 L styrofoam containers (18 cm high, 100 cm length and 50 cm width) filled with Perlite-206 (mean particle size 0.8 mm) (Agrikal Industries, Habonim, Israel). New perlite was used in both years. In the first experiment (Soilless 1), 30 day old seedlings were transplanted on May 29, 2011, grown for 165 days, and irrigated with desalinated water with uniform fertilization concentration for the following two weeks. Each of the 5 blocks contained three rows of containers. Initially, the plants were fertilized with liquid fertilizer (Shafir Gat fertilizers Ltd, Israel) in which N, K2 O, and P2 O5 concentration was 6, 6, and 6%, respectively. This fertilizer was provided at a rate of 0.75 L m−3 in order to deliver N, K and P concentrations in irrigation water of 4.3, 1.2 and 0.84 mM, respectively. The fertilizer contained microelements (Gat fertilizers Ltd, Israel). After the first two weeks the N and salinity treatments were initiated. In second experiment (Soilless 2), the seedlings were transplanted on May 28, 2012 and grown for 142 days, the water quality treatments were initiated immediately thereafter with fertilizer concentration identical to that described for the Soilless 1 experiment. In both Soilless 1 and 2 experiments, the area of each plot was 3.4 m2 , replicated area was 10.2 m2 and treatment area was 51 m2 . There were 6 plants per container in Soilless 1 and 5 in Soilless 2. The irrigation water for each treatment was prepared in a 1.5 m3 tank and pumped daily to the containers via a drip irrigation system with inline 1.6 L h−1 drippers (Netafim, Tel-Aviv, Israel) spaced every 20 cm. Target salinity levels were reached by adding NaCl. Salts used to prepare the irrigation solutions were: KNO3 , Ca(NO3 )2 , KH2 PO4 , MgSO4 , Mg(NO3 )2 , and K2 SO4 . Microelements, Fe, Mn, Zn and Cu were given at concentrations of 0.02, 0.01, 0.004 and 0.0009 mM, respectively. The ratio of N NH4 to total N was 20, 10 and 5%, in the low, medium and high N treatments, respectively. The average concentrations in irrigation water of P, Ca, K, S and B were 0.42 ± 0.04, 1.30 ± 0.01, 4.1 ± 0.3, 0.86 ± 0.08 and 0.30 ± 0.05 mM, respectively. The pH of the fertigated water ranged between 6.0 and 6.5 in all treatments. Average and standard deviation of EC, and of N, Na, and Cl concentration in irrigation water over time are detailed in Table 1. 2.3. Description of the field experiment Bell pepper seedlings (Canon, 7158, Zeraim Gedera, Israel) were planted on September 15, 2012, grown for 220 days in a sandy soil (93% sand, 3% silt and 4% clay) and irrigated with either desalinated water (EC ∼ 1.0 dS m−1 , P, K, Ca, S and Mg concentrations were <0.03, <0.15, 1.57, 1.83, and 1.09 mM, respectively), local brackish water (∼2.5 dS m−1 , P, K, Ca, S and Mg concentrations were <0.03, 0.37, 4.86, 6.49, and 4.44 mM, respectively), or local brackish water with addition of NaCl (∼4.0 dS m−1 ). Salts used to prepare the solutions were: NH4 NO3 , KNO3 , KH2 PO4 , MgSO4 , NaNO3 , and KCl. Micro-elements were added similarly to the soilless experiments. The N NH4 to total N ratio was 30% in all N treatments. The pH of the irrigation solutions ranged from 6.0 to 6.5 in all treatments. The average and standard deviation of EC and N, Na, and Cl concentration in irrigation water are detailed in Table 1. Plants were irrigated using a drip system consisting of laterals adjacent to each pepper row, with inline 1.6 L−l h−1 drippers spaced every

Field

6.8 ± 0.3 7.2 ± 0.2 7.8 ± 0.2 10.0 ± 0.5 10.2 ± 0.3 10.3 ± 0.3 22.1 ± 0.9 22.7 ± 1.2 23.2 ± 1.1

Soilless 2

1.5 ± 0.4 1.4 ± 0.6 1.3 ± 0.4 10.3 ± 0.2 10.4 ± 6.8 10.3 ± 7.2 30.9 ± 5.3 30.6 ± 5.6 33.0 ± 5.3

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

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40 cm (Netafim, Tel-Aviv, Israel). Each bed consisted of two plant rows with 40 cm between rows and 40 cm between plants within each row. The distance between beds was 150 cm (center to center). The resulting density, 31,250 plants ha−1 , was in accordance with common local practice (S. Cohen, 2014, Central Arava R&D, Yair Experimental Station, personal communication).

2.1 ± 0.7 1.9 ± 0.6 1.8 ± 0.4 9.0 ± 0.1 8.7 ± 6.8 8.9 ± 7.0 34.7 ± 5.6 34.3 ± 5.6 34.6 ± 5.7 7.2 ± 0.3 6.9 ± 0.2 6.9 ± 0.2 10.2 ± 0.4 10.3 ± 0.3 10.4 ± 0.0 22.7 ± 0.9 24.7 ± 1.2 24.9 ± 1.1 1.7 ± 0.4 1.9 ± 0.5 1.5 ± 0.6 9.4 ± 0.5 9.8 ± 0.8 9.8 ± 0.9 32.1 ± 1.8 31.1 ± 1.4 32.2 ± 1.6 Values represent average ± standard error.

High

Medium

1.1 ± 0.0 1.4 ± 0.0 1.5 ± 0.1 2.6 ± 0.2 2.7 ± 0.1 2.9 ± 0.1 3.8 ± 0.1 4.2 ± 0.1 4.3 ± 0.1 Low

Low Medium High Low Medium High Low Medium High

§

Soilless 1 Field Soilless 2

2.4.2. Mineral concentration in diagnostic leaves Diagnostic leaves (the youngest fully developed leaf, usually the fourth leaf from the shoot apical meristem) were sampled 5, 4 and 3 times during the growing season in Soilless 1 experiment at 50, 80, 107, 134 and 155 DAP, Soilless 2 experiment at 49, 72, 100 and 139 DAP and in the field experiment at 68, 102 and 131 DAP. Twelve leaves for each replicate were sampled at each sampling date. Sampled leaves were rinsed for 15 s with de-ionized water, dried at 70 ◦ C and ground to a fine powder. Leaf powder was digested with sulfuric acid and peroxide (Snell and Snell, 1949). Nitrogen was determined in an autoanalyzer (Lachat Instruments, Milwaukee, WIS, USA) and Na concentration was determined using atomic absorption (AA 800, Perkin Elmer, Norwalk, CT, USA). Chloride was extracted from the leaf powder in water (100:1 water/dry matter) and determined with a Cl analyzer (Sherwood-Scientific, chloride analyzer 926, Cambridge, UK).

1.7 ± 0.4 1.6 ± 0.5 1.6 ± 0.4 9.7 ± 0.5 9.7 ± 0.7 9.6 ± 1.0 32.1 ± 1.4 32.2 ± 1.6 32.1 ± 1.3

Soilless 1

2.6 ± 0.3 4.5 ± 0.9 8.7 ± 1.3 2.5 ± 0.5 3.8 ± 1.0 7.9 ± 0.9 2.6 ± 0.6 4.0 ± 0.4 8.1 ± 0.8 1.2 ± 0.1 1.2 ± 0.1 1.5 ± 0.2 2.2 ± 0.3 2.2 ± 0.3 2.6 ± 0.3 4.8 ± 0.5 4.9 ± 0.6 5.2 ± 0.5

Field Soilless 2

2.0 ± 0.2 3.9 ± 0.4 7.8 ± 0.9 1.9 ± 0.4 3.9 ± 0.9 7.5 ± 0.8 2.0 ± 0.6 3.7 ± 0.3 7.9 ± 0.7

Soilless 1 Soilless 2

1.1 ± 0.1 1.1 ± 0.1 1.2 ± 0.2 2.0 ± 0.2 2.0 ± 0.2 2.1 ± 0.3 4.8 ± 0.5 4.8 ± 0.4 5.0 ± 0.3

Soilless 1 EC N

Field

2.4.1. Biomass parameters One plant was removed at 72 days after transplanting (DAP) from each plot. This date was chosen because no fruit had yet been removed and therefore both vegetative and productive organs could be analyzed. Shoot biomass was determined following oven drying at 70 ◦ C. During the growing season, ripe fruits were harvested and weighed on a weekly basis. At the end of each growing season, total yield was calculated as accumulated fresh fruit weight.

3.6 ± 0.6 6.8 ± 1.4 9.0 ± 1.0 3.2 ± 0.6 7.6 ± 1.4 8.8 ± 1.4 3.2 ± 0.6 7.6 ± 1.4 9.0 ± 2.0

Cl (mM) N (mM) EC (dS m−1 ) Treatment

Table 1 Electrical conductivity (EC), nitrogen (N), chloride (Cl) and sodium (Na) concentrations in applied irrigation water during the experiments.§

Na (mM)

2.4. Plant measurements and analysis

2.4.3. Petiole mineral concentration Six leaf petioles from each treatment were collected 3 times, at 50, 72 and 107 DAP and at 68, 102 and 131 DAP in the Soilless 1 experiment and in the field experiment, respectively. Petioles were collected at the same time of the day (10:00 am) throughout the growing season. The petioles were weighed and dried at 70 ◦ C in order to determine water content. The dry petioles were ground and samples were mixed with de-ionized water (100:1 water/dry matter), shaken overnight, and used to determine NO3 and Cl concentration. The concentrations of NO3 and Cl in filtered solution were determined by auto analyzer and chloride analyzer, respectively, using the instruments detailed above.

2.4.4. Plant tissue mineral concentrations In Soilless 2, one plant was removed at 72 DAP from each plot. The plants were separated into leaves, stems, fruits and roots and weighed fresh. The fresh tissue was rinsed for 15 s with de-ionized water, dried at 70 ◦ C and weighed again in order to determine dry matter content. The dry matter of each plant part was ground and analyzed for N, Cl and Na concentration using the methods and instruments detailed above. Mineral content for each plant organ was calculated by multiplying the organ mineral concentration with organ dry weight.

144.6 A 124.6 AB 103.2 B n.s. 3291 A 3060 B 2202 C n.s. 2311 A 2152 B 1758 C n.s. 84.4 A 90.1 A 72.9 B n.s.

104.1 A 96.1 A 75.8 B n.s.

101.2 B 136.5 A 134.7 A 2240 B 3091 A 3221 A 73.0 B 89.0 B 113.9 A 1878 B 2139 A 2205 A

N Low Medium High EC Low Medium High N × EC

High

66.6C 79.1 B 102.7 A

116.6 166.8 158.5 93.3 131.7 148.8 93.8 111.1 104.8

Shoot dry weight (g/plant) Fruits FW (g/plant)

2484 3614 3776 2551 3298 3341 1685 2364 2556 81.1 89.9 141.4 72.7 106.9 108.6 65.3 70.3 91.7 1994 2378 2465 1913 2128 2264 1538 1751 1763 Medium

Shoot dry mater and fruit weights from the three experiments are presented in Table 2. The two-way ANOVA analysis showed no interaction between EC and applied N level on shoot dry mater and fruit weight in all three experiments (Table 2). Therefore, the effect of the main factors (N and EC) was analyzed separately. The average plant shoot dry weight and fruit yield (Table 2) increased significantly with increased applied N, and decreased significantly as irrigation water EC increased in Soilless 1 and Soilless 2. Under field conditions when pepper plants were grown in a sandy soil,

69.1 81.8 104.0 74.1 86.2 115.3 58.5 69.6 90.6

3.1. Plant biomass and yield

Low

3. Results

Low Medium High Low Medium High Low Medium High

Where RSOx,y is the observed value for plants grown in a solution with N-concentration x, and salinity level y. If AR = 1, then the combined effect of N and salinity on growth or yield is as expected (additive). If AR < 1, the effect is synergistic and if AR > 1 it is antagonistic (Levy et al., 1986). The AR of individual data sets was analyzed with the analytical tools in Microsoft Excel at confidence values set at 0.95. The effect of main treatments was tested by one-way ANOVA. Default significance levels were set at ˛ = 0.05. The interaction effect of the two treatments was analyzed by two-way ANOVA. Best fit linear and nonlinear regression was determined using SigmaPlot (SPSS Inc., Chicago, IL) software for relative shoot biomass and relative yield as a function of solution N concentration and salinity, for the relationship between the N and Cl concentration in diagnostic leaves and between NO3 and Cl concentrations in petioles.

Soilless 2

(3)

Shoot dry weight (g/plant)

RSOx, y RSEx, y

Fruits FW (g/plant)

AR =

Shoot dry weight (g/plant)

Where RSx is the RS for plants grown in a solution with Nconcentration x at the lowest concentration of NaCl, and RSy is the RS for plants grown in a solution with NaCl-concentration y at the lowest concentration of N. After determination of RSEx,y, the “antagonist ratio” (AR) was calculated as:

Soilless 1

(2)

EC

RSy 100

N

RSEx, y = RSx

Treatment

Where Si is the mean shoot biomass for given treatment i and Sh is the highest mean shoot biomass. In Soilless 1, the highest mean values for RS occurred when the N and Cl concentrations in irrigation solution were 8.7 and 1.6 mM, respectively. In Soilless 2, the highest mean values for RS occurred when the N and Cl concentrations were 7.8 and 1.5 mM, respectively. And in the field experiment, the highest mean values for RS occurred when the N and Cl concentrations were 9.0 and 6.3 mM, respectively (Tables 1 and 2). Characterization of the interaction between N and salinity was determined for the data from our experiments using the Abbott Method as presented by Levy et al. (1986) and Kosman and Cohen (1996). The method compares expected values based on prior knowledge of behavior of the single stress-causing factors with observed, experimental values (Yermiyahu et al., 2008). Expected values were calculated based on the effect of each stress factor alone, e.g., the expected value of the shoot biomass (RSE) for a given N concentration (x) and a given NaCl concentration (y) was calculated as:

Field

(1)

Treatments accompanied with the same letter are not significantly different according to Tukey’s honestly significant difference two-way analysis of variance. Default significance levels were set at a = 0.05. n.s. = non-significant.

Si Sh

Table 2 Nitrogen (N) and salinity (electrical conductivity, EC) effects on plant shoot biomass and fruit fresh weight (FW) yield in the three experiments.§

RS = 100

§

In order to compare the data from the three different experiments, plant shoot biomass and fruit yield were normalized. Relative shoot biomass (RS) was calculated as:

3648 A 3532 A 3264 A n.s.

Fruits FW (g/plant)

2.5. Calculations and Statistics

3402 A 3490 A 3552 A

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

3996 3967 4309 3477 3562 3527 3097 2976 2590

60

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

61

production as salinity and N concentration increase. For example, at sufficient N levels (5 mM), increasing the EC of irrigation water from the low to medium level and from medium to the high level decreased the relative shoot biomass by 20 and 23%, respectively (Fig. 1A). The increase in relative fruit biomass as N level increased from 2 to 4 mM was 51, 44 and 37% for the low, medium and high salinity levels, respectively. A further increase in N level from 4 to 8 mM increased the relative fruit biomass by 26, 20 and 14%, for the low, medium and high salinity levels, respectively (Fig. 1B). However, the quantitative effects of N level and salinity on fruit production were smaller. At sufficient N levels (5 mM), increasing the EC of irrigation water from the low to medium level and from medium to the high level decreased the relative fruit biomass by 11 and 30%, respectively (Fig. 1B). The increase in relative shoot biomass as N level increased from 2 to 4 mM was 28, 19 and 22% for the low, medium and high salinity levels, respectively (Fig. 1A). A further increase in N from 4 to 8 mM increased the relative fruit biomass by 8, 4 and 5%, for the low, medium and high salinity levels, respectively (Fig. 1B). 3.2. Minerals in petioles and leaves

Fig. 1. Relative shoot biomass (A) and relative fruit yield (B) as a function of applied N under different salinity levels in all experiments. Plants were irrigated with low (green triangles, 1.0–1.6 dS m−1 ), medium (red circles, 1.8–3.0 dS m−1 ) or high (blue squares, 3.7–5.7 dS m−1 ) salinity water. The lines are best fit correlation for Y = a (1 − bx ). Statistical and equation parameters are presented in Table 3. Table 3 Regression parameters for equation 4 (Y = a (1 − bx )) and statistical parameters for the fitted lines presented in Fig. 1. EC (dS m−1 ) 1–1.6

1.8–3.0

3.7–5.7

Relative shoot biomass a b R2 P

1.062 0.713 0.869 0.0002

0.793 0.665 0.629 0.011

0.725 0.612 0.753 0.019

Relative fruit yield a b R2 P

1.001 0.527 0.893 0.0001

0.871 0.437 0.766 0.002

0.689 0.472 0.570 0.019

average shoot dry weight was significantly greater in the high compared to the low level of applied N. Similarly to the soilless culture experiments, increasing irrigation water EC in the field experiment also reduced shoot dry weight. However, unlike the soilless culture experiments fruit yield was not significantly affected either by N application level, or by the EC of irrigation water (Table 2). When normalized, relative shoot biomass and relative fruit yield from all three experiments showed identical response behavior to salinity and N combinations, regardless of growing medium or season (Fig. 1). Increased relative shoot biomass and fruit yield as a function of N level in the irrigation solution were best represented by an exponential equation:



Y = a 1 − bx



(4)

Where Y is the relative biomass (shoot or fruit), x is the N level (mM) and a and b are empirical coefficients. Regression parameters and statistical analysis for each salinity level in Fig. 1 are presented in Table 3. Using Eq. (4) with the obtained coefficient demonstrates the decreasing effect of N on shoot and fruit biomass

Mineral concentrations in diagnostic leaves and leaf petioles in the three experiments are presented in Table 4. The two-way ANOVA analysis showed no interaction between the main factors and therefore their effects were analyzed separately (Table 4). Increasing N concentration in irrigation water significantly increased N NO3 concentration and decreased Cl concentration in leaf petioles both in the soilless and field experiments. Increasing salinity in irrigation water significantly increased Cl concentration in leaf petioles in all experiments. However, in the soilless experiments, leaf petiole N NO3 concentration was not significantly affected by the salinity treatment while, in the field experiment, leaf petiole N NO3 was slightly higher in the high salinity than the low salinity treatment. Increasing N concentration in irrigation solution consistently led to increased N and a parallel reduction in Cl concentration in diagnostic leaves (Table 4). Increasing irrigation water salinity resulted in significant increase of Cl in diagnostic leaves in all experiments. Increased salinity of irrigation water did not affect N concentration in diagnostic leaves, except in Soilless 1 experiment where a minor significant increase of N concentration was observed for the high compared to the low salinity level. The overall Na concentrations detected in diagnostic leaves in all treatments and experiments were very low relative to the Cl concentrations (Table 4). In both soilless experiments, increased N concentration also led to significant increases in Na concentration in diagnostic leaves, whereas no such effect was observed in the field experiment. Increasing irrigation salinity resulted in significant increase of Na in diagnostic leaves in the soilless experiments, whereas no such effect was obtained in the field experiment (Table 4). Pepper leaf petiole Cl decreased linearly as petiole N NO3 concentration increased for each salinity level in both soilless culture and soil grown experiments (Fig. 2). In both growing systems the intercepts of the petiole Cl N NO3 relationship increased significantly as the salinity level increased from the lowest to the medium level and to the highest level. The slopes of the regression line describing Cl decrease as a function of NO3 increase in the soilless culture experiments did not differ significantly (Soilless 1, Fig. 2A, Table 5), whereas the slopes describing this relationship in the field experiment increased significantly with the salinity level (Fig. 2B, Table 5). Similar to the relationship between leaf petiole N NO3 and Cl, pepper leaf Cl decreased linearly as leaf N concentration increased for each salinity level (Fig. 3). In the soilless culture experiments both regression parameters, the intercepts and the slopes,

§ Treatments accompanied with the same letter are not significantly different according to Tukey’s honestly significant difference two-way analysis of variance with JMP 10.0 software (SAS Institute Inc., Cary, NC). N NO3 − and Cl− in petioles and accumulated N, Cl and Na in diagnostic leaves values are average of five replicates (in blocks) at three sampling dates during the growing seasons (see material and methods for more information). Default significance levels were set at a = 0.05. n.s. = non-significant.

0.08 A 0.08 A 0.08 A n.s 0.9 B 0.9 B 1.2 A n.s 4.0 A 4.0 A 4.0 A n.s 51.7 B 55.1 B 70.2 A n.s 0.05 B 0.06 B 0.14 A n.s 0.5 C 1.0 B 1.7 A n.s 3.8 A 3.8 A 3.9 A n.s 0.05 B 0.05 B 0.10 A n.s 65.3 C 104.7 B 148.9 A n.s 148.0 A 139.8 A 146.3 A n.s

3.2 B 3.3 AB 3.4 A n.s

0.8 C 1.3 B 2.0 A n.s

83.4 B 85.8 AB 93.3 A n.s

0.08 A 0.08 A 0.08 A 1.3 A 0.9 B 0.8 B 3.6 B 4.1 A 4.2 A 73.7 A 54.9 B 48.5 B 0.07 B 0.08 AB 0.11 A 1.4 A 1.1 B 0.7 C 3.1 C 3.9 B 4.5 A 0.05 B 0.07 AB 0.08 A 137.6 A 102.2 B 79.0 C 112.1 C 142.4 B 179.6 A

N Low Medium High EC Low Medium High N × EC

High

Medium

112.8 141.2 190.1 105.6 146.1 174.1 118.0 146.1 174.7 Low

Low Medium High Low Medium High Low Medium High

2.9 C 3.3 B 3.8 A

1.9 A 1.2 B 1.0 C

65.3 B 97.9 A 99.4 A

1.4 0.7 0.6 1.2 0.7 0.7 1.4 1.1 1.0 3.5 4.1 4.3 3.6 4.0 4.3 3.7 4.1 4.2 66.5 48.6 40.0 76.0 45.6 43.8 78.6 70.4 61.6 0.07 0.05 0.05 0.06 0.05 0.07 0.09 0.14 0.20 0.6 0.6 0.2 1.3 1.1 0.6 2.3 1.6 1.2 3.0 3.8 4.5 3.1 4.0 4.5 3.2 4.1 4.5

N NO3 (mM) N

92.0 72.1 31.9 142.2 95.4 76.4 178.6 139.2 128.7

2.8 3.2 3.8 2.8 3.2 3.8 3.0 3.4 3.8

1.0 0.8 0.6 2.0 1.3 0.8 2.6 1.7 1.6

0.05 0.04 0.05 0.04 0.05 0.05 0.07 0.10 0.13

55.7 94.6 100.1 65.3 113.4 101.2 75.0 85.7 96.8

Cl (%) N (%)

Diagnostic leaves

Cl (mM) Petiole

N NO3 (mM) Na (%) Cl (%)

Diagnostic leaves

N (%) Na (%) Cl (%) N (%)

Petiole

EC Treatment

Cl (mM)

Diagnostic leaves

Field Soilless 2 Soilless 1

Table 4 Concentrations of N NO3 − and Cl− in petioles and accumulated N, Cl and Na in diagnostic leaves.§

0.08 0.08 0.07 0.08 0.09 0.07 0.09 0.09 0.08

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

Na (%)

62

Fig. 2. The relationship between Cl and N NO3 concentrations in leaf petioles. A) Soilless 1 experiment. B) Field experiment. Low salinity irrigation water (green), medium salinity (red), and high salinity (blue). Data of each treatment was collected from 5 replicates and 3 dates of sampling. Each data point represents one petiole analysis and the line representing linear regression with 95% confidence curve (broken line). Regression parameters are given in Table 5.

increased significantly with the increase in salinity level, whereas in the soil grown experiment only the intercept of the highest salinity level was significantly higher than that of the low and medium salinity treatments and no significant difference between the slopes was obtained (Fig. 3, Table 5). 3.3. Distribution of N and Cl in plant organs Nitrogen and Cl concentrations and contents in pepper plant organs at 72 DAP from the Soilless 2 experiment are presented in Tables 6 and 7, respectively. Similar effects of the treatments on N and Cl concentrations and contents in plant organs were obtained in the other experiments (data not shown). Two-way ANOVA analysis showed no interaction between the main factors and therefore the effect of the main factors was analyzed separately (Tables 6 and 7). Increasing N irrigation concentration from 1.9 mM to 7.7 mM increased N concentration in fruit, roots and leaves by 1.4, 1.5 and 1.6 times, respectively, while an increase of 2.8 times was obtained in stems (Table 6). The whole plant total N content increased 2.2 times as N concentration in irrigation water increased from 1.9 mM to 7.7 mM. Nitrogen content in leaves and stems increased significantly by 3.3 and 3.6 times as N irrigation concentration increased from 1.9 mM to 7.7 mM, whereas an insignificant increase of 1.3 times was obtained in the roots and fruit (Table 5). Increasing N application shifted N allocation from fruit to vegetative organs (Fig. S1, supplementary file, available online). Increasing irrigation salinity from the lowest to the highest concentration had no effect on N concentration in plant organs, whereas whole plant total N content and leaf and stem N content decreased significantly by 27%, 27% and 38%, respectively. Slight and insignificant reduction in N content in roots and fruit was

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

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stems decreased as salinity increased while Cl in leaves increased (Table 7 and Fig. S1, supplementary file, available online). Increasing concentration of N in irrigation water from 1.9 mM to 7.7 mM decreased Cl concentration in the fruit, roots, stems and leaves by 2.0, 1.4, 1.9 and 2.2-fold, respectively, whereas Cl content in the fruit, roots, stems and leaves decreased by 43%, 42%, 39% and 19%, respectively. The total reduction in whole plant Cl content in response to an increase in N concentration in irrigation water from 1.9 mM to 7.7 mM was 35%. Increasing applied N significantly increased the fraction of Cl accumulated in the leaves from 22% to 28% (Table 7 and Fig. S1, supplementary file, available online).

4. Discussion 4.1. Plant biomass and yield

Fig. 3. The relationship between Cl and N concentrations in diagnostic leaves. A) Soilless 1 and 2 experiments. B) Field experiment. Low salinity irrigation water (green), medium salinity (red), and high salinity (blue). Data of each treatment was collected from 5 replicates and 4 to 5 dates of sampling. Each data point represents one leaf analysis and the line representing linear regression with 95% confidence curve (broken line). Regression parameters are given in Table 5.

obtained as a function of the same increase in irrigation water salinity. Nitrogen distribution between plant organs was not affected by salinity treatments (Fig. S1, supplementary file, available online). Fruit and leaves accumulated a high proportion (∼75%) of the applied N. Fruit accumulated >40% and leaves around 35%, while rest of the N was accumulated in stems (∼19%) and roots (∼4%). Increasing salinity of irrigation water resulted in significant increased Cl concentrations and contents in all plant organs, the highest increase was obtained in the leaves (Table 7). Chloride accumulated mostly in stems (55–60%), with ∼25% in leaves, ∼12% in fruit and the rest ∼3% found in roots. The relative amount of Cl in

Vegetative and fruit production were studied in two systems, soil and soilless culture, under different environmental conditions. Under both systems, increasing salinity above 1.00–1.5 dS m−1 caused shoot biomass and yield reduction, while increasing N fertilization enhanced shoot biomass (Table 2). The response of fruit yield in the two soilless experiments was similar while in the field experiment the trend was not significant (Table 2). The discrepancy in the field experiment was likely due to its unique irrigation water mineral composition and subsequent different quantity of applied Cl (Table 1). However, a combined data analysis of relative yields from all experiments from both growing systems showed that increased biomass production as a function of increased N fertilization reached plateaus at moderate N levels (4–6 mM, Fig. 1). This suggests a general effect of combined salinity and N fertilization supporting previous findings by Yasuor et al. (2013) where maximum pepper plant height and shoot biomass were found when 4 mM of N was applied and not at higher N concentrations. Our hypothesis was that under exposure to high salinity, plant response to N concentration in the irrigation water would be stronger than under conditions of low salinity. However, N was not able to overcome the negative effect of increasing salinity under our experimental setup, meaning that when salinity was high it was the limiting factor affecting growth and yield. In spite of this, under low salinity, increasing N concentration increased yield (Table 2). These findings are in agreement with those found in several works (Bernstein et al., 1974; Grattan and Grieve 1992) which support a “dual abiotic stress model” promoted by Shani and Dudley (2001) and Shani et al. (2005) where the most growth limiting stress controls the overall crop response. Kafkafi et al. (1982) suggested that increasing N in the irrigation water would overcome the reduction of plant biomass and yield

Table 5 Parameters for best fit linear regression (Y = a − b ∗ x) and statistical parameters for Figs. 2 and 3. Values in brackets represent standard errors of the parameters. Parameters Experiment petiole Soilless

Field

leaves Soilless

Field

salinity

a

b

F

Low Medium High Low Medium High

166 (15) b 209 (20) a 238 (22) a 87 (12) c 112 (9) b 134 (11) a

−0.68 (0.10) a −0.75 (0.13) a −0.61 (0.15) a −0.42 (0.14) c −0.61 (0.10) b −0.75 (0.13) a

>0.0001 >0.0001 >0.0001 >0.0001 >0.0001 >0.0001

Low Medium High

1.68 (0.09) c 3.02 (0.16) b 4.25 (0.21) a

−0.31 (0.03) c −0.52 (0.04) b −0.65 (0.06) a

>0.0001 >0.0001 >0.0001

Low Medium High

4.25 (0.43) b 4.21 (0.42) b 4.95 (0.40) a

−0.77 (0.11) a −0.75 (0.11) a −0.73 (0.10) a

>0.0001 >0.0001 >0.0001

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H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

Table 6 Concentration and content of N in pepper plant organs§ , 72 days after transplanting in the Soilless 2 experiment. Treatment

Nitrogen content (mg plant−1 )

Nitrogen concentration (%)

N

EC

Leaves

Stem

Root

Fruit

Leaves

Stem

Root

Fruit

Total

Low Medium High Low Medium High Low Medium High

Low

2.5 3.3 4.3 2.7 3.5 4.3 2.7 3.5 4.1

0.8 1.6 2.7 0.9 1.7 2.4 0.9 1.6 2.2

1.6 1.9 2.5 1.8 2.0 2.5 1.6 2.1 2.4

1.7 2.2 2.5 1.7 2.3 2.4 1.7 2.2 2.4

748 1257 3082 746 1684 2303 687 1183 1822

402 772 1765 381 909 1268 321 535 958

106 156 200 156 178 184 132 104 129

1466 2042 1911 1611 2186 1886 1119 1435 1773

2723 4228 6958 2895 4958 5643 2259 3258 4683

2.6C 3.4 B 4.2 A

0.9C 1.6 B 2.5 A

1.7C 2.0 B 2.5 A

1.7C 2.2 B 2.4 A

727C 1375 B 2402 A

368C 739 B 1330 A

131 A 146 A 171 A

1398 A 1887 A 1856 A

2626C 4148 B 5761 A

3.4 A 3.5 A 3.4 A n.s

1.7 A 1.7 A 1.7 A n.s

2.0 A 2.1 A 2.0 A n.s

2.1 A 2.1 A 2.1 A n.s

1696 A 1578 AB 1230 B n.s

980 A 853 A 604 B n.s

154 A 173 A 122 A n.s

1806 A 1894 A 1442 A n.s

4637 A 4498 A 3400 B n.s

Medium

High

N Low Medium High EC Low Medium High N × EC

§ Each value is an average of five replicates (in blocks). Treatments accompanied with the same letter are not significantly different according to Tukey’s honestly significant difference two-way analysis of variance with JMP 10.0 software (SAS Institute Inc., Cary, NC). Default significance levels were set at a = 0.05. n.s. = non-significant.

Table 7 Concentration and content of Cl in pepper plant organs§ , 72 days after transplanting in the Soilless 2 experiment. Treatment

Cl content (mg plant−1 )

Cl concentration (%)

N

EC

Leaves

Stem

Root

Fruit

Leaves

Stem

Root

Fruit

Total

Low Medium High Low Medium High Low Medium High

Low

1.0 0.8 0.2 1.9 1.6 0.9 3.1 2.8 1.6

2.2 1.7 0.5 3.3 2.8 1.9 4.8 3.7 3.1

1.1 1.0 0.4 1.7 1.5 1.3 1.7 1.7 1.5

0.3 0.2 0.1 0.4 0.3 0.2 0.6 0.4 0.3

282 310 145 508 766 451 796 894 681

1051 811 313 1401 1537 971 1731 1224 1287

74 82 31 149 131 98 137 83 82

214 193 82 337 294 189 359 253 245

1622 1397 573 2395 2728 1711 3024 2456 2296

2.0 A 1.7 B 0.9 C

3.4 A 2.7 B 1.8 C

1.5 A 1.4 A 1.1 B

0.4 A 0.3 B 0.2 C

528 A 656 A 426 A

1394 A 1191 A 857 B

120 A 99 AB 70 B

303 A 246 AB 172 B

2347 A 2194 A 1526 B

0.7 C 1.4 B 2.5 A n.s

1.5 C 2.7 B 3.9 A n.s

0.9 B 1.5 A 1.6 A n.s

0.2 C 0.3 B 0.4 A n.s

246 C 575 B 790 A n.s

725 B 1303 A 1414 A n.s

62 B 126 A 101 A n.s

163 B 273 A 285 A n.s

1197 B 2278 A 2592 A n.s

N Low Medium High EC Low Medium High N × EC

Medium

High

§ Each value is an average of five replicates (in blocks). Treatments accompanied with the same letter are not significantly different according to Tukey’s honestly significant difference two-way analysis of variance with JMP 10.0 software (SAS Institute Inc., Cary, NC). Default significance levels were set at a = 0.05. n.s. = non-significant.

caused by salinity. In our study the analysis of variance showed no significant interaction effects of N and salinity on shoot biomass and fruit production in pepper in any of the experiments (Table 2). The combined relationship of these factors was tested further using Eq. (2) (Fig. 4). The broken line represents a theoretical additive effect for combined responses to N and salinity without interaction between them. If measured data are higher than that predicted by the additive model, the points fall below the line, indicating that increasing N concentration under salinity enhanced production (a synergistic relationship). If the predicted data are higher than the measured, the points fall above the line indicating an antagonistic relationship (Yermiyahu et al., 2008). Most of the points of predicted against measured yield and shoots biomass of pepper plant in Fig. 4 are very close to the line 1:1 and spread slightly above or below it. This suggests that the combined effect of applied N level and salinity in pepper plants was additive and therefore, increased N application did not overcome the negative effects of salinity on pepper plant biomass or fruit yield. The same conclusions regarding additive combined effects of N and salinity were previously

Fig. 4. The relationship between measured relative biomass (filled symbols) and yield (empty symbols) and predicted relative biomass and yield in experiments 1(triangle), 2 (circle) and 3 (square) irrigated with different salinity and N concentration in water.

H. Yasuor et al. / Agricultural Water Management 191 (2017) 57–66

reported for corn (Shenker et al., 2003) and cotton (Chen et al., 2010; Min et al., 2014). 4.2. Leaf and petiole N NO3 − and Cl− Our hypothesis was that low salinity (desalinated) irrigation water would improve N uptake by crops leading to increased and improved yield and that, contrarily, irrigation with water high in salts would reduce N uptake and decrease yield relative to low salinity irrigation water. The total N accumulated in whole plants indeed decreased with salinity (Table 6) in agreement with the hypothesis. However, the results of all the three experiments showed that the concentrations of N in diagnostic or total leaves, roots, stems and fruits failed to decrease significantly as salinity increased (Tables 4 and 6). Thus, the effect on total N accumulation was due to the effect of salinity on total biomass production. The concentration of NO3 in the petioles was not affected by salinity (Table 4). The petiole is an important organ, ensuring nitrate distribution towards the leaves (Dechorgnat et al., 2011). Measurements of Cl and NO3 concentrations in this organ indicate the temporal concentrations of the elements independently of biomass production. Our results, that Cl had no effect on N uptake, are in contradiction to Kafkafi et al. (1982) and De Pascale et al. (2003) who showed reduction in N concentration due to increased Cl concentration in pepper plants. In the present study, for both soil and soilless systems, increasing N concentration in diagnostic leaves of pepper plants led to decreased Cl concentration (Fig. 3). A similar relationship between NO3 concentration and Cl concentration was found in pepper plant petioles (Fig. 2). These results are in agreement with Kafkafi et al. (1982) who showed that increasing of NO3 concentration in the root medium led to decreased Cl uptake of pepper plants. In the soilless experiments, the effect of N increased significantly with salinity, whereas in the soil no difference in the strength of the effect was found (Fig. 3 and Table 7). These differences between the soilless and soil systems are probably due to difference in the ionic composition of the irrigation solutions. In the soilless experiments the increase in salinity was reached by increasing NaCl concentration. Whereas, in the soil experiment both Cl and SO4 concentrations changed with salinity, therefore the range of Cl concentration in the soil experiment was much smaller than in the soilless experiments. Other differences between the soilless and soil experiments which could have attributed to the different responses include the different growing conditions (summer vs winter cropping) and the percentage of NH4 in the irrigation solutions. 4.3. Plant organ N and Cl distribution The major fraction of N in pepper plants was accumulated in leaves and fruit independent of salinity (Table 6). At low application levels, N was mainly accumulated in fruit (Table 6 and Fig. S1, supplementary file, available online) and with increased applied N, a higher proportion was found in leaves and stems. These results are in agreement with Yasuor et al. (2013), when N accumulation in different pepper plant organs was evaluated at different N levels in desalinated water. The fact that salinity had no significant effect on N distribution indicates that the negative effect of high Cl was not due to restricted N transport to the leaves, which are the major photosynthetic organs. The major fraction of Cl in pepper plants was accumulated in the largely non-photosynthetic stems (Table 7 and Fig. S1, supplementary file, available online), thus reducing Cl accumulation in leaves and therefore minimizing its toxic effects on the plant. These results are in agreement with Bot´␫a et al. (2005), who reported that melon plants accumulated Na and Cl in their stems. Bot´␫a et al. (2005) suggested that this mechanism for avoiding high concentrations of Cl ions in leaves reduces toxicity. However, the

65

increase of leaf Cl concentration up to 3.1% (Tables 4 and 7) due to elevated salinity, compared to leaf Na concentrations that were at least 10-fold lower than that of Cl (Table 4), indicate the possibility of a specific Cl toxicity effect. Sodium did not accumulate in above ground pepper plant organs including leaves and petioles (Table 4) and therefore its contribution to reduced biomass production and fruit yield, if any, was limited to an osmotic role or to toxicity at the root scale. These results are in contradiction to findings of De Pascale et al. (2003) which showed increasing Na concentration in pepper plant leaves under salinity. The contradiction may be due to higher salinity levels imposed, up to 8.5 dS m−1 , or due to the use of diluted seawater as a source of salt in the De Pascale et al. (2003) study. The reduction of Cl accumulation in pepper leaves with the increase of N in the leaves might be explained by the possibility that the ions share cellular transporters. Nitrate passes through the tonoplast and is stored in vacuoles, a step that involves Cl channels (Dechorgnat et al., 2011). The Arabidopsis Cl channels are able to specifically accumulate NO3 in vacuoles and behave as a 2NO3 − /H+ antiporter having high selectivity for NO3 rather than Cl ions (von der Fecht-Bartenbach et al., 2010; Dechorgnat et al., 2011). 5. Conclusions The assumption of this study was that the response of pepper biomass, fruit and N content to N concentration in irrigation water would be more acute under conditions of high compared to low salinity. However, N was not able to overcome the negative effects of increasing salinity, meaning that when salinity was high it was the limiting factor affecting growth and yield, rather than Cl competition with N. Chloride accumulated mainly in the stems and when salinity increased the fraction of Cl in leaves increased. Increasing N application resulted in reduced Cl uptake and accumulation in pepper organs, including leaves and petioles. Pepper plant biomass and yield response to N fertilization increased as water quality improved. However, there was no difference in the rate of Cl concentration as a function of N concentration between the lower salinity levels. Acknowledgements The research was supported by Israel’s Ministry of Agriculture and Rural Development Chief Scientist Research Grant [grant number 301-0656-11]. The authors would like to thank Gat fertilizers Ltd for the fertilizer supply. We thank Rivka Offenbach and the Central and Northern Arava R&D Center staff for experimental management and to Inna Faingold and Ludmilia Yusupov for technical support. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at 10.1016/j.agwat.2017.05.012. References Bar-Tal, A., Aloni, B., Karni, L., Oserovitz, J., Hazan, A., Itach, M., Gantz, S., Avidan, A., Posalski, I., Tratkovski, N., Rosenberg, R., 2001. Nitrogen nutrition of greenhouse pepper. I. Effects of nitrogen concentration and NO3 :NH4 ratio on yield fruit shape, and the incidence of blossom-end rot in relation to plant mineral composition. HortSci. 36, 1244–1251. Beltrán, M.J., 1999. Irrigation with saline water: benefits and environmental impact. Agric. Water Manag. 40, 183–194. Ben-Gal, A., Ityel, E., Dudley, L., Cohen, S., Yermiyahu, U., Presnov, E., Zigmond, L., Shani, U., 2008. Effect of irrigation water salinity on transpiration and on leaching requirements: a case study for bell peppers. Agric. Water Manag. 95, 587–597.

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