Dr. Ashraf SB 2017 Archives

Archives of Agronomy and Soil Science
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Nitrogen nutrition and plant adaptation to saline

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environment: a review
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Journal: Archives of Agronomy and Soil Science
Manuscript ID GAGS-2017-0347.R1
Manuscript Type: Review Articles

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Ion toxicity, nitrogen forms, nitrogen metabolism, nutrient imbalance,

Keywords:
osmolytes
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URL: http://mc.manuscriptcentral.com/GAGS E-mail:

Page 1 of 35 Archives of Agronomy and Soil Science
1 Nitrogen nutrition and plant adaptation to saline environment: a review

2 Muhammad Ashraf1*, Sher Muhammad Shahzad1, Muhammad Imtiaz2, Muhammad Shahid
3 Rizwan3, Muhammad Saleem Arif4, Rizwana Kausar5
4
1
5 Department of Soil and Environmental Sciences, University College of Agriculture, University
6 of Sargodha, Sargodha 40100, Pakistan
2
7 School of Environmental Science and Engineering, Guangzhou University, Guangzhou 510275,
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8 China
3
9 Bahauddin Zakariya University, Layyah, Punjab, Pakistan
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4
10 Department of Environmental Sciences and Engineering, Government College University
11 Faisalabad, Faisalabad 38000, Pakistan
5
12 Soil and Water Testing Laboratory for Research, Sargodha, Punjab, Pakistan
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13 *Corresponding author’s e-mail: mashraf_1972@yahoo.com

14
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15 Abstract
16 Relations between nitrogen (N) nutrition and salinity tolerance in plants are multifaceted and
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17 varies significantly depending on many soil and plant factors. Saline environment might
18 experience an N dilemma due to the opposing effects of salt ions on N uptake, translocation and
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19 metabolism within the plant body. Adequate regulation of N under saline conditions can be a
20 promising approach to alleviate salinity’s effects on plants by ameliorating ion toxicity and
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21 nutrient imbalances through its impacts on uptake and redistribution of salt ions within the plant.
Certain N-containing compounds including proline, glycine betaine, proteins and polyamines
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22
23 help the plants to tolerate salinity through their involvement in improving water uptake and water
24 use efficiency, membrane integrity, enzyme activation, hormonal balance, chlorophyll synthesis,
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25 stimulation of photosystems and CO2 assimilation under salinity stress. Nitrogen, particularly
26 NO3- represents a stress signal that triggers the activation of antioxidant enzymes to protect the
27 plants against salinity-induced oxidative damage. Furthermore, the source/form of N application
28 can affect not only N-interactions but also the behavior of other nutrients in stress environment.
29 The present review deals with N-salinity relations in plants, particularly glycophytes,
30 emphasizing on N-induced mechanisms which can improve plant adaptation to saline
31 environment.

Archives of Agronomy and Soil Science Page 2 of 35
32 Keywords: Ion toxicity, nitrogen forms, nitrogen metabolism, nutrient imbalance, osmolytes,
33 salinity tolerance
34
35 Introduction
36 Global increase in soil salinization constitutes a most devastating environmental threat for crop
37 yield and food quality (Asrar et al. 2017). High salinity can inhibit plant growth through osmotic
38 stress (Maia et al. 2010), nutritional imbalance (Chinnusamy and Zhu 2003), oxidative damage
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39 (Ahmad 2010) and/or specific ion toxicity (Chinnusamy et al. 2005). In saline environment,
40 sodium (Na+) and chloride (Cl-) interfere with the uptake, translocation and assimilation of plant
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41 nutrients such as ammonium (NH4+), potassium (K+), calcium (Ca2+), magnesium (Mg2+), nitrate
42 (NO3-) and sulfate (SO42-), leading to disruption of ion homeostasis. Nitrogen (N) occupies a
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43 prominent position among essential plant nutrients absorbed by plants. It is an integral

44 component of proteins that construct cell materials, plant tissues, and hence vital for plant growth
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45 and development. However, N uptake and assimilation is severely restricted by salt ions in plants
46 under salinity stress, and examples of such interactions have been found in many crops such as
47 Cicer arietinum L. (Atieno et al. 2017); Zea mays L. (Hutsch et al. 2016); Brassica juncea L.
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48 (Iqbal et al. 2015); Gossypium hirsutum L. (Chen et al. 2010); Lycopersicon esculentum Mill.
49 (Flores et al. 2001). The salinity’s effects on N uptake and assimilation could be attributed to Na+
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50 and Cl- antagonism with NH4+ and NO3-, respectively (Shawer 2014), salinity-induced reduction
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51 in water uptake by plants (Ashraf and Harris 2004), inhibition of plant growth or alteration in N
52 metabolism (Parida and Das 2005). NH4+ assimilation in plants under saline condition might also
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53 be inhibited due to the down regulation of genes responsible for NH4+ assimilation (Wang et al.
54 2012).
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55 Adaptation of plants to stress environment including salinity stress is generally the result of
56 many factors and processes functioning at ionic, morphological, physiological, biochemical and
57 genetic levels within the plants (Rahnama et al. 2010). Among different strategies, adequate
58 regulation of mineral nutrients is of increasing importance to improve plant survival under
59 salinity stress (Guo et al. 2017). N is particularly known amongst the mineral nutrients for
60 enhancing plant capabilities to endure salinity stress through its involvement in osmotic
61 adjustment (Nasab et al. 2014), stimulation of antioxidant defense system (Rais et al. 2013),

62 alleviation of ion toxicity (Iqbal et al. 2015), maintaining ionic balance (Khan et al. 2016) and
63 activating various enzymes (Aragão et al. 2012). de Souza-Miranda et al. (2013) have found that
64 N enhanced plant adaptation to saline environment by ameliorating ion toxicity and maintaining
65 ionic balance. While, Iglesias et al. (2004) reported that appropriate N supply under saline
66 conditions stimulated the plant growth, leading to salt dilution which consequently enhanced
67 plant survival in stress environment. Kamel (2012) found that N could help to improve salt
68 tolerance by adjusting osmotic stress, in addition to its vital role in the general growth processes.
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69 Rais et al. (2013) suggested that contribution of N in osmotic adjustment, chlorophyll synthesis
70 and proline accumulation are the main factors inducing tolerance to salinity in plants. Siddiqui et
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71 al. (2010) found that detoxification of radical oxygen species (ROS) by N-induced synthesis of
72 osmoprotectants such as proline and glycine betaine (GB) contributed to salt tolerance in plants.
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73 NH4+ and NO3- are the principal plant available forms of N which can influence its
74 protective role against salinity stress (Zhonghua et al. 2011). Although, NH4+ assimilation is
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75 energetically more favorable than NO3- but it is usually toxic at higher concentration for most of
76 the plant species (Britto and Kronzucker 2002). Moreover, NH4+-fed plants may be more
77 sensitive to salinity than NO3--fed plants as these plants have greater Cl- but lower K+, Ca2+ and
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78 Mg2+ concentration as compared to NO3--fed plants (Ashraf and Sultana 2000). On the other
79 hand, Ashraf (1999) reported that NO3- and NaCl interacted to inhibit plant growth more than did
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80 NH4+ under saline conditions. Some other investigations, for example, Kant et al. (2007) have
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81 suggested that integrated use NH4+ and NO3- is more effective in alleviating adverse effects of
82 salts on plants as compared to their sole application.
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83 The reconciliation of research on N-salinity interaction in plants is a big challenge because it

84 varies widely depending on plant nature, growth stage, concentration and composition of salts in
the rhizosphere, salinity stress duration, growth medium, form and level of N application under
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86 saline conditions. However, for evaluating the role of N in saline environment, it is imperative to
87 understand the involvement of N in basic processes and mechanisms contributing to salt
88 tolerance in plants. The present paper reviewed the contribution of N to salt tolerance, with an
89 emphasis on its involvement in osmotic adjustment, protection of cellular structure, maintenance
90 of ionic balance, mitigation of ion toxicity and scavenging of free radicals under salinity stress as
91 well as the relation of N forms with salinity tolerance of plants, in particular glycophytes.
92

93 Plant growth in saline environment

94 Soil salinity as a noxious environmental stress adversely influences almost all the growth,
95 yield and quality traits of different plant species, particularly glycophytes (Ashraf et al. 2012).
96 Soil salinization initially damages the plant roots, disturbs soil water potential and thus leading to
97 osmotic stress. The buildup of salt ions in the growth media as well as their accumulation and
98 distribution within the plant body have marked influence on the uptake and translocation of plant
99 nutrients, resulting in ionic imbalances and toxicity (Zaki et al. 2016). In addition, increasing
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100 salinity disturbs plant metabolism, leading to enhanced generation of ROS and thus oxidative
101 stress (Hernandez and Alamansa 2002). Higher cellular salt buildup also causes leaf abscission,
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102 chlorophyll and photosystem damage, disruption of hormonal balance, and consequently
103 inhibition of plant growth and development (Figure 1). Salinity stress effects and mechanisms in
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104 various plant species have been presented in Table 1. In salinity-induced osmotic stress,
105 excessive accumulation of salts in the rhizosphere depresses soil water potential, inhibits the
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106 movement of water from soil to plant or even water starts to move from plant roots to soil in
107 more severe cases, causing plant dehydration (Munns and Tester 2008). Under these conditions,
108 plants have to use more energy to make biochemical adjustments through the accumulation of
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109 osmolytes for extracting water from soil. This energy is diverted from the plant growth processes
110 which results in marked decline in plant growth, development and yield. Furthermore, higher
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111 accumulation of salt ions in leaves disrupts various metabolic processes which reduces the net
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112 CO2 assimilation, and consequently leading to a significant yield reduction (Frechilla et al.
113 2001).
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114 Under salinity stress, nutrient imbalances usually results from the effects of salt ions on
115 nutrient phytoavailability, uptake, translocation or distribution within the plant body which
116 causes a significant decline in crop yield and quality (Camara-Zapata et al. 2004). Various
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117 interactions of salt ions with the essential plant nutrients have been widely described, for
118 example, Na+ interacts with Ca2+, Mg2+, K+ and NH4+ while Cl- with NO3- and SO42- (Gimeno et
119 al. 2009), leading to nutrient imbalances which consequently reduces plant growth and
120 productivity. Yousufinia et al. (2013) have observed that antagonistic effects of Na+ with NH4+
121 or Cl- with NO3- reduces N accumulation in salt stressed plants. Salt stress also deregulates the
122 stomatal opening which decreases CO2/O2 ratio in leaves and inhibits the fixation of CO2 within
123 plants (Hernández and Almansa 2002). Salinity causes impaired electron transport during CO2

124 fixation and enhances ROS production in plants (Demidchik and Maathuis 2007). Enhanced
125 generation of ROS under salinity stress damages the cell membrane, chlorophyll, proteins, lipids
126 and nucleic acids, and ultimately leading to a significant decline in crop yield and quality
127 through oxidative stress (Ahmad and Umar 2011).
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129 Nitrogen effects on plant growth in saline environment

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130 Adequate supplementation of N under saline conditions can provide an important strategy to
131 sustain or even improve the productivity of salt affected soils. Many researchers have studied the
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132 interactions between N nutrition and salinity to improve plant growth and development because
133 soil salinization is an emerging global threat to food security and safety (Guo et al. 2017; Khan et
134 al. 2016; Nadian et al. 2012; Akram et al. 2010; Siddiqui et al. 2008; Figueira and Caldeira 2005;
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135 Ashraf and Harris 2004). The ameliorative role of N against the deleterious effects of salts in
136 plants is mainly associated with its involvement in adjusting osmotic stress (Heidari et al. 2011),
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137 stomatal conductance (Akram and Ashraf 2009), antioxidant activities (Fayez and Bazaid 2014),
138 alleviation of ion toxicity (Bahmanzadegan and Aboutalebi 2013), nutrient uptake (Shawer
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139 2014), photosynthesis (Iglesias et al. 2004), activities of nitrate reductase (Rais et al. 2013) and
140 carbonic anhydrase enzymes (Soussi et al. 1998), membrane permeability (Aragão et al. 2012)
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141 and N-use efficiency (Bybordi et al. 2010). Nitrogen nutrition under salinity stress increases
142 plant biomass by stimulating vegetative growth or decreasing leaf abscission which causes salt
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143 dilution within the plant body and hence reduces salt ions toxicity, the critical parameter for salt
144 damage (Figure 2). Furthermore, larger plant root system under high salinity with adequate N
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145 supply have the potential benefit to increase the ability of plant roots to exploit greater volume of
146 soil for nutrients and water, and hence might present an adaptive mechanism to improve plant
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147 tolerance to salinity (Nhung et al. 2017). Nitrogen nutrition in saline environment also improves
148 the selectivity of plant roots for the uptake of essential elements and exclusion ability of harmful
149 Na+ from leaf tissues, and eventually contributes to salt tolerance of plants (Tabatabaei 2006;
150 Kabir et al. 2005). Some other studies have demonstrated that N-induced plant tolerance to
151 salinity might also be related to the stimulation of NO3- assimilatory pathway which enhances the
152 assimilation of CO2 while reduces photo-damage (Aragão et al. 2012, Jatropha curcas); higher
153 leaf proline content (Nadian et al. 2012, Saccharum officinarum L.); increased abscisic acid

154 accumulation (Fernández-Crespo et al. 2012, Citrus sinensis L.); increased fluorescence, higher
155 efficiency of photosynthetic apparatus (Akram et al. 2010, Zea mays L.) or osmotic adjustment
156 (Mansour 2000). In summary, N-induced increase in biomass accumulation, reduction in leaf
157 abscission, stimulation of enzyme activities, higher photosynthetic efficiency, reduction in salt
158 ion uptake (Na+ and Cl-), increase in the uptake of different essential elements and maintenance
159 of water balance are the principal factors contributing to better plant adaptation to saline
160 environment. The protective role of N against salinity stress is found to be more prominent when
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161 N supply is higher than optimum under saline conditions. However, relations of N with salinity
162 varies greatly depending on plant type, plant age, N source and level as well as salinity
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163 composition and concentration.
164
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165 N-induced adaptation mechanisms against salinity stress

166 N-mediated mitigation of specific ion toxicity
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167 Specific ion toxicity develops by increased absorption of salt ions is a major growth limiting
168 factor for many plant species growing in saline environment (Hassan et al. 2014). However,
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169 plant performance under saline conditions might be improved by the adequate supply of plant
170 nutrients through the mitigation of specific ion toxicity (Bahmanzadegan and Aboutalebi 2013).
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171 Inhibition of Na+ and Cl- accumulation in plants grown under salinity stress is considered an
172 important physiological process conferring salt tolerance, and this inhibition might be related to
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173 N nutrition as NO3- and NH4+ have antagonistic effect with Cl- and Na+, respectively (Table 2).
174 Increased N nutrition in saline environment is generally interacted with salt ions to decrease their
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175 toxicity in different plant species, for example, Glycine max (Guo et al. 2017); Zea mays L.
176 (Hutsch et al. 2016); Brassica juncea L. (Iqbal et al. 2015); Tageta patula (Bahmanzadegan and
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177 Aboutalebi 2013); Medicago sativa (Abbasi-Shahmersi and Ebadi 2012); Helianthus annuus L.
178 and Carthamus tinctorius L. (Jabeen and Ahmad 2011); Gossypium hirsutum L. (Chen et al.
179 2010).
180 Enhanced Cl- accumulation under salinity stress is considered to be a principal cause of ion
181 toxicity in certain plant species, and thus reduction in Cl- uptake might be an important
182 mechanism to enhance plant adaptability to saline environment (Moya et al. 2003). N,
183 particularly in the form of NO3- interacts with Cl-, reduces its uptake and accumulation within the

184 plant body (Hutsch et al. 2016). Two mechanisms including Cl- dilution effect by NO3--induced
185 growth stimulation or reduction in leaf abscission, and an anionic antagonism between NO3- and
186 Cl- have been suggested for reducing Cl- toxicity by NO3- under salinity stress (Shawer 2014).
187 High salinity can enhance leaf abscission by stimulating ethylene synthesis and aggravating the
188 extent of ion toxicity (Gómez-Cadenas et al. 1998), but N supplementation under saline
189 conditions can inhibit ethylene production (Noiraud et al. 2001) and reduce leaf abscission,
190 alleviating salt toxicity through dilution effect (Gómez-Cadenas et al. 2000). High NO3-
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191 concentration may also inhibit Cl- accumulation in plants by an allosteric effect of NO3- on the
192 uptake sites of Cl- (Aroiee et al. 2005; Iqbal et al. 2015). Many other studies, for example Jabeen
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193 and Ahmad (2011) Helianthus annuus L. and Carthamus tinctorius L.; Bybordi et al. (2010)
194 Brassica napus L.; Tabatabaei and Fakhrzad (2008) Lolium perenne; Abdelgadir et al. (2005)
Oryza sativa L.; Ebert et al. (2002) Psidium guajava L. have found a negative correlation
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195
196 between NO3- and Cl-, and NO3--N frequently inhibits the uptake and accumulation of Cl-, and
thus reduces Cl- toxicity under saline conditions.
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197
198 Na+ is another ion that is toxic at higher concentration for different aspects of plant growth
199 and metabolism (Tabatabaei 2006). In saline environment, lower Na+ uptake or higher K+
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200 accumulation and an increasing K+:Na+ ratio might be an important strategy to enhance plant
201 adaptability (Han et al. 2015; Feki et al. 2014; Hasegawa 2013). Inhibition of Na+ influx and/or
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202 increase in efflux is the major factor responsible for lower accumulation of this ion in the roots
203 (de Souza-Miranda et al. 2013). Furthermore, lower Na+ movement from roots to shoots via
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204 xylem or higher Na+ retranslocation via the phloem also decreases Na+ buildup in shoots
(Davenport et al. 2005). When salt stressed plants are supplied with N, particularly NH4+, it
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206 interacts with Na+, reduces its uptake and accumulation within the plant (Esmaili et al. 2008).
207 NH4+-N nutrition induces the activity of Na+/H+ antiporter which helps to maintain Na+ balance
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208 under saline conditions (Mansour 2014). Moreover, NH4+ competes with Na+ for absorption sites
209 on roots and thus reduces Na+ uptake and translocation within salt stressed plants (Fernández-
210 Crespo et al. 2012). Kant et al. (2007) also reported an antagonistic effect of NH4+ on Na+ which
211 decreases Na+ uptake and translocation, thereby inhibiting Na+ while improving K+ accumulation
212 within plant leaves under salinity stress. It is summarized that increasing N application in saline
213 environment enhances NH4+ and NO3- uptake which compete with Na+ and Cl-, major ions in
214 saline environment. Such interactions result in the mitigation of ion toxicity and improve plant

215 growth under salinity stress. Moreover, N nutrition stimulates plant growth while reduces leaf
216 abscission, and hence mitigates ion toxicity through dilution effect.
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218 N-mediated maintenance of nutrient balance
219 In saline environment, salt ions interfere with nutrient uptake, translocation and/or distribution
220 within the plants, leading to nutrient imbalances (Renault et al. 2016). Adequate regulation of N
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221 under saline condition is involved in the maintenance ionic balance in plants, and thus
222 contributes to salt tolerance in many plant species, for example, Gossypium hirsutum L. (Khan et
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223 al. 2016); Oryza sativa (Zaki 2016); Cucumis sativus L. (Shawer 2014); Saccharum officinarum
224 L. (Nadian et al. 2012); Sorghum bicolor L. (Serrao et al. 2012); Brassica napus L. (Bybordi et
225 al. 2010); Lolium perenne (Tabatabaei and Fakhrzad 2008); Pisum sativum L. (Figueira and
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226 Caldeira 2005); Vigna radiata L. (Kabir et al. 2005); Psidium guajava L. (Ebert et al. 2002)
227 (Table 3). These studies have demonstrated that soil salinity reduces NH4+, NO3-, K+, Ca2+ and
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228 Mg2+ while increases Na+ and Cl- concentrations in the plant tissues. N fertilization in saline
229 environment interacts with salt ions, reduces their uptake and accumulation with a corresponding
increase in the uptake of NH4+, NO3-, K+ and to some extent Ca2+ and Mg2+, and subsequently
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230
231 improves salt tolerance. Under salinity stress, NO3--N has antagonistic effect on Cl- uptake and
distribution, while NH4+ can balance the Na+ accumulation, alleviating the detrimental effects of
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233 increasing salinity on plant metabolism (Esmaili et al. 2008; Camara-Zapata et al. 2004).
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234 Nitrogen nutrition also improves membrane permeability and selectivity, leading to reduced
235 uptake of salt ions and thus maintenance of ionic balance, which otherwise damaged due to
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236 increased uptake of salt ions under saline conditions (Aragão et al. 2012; Ebert et al. 2002).
237 Higher K+/Na+ selectivity in plants is an important protective mechanism against salinity
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238 stress and has been suggested as a good criterion for evaluating plant tolerance to salinity (de
239 Souza-Miranda et al. 2016). Exogenous application of N, particularly in the form of NH4+ in
240 saline environment causes a marked reduction in Na+ accompanied with the maintenance of
241 higher NH4+, K+ and K+:Na+ ratio which associates with salt tolerance in plants (Siddiqui et al.
242 2010). In summary, proper fertilization with N in saline environment influences the uptake and
243 transport of essential nutrients and helps to correct salinity-induced nutrient imbalance. Salinity
244 stress generally results in higher accumulation of Na+ and Cl- accompanied with a lower uptake

245 of NH4+, K+, Ca2+ and NO3-. N nutrition increases NH4+, NO3-, K+ and to some extent Ca2+ and
246 Mg2+ uptake but decreases Na+ and Cl- concentrations. Consequently, all these result in the
247 maintenance of ionic balance, leading to improved plant tolerance to salinity.
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249 N-mediated osmotic adjustment
250 Osmotic adjustment is a principal mechanism in plants to maintain their water status under
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251 different environmental stresses including salinity (Kamel 2012). Osmotic adjustment is ensured
252 by the accumulation/synthesis, translocation and redistribution of ions or organic substances that
253 serve as osmprotectants, enabling the plants to extract water from soil under stressed conditions
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254 (Rontein et al. 2002). These osmoprotectants are non-charged, highly water soluble, low-weight
255 molecules which are non-toxic at higher concentration to plant metabolism and help the plants to
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256 balance the salinity-induced external osmotic pressure for the absorption of water in stressed
257 environment (Munns 2002). N plays a pivotal role in osmotic adjustment through ionic
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258 accumulation as well as by inducing the synthesis of organic osmolytes which help the plants to
259 extract water when plants are growing under salinity stress (Heidari et al. 2011). When NO3-
260 uptake is greater than its reduction, NO3- compartmentalizes in the vacuole and functions to
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261 adjust osmotic stress under saline conditions. N is involved in the synthesis of osmolytes
262 including proline, asparagine, GB, proteins and polyamines which function to maintain plant
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263 turgor under salinity stress (Mansour 2000). Many studies, for example, Nasab et al. (2014)
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264 Pistacia vera L.; Kamel (2012) Vicia faba L.; Heidari et al. (2011) Plantago ovata F.; Tattersall
265 et al. (2009) Thellungiella salsuginea; Heidari et al. (2007) Triticum aestivum L.; Carillo et al.
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266 (2005) Triticum durum have reported the involvement of N in improving salt tolerance through
267 the adjustment of osmotic stress (Table 4). These studies have reported that N containing
compounds can function as osmolytes to balance water potential within the cell, especially when
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269 N availability exceeds the need for plant growth. Therefore, N application rate in saline
270 environment should be higher that considered optimum under non-saline conditions because a
271 greater proportion of the plant N pool would be allocated to the synthesis of compatible
272 nitrogenous osmolytes. Moreover, plants have to use energy for the synthesis of these organic
273 solutes. The ATP requirement is 52 mol ATP mole-1 for sucrose, 50 mol ATP mole-1 for GB, 41
274 mol ATP mole-1 for proline and 34 mol ATP mole-1 for mannitol as compared to 3.5 mol ATP
275 mole-1 for Na+ accumulation when N is supplied in the form of NO3- (Munns 2002). Thus,

276 adequate supply of essential plant nutrients including N is vital for sustaining the productivity of
277 salt affected soils. Some other studies have demonstrated that N supplementation under saline
278 conditions regulates the opening and closing of stomata and improves plant water use efficiency,
279 photosynthesis and many other metabolic process, leading to improved salt tolerance (Akram
280 and Ashraf 2009). In conclusion, N being an integral component of organic osmolytes is
281 involved in osmotic adjustment, enabling the plants to extract water from soil and tolerate
282 salinity stress by maintaining sufficient turgor for growth. Moreover, when N availability
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283 exceeds the plant requirements, the excess N is accumulated in vacuole as NO3- which serves not
284 only as N source for plant structural growth but also helps to improve plant tolerance to salinity
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285 through osmotic adjustment.
286
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287 N effects on oxidative damage

288 Metabolic acclimation by accumulating/synthesizing different osmolytes provides protection to
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289 plants against salinity-induced oxidative stress (Polesskaya et al. 2006). Many of these osmolytes
290 are nitrogenous compounds enabling the plants to overcome oxidative stress by protecting
291 photosynthetic pigments and photosystem II, stabilizing the protein and enzyme structure against
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292 denaturation, improving membrane stability and ROS scavenging (Cuin and Shabala 2007).
293 Many studies, for example, Fayez and Bazaid (2014); Rais et al. (2013); Aragão et al. (2012);
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294 Bybordi et al. (2010); Siddiqui et al. (2010); Gimeno et al. (2009); Xiao-Hua et al. (2008);
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295 Ashraf and Foolad (2007); Jeong-Jin and Yeon-Sik (2006) have demonstrated that plants tend to
296 accumulate N containing compatible solutes including GB, proline, asparagine, sucrose, glucose,
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297 dimethyl sulphoniopropionate etc. in response to N supplementation under salinity stress (Table
298 5). Among these, proline is particularly known for its key role in stimulating antioxidant defense
system in saline environment which otherwise not capable to protect plants against salinity stress
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299
300 (Koca et al. 2007). Proline is extremely soluble in water and binds with water molecules to forms
301 clusters which are attached to macromolecules, and protect them against salinity-induced
302 oxidative damage (Mittal et al. 2012). Proline being involved in stabilization of membrane
303 structure can enable the plants to maintain plant water status and ionic balance (Gimeno et al.
304 2009), and help to mitigate oxidative damage by scavenging ROS (Ashraf and Foolad 2007).
305 Proline metabolism might also affect the redox potential of plant cells associated with signaling
306 development and leading to plant tolerance to salinity (Heidari et al. 2011). Similarly, N-induced

307 GB synthesis contributes to maintain the integrity of thylakoid and plasma membranes, protects
308 the protein, chlorophyll and photosystem against salinity stress (Tattersall et al. 2009), and thus
309 frequently reverses the damaging effects of salinity on plant metabolism (Rais et al. 2013). Some
310 other studies, for example, Nadian et al. (2012); Gimeno et al. (2009); Ehlting et al. (2007);
311 Shabala and Cuin (2006); Aroiee et al. (2005) have demonstrated that application of N fertilizer
312 to saline environment might help to mitigate the harmful effects of salts on plant growth by
313 enhancing the accumulation of osmolytes which are responsible for the detoxification of ROS
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314 and alleviate the oxidative damage.
315 Accumulation of MDA in plant body increases with salinity which indicates the level of
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316 lipid peroxidation and is used as an important criterion for determining plant adaptation to saline
317 environment (Giannakoula et al. 2008). N nutrition under saline conditions increases the
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318 synthesis of osmoprotectants which improves plant tolerance to salinity as measured by

319 reduction in MDA concentration. Siddiqui et al. (2008) have shown that plants fed with
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320 additional N under saline conditions generally have decreased MDA accumulation. N-induced
321 decline in MDA results from the increased accumulation of N containing compounds which
322 subsequently improves plant adaptation to saline environment by stabilizing the macromolecules,
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323 maintaining ROS balance, and resisting a change in redox potential of plant cells. In conclusion,
324 N-induced accumulation of osmolytes contributes to plant tolerance to salinity by maintaining
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325 membrane integrity, improvement in photosynthetic efficiency, reduction in protein and enzyme
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326 denaturation, stimulation of antioxidant defense system and protection of plant macromolecules
327 against ROS.
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329 Nitrogen forms and salinity tolerance
Plants absorb N principally as NH4+ and/or NO3- (Zhonghua et al. 2011). Plant response to N
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330
331 application under salinity stress varies greatly depending on whether NH4+ and/or NO3- are
332 added to growth medium (Crawford and Forde 2002). There may be a higher sensitivity to
333 salinity in NH4+-fed plants (Leidi et al. 1991), no effect of N form on plant response to salinity
334 stress (Ashraf and Sultana 2000), or more sensitivity in case of NO3--N (Arghavani et al. 2017).
335 These differences in plant response to N nutrition in saline environment have been explained on
336 the basis of absorption and metabolism of NO3- and NH4+ that require different ionic equilibria in
337 which organic and inorganic cations and anions have a part. Several plant species such as

338 Hordeum vulgare L. (Kant et al. 2007), Helianthus annuus L. and Zea mays L. (Rios-Gonzalez et
339 al. 2002); Pisum sativum L. (Frechilla et al. 2001) have shown more salt tolerance with NO3-
340 nutrition in saline environment, other plant species such as Sorghum bicolor L. (de Souza-
341 Miranda et al. 2014); Catharanthus roseus (Zhonghua et al. 2011), Vicia faba L. (Kamel 2012);
342 Solanum lycopersicum L. (Flores et al. 2001) have performed better when growth medium is
343 containing NH4+ plus NO3- in equal concentration while Helianthus annuus L. (Ashraf 1999);
344 Hordeum vulgare L. (Kant et al. 2007); Sorghum bicolor (de Souza Miranda et al. 2016) and
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345 many others exhibited greater response to NH4+ application. In general, plants response to N
346 forms under salinity stress differs greatly depending upon plant species, salt concentration and
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347 composition as well as rate of N application (Table 6, Figure 3).
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NH4+-N and salinity interactions
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349
350 NH4+-fed plants are comparatively less tolerant to salinity than NO3--fed plants. The
underlying mechanisms could be (a) NO3- assimilation takes place primarily in the shoots while
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351
352 NH4+ assimilation in the roots. As roots are in immediate contact with the salt containing growth
353 medium, it is possible that N assimilation in NH4+-fed plants is dislocated by salt ionic effects
ev
354 which would not interfere with shoot-based NO3--N assimilation; (b) in NO3--fed plants, a
355 malate-nitrate shuttle is operative between root and shoot (Lewis et al. 1989). The absence of this
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356 shuttle in NH4+-fed plants could bring about ion translocatory problems which are exacerbated
357 by the uptake of NaCl; (c) in NH4+-fed plants, carbon utilization during N assimilation resulting
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358 in low availability of carbon for root development. Furthermore, higher salt ions availability in
the root medium greatly inhibits carbon metabolism in case of NH4+-fed plants. (Dluzniewska et
On
359
360 al. 2007). Generally, two processes are competing for the energy utilization in roots of NH4+-fed
361 plants; NH4+ assimilation and Na+ exclusion which could be responsible, at least in part, for low
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362 tolerance of NH4+-fed plants in saline environment. High concentration of NH4+ in the growth
363 medium may result in NH4+ toxicity which leads to leaf chlorosis, reduced crop yield, nutrient
364 imbalance, rhizosphere acidification and alteration in plant metabolism. Some other studies, for
365 example Rios-Gonzalez et al. (2002); Frechilla et al. (2001); Lewis et al. (1989) have been
366 observed that NH4+-fed plants operated the metabolic pathways which generated more ROS and
367 produced little beneficial effects on plant tolerance than NO3--fed plants. Ashraf and Sultana

368 (2000) also observed NH4-treated Helianthus annuus L. plants accumulated more Cl- while less
369 K+, Ca2+ and Mg2+ than NO3--fed plants, and are less tolerant to salinity.
370 On the other hand, Fernández-Crespo et al. (2012) have reported that NH4+ supplementation
371 could enhance salt tolerance in Citrus sinensis L. because NH4+ toxicity causes mild stress,
372 leading to stress-induced morphogenetic responses (SIMRs). These responses produce an
373 acclimation stage which provides better protection to plants against succeeding salinity stress.
374 SIMRs initially increases H2O2 generation which serve as a modulator of stress signal and
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375 enhances plant adaptation to salinity stress. Another protective mechanism induced by NH4+
376 against salinity stress is the maintenance of higher K+:Na+ which could result from restricted
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377 uptake and translocation of Na+ and/ or increased Na+ exclusion (de Souza-Miranda et al. 2013).
378 The stimulation of K+ depletion capacity by NH4+ might be associated with plasma membrane
H+-ATPase-mediated higher H+ transport activity which improves plant tolerance to salinity
ee
379
380 (Álvarez-Pizarro et al. 2011). Moreover, NH4+ nutrition enhances the synthesis of osmolytes
which improves salt tolerance through osmotic adjustment and stimulation of antioxidant defense
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381
382 system. In conclusion, NH4+-induced salt tolerance in plants might be attributed to low energy
383 cost of N assimilation, reduced Na+ uptake, higher synthesis of organic osmolytes and regulation
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384 of K+/Na+ homeostasis (Figure 3a).

385
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386 NO3--N and salinity interactions

387 NO3- is the principal form of N used by plants in aerobic growth medium/soil environment.
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388 However, NO3- has to be reduced to NH4+ prior to its incorporation into organic N compounds
using energy. NO3- assimilation uses 20 mol ATP mol-1, whereas 5 mol ATP mol-1 are required
On
389
390 for NH4+ assimilation (Salsac et al. 1987). In spite of high energy requirements, plants use N
391 mostly in the form of NO3- because NH4+ accumulation at higher concentration within the plant
ly
392 body often leads to ion toxicity in plants (Meng et al. 2016). While, NO3- can accumulate in
393 vacuoles that can play a key role in plant nutrition and osmotic adjustment, conferring more salt
394 tolerance than NH4+ (Irshad et al. 2002). Furthermore, NO3-assimilation is metabolically less
395 expensive because it occurs in shoots which is less affected by rhizosphere salts as compared to
396 NH4+ assimilation that occurs in roots. Another mechanism for higher plant tolerance to salinity
397 by NO3--N is its rapid translocation and accumulation in shoot that serves as a signal for the
398 efficient regulation of shoot-root allocation (Crawford 1995). In some studies, however, NO3--

399 grown plants have been found relatively less tolerant to salinity than NH4+-grown plants because
400 Cl- might reduce the NO3- uptake by plants due to antagonistic effect (Kant et al. 2007), NO3-
401 might favor the Na+ uptake and accumulation within the plant cells (Zhonghua et al. 2011), or
402 due to reduction in water use efficiency and carbon assimilation rate (Ashraf 1999) (Figure 3b).
403
404 Combination of NH4+ and NO3--N and salinity interactions
405 The protective role of N against salinity stress is often more effective when both NH4+ and
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406 NO3- are applied in combination to saline environment compared to their sole application. N
407 application with same amounts of NO3- and NH4+ protects the photosynthetic pigments against
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408 salinity stress, leading to high PSII efficiency under saline conditions. The better performance of
409 combined application of NO3- and NH4+ at 50:50 ratio to improve plant growth in saline
environment might be attributed to high photosynthetic efficiency, improved N assimilation,
ee
410
411 reduced ROS generation, decreased specific ion toxicity, balanced ionic accumulation and better
osmotic adjustment (de Souza-Miranda et al. 2014). Some other studies, for example, Miller et
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412
413 al. (2010); Lu and Zhang (2000) assigned it to the regulation of photosynthetic electron transport
414 with minimum generation of ROS under salinity stress. Even, the partial substitution of NO3-
ev
415 with NH4+ in the growth medium can improve plant adaptation to salinity stress because of
416 improved N assimilation, particularly via alternative NH4+ assimilation pathway which reduces
ie
417 the requirement of energy for N assimilation than the sole application of NO3--N (Kant et al.
418 2007). Better plant performance with combined use of NH4+ and NO3- under salinity stress might
w
419 be due to pH maintenance resulting from similar rate of H+ generation and H+ consumption, low
energy cost for N assimilation and improved photosynthetic rate. Zhonghua et al. (2011) have
On
420
421 reported that underlying mechanisms for improved plant growth with combined N forms might
422 be: (a) improved water absorption through osmotic adjustment; (b) antagonism between NH4+
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423 and Na+ or NO3- and Cl- leading to reduced uptake and translocation of salt ions; (c) enhanced
424 synthesis/accumulation of osmolytes and (d) maintenance of ion homeostasis. However, the
425 response of N forms to salinity stress varies widely depending upon many plant as well as soil
426 factors, and the selection of an appropriate N form should be a major concern in N-salinity
427 interaction studies. In summary, NH4+-N is energetically inexpensive but it causes ion toxicity at
428 higher concentration and inhibits the uptake of other ions such as K+, Ca2+ and Mg2+, while NO3-
429 has incremental effect on these ions but it is energetically expensive. It is believed that for most

430 plant species, NO3- is preferred form of N under saline conditions, while a small number of
431 plants prefer NH4+, however mixtures of NH4+ and NO3- at ratio of 50:50 can exert consistent
432 beneficial effects on plant growth and metabolism in saline environment (Figure 3c).
433
434 Conclusion and future prospects

435 Salinity stress causes several metabolic alterations in plants such as reduction in water
436 uptake, disturbance in nutrient balance, specific ion toxicity, increase in ROS generation,
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437 disruption of hormonal balance, inactivation of enzymes, peroxidation of lipids, reduction in
438 chlorophyll synthesis and the damage of photosystem which lead to reduced plant productivity.
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439 Plant adaptation to salinity is a result of different ionic, physiological and biochemical
440 mechanisms such as regulation of ion uptake, translocation and compartmentation, maintenance
ee
441 of plant water status and ionic balance, biosynthesis of osmolytes and enzyme activation.
442 Exposure of plants to elevated salinity levels reduces the N uptake and assimilation, probably
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443 due to direct interaction between salinity and the processes involved in N uptake, utilization or
444 translocation within the plant or via a salinity-induced reduction of the relative growth rate
445 resulting in a lower N demand. A wide discrepancy has been found in plant growth behavior to N
ev
446 nutrition under saline conditions depending upon salt nature and concentration in the root zone,
447 N form applied and plant type. At low to moderate salinity level, increasing supply of N can
ie
448 efficiently reverse the salinity effects on plant growth. At higher level of soil salinization,
w
449 adequate N nutrition partly alleviates the salinity effects but over N fertilization may aggravate
450 the deleterious effects of salinity. Nitrogen is contributed to salt tolerance by regulating ion
On
451 uptake, translocation and distribution, stimulating plant growth and reducing leaf abscission,
452 activating enzymes, maintaining hormonal balance and synthesizing N containing compounds
453 which can contribute to osmotic adjustment, stabilize the cellular structures and scavenging ROS
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454 under saline conditions. The understanding of the N metabolism under salinity stress might be
455 crucial for salt tolerance research, and will be an important research direction for salt stress
456 physiology in future. Since, plant response to N nutrition in saline environment changes with
457 stage of plant growth, emphasizing that such interactions should be studied during the entire life
458 cycle of a plant to find alleviative effect of N against salinity stress at a specific stage of plant
459 development as well as over time.
460

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687 accumulation in two groundnut cultivars (Arachis hypogaea L.) with contrasting salt
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688 tolerance. Afr J Plant Sci. 7:586-592.

689 Renault S, Wolfe S, Markham J, Avila-Sakar G. 2016. Increased resistance to a generalist
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690 herbivore in a salinity-stressed non-halophytic plant. AoB PLANTS 8, plw028;

691 doi:10.1093/aobpla/plw028.
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692 Rios-Gonzalez K, Erdei L, Herman S. 2002. The activity of antioxidant enzymes in maize and
sunflower seedlings as affected by salinity and different nitrogen sources. Plant Sci.
On
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694 162:923-930.
695 Rontein D, Basset G, Hanson AD. 2002. Metabolic engineering of osmoprotectants
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696 accumulation in plants. Metab Eng. 4:49-56.

697 Salsac L, Chaillou S, Morot-Gaudry JF, Lesaint C, Jolivet E. 1987. Nitrate and ammonium
698 nutrition in plants. Plant Physiol Biochem. 25:805-812.
699 Serrao MG, Menino MR, Martins JC, Castanheira N, Lourenco ME, Januario I, Fernandes ML,
700 Goncalves MC. 2012. Mineral leaf composition of sweet sorghum in relation to biomass and
701 yields under different nitrogen and salinity conditions. Commun Soil Sci Plant Anal.
702 43:2376-2388.

703 Shabala S, Cuin TA. 2006. Osmoregulation versus osmoprotection: re-evaluating the role of
704 compatible solutes. In: JT. da Silva (Eds.), Floriculture, ornamental and plant biotechnology,
705 advances and topical issues, Global Science Books, Tokyo, Japan, pp. 405-416.
706 Shawer SS. 2014. Interaction effect between nitrate and chloride on yield, uptake and
707 translocation of nutrients in cucumber plant under nutrient film technique (NFT). Middle
708 East J Agri Res. 3:42-48.
709 Siddiqui MH, Mohammad F, Khan MN, Al-Whaibi MH, Bahkali AH. 2010. Nitrogen in relation
Fo
710 to photosynthetic capacity and accumulation of osmoprotectant and nutrients in Brassica
711 genotypes grown under salt stress. Agri Sci China. 9:671-680.
rP
712 Siddiqui MH, Khan MN, Mohammad F, Khan MMA. 2008. Role of nitrogen and gibberellin
713 (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica
juncea L. under salt stress. J Agron Crop Sci. 194:214-224.
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714
715 Soussi M, Ocan A, Lluch C. 1998. Effects of salt stress on growth, photosynthesis and nitrogen
fixation in chickpea (Cicer arietinum L.). J Exp Bot. 49:1329-1337.
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716
717 Tabatabaei SJ, Fakhrzad F. 2008. Foliar and soil application of potassium nitrate affects the
718 tolerance of salinity and canopy growth of perennial ryegrass (Lolium perenne var
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719 ‘Boulevard’). Am J Agri Biol Sci. 3:544-550.

720 Tabatabaei SJ. 2006. Effects of salinity and N on the growth, photosynthesis and N status of
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721 olive (Olea europaea L.) trees. Sci. Horti. 108:432-438.

722 Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM. 2016. Effect of salt stress
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723 on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in
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Fo
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ee
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ev
ie
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On
ly

Table 1. Salinity stress effects and mechanisms in plants.

Plant species Treatment Effect Mechanism Referenc
e
Chickpea
(Cicer arietinum L.)
Fo
Seedlings of 245 lines of chickpea, 186 lines
of desi type while 59 lines of kabuli type,
were exposed to 0 and 40 mM NaCl.
On an average, salinity increased Na+ by 203% while reduced K+/Na+ ratio 84%, plant growth rate
20%, plant height 15%, shoot biomass 28%, seed number 16% and seed yield 32% compared to
control.
Na+ toxicity Atieno et
al. (2017)
rP
Okra Two cultivars (Chinese green and Chinese 18% salinity stress reduced net photosynthetic rate by 84 and 80%, stomatal conductance 95 and Osmotic stress Azeem et
(Abelmoschus esculentus L.) red) were subjected to salt stress (0%, 6%, 83%, transpiration 72 and 85%, water use efficiency 47 and 17%, water content 38 and 40%, plant al. (2017)
12% and 18%) with equal proportions of height 83 and 87%, and fresh weight 91 and 88% in Chinese green and Chinese red, respectively
NaCl and CaCl2 in Hoagland’s nutrient compared to control.
ee
solution.
Indian mustard, Four weeks old plants were grown in NaCl decreased total biomass 24 and 35%, leaf protein 16 and 55%, chlorophyll 11 and 27%, Ion toxicity and Renault et
(Brassica juncea) hydroponics at 0, 50 and 100 mM NaCl for transpiration 2 and 11%, N 8 and 24%, K 56 and 75%, Mg2+ 20 and 38%, Ca2+ 17 and 41% while nutrient al. (2016)
rR
two weeks. increased Na+ 358- and 650-folds, proline 2.6- and 11.9-folds, Cu 37 and 87%, Fe 3 and 8%, Mn 27 imbalance.
and 67%, Zn 34 and 75% with 50 and 100 mM NaCl, respectively compared to control.
Common bean Bean plants of two genotypes, Tema and 200 mM NaCl increased leaf Na+ by 5- and 7-folds, catalase activity 4- and 2-folds, glutathione Oxidative stress Taïbi et al.
(Phaseolus vulgaris) Djadida, were sown for 7 days at 4 levels of reductase 60 and 20%, ascorbate 33 and 26%, flavonoids 47 and 70% while decreased shoot dry and ion toxicity (2016)
ev
NaCl (0, 50, 100 and 200 mM) in a mixture weight 30 and 27%, root dry weight 59 and 61%, Chlorophyll-b 33 and 43%, carotenoids 18 and
of commercial peat and vermiculite. 19%, and K+ 32 and 35% in Tema and Djadida, respectively compared to control.
Cotton Plants were exposed to 0, 100, 150 and 200 200 mM NaCl increased leaf Cl- by 24- and 3-folds, leaf Na+ 50 and 104%, while decreased leaf K+ Ion toxicity and Hassan et
(Gossypium hirsutum L.)
Groundnut
(Arachis hypogaea L.)
mM NaCl for 3 weeks by irrigating with
saline water after every 2nd day.
Seeds of 2 cultivars, K-134 and JL-24 were
germinated at 4 levels of NaCl (0, 50, 100
and 150 mM) and grown for 9 days.
control.
iew
51 and 22%, stomatal conductance 32 and 45% in FDH 171 and FDH 786, respectively compared to
At 150 mM NaCl, free proline content were increased by 3- and 2.6-folds, soluble sugars 3.3- and
2.5-folds, free amino acids 2- and 1.8-folds, total amino acids 2.1- and 1.8-folds, total polyamines
1.6- and 1.4-folds, glycine betaine 1.8- and 1.5-folds in K-134 and JL-24, respectively compared to
osmotic stress
Osmotic
oxidative stress
and
al. (2014)
Ranganaya
kulu et al.
(2013)
On
control.
Barley 15-day-old seedlings of 4 cultivars Dasht, 100 mM NaCl increased leaf Na+ by 99% in Sahand, 73% in Sahra, 31% in Dasht and 15% in Lisivy Specific ion Yousufinia
(Hordeum vulgare L.) Lisivy, Sahra and Sahand were exposed to 2 while decreased leaf K+ by 16% in Dasht and Lisivy, 25% in Sahra and 36% in Sahand with a toxicity et al.
levels of NaCl (0 and 100 mM) for 10 days. reduction in K+:Na+ ratio by 36% in Dasht, 26% in Lisivy, 55% in Sahra and 72% in Sahand (2013)
ly
compared to control.
Pea 17-day-old seedlings were exposed to 0 and 80 mM NaCl increased Leaf Na+ by 120-folds, root Na+ 26-folds, xylem sap Na+ 4.1-folds, leaf Specific ion Pandolfia et
(Pisum sativum L.) 80 mM NaCl for 14 days. osmolality 97%, root osmolality 59% but decreased leaf K+ 65%, root K+ 59%, stomatal toxicity and al. (2012)
conductance 82% and SPAD value 27% compared to control. osmotic stress
Cowpea 4-day-old seedlings of 2 cultivars; Pérola and 100 mM NaCl increased Na by 77 and 78%, electrolyte leakage 65 and 58% while reduced K+ by 7
+
Specific ion Maia et al.
(Vigna unguiculata L.) Pitiúba were shifted to paper and moistened and 11%, K+:Na+ 82 and 80%, lipid peroxidation 28 and 30%, relative water content 2 and 6%, toxicity (2010)
with deionized water (control) or 100 mM superoxide dismutase 12 and 26%, peroxidase 47 and 55%, catalase 7 and 58% but increased
NaCl solution for 2 days. ascorbate peroxidase activity by 12 and 26% in Perola and Pitiuba, respectively compared to control.
Wheat Two wheat genotypes (Sardari and Alvand) superoxide dismutase activities were increased by 66, 180, 233 and 226% in Sardari while 87, 8.7, Oxidative stress Esfandiari
(Triticum aestivum L.) were grown in Hoagland’s solution salinized no effect and 8.7% in Alvand; catalase by 800, 366, 283 and 200% in Sardari while 80, 40, 25 and et al.
with 0, 50, 100, 150 and 200 mM NaCl for 85% in Alvand; glutathione reductase first increased by 27% then decreased by 18, 48 and 47% in (2007)
10 days. Sardari while decreased by 43, 56, 63 and 80% in Alvand; malondialdehyde first decreased by 7%
then increased by 22, 4 and 7% in Sardari while first decreased by 6% then increased by 41, 72 and
153% in Alvand with 50, 100, 150 and 200 mM NaCl, respectively over control.

Table 2. Nitrogen-mediated mitigation of specific ion toxicity in plants under salinity stress.
Plant species
Soybean
Fo
Treatment
Plants were grown at 50 and 100 mmol L -1
Effect
In Glycine max, leaf Cl -
/NO3- ratios
were decreased by 87% in Lee 68; 38
Mechanism
NO3- supply increased NO3- while
Reference
Guo et al. (2017)
(Glycine max)
(Glycine soja) supply.
rP
NaCl with 0.75, 7.5 and 15 mmol L-1 NO3- and 56% in Jackson, while in Glycine soja, 75 and 87% in BB52; 73 and
83% in N23227 at 100 mmol L-1 NaCl with 7.5 and 15 mmol L-1 NO3-,
respectively compared to 100 mmol L-1 NaCl+0.75 mmol L-1 NO3-.
decreased Cl- contents within plants,
leading to lower Cl-/NO3- ratios.
ee
Maize Plants were grown for 23 days at 4 NaCl With increasing NaCl stress, NO3- uptake was decreased from 150 to 80 Cl-/NO3- antagonism and Cl- Hutsch et al. (2016)
(Zea mays L.) levels (control, 50, 100, 150 mM) with N at mg plant-1, Cl- uptake was increased from 90 to 120 mg plant-1. exclusion ability of maize.
2 mM Ca(NO3)2. Plants in half of the pots Correlation between NO3- and Cl- uptake was r = –0.63, r2 = 40%. At 100
rR
were treated with additional 1 mM NH4NO3 and 150 mM NaCl, net root-to-shoot translocation of total N was
2 days after start of the NaCl application. decreased by 16 and 20%, which were improved by 25 and 30% with
additional N.
Mustard Plants were grown in full strength Hoagland N fertilization reduced Na+ concentration by 12, 52 and 75% while Cl- by N-induced antagonistic and dilution Iqbal et al. (2015)
ev
(Brassica juncea L.) solution at 0 and 100 mM NaCl with 0, 5, 16, 39 and 60% with 5, 10 and 20 mM N, respectively at 100 mM NaCl effects.
10 and 20 mM NO3- as KNO3 for 30 days. compared to NaCl treated plants without N.
French marigolds Plants were raised at four salinity levels At 6.0 mmohs cm-1 salinity, shoot Na+ concentration was enhanced by 15 NH4+ decreased K+ uptake but Bahmanzadegan
(Tageta patula) (0.49, 2.0, 4.0, 6.0 and 8.0 mmohs cm-1) and and 38% while shoot K+ was decreased by 19 and 21% with 15 and 30 g enhanced Na+ while NO3- caused and Aboutalebi
Alfalfa
(Medicago sativa L.)
3 NH4NO3 levels (0, 15 and 30 g L-1).
Four levels of N (0, 30, 60 and 90 kg ha-1)
as urea were applied at 4-6 leaf stage while
3 levels of NaCl (0, 100 and 200 mM) were
imposed 7 day after N application.
iew
L-1 NH4NO3, respectively compared to salt stressed plants without N.
Salinity caused an increase of 100 and 187% in Na+, 60 and 100% in
Ca2+, no effect on K+ with a reduction of 51 and 65% in K+:Na+ ratio in
leaves. N fertilization had no significant effect on Na+, Ca2+ as well as K+
uptake and accumulation under salt stress.
higher Na+ uptake.
Salinity was the dominant factor
which governed plant growth and
ion uptake at higher salinity levels.
(2013)
Abbasi-Shahmersi,
and Ebadi (2012)
Citrange Carrizo
(Citrus sinensis L.)
Sunflower
(Helianthus annuus L.) and
3-month-old plants were grown at 90 mM
NaCl with 5 mM (NH4)2SO4 for 14 days.
Seeds were sown under non saline (ECiw 0.5
dS m-1) conditions, and irrigation with
On
Salt stressed NH4+-fed plants accumulated 40% less Cl- and displayed
30% more healthy leaves than salt stressed plants without NH4+-N.
In salt stressed plants sprayed with KNO3, leaf NO3- concentration was
increased by 17 and 20% in sunflower, 16 and 17% in safflower at ECiw
Inhibition of chloride channel-like
proteins which reduced Cl- toxicity.
KNO3 increased leaf
concentration with a subsequent
NO3-
Fernández-Crespo
et al. (2012)
Jabeen and Ahmad
(2011)
Safflower
(Carthamus tinctorius L.)
Olive
saline water (ECiw 4.8 and 8.6 dS m-1) was
started at 3 leaf stage. KNO3 was sprayed @
250 ppm. Data were recorded at flowering
stage.
Experiment consisted of 4 levels of NaCl 0,
of 4.8 and 8.6 dS m-1, respectively with a subsequent reduction in leaf Cl-
concentration of 42% and 45% in sunflower and 38% and 42% in
safflower as compared to saline water irrigation without KNO3.
Under saline conditions, increasing N up to 200 mg l-1 increased leaf NO3-

ly
decrease in Cl- and offset its toxic
effects under saline water irrigation.
N-induced alleviation of specific ion Tabatabaei (2006)

(Olea europaea L.) 50, 100, 150 mM and 3 levels of N 100, concentration by 176% in Mission cultivar, 305% in Manzanillo and 28- toxicity.
200, 300 mg 1-1 as NH4NO3. NaCl and N folds in Zard with a subsequent reduction in leaf Na+ accumulation by
treatments were started when plants were 20% in Mission, 8% in Manzanillo and 18% in Zard compared to 100
25-30 cm in height and continued for 12 mg L-1 N under salt stress.
months.
Navelina orange scion One-year-old potted plants were irrigated 3 NO3- addition at 25 mM NaCl:CaCl2 caused a decrease of 50 and 60% NO3- reduced Cl- concentration, Iglesias et al. (2004)
(Citrus sinensis) grafted onto times per week with saline water having 25 but increase of 7% in Cl- concentration; a decrease of 38, 28 and 55% in reduced leaf abscission which
C. citrange, C. macrophylla mM NaCl: CaCl2 (15:1) with or without 10 leaf abscission; an increase of 23, 40 and 345% in photosynthetic rate in resulted in Cl- dilution, and thus
or C. mandarin rootstock. mM NO3 for 60 days. C. citrange, C. macrophylla and C. mandarin, respectively than without alleviated Cl- toxicity.

N.
Strawberry Nutrient solution alone (C); C+5 mM N content were increased by 15, 38 and 57% in Oso Grande and 17, 28 Supplementary Ca(NO3)2 and/ or Kaya et al. (2003)
(Fragaria ananassa) Ca(NO3)2 + 5 mM KNO3; C + 35 mM and 45% in Camarosa with a subsequent Na+ reduction by 14, 16 and KNO3 could achieve full mitigation
(2 cultivars, Oso Grande and NaCl (C + S); C + S + 5 mM Ca(NO3)2; C 30% in Oso Grande and 20, 24 and 41% in Camarosa with KNO3, of salt stress through reducing Na+
Camarosa) + S + 5 mM KNO3 and C + S + 5 mM Ca(NO3)2 and KNO3+Ca(NO3)2, respectively compared to salt stressed ion toxicity.
Ca(NO3)2 + 5mM KNO3. plants without KNO3 and/or Ca(NO3).
Treatment
Fo
Table 3. Nitrogen-mediated maintenance of nutrient balance in plants under salinity stress.
Plant species Effect Mechanism Reference
Cotton
(Gossypium hirsutum L.) rP
Ten treatments comprising of N, P, K and Zn
with and without farm yard manure at 10 dS m-1
electrical conductivity.
-1 +
100 mg N kg soil as urea decreased leaf Na by 43% while
improved K+ 32%, K+:Na+ 133%, P 21%, Zn 33%, plant height
50%, bolls plant-1 60% compared to salt stressed plants without
N-induced improvement in ionic
balance.
Khan et al. (2016)
Rice
(Oryza sativa) ee
Plants were grown in saline soil having 20.5 dS
m-1 EC by adding compost at 5 and 10 tons fed-1
additional N.
Under salinity stress, N @ 70 kg fed-1 with 5 ton fed-1 compost
increased N by 31 and 40%, P 42 and 53%, K 29 and 31%, Fe 30
Maintenance of nutrient balance due
to increased internal nutrient demand
Zaki (2016)
rR
and N at 35, 50 and 70 kg N fed-1. and 41% and Mn 40 and 60% in straw and grain, respectively resulted from N-induced improved
compared to lower N level (35 kg N fed-1 with 5 ton fed-1 compost). plant growth.
Cucumber Plants were grown for 84 days at 0, 4, 8 and 12 N addition caused an increase of 31, 59 and 76% in shoot N NO3- alleviated Cl- induced nutrient Shawer (2014)
(Cucumis sativus L.) mM NO3- added as KNO3; and 0, 5, 10 and 15 content; 13 and 35% in shoot P content; 26, 54 and 68% in shoot K imbalance by reducing competition
ev
mM Cl- added as KCl at (0.25) Hoagland content with a reduction of 6, 11 and 14% in shoot Cl- content by 4, between nutrients for specific
nutrient solution using nutrient film technique. 8 and 12 mM NO3--N, respectively compared to 15 mM Cl- without absorption sites in roots.
NO3--N.
iew
Sugarcane Plants were grown till maturity at 4 salinity At 8 dS m-1 salinity, N @ 400 kg urea ha-1 reduced leaf Na+ N alleviated the salinity effects by Nadian et al. (2012)
(Saccharum officinarum L) levels (1, 2, 4 and 8 dS m-1) and 3 N fertilizer concentration by 92% while increased leaf K+ concentration 24% reducing Na+ and increasing K+
rates (200, 300 and 400 kg urea ha-1). compared to lower N level (200 kg urea ha-1) at the same salinity. accumulation under salinity stress.
Sweet sorghum Plants were grown for 3 months at 3 Na levels N at 13.7, 27.4 and 41.1 g m-2 increased leaf P concentration by 37, N nutrition mitigated nutrient Serrao et al. (2012)
(Sorghum bicolor L.) (158, 1162 and 2166 g m-2 as NaCl) and 4 N 32 and 37% at 1162 and 11, 16 and 16% at 2166 g m-2 Na while disorders, increased the leaf contents
levels (0, 13.7, 27.4 and 41.1 g m-2 as NH4NO3). leaf Mg2+ 29, 65 and 53% at 1162 and 11, 39 and 56% at 2166 g m-2 of the various major elements with
Canola 8-day-old plants were grown for 21 days in full

On
Na with an increase in stem yield by 85, 131 and 98 at 1162 and 46,
72 and 52% at 2166 g m-2 Na compared to N0 at same salinity
levels.
At 120 mM NaCl, NO3--fed plants accumulated 19% less Na+, 50%
the consequent improvement in plant
productivity under saline conditions.
Salinity-induced nutrient imbalance Bybordi et al.

(Brassica napus L.)
Sorghum
strength Hoagland nutrient solution at 0, 50, 100
and 150 mM NaCl, and 10 mM NO3- or NH4+
applied as KNO3 or (NH4)2SO4.
-1
Saline water of EC 8 dS m was used with 8 N
less Cl-, 19% more K+, 3% more N, 58% more Ca2+ in shoots while
35% more Na+, 3% less Cl-, 44% more K+, 2% more N and 53%
more Ca2+ in roots compared to NH4+-fed plants at same salinity
level.
-1 -1
160 kg N ha at 8 dS m EC increased N by 27 and 30%; K 12 +
ly
was corrected by NO3- nutrition
through inhibiting the uptake of Na+
and Cl- while improving K+ and
Ca2+.
N interacted with Na+ and Cl-,
(2010)
Esmaili et al. (2008)

(Sorghum bicolor L.) levels; no N-fertilizers, basal fertilizer without and 10%; Ca2+ 16 and 13%; Mg2+ 15 and 10% with a subsequent reduced their uptake, and alleviated
N, urea and NH4NO3 treatments, each consisted reduction in Cl- by 10 and 15%; Na+ 24 and 28% with urea and salinity-induced nutritional
of 3 levels including 114, 137 and 160 kg N ha- NH4NO3, respectively compared to salt treated plants without N. disorders.
1
.

Ryegrass Plants were grown at 0 and 60 mM NaCl with 0, KNO3 at 60 mM NaCl increased leaf K+:Na+ by 22, 64 and 39% in KNO3 either as foliar or soil Tabatabaei and
(Lolium perenne) 5, 10 and 15 mM KNO3. KNO3 was applied foliar; 24, 51 and 27% in soil, NO3- 14, 71% and no effect in foliar; application involved in alleviating Fakhrzad (2008)
either as soil application or foliar spray. 7, 80 and 7% in soil with a reduction in Cl- by no effect, 14 and salt-induced nutrient imbalance by
159% in foliar; 166, 366% and no effect in soil application by 5, 10 increasing K+:Na+ and NO3- while
and 15 mM KNO3, respectively compared to salt stressed plants reducing Na+ and Cl- concentrations.
without N.
Pea
(Pisum sativum L.)
Fo
Plants were grown at 0 or 90 mM NaCl and 5
mM mineral N as NO3-, NH4+, or NH4NO3 or N
by BNF (Rhizobium leguminosarum) for 15, 30,
After 60 days of salt exposure, leaf Na+ concentration was
increased by 3.3, 5.5 and 4.7 folds, Cl- by 162, 625 and 225% while
K+ was increased by 31% but decreased by 47 and 62% with NO3-,
NH4+ and NH4NO3-N, respectively compared to control.
NO3--fed plants were more efficient
to inhibit Na+ and Cl- uptake but
enhanced K+ and thus mitigated
Figueira,
Caldeira (2005)
and
rP
45 and 60 day after treatment completion. salinity-induced nutrient imbalance.
Guava 11-month-old plants were grown for 10 weeks 15 mM Ca(NO3)2 decreased Na+ concentration by 65 and 76%, Cl- Enhanced supply of Ca2+ and NO3- Ebert et al. (2002)
(Psidium guajava L.) at 30 and 60 mM NaCl by supplying 0, 5, 10 32 and 33% while increased N by 246 and 114%, Ca2+ 88 and restricted the uptake of Na+ and Cl-
and 15 mM Ca(NO3)2. 220% and K+ 213 and 118% in new leaves at 30 and 60 mM NaCl, and alleviated the salinity-induced
ee
respectively compared to NaCl treated plants without Ca(NO3)2. nutrient imbalance.
Treatment rR
Table 4. Nitrogen-mediated adjustment of osmotic stress in plants under salinity stress.
Plant species Effect Mechanism Reference
ev
-1 -1
Pistachio Plants were grown at 0, 800, 1600 and 2400 mg At 2400 mg NaCl kg soil, N @ 180 mg kg soil increased proline by N-induced increase in proline, Nasab et al.
(Pistacia vera L.) NaCl kg-1 soil with 0, 60, 120, and 180 mg N kg-1 15%, reducing sugar 10%, shoot Ca2+ 47%, root Ca2+ 14%, shoot Mg2+ reducing sugars and Ca2+ improved (2014)
soil as urea. 25% and root Mg2+ 18% compared to 0 N at same salinity level. the osmotic adaptation.
Faba beans
(Vicia faba L.)
Plants were irrigated with mixture of tap and sea
water at 5, 10, 15 and 20% seawater (v:v) and
treated with 5 mM KNO3 or 5mM (NH4)2SO4.
Plants were grown till flowering stage.
iew
Plants irrigated with 20% seawater + N, accumulated 63 and 23%
more Ca2+, 14% more soluble sugars, 22 and 3% more water content
with KNO3 and (NH4)2SO4, respectively, while 17% more K+ with
KNO3, 174% more Na+ and 25% more SO4- with (NH4)2SO4 in shoots
as compared to 20% seawater without N.
N-induced osmotic readjustment
under seawater irrigation was mainly
attributed to changes in ion fluxes
than the synthesis of compatible
solutes.
Kamel (2012)
Psyllium
(Plantago ovata F.)
Seedlings were grown for 30 days in solution
containing N as (NH4)2SO4 and Ca(NO3)2 or 1/2
NH4+ and 1/2 NO3- with 0, 100 and 200 mM NaCl. On
Application of N in mixed form at 200 mM NaCl increased soluble
carbohydrates by 112%, proline by 6-folds while soluble proteins were
decreased by 18% compared to salt treated plants without N.
Osmotic adjustment through N-
induced synthesis of proline and
soluble carbohydrates.
Heidari et al.
(2011)
ly
Catharanthus roseus Plant were grown for two weeks with 6 mM N The combined N forms under saline conditions decreased leaf Na+ by Osmotic adjustment, reduction in ion Zhonghua et
either in the form of NO3- or NH4+, or 3 mM NO3- + 34%, increased NH4+ by 20%, relative water content 9%, gas toxicity, decreased transpiration rates al. (2011)
3 mM NH4+ with and without 200 mM NaCl. exchange 383%, leaf photosynthesis 183%, glucose 102%, sucrose and well-kept water relations.
130%, proline 23%, glycine 14% compared to salt stressed plants with
NO3- only.
Sunflower Plants were grown for 20 days at 0 and 150 mM Optimum level of KNO3 to alleviate adverse effects of salinity was Foliarly applied KNO3 involved in Akram, and
(Helianthus annuus L.) NaCl with different KNO3 levels (no spray, spray found to be 1% K+ and 1.6% NO3- which improved net CO2 osmotic adjustment and stomatal Ashraf (2009)
of water + 0.1% Tween 20 solution, 0.5% K+ + assimilation by 78%, stomatal conductance 33%, leaf osmotic regulation, thereby maintaining high
0.8% NO3-, 1% K+ + 1.6% NO3-, 1.5% K+ + 2.4% potential 25%, leaf turgor potential 11%, water use efficiency 62%, tissue water content in stressful
NO3- and 2% K+ + 3.2% NO3- in 0.1% Tween 20 leaf K+ 16% and leaf K+:Na+ ratio 21% as compared to salt treatment environments.
solution). without KNO3.
Thellungiella Seedlings were grown for 1-2 weeks at 0 and 100 Plants at 1.0 mM N+100 mM NaCl had a higher content of N-induced synthesis of proline Tattersall et
salsuginea mM NaCI supplied with 0.1 or 1.0 mM N. nitrogenous solutes, particularly proline by 6.3-folds than in seedlings helped to restore cellular osmotic al. (2009)
grown with low N (0.1 mM) at the same salinity level. balance in saline environment.

Durum wheat Plants were grown in hydroponics at 0 and 100 10 mM NO3- increased proline by 74% and 10.8-folds, serine 2.2- and N containing compounds could serve Carillo et al.
(Triticum durum mM NaCl with 0, 0.1, 1 or 10 mM NO3- as KNO3. 2.18-folds, asparagine 13- and 11-folds, soluble proteins 2.02- and as osmolytes to balance water (2005)
Desf.) 1.46-fold, glycine betaine 3.75- and 2.63-folds in shoot and root, potential within the cell.
respectively at 100 mM NaCl compared to NaCl stressed plants
without NO3-.
Mungbean
(Vigna radiata L.)
Fo
Plants were grown in soil with 13.3, 40 and 60 kg
N ha-1. 100 ml of 75 mM NaCl solution was
applied at 3-day intervals and continued till
N application @ 60 kg ha-1 at 75 mM NaCl caused a reduction of 31%
in leaf Na+ with an increase of 15% in leaf Ca2+ and 19% in K+, 3.82%
in relative water content, 16% in exudation rate and 23% in leaf water
N-induced accumulation
inorganic ions and soluble proteins
in leaves contributed to osmotic
of Kabir et al.
(2005)
rP
maturity. Measurements were made 30 days after potential compared to lower N levels at same salinity level. adjustment under saline conditions.
treatment.
ee
rR
Table 5. Nitrogen-mediated amelioration of oxidative damage in plants under salinity stress.
Plant species Treatment Effect ev Mechanism Reference
Barley
(Hordeum vulgare L.)
Plants were grown at 50, 100 and 150 mM NaCl, with
10 mM KNO3 for 2 weeks. iew
KNO3 at 150 mM NaCl caused a decrease of 20% in leaf Na+, 58% in leaf
Na+:K+, 20% in malondialdehyde and 6% in total antioxidant activity with
a subsequent increase of 71% and 64% in chlorophyll a and b, 84% in
carotenoids, 89% in leaf K+ compared to salt stressed plants without
Protection against oxidative stress
through synthesizing N containing
compounds.
Fayez and
Bazaid
(2014)
On
KNO3.
Mustard Plants were grown for 30 days in soil consisting of peat Combined use of N and S caused 30-44% more proline, 38-81% higher N and S regulated the formation of Rais et al.
(Brassica juncea L.) and compost (4:1, w/w) and mixed with sand (3:1, chlorophyll fluorescence, 157-290% higher chlorophyll content, 105-127% osmolytes which involved in (2013)
w/w). Plants were treated with 100 mM NaCl with and more N accumulation, 156-200% more nitrate reductase activity and 225- osmotic adjustment and protected
without N or/and S at 100 mg kg-1 soil.
ly
275% greater dry mass compared to salt stressed plants without N or S. plants against oxidative damage.
Barbados nut 23-day-old plants were grown at 2 NO3- levels; 1 and N-NO3- supply under salt stress increased net NO3- uptake by 250%, leaf NO3- assimilatory reduction and Aragão et al.
(Jatropha curcas) 10 mM as KNO3 and Ca(NO3)2 and 2 NaCl levels (0 CO2 assimilation rate 57%, stomatal conductance 43%, carboxylation NH4+ assimilation in chloroplast (2012)
and 100 mM). Measurements were taken 10 days after instantaneous efficiency 104%, total free amino acid 10% while decreased provide a sink for electrons, leading
treatments completion. electrolyte leakage by 12% compared to salt stressed plants without N. to reduced photo-damage
Canola Plants were grown at 0 and 200 mM NaCl with 0:100, At 75:25 NH4+:NO3- ratios, plants showed 33% and 28% higher catalase, NH4+ ion may represent a stress Bybordi et
(Brassica napus L.) 75:25, 50:50 and 25:75 ratios of NO3- and NH4+. 22% and 92% higher glutathione reductase and 133% and 48% higher signal that triggers the activation of al. (2010)
glutathione S-Transferase activities in leaves and roots, respectively as antioxidant enzymes.
compared to 0:100 NH4+:NO3- ratios.
Mustard 14-day-old seedlings differing in salinity tolerance The synthesis of proline and glycine betaine was increased by 128 and N-containing compounds help to Siddiqui et
(Brassica juncea L.) were grown at 2 NaCl levels (0 and 90 mM) and 5 N 106%, in sensitive while 135 and 109% in tolerant genotypes at 90 mmol stabilize sub-cellular structures al. (2010)
concentrations (0, 30, 60, 90 and 120 mg kg-1 sand). L-1 NaCl + 60 mg N kg-1 sand as compared to respective control. against oxidative damage.
Fino lemon 2-year-old plants grafted on salt tolerant and salt N fertilization via soil solution had beneficial effects on salinity tolerance, N-induced accumulation of proline, Gimeno et
(Citrus limon Burm.) sensitive rootstocks were irrigated for 12 weeks with particularly in salt sensitive rootstocks where N decreased leaf Na+ by quaternary ammonium compounds al. (2009)

complete nutrient solution containing 0 or 50 mM 59%, leaf Cl- 54% but improved leaf K+ 16%, proline 27% and quaternary and K+ contributed to minimizing
NaCl with 10 mM KNO3, or 1% KNO3 foliar spray. ammonium compounds 23% compared to NaCl stress without additional oxidative and/or osmotic stress.
N.
Indian mustard Plants were grown for 50 days at control, 100 mM Combined application of N and GA3 had maximum alleviating effect on N-containing compounds lowered Siddiqui et
(Brassica juncea L.) NaCl, 40 mg N kg-1 sand (in 2 splits), 10-5 M GA3 salt stress by increasing proline 57%, glycine betaine 44%, K+ 74% with a the generation of free radicals and al. (2008)
(spray), 100 mM NaCl + 40 mg N kg-1 sand, 100 mM decrease of 50% in malondialdehyde, 42% in electrolyte leakage and 35% reduced lipid peroxidation linked
Jerusalem Artichoke Fo
NaCl + 10-5 M GA3, 100 mM NaCl + 40 mg N kg-1
sand + 10-5 M GA3.
At 3rd leaf, uniform sized slices were exposed to 0, 10
in Na+ accumulation compared to NaCl without N and/or GA3.
N with 25% seawater decreased Na+ by 24%, Cl- 15%, malondialdehyde

membrane damage under salt
stress.
N-induced activation of antioxidant Xiao-Hua et
rP
(Helianthus tuberosus) and 25% seawater with and without 7.5 mmol N L-1 as 12%, electrolyte leakage 8% while increased K+ 18%, proline 32%, soluble enzymes and increased synthesis of al. (2008)
NaNO3. Measurements were made after 4, 8 and 12 sugar 45%, catalase 23%, superoxide dismutase 33% and peroxidase 21% osmolytes under seawater
days of treatment completion. in aerial plant parts compared to 25% seawater without N. irrigation.
Soybean Seedlings were transferred into N-free (control) and N- At 100 mM NaCl, superoxide dismutase (SOD)/ascorbate peroxidase NH4NO3-supplied plants were Jeong-Jin
ee
(Glycine max) treatment group (NH4NO3-N, KNO3-N @ 5 and 10 (APX) ratio was increased by 212 and 35% with 5 and 10 mM KNO3 better able to effective removal of and Yeon-
mM) and received modified McKnight's solution of while decreased by 16 and 28% with 5 and 10 mM NH4NO3. At 150 mM oxidative products through Sik (2006)
100 ml having 0, 50, 100 or 150 mM NaCl daily. NaCl, SOD/APX ratio was decreased by 26% and 27% with 5 and 10 mM increasing the balanced activity of
Measurements were taken 12 days after treatment. KNO3, while decreased by 34% and 8% with 5 and 10 mM NH4NO3, SOD and APX in salt environment.
Wheat
(Triticum aestivum L.)
17-day-old seedlings were grown in 0.2 strength
Hoagland solution salinized with 300 mM NaCl with
N-deficient, 3 mM NO3- or 3 mM NH4+. Plants were
rR
respectively.
NO3- or NH4+ nutrition produced 4-50% more chlorophyll-a, 12-55% more
chlorophyll-b, 2-30% more carotenoids, 13-19% more glutathione
N-induced plant tolerance to
salinity was correlated with the
Polesskaya
et al. (2006)
ev
reductase activity while a reduction of 34-41% in SOD, 5-10% peroxidase activation of antioxidant enzymes,
harvested 3 days after treatment completion. and 7.6-27% in catalase activities compared to salt stressed N-deficient accumulation of chlorophyll and
plants. carotenoids.
Table 6. Nitrogen forms and plant adaptation to saline environment. iew

On
Plant species Treatment Effect Mechanism Reference
Kentucky bluegrass Three salinity levels (0, 40 and 80 mM NaCl) 80 mM NaCl caused a reduction of 48, 57 and 63% in dry weight; 35, Effects of increasing NH4+
on the Arghavani et al.
(Poa pratensis L.) and three NO3-/NH4+ ratios (6/0.5, 6/1 and 6/2) 50 and 57% in turf quality; 20, 30 and 45% in K+ concentration while decreased K+ content and lower (2017)
were applied in nutrient solutions. an increase of 800, 850 and 1050% in Na+ concentration with 6/0.5, K+:Na+ ratio.
Rice
(Oryza sativa L.)
Sorghum
Two N forms – NH4NO3 and urea with three N
levels 1.4, 2.1 and 2.8 mM were applied to
Yoshida solution salinized with 113 mM
NaCl.
Plants were grown at 75 mM NaCl with 5
6/1 and 6/2 NO3-:NH4+ ratios compared to control.
In Cuom cultivar, urea produced 400 and 100% higher dry weight, 290
and 60% root length, 84 and 71% SPAD value, 85 and 64% leaf area,
475 and 67% N use efficiency at 1.4 and 2.1 mM N, respectively than
NH4NO3.
Decrease in leaf area and shoot dry mass of 0:100 N-fed stressed
ly
Urea required less energy for
assimilation than nitrate which
firstly reduced to ammonium.
Improved plant photosynthetic

Nhung
(2017)
de Souza
et al.
(Sorghum bicolor L.) NO3-:NH4+ ratios (100:0, 75:25, 50:50, 25:75 plants was minimum (40 and 17%) compared to 25:75 (72 and 50%), performance, which reflected an Miranda et al.
and 0:100) for 10 days. 50:50 (88 and 67%), 75:25 (66 and 51%) and 100:0 (65 and 47%) alleviated Na+ toxic effects by (2016)
treatments. NH4+.
Populus simonii Plants were grown in hydroponics at 75 mM NH4+-fed plants were less tolerant to salinity; root biomass was Increased Na+:NH4+ ratio and Meng et al.
NaCl supplemented with 1 mM NH4Cl or decreased by 18 and 14%, root length 32 and 17%, stem height 23 and competitive inhibition of Na+ and (2016)
KNO3 as the N source 16%, chlorophyll content 63 and 50%, photosynthetic rate 59 and 29% NH4+
in NH4+- and NO3--fed plants, respectively at 75 mM NaCl.
Sorghum 4-day-old plants were transferred to Hoagland NO3-:NH4+ ratio of 50:50 increased chlorophyll-b by 34 and 22%, N with 50:50 ratio of NO3-:NH4+ de Souza-

(Sorghum bicolor L.) solution salinized with 75 mM NaCl and anthocyanins 12 and 23% compared to NO3-:NH4+ of 100:0 and 0:100, protects photosynthetic pigments Miranda et al.
enriched with 5 mM N in NO3-:NH4+ ratios of respectively. Photosynthetic efficiency was also increased by 50:50 from degradation and allows higher (2013)
100:0, 75:25, 50:50, 25:75 and 0:100. ratio but non-significantly. PSII efficiency under salt stress.
Barley 5-day-old seedlings were grown at 6 mM N in Mixed NH4+:NO3-N supply produced higher leaf number 42%, shoot Energy savings associated with N Kant et al.
(Hordeum vulgare L.) the form of NO3- or NO3- + NH4+ in the ratio of and root fresh weights 75% and 60%, total N 11-17% in leaves, assimilation and more energy (2007)
75:25 with 2 NaCl levels (0 and 120 mM) for glutamine synthetase activity 23%, glutamate dehydrogenase 55% allocation towards salt tolerance
Tomato
(Lycopersicon
25 days.
Fo
Plants were grown with 14 mM N at NO3-
:NH4+ ratios of 14:0, 12:2 and 10:4. NaCl
while 11-15% lowered Na+ than NO3- alone at the same salinity level.
At 60 mM NaCl, leaf Cl- was increased by 122 and 97%, leaf Na+ 5.6-
and 3.5-folds, compared to control, at NO3-:NH4+ ratio of 14:0 and
10:4, respectively. NO3-:NH4+ ratio of 10:4 increased glucose by 40%,
mechanisms with mixed supply.
Reduced accumulation of Na+ and
Cl- and increased reducing sugars
in leaves at NO3-:NH4+ ratio of 10:4
Flores et al.
(2001)
rP
esculentum Mill.) levels of 0, 30 and 60 mM were imposed 28
days after transplanting and plants were fructose 31%, Chl a+b 18% and leaf Fe 65% compared NO3-:NH4+ contributed to higher salt tolerance
harvested 42 days after transplanting. ratio of 14:0 at 60 mM NaCl. than 14:0.
Pea Seedlings were grown in hydroponics for 21 NH4+-fed plants were less tolerant to salinity as shown by a reduction Specific Na+ toxicity, low soil Frechilla et al.
ee
(Pisum sativum L.) days with 5 mM N either as Ca(NO3)2, or in total soluble sugars of 21% in shoot, 20% in root; organic acids water potential or inhibition of the (2001)
(NH4)2SO4. Saline treatments consisted of 1 48% in shoot; anions 102% in shoot, 269% in root; cations 40% in uptake of essential nutrients
and 30 mM NaCl. shoot, 383% in root while an increase of 5-fold in plant Na+ than NO3-- causing nutrient imbalances in the
fed plants. plant.
Sunflower
(Helianthus annuus L.)
8-day-old seedling were grown in Hoagland
solution salinized with 0, 60 and 120 mM
NaCl and supplied with 8 mM N either as
KNO3 or NH4Cl for 21 days.
rR
At 120 mM NaCl, N-forms have no effect on shoot Na+ and Cl- while
shoot K+ was decreased by 93% and Ca2+ 100% with NH4+ compared
to NO3--N. In roots, Na+ was increased by 11%, Cl- 33%, while K+ was
decreased by 196% and Ca2+ 97% with NH4+ compared to NO3--N.
NH4+-induced inhibition in cations
uptake.
Ashraf and
Sultana (2000)
ev
Maize 7-day-old plants were exposed to 20, 50 and At 80 mM NaCl, NH4+-fed plants exhibited a reduction of 54% in NH4+ assimilation in roots, absence Lewis et al.
(Zea mays L.) 80 mM NaCl with 4 mM NH4+ or NO3-. fresh biomass, 59% in stomatal conductance, 58% in net of ion translocatory shuttle, higher (1989)
photosynthesis and 30% in transpiration rate compared to NO3--fed osmotic effects in NH4+-fed plants.
iew
plants at same salinity.
On
ly

Fo
rP
ee
rR
ev
Figure 1. Schematic summary of major salinity stress mechanisms of plants.

ie
w
On
ly

Fo
rP
ee
rR
Figure 2. Nitrogen-induced ionic, physiological and biochemical mechanisms of plants

ev
for their adaptation to saline environment.

ie
w
On
ly

Fo
rP
♦♦♦
ee
rR
ev
ie
w
♦♦♦
On
ly
Figure 3. Nitrogen forms (NH4+ and NO3-) effects on plant adaptation to saline environment.

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Archives of Agronomy and Soil Science

Nitrogen nutrition and plant adaptation to saline

Manuscript Type: Review Articles

Ion toxicity, nitrogen forms, nitrogen metabolism, nutrient imbalance,

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1 Nitrogen nutrition and plant adaptation to saline environment: a review

13 *Corresponding author’s e-mail: mashraf_1972@yahoo.com

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43 prominent position among essential plant nutrients absorbed by plants. It is an integral

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83 The reconciliation of research on N-salinity interaction in plants is a big challenge because it

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93 Plant growth in saline environment

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129 Nitrogen effects on plant growth in saline environment

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165 N-induced adaptation mechanisms against salinity stress

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287 N effects on oxidative damage

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318 synthesis of osmoprotectants which improves plant tolerance to salinity as measured by

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384 of K+/Na+ homeostasis (Figure 3a).

386 NO3--N and salinity interactions

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434 Conclusion and future prospects

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480 Physiol. 168:1617-1626.

485 bluegrass as affected by nitrogen fertilization. J Agr Sci Tech. 19:173-183.

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510 Appl Sci. 2S:835-840.

512 Physiol. 159:567-584.

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540 ammonium nutrition alleviates detrimental effects of salinity by enhancing photosystem II

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570 nitrogen nutrition (ammonium or nitrate). Plant Growth Regul. 35:171-179.

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599 leaf water relations of pea leaves. Physiol Plant. 115:251-257.

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637 stress in maize and wheat. New Phytol. 111:155-160.

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688 tolerance. Afr J Plant Sci. 7:586-592.

690 herbivore in a salinity-stressed non-halophytic plant. AoB PLANTS 8, plw028;

696 accumulation in plants. Metab Eng. 4:49-56.

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719 ‘Boulevard’). Am J Agri Biol Sci. 3:544-550.

721 olive (Olea europaea L.) trees. Sci. Horti. 108:432-438.

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Table 1. Salinity stress effects and mechanisms in plants.

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Under saline conditions, increasing N up to 200 mg l-1 increased leaf NO3-

N-induced alleviation of specific ion Tabatabaei (2006)

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Canola 8-day-old plants were grown for 21 days in full

Salinity-induced nutrient imbalance Bybordi et al.

Esmaili et al. (2008)