00.0 Nitrogen Nutrition and Adaptation of Glycophytes

Archives of Agronomy and Soil Science
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Nitrogen nutrition and adaptation of glycophytes

to saline environment: a review
Muhammad Ashraf, Sher Muhammad Shahzad, Muhammad Imtiaz,

Muhammad Shahid Rizwan, Muhammad Saleem Arif & Rizwana Kausar
To cite this article: Muhammad Ashraf, Sher Muhammad Shahzad, Muhammad Imtiaz,
Muhammad Shahid Rizwan, Muhammad Saleem Arif & Rizwana Kausar (2018): Nitrogen nutrition
and adaptation of glycophytes to saline environment: a review, Archives of Agronomy and Soil
Science, DOI: 10.1080/03650340.2017.1419571
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ARCHIVES OF AGRONOMY AND SOIL SCIENCE, 2018
https://doi.org/10.1080/03650340.2017.1419571
REVIEW ARTICLE
Nitrogen nutrition and adaptation of glycophytes to saline

environment: a review
Muhammad Ashrafa, Sher Muhammad Shahzada, Muhammad Imtiazb,
Muhammad Shahid Rizwanc, Muhammad Saleem Arifd and Rizwana Kausare
a
Department of Soil and Environmental Sciences, University College of Agriculture, University of Sargodha,
Sargodha, Pakistan; bSchool of Environmental Science and Engineering, Guangzhou University, Guangzhou,
China; cDepartment of Soil Science, Bahauddin Zakariya University, Layyah, Punjab, Pakistan; dDepartment of
Environmental Sciences and Engineering, Government College University Faisalabad, Faisalabad, Pakistan; eSoil
and Water Testing Laboratory for Research, Sargodha, Punjab, Pakistan
Downloaded by [University of Cambridge] at 23:08 08 January 2018
ABSTRACT ARTICLE HISTORY

Relations between nitrogen (N) nutrition and salinity tolerance in plants Received 9 April 2017
are multifaceted and varies significantly depending on many soil and Accepted 17 December 2017
plant factors. Saline environment might experience an N dilemma due to KEYWORDS
the opposing effects of salt ions on N uptake, translocation and meta- Ion toxicity; nitrogen forms;
bolism within the plant body. Adequate regulation of N under saline nitrogen metabolism;
conditions can be a promising approach to alleviate salinity’s effects on nutrient imbalance; salinity
plants by ameliorating ion toxicity and nutrient imbalances through its tolerance
impacts on the uptake and redistribution of salt ions within the plant.
Certain N-containing compounds including proline, glycine betaine, pro-
teins and polyamines help the plants to tolerate salinity through their
involvement in improving water uptake and water use efficiency, mem-
brane integrity, enzyme activation, hormonal balance, chlorophyll synth-
esis, stimulation of photosystems and CO2 assimilation under salinity
stress. Nitrogen, particularly NO3− represents a stress signal that triggers
the activation of antioxidant enzymes to protect the plants against
salinity-induced oxidative damage. Furthermore, the source/form of N
application can affect not only N-interactions but also the behavior of
other nutrients in stress environment. The present review deals with
N-salinity relations in plants, particularly glycophytes, emphasizing on
N-induced mechanisms which can improve plant adaptation to saline
environment.
Introduction
Global increase in soil salinization constitutes a most devastating environmental threat for crop
yield and food quality (Asrar et al. 2017). High salinity can inhibit plant growth through osmotic
stress (Maia et al. 2010), nutritional imbalance (Chinnusamy & Zhu 2003), oxidative damage (Ahmad
2010) and/or specific ion toxicity (Chinnusamy et al. 2005). In saline environment, sodium (Na+) and
chloride (Cl−) interfere with the uptake, translocation and assimilation of plant nutrients such as
ammonium (NH4+), potassium (K+), calcium (Ca2+), magnesium (Mg2+), nitrate (NO3−) and sulfate
(SO42−), leading to disruption of ion homeostasis. Nitrogen (N) occupies a prominent position
among essential plant nutrients absorbed by plants. It is an integral component of proteins that
construct cell materials, plant tissues, and hence vital for plant growth and development. However,
CONTACT Muhammad Ashraf mashraf_1972@yahoo.com Department of Soil and Environmental Sciences; University
College of Agriculture, University of Sargodha, Sargodha, Pakistan
© 2018 Informa UK Limited, trading as Taylor & Francis Group
2 M. ASHRAF ET AL.
N accumulation by plants, particularly glycophytes is severely restricted by salt ions in saline

environment, and examples of such interactions have been found in many crops such as
Lycopersicon esculentum Mill. (Flores et al. 2001), Gossypium hirsutum L. (Chen et al. 2010),
Brassica juncea L. (Iqbal et al. 2015), Zea mays L. (Hütsch et al. 2016), Cicer arietinum L. (Atieno
et al. 2017). The salinity’s effects on N uptake and assimilation could be attributed to Na+ and Cl−
antagonism with NH4+ and NO3−, respectively (Shawer 2014), salinity-induced reduction in water
uptake by plants (Ashraf & Harris 2004), inhibition of plant growth or alteration in N metabolism
(Parida & Das 2005). NH4+ assimilation in plants under saline condition might also be inhibited due
to the down regulation of genes responsible for NH4+ assimilation (Wang et al. 2012).
Adaptation of plants to stress environment including salinity stress is generally the result of many
factors and processes functioning at ionic, morphological, physiological, biochemical and genetic levels
within the plants (Rahnama et al. 2010). Among different strategies, adequate regulation of mineral
nutrients is of increasing importance to improve plant survival under salinity stress (Guo et al. 2017).
Nitrogen is particularly known amongst the mineral nutrients for enhancing plant capabilities to endure
salinity stress through its involvement in osmotic adjustment (Nasab et al. 2014), stimulation of antiox-
idant defense system (Rais et al. 2013), alleviation of ion toxicity (Iqbal et al. 2015), maintaining ionic
balance (Khan et al. 2016) and activating various enzymes (Aragão et al. 2012). According to de Souza-
Miranda et al. (2013), N could improveplant adaptation to saline environment by reducing ion toxicity
and maintaining the ionic balance. While, Iglesias et al. (2004) reported that appropriate N supply under
saline conditions stimulated the plant growth, leading to salt dilution which consequently enhanced
plant survival in stress environment. Kamel (2012) found that N could help to improve salt tolerance by
adjusting osmotic stress, in addition to its vital role in the general growth processes. Rais et al. (2013)
suggested that contribution of N to osmotic adjustment, chlorophyll synthesis and proline accumulation
constitutes the major mechanisms for inducing salt tolerance in plants. Siddiqui et al. (2010) found that
detoxification of radical oxygen species (ROS) by N-induced synthesis of osmoprotectants such as proline
and glycine betaine (GB) contributed to salt tolerance in plants.
NH4+ and NO3− are the principal plant available forms of N in the soil which can influence its
protective role against salinity stress (Zhonghua et al. 2011). Although, NH4+ assimilation is
energetically more favorable than NO3− but it is usually toxic at higher concentration for most of
the plant species (Britto and Kronzucker 2002). Moreover, NH4+-fed plants may be more sensitive to
salinity than NO3–fed plants as these plants have greater Cl− but lower K+, Ca2+ and Mg2+
concentration as compared to NO3–fed plants (Ashraf & Sultana 2000). On the other hand, Ashraf
(1999) reported that NO3− and NaCl interacted to inhibit plant growth more than did NH4+ under
saline conditions. Some other investigations (e.g. Kant et al. 2007; Zhonghua et al. 2011) suggested
that integrated use NH4+ and NO3− is more effective in alleviating adverse effects of salts on plants
as compared to their sole application.
The reconciliation of research on N-salinity interaction in plants is a big challenge because it
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
saline conditions. However, for evaluating the role of N in saline environment, it is imperative to
understand the involvement of N in basic processes and mechanisms contributing to salt tolerance
in plants. The present paper reviewed the contribution of N to salt tolerance, with an emphasis on
its involvement in osmotic adjustment, protection of cellular structure, maintenance of ionic
balance, mitigation of ion toxicity and scavenging of free radicals under salinity stress as well as
the relation of N forms with salinity tolerance of plants, in particular glycophytes.
Plant growth in saline environment

Soil salinity as a noxious environmental stress adversely influences almost all the growth, yield and
quality traits of different plant species, particularly glycophytes (Ashraf et al. 2012). Soil salinization
initially damages the plant roots, disturbs soil water potential and thus leading to osmotic stress.
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 3
Figure 1. Schematic summary of major salinity stress mechanisms of plants.
The buildup of salt ions in the growth media as well as their accumulation and distribution within
the plant body have marked influence on the uptake and translocation of plant nutrients, resulting
in ionic imbalances and toxicity (Zaki 2016). In addition, increasing salinity disturbs plant metabo-
lism, leading to enhanced generation of ROS and thus oxidative stress (Hernandez and Almansa
2002). Higher cellular salt buildup also causes leaf abscission, chlorophyll and photosystem
damage, disruption of hormonal balance, and consequently inhibition of plant growth and devel-
opment (Figure 1). Salinity stress effects and mechanisms in various plant species are presented in
Table 1. In salinity-induced osmotic stress, excessive accumulation of salts in the rhizosphere
depresses soil water potential and inhibits the movement of water from soil to plant. In more
severe cases, water even starts to move from plant roots to soil causing plant dehydration (Munns
& Tester 2008). Under these conditions, plants have to use more energy to make biochemical
adjustments through the accumulation of osmolytes for extracting water from soil. This energy is
diverted from the plant growth processes which results in marked decline in plant growth,
development and yield. Furthermore, higher accumulation of salt ions in leaves disrupts various
metabolic processes which reduces the net CO2 assimilation, and consequently leading to a
significant yield reduction (Frechilla et al. 2001).
Under salinity stress, nutrient imbalances usually result from the effects of salt ions on nutrient
phytoavailability, uptake, translocation or distribution within the plant body which causes a
significant decline in crop yield and quality (Cámara-Zapata et al. 2004). Various interactions of
salt ions with the essential plant nutrients have been widely described, for example, Na+ interacts
with Ca2+, Mg2+, K+ and NH4+ while Cl− with NO3− and SO42− (Gimeno et al. 2009), leading to
nutrient imbalances which consequently reduces plant growth and productivity. Yousufinia et al.
(2013) have observed that antagonistic effects of Na+ with NH4+ or Cl− with NO3− reduce the N
accumulation in salt stressed plants. Salt stress also deregulates the stomatal opening which
decreases CO2/O2 ratio in leaves and inhibits the fixation of CO2 within the plants (Hernández &
Table 1. Salinity stress effects and mechanisms in plants.

Plant species Treatment Effect Mechanism Reference
Chickpea Seedlings of 245 lines of chickpea, 186 lines of desi type while 59 On an average, salinity increased Na+ by 203% while reduced K+/Na+ Na+ toxicity Atieno et al.
(Cicer lines of kabuli type, were exposed to 0 and 40 mM NaCl. ratio 84%, plant growth rate 20%, plant height 15%, shoot biomass (2017)
arietinum L.) 28%, seed number 16% and seed yield 32% compared to control.
Okra Two cultivars (Chinese green and Chinese red) were subjected to 18% salinity stress reduced net photosynthetic rate by 84 and 80%, Osmotic stress Azeem et al.
(Abelmoschus salt stress (0%, 6%, 12% and 18%) with equal proportions of stomatal conductance 95 and 83%, transpiration 72 and 85%, water (2017)
esculentus L.) NaCl and CaCl2 in Hoagland’s nutrient solution. use efficiency 47 and 17%, water content 38 and 40%, plant height
M. ASHRAF ET AL.
83 and 87%, and fresh weight 91 and 88% in Chinese green and
Chinese red, respectively compared to control.
Indian mustard, Four weeks old plants were grown in hydroponics at 0, 50 and NaCl decreased total biomass 24 and 35%, leaf protein 16 and 55%, Ion toxicity Renault et al.
(Brassica 100 mM NaCl for two weeks. chlorophyll 11 and 27%, transpiration 2 and 11%, N 8 and 24%, K 56 and (2016)
juncea) and 75%, Mg2+ 20 and 38%, Ca2+ 17 and 41% while increased Na+ nutrient
358- and 650-folds, proline 2.6- and 11.9-folds, Cu 37 and 87%, Fe 3 imbalance.
and 8%, Mn 27 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 Djadida, were sown for 200 mM NaCl increased leaf Na+ by 5- and 7-folds, catalase activity 4- Oxidative Taïbi et al.
(Phaseolus 7 days at 4 levels of NaCl (0, 50, 100 and 200 mM) in a mixture and 2-folds, glutathione reductase 60 and 20%, ascorbate 33 and stress and (2016)
vulgaris) of commercial peat and vermiculite. 26%, flavonoids 47 and 70% while decreased shoot dry weight 30 ion toxicity
and 27%, root dry weight 59 and 61%, Chlorophyll-b 33 and 43%,
carotenoids 18 and 19%, and K+ 32 and 35% in Tema and Djadida,
Cotton Plants were exposed to 0, 100, 150 and 200 mM NaCl for 3 weeks 200 mM NaCl increased leaf Cl− by 24- and 3-folds, leaf Na+ 50 and Ion toxicity Hassan et al.
(Gossypium by irrigating with saline water after every 2nd day. 104%, while decreased leaf K+ 51 and 22%, stomatal conductance 32 and (2014)
hirsutum L.) and 45% in FDH 171 and FDH 786, respectively compared to control. osmotic
stress
Groundnut Seeds of 2 cultivars, K-134 and JL-24 were germinated at 4 levels At 150 mM NaCl, free proline content were increased by 3- and 2.6- Osmotic and Ranganayakulu
(Arachis of NaCl (0, 50, 100 and 150 mM) and grown for 9 days. folds, soluble sugars 3.3- and 2.5-folds, free amino acids 2- and 1.8- oxidative et al. (2013)
hypogaea L.) folds, total amino acids 2.1- and 1.8-folds, total polyamines 1.6- and stress
1.4-folds, glycine betaine 1.8- and 1.5-folds in K-134 and JL-24,
Barley 15-day-old seedlings of 4 cultivars Dasht, Lisivy, Sahra and 100 mM NaCl increased leaf Na+ by 99% in Sahand, 73% in Sahra, 31% Specific ion Yousufinia et al.
(Hordeum Sahand were exposed to 2 levels of NaCl (0 and 100 mM) for in Dasht and 15% in Lisivy while decreased leaf K+ by 16% in Dasht toxicity (2013)
vulgare L.) 10 days. and Lisivy, 25% in Sahra and 36% in Sahand with a reduction in K+:
Na+ ratio by 36% in Dasht, 26% in Lisivy, 55% in Sahra and 72% in
Sahand compared to control.
Pea 17-day-old seedlings were exposed to 0 and 80 mM NaCl for 80 mM NaCl increased Leaf Na+ by 120-folds, root Na+ 26-folds, xylem Specific ion Pandolfia et al.
(Pisum 14 days. sap Na+ 4.1-folds, leaf osmolality 97%, root osmolality 59% but toxicity and (2012)
sativum L.) decreased leaf K+ 65%, root K+ 59%, stomatal conductance 82% and osmotic
SPAD value 27% compared to control. stress
(Continued )
Table 1. (Continued).
Cowpea 4-day-old seedlings of 2 cultivars; Pérola and Pitiúba were shifted 100 mM NaCl increased Na+ by 77 and 78%, electrolyte leakage 65 and Specific ion Maia et al.
(Vigna to paper and moistened with deionized water (control) or 58% while reduced K+ by 7 and 11%, K+:Na+ 82 and 80%, lipid toxicity (2010)
unguiculata 100 mM NaCl solution for 2 days. peroxidation 28 and 30%, relative water content 2 and 6%,
L.) superoxide dismutase 12 and 26%, peroxidase 47 and 55%, catalase
7 and 58% but increased ascorbate peroxidase activity by 12 and
26% in Perola and Pitiuba, respectively compared to control.
Wheat Two wheat genotypes (Sardari and Alvand) were grown in superoxide dismutase activities were increased by 66, 180, 233 and Oxidative Esfandiari et al.
(Triticum Hoagland’s solution salinized with 0, 50, 100, 150 and 200 mM 226% in Sardari while 87, 8.7, no effect and 8.7% in Alvand; catalase stress (2007)
aestivum L.) NaCl for 10 days. by 800, 366, 283 and 200% in Sardari while 80, 40, 25 and 85% in
Alvand; glutathione reductase first increased by 27% then decreased
by 18, 48 and 47% in 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.
ARCHIVES OF AGRONOMY AND SOIL SCIENCE
5
6 M. ASHRAF ET AL.
Almansa 2002). Salinity causes impaired electron transport during CO2 fixation and increases ROS
production in plants (Demidchik & Maathuis 2007). Increased generation of ROS under salinity
stress damages the cell membrane, chlorophyll, proteins, lipids and nucleic acids, and ultimately
leads to a significant decline in crop yield and quality through oxidative stress (Ahmad & Umar
2011).
Nitrogen effects on plant growth in saline environment

Adequate supplementation of N under saline conditions can provide an important strategy to
sustain or even improve the productivity of salt affected soils. Interactions between N nutrition and
salinity have been extensively studied because soil salinization is an emerging global threat to food
security and safety (Ashraf & Harris 2004; Figueira & Caldeira 2005; Siddiqui et al. 2008; Akram et al.
2010; Nadian et al. 2012; Khan et al. 2016; Guo et al. 2017). The protective role of N against the
deleterious effects of salts in plants is mainly associated with its involvement in adjusting osmotic
stress (Heidari et al. 2011), stomatal conductance (Akram & Ashraf 2009), antioxidant activities
(Fayez & Bazaid 2014), alleviation of ion toxicity (Bahmanzadegan & Aboutalebi 2013), nutrient
uptake (Shawer 2014), photosynthesis (Iglesias et al. 2004), activities of nitrate reductase (Rais et al.
2013) and carbonic anhydrase enzymes (Soussi et al. 1998), membrane permeability (Aragão et al.
2012) and finally N-use efficiency (Bybordi et al. 2010). Nitrogen nutrition under salinity stress
increases plant biomass by stimulating vegetative growth or decreasing leaf abscission which
causes salt dilution within the plant body and hence reduces salt ions toxicity, the critical para-
meter for salt damage (Figure 2). Furthermore, larger plant root systems under high salinity caused
by adequate N supply have the potential benefit to exploit greater volume of soil for nutrients and
water, and hence might present an adaptive mechanism to improve plant tolerance to salinity
(Nhung et al. 2017). Nitrogen nutrition in saline environment also improves the selectivity of plant
roots for the uptake of essential elements and exclusion ability of harmful Na+ from leaf tissues,
and eventually contributes to salt tolerance of plants (Kabir et al. 2005; Tabatabaei 2006). Some
other studies have demonstrated that N-induced plant tolerance to salinity might also be related to
the stimulation of NO3− assimilatory pathway which enhances the assimilation of CO2 while
Figure 2. Nitrogen-induced ionic, physiological and biochemical mechanisms of plants for their adaptation to saline
environment.
reduces photo-damage (Aragão et al. 2012, Jatropha curcas), higher leaf proline content (Nadian
et al. 2012, Saccharum officinarum L.), increased abscisic acid accumulation (Fernández-Crespo et al.
2012, Citrus sinensis L.), increased fluorescence, higher efficiency of photosynthetic apparatus
(Akram et al. 2010, Zea mays L.) or osmotic adjustment (Mansour 2000). In summary, adequate
regulation of N under saline conditions causes an improvement in plant growth, reduction in leaf
abscission, adjustment of osmotic stress, stimulation of enzyme activities, higher photosynthetic
efficiency, reduction in the uptake of Na+ and Cl− and maintenance of nutrient balance, all these
constitute the major mechanisms of salt tolerance in plants, particularly glycophytes. Furthermore,
the protective role of N against salinity stress is found to be more prominent when N supply is
higher than the level considered optimum under non-saline conditions.
N-induced adaptation mechanisms against salinity stress

N-mediated mitigation of specific ion toxicity

Specific ion toxicity develops by increased absorption of salt ions is a major growth limiting factor
for many plant species growing in saline environment (Hassan et al. 2014). However, plant
performance under saline conditions might be improved by the adequate supply of plant nutrients
through the mitigation of specific ion toxicity (Bahmanzadegan & Aboutalebi 2013). Inhibition of
Na+ and Cl− accumulation in plants grown under salinity stress is considered an important
physiological process conferring salt tolerance, and this inhibition might be related to N nutrition
as NO3− and NH4+ have antagonistic effect with Cl− and Na+, respectively (Table 2). Increased N
supply in saline environment generally interacts with salt ions and often results in a decrease of
their toxicity in different plant species, for example, Gossypium hirsutum L. (Chen et al. 2010),
Helianthus annuus L. and Carthamus tinctorius L. (Jabeen & Ahmad 2011), Medicago sativa (Abbasi-
Shahmersi & Ebadi 2012), Tageta patula (Bahmanzadegan & Aboutalebi 2013), Brassica juncea L.
(Iqbal et al. 2015), Zea mays L. (Hütsch et al. 2016), Glycine max (Guo et al. 2017), .
Increasing Cl− buildup in soil and its accumulation in plants under salinity stress may establish a
principal mechanism of ion toxicity in certain plant species, and thus reduction in Cl− uptake by
plants might be an important strategy to enhance plant adaptability to saline environment (Moya
et al. 2003). Nitrogen, particularly in the form of NO3− interacts with Cl−, reduces its uptake and
accumulation within the plant body (Hütsch et al. 2016). Two mechanisms including Cl− dilution
effect by NO3–induced growth stimulation or reduction in leaf abscission, and an anionic antagon-
ism between NO3− and Cl− have been suggested for reducing Cl− toxicity by NO3− under salinity
stress (Shawer 2014). High salinity can enhance leaf abscission by stimulating ethylene synthesis
and aggravating the extent of ion toxicity (Gomez-Cadenas et al. 1998), but N supplementation
under saline conditions can inhibit ethylene production (Noiraud et al. 2001) and reduce leaf
abscission, alleviating salt toxicity through dilution effect (Gómez-Cadenas et al. 2000).
Maintenance of high NO3− concentration in the soil solution may reduce Cl− accumulation by
plants due to its antagonistic relation with Cl− (Aroiee et al. 2005; Iqbal et al. 2015). Many other
studies, for example, Ebert et al. (2002) Psidium guajava L., Abdelgadir et al. (2005) Oryza sativa L.,
Tabatabaei and Fakhrzad (2008) Lolium perenne, Bybordi et al. (2010) Brassica napus L., Jabeen and
Ahmad (2011) Helianthus annuus L. and Carthamus tinctorius L., have reported a negative correla-
tion between NO3− and Cl−, and NO3–N frequently inhibits the uptake and accumulation of Cl−, and
thus reduces Cl− toxicity under saline conditions.
Na+ is another ion that is toxic at higher concentration for different aspects of plant growth and
metabolism (Tabatabaei 2006). In saline environment, lower Na+ uptake or higher K+ accumulation
and an increasing K+:Na+ ratio might be an important strategy to enhance plant adaptability
(Hasegawa 2013; Feki et al. 2014; Han et al. 2015). Inhibition of Na+ influx and/or increase in efflux
is the major factor responsible for lower accumulation of this ion in the roots (de Souza-Miranda
et al. 2013). Furthermore, lower Na+ movement from roots to shoots via xylem or higher Na+
Table 2. Nitrogen-mediated mitigation of specific ion toxicity in plants under salinity stress.
Soybean Plants were grown at 50 and 100 mmol L−1 NaCl In Glycine max, leaf Cl−/NO3− ratios were decreased NO3− supply increased NO3− while Guo et al. (2017)
(Glycine max) with 0.75, 7.5 and 15 mmol L−1 NO3− supply. by 87% in Lee 68; 38 and 56% in Jackson, while decreased Cl− contents within
(Glycine soja) in Glycine soja, 75 and 87% in BB52; 73 and 83% plants, leading to lower Cl−/
in N23227 at 100 mmol L−1 NaCl with 7.5 and NO3− ratios.
15 mmol L−1 NO3−, respectively compared to
100 mmol L−1 NaCl+0.75 mmol L−1 NO3−.
Maize Plants were grown for 23 days at 4 NaCl levels With increasing NaCl stress, NO3− uptake was Cl−/NO3− antagonism and Cl− Hütsch et al.
M. ASHRAF ET AL.
(Zea mays L.) (control, 50, 100, 150 mM) with N at 2 mM Ca decreased from 150 to 80 mg plant−1, Cl− uptake exclusion ability of maize. (2016)
(NO3)2. Plants in half of the pots were treated was increased from 90 to 120 mg plant−1.
with additional 1 mM NH4NO3 2 days after start Correlation between NO3− and Cl− uptake was
of the NaCl application. r = – 0.63, r2 = 40%. At 100 and 150 mM NaCl,
net root-to-shoot translocation of total N was
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 N-induced antagonistic and Iqbal et al. (2015)
(Brassica juncea L.) solution at 0 and 100 mM NaCl with 0, 5, 10 and and 75% while Cl− by 16, 39 and 60% with 5, 10 dilution effects.
20 mM NO3− as KNO3 for 30 days. and 20 mM N, respectively at 100 mM NaCl
compared to NaCl treated plants without N.
French marigolds Plants were raised at four salinity levels (0.49, 2.0, At 6.0 mmohs cm−1 salinity, shoot Na+ NH4+ decreased K+ uptake but Bahmanzadegan
(Tageta patula) 4.0, 6.0 and 8.0 mmohs cm−1) and 3 NH4NO3 concentration was enhanced by 15 and 38% enhanced Na+ while NO3− & Aboutalebi
levels (0, 15 and 30 g L−1). while shoot K+ was decreased by 19 and 21% caused higher Na+ uptake. (2013)
with 15 and 30 g L−1 NH4NO3, respectively
compared to salt stressed plants without N.
Alfalfa Four levels of N (0, 30, 60 and 90 kg ha−1) as urea Salinity caused an increase of 100 and 187% in Na+, Salinity was the dominant factor Abbasi-
(Medicago sativa L.) were applied at 4–6 leaf stage while 3 levels of 60 and 100% in Ca2+, no effect on K+ with a which governed plant growth Shahmersi &
NaCl (0, 100 and 200 mM) were imposed 7 day reduction of 51 and 65% in K+:Na+ ratio in and ion uptake at higher salinity Ebadi (2012)
after N application. leaves. N fertilization had no significant effect on levels.
Na+, Ca2+ as well as K+ uptake and accumulation
under salt stress.
Citrange Carrizo 3-month-old plants were grown at 90 mM NaCl Salt stressed NH4+-fed plants accumulated 40% less Inhibition of chloride channel-like Fernández-
(Citrus sinensis L.) with 5 mM (NH4)2SO4 for 14 days. Cl− and displayed 30% more healthy leaves than proteins which reduced Cl− Crespo et al.
salt stressed plants without NH4+-N. toxicity. (2012)
Sunflower Seeds were sown under non saline (ECiw 0.5 dS In salt stressed plants sprayed with KNO3, leaf NO3− KNO3 increased leaf NO3− Jabeen & Ahmad
(Helianthus annuus L.) m−1) conditions, and irrigation with saline water concentration was increased by 17 and 20% in concentration with a subsequent (2011)
and Safflower (ECiw 4.8 and 8.6 dS m−1) was started at 3 leaf sunflower, 16 and 17% in safflower at ECiw of 4.8 decrease in Cl− and offset its
(Carthamus tinctorius L.) stage. KNO3 was sprayed @ 250 ppm. Data were and 8.6 dS m−1, respectively with a subsequent toxic effects under saline water
recorded at flowering stage. reduction in leaf Cl− concentration of 42% and irrigation.
45% in sunflower and 38% and 42% in safflower
as compared to saline water irrigation without
KNO3.
(Continued )
Olive Experiment consisted of 4 levels of NaCl 0, 50, 100, Under saline conditions, increasing N up to 200 mg N-induced alleviation of specific ion Tabatabaei
(Olea europaea L.) 150 mM and 3 levels of N 100, 200, 300 mg 1–1 l−1 increased leaf NO3− concentration by 176% in toxicity. (2006)
as NH4NO3. NaCl and N treatments were started Mission cultivar, 305% in Manzanillo and 28-folds
+
when plants were 25–30 cm in height and in Zard with a subsequent reduction in leaf Na
continued for 12 months. accumulation by 20% in Mission, 8% in
Manzanillo and 18% in Zard compared to
100 mg L−1 N under salt stress.
Navelina orange scion One-year-old potted plants were irrigated 3 times NO3− addition at 25 mM NaCl:CaCl2 caused a NO3− reduced Cl− concentration, Iglesias et al.
(Citrus sinensis) grafted per week with saline water having 25 mM NaCl: decrease of 50 and 60% but increase of 7% in Cl− reduced leaf abscission which (2004)
onto C. citrange, C. CaCl2 (15:1) with or without 10 mM NO3 for concentration; a decrease of 38, 28 and 55% in resulted in Cl− dilution, and thus
macrophylla or C. 60 days. leaf abscission; an increase of 23, 40 and 345% in alleviated Cl− toxicity.
mandarin rootstock. photosynthetic rate in C. citrange, C. macrophylla
and C. mandarin, respectively than without N.
Strawberry Nutrient solution alone (C); C + 5 mM Ca(NO3) N content were increased by 15, 38 and 57% in Oso Supplementary Ca(NO3)2 and/or Kaya et al. (2003)
(Fragaria ananassa) 2 + 5 mM KNO3; C + 35 mM NaCl (C + S); Grande and 17, 28 and 45% in Camarosa with a KNO3 could achieve full
+
(2 cultivars, Oso Grande C + S + 5 mM Ca(NO3)2; C + S + 5 mM KNO3 and subsequent Na reduction by 14, 16 and 30% in mitigation of salt stress through
and Camarosa) C + S + 5 mM Ca(NO3)2 + 5mM KNO3. Oso Grande and 20, 24 and 41% in Camarosa reducing Na+ ion toxicity.
with KNO3, Ca(NO3)2 and KNO3+Ca(NO3)2,
respectively compared to salt stressed plants
without KNO3 and/or Ca(NO3).
9
10 M. ASHRAF ET AL.
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 interacts with Na+, reduces its uptake
and accumulation within the plant (Esmaili et al. 2008). NH4+-N nutrition induces the activity of
Na+/H+ antiporter which helps to maintain Na+ balance under saline conditions (Mansour 2014).
Moreover, NH4+ competes with Na+ for the absorption sites in root membranes and thus reduces
Na+ uptake by salt stressed plants (Fernández-Crespo et al. 2012). Kant et al. (2007) also reported an
antagonistic effect of NH4+ on Na+ which decreases Na+ uptake and translocation, thereby inhibit-
ing Na+ while improving K+ accumulation within plant leaves under salinity stress. It is summarized
that increasing N application in saline environment enhances NH4+ and NO3− uptake which
compete with Na+ and Cl−, major ions in saline environment. Such interactions result in the
mitigation of ion toxicity and improve plant growth under salinity stress. Moreover, N nutrition
stimulates plant growth while reduces leaf abscission, and hence mitigates ion toxicity through
dilution effect.
N-mediated maintenance of nutrient balance

In saline environment, salt ions interfere with nutrient uptake, translocation and/or distribution
within the plants, leading to nutrient imbalances (Renault et al. 2016). Adequate regulation of N
under saline condition is involved in the maintenance ionic balance in plants, and thus contributes
to salt tolerance in many plant species, for example, Psidium guajava L. (Ebert et al. 2002), Pisum
sativum L. (Figueira & Caldeira 2005), Vigna radiata L. (Kabir et al. 2005), Lolium perenne (Tabatabaei
& Fakhrzad 2008), Brassica napus L. (Bybordi et al. 2010), Saccharum officinarum L. (Nadian et al.
2012), Sorghum bicolor L. (Serrão et al. 2012), Cucumis sativus L. (Shawer 2014), Gossypium hirsutum
L. (Khan et al. 2016), Oryza sativa (Zaki 2016), (Table 3). These studies have demonstrated that soil
salinity reduces NH4+, NO3−, K+, Ca2+ and Mg2+ while increases Na+ and Cl− concentrations in the
plant tissues. Nitrogen fertilization in saline 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 improves salt tolerance. Under salinity stress, NO3–N
has antagonistic effect on Cl− uptake and distribution, while NH4+ can balance the Na+ accumula-
tion, alleviating the detrimental effects of increasing salinity on plant metabolism (Cámara-Zapata
et al. 2004; Esmaili et al. 2008). Nitrogen nutrition also improves membrane permeability and
selectivity, leading to reduced uptake of salt ions and thus maintenance of ionic balance, which
otherwise damaged due to increased uptake of salt ions under saline conditions (Ebert et al. 2002;
Aragão et al. 2012).
Higher K+/Na+ selectivity in plants is an important protective mechanism against salinity stress
and has been suggested as a good criterion for evaluating plant tolerance to salinity (de Souza-
Miranda et al. 2016). Exogenous application of N, particularly in the form of NH4+ in saline
environment causes a marked reduction in Na+ accompanied with the maintenance of higher
NH4+, K+ and K+:Na+ ratio which associates with salt tolerance in plants (Siddiqui et al. 2010). In
summary, proper fertilization with N in saline environment influences the uptake and transport of
essential nutrients and helps to correct salinity-induced nutrient imbalance. Salinity stress generally
results in higher accumulation of Na+ and Cl− accompanied with a lower uptake of NH4+, K+, Ca2+
and NO3−. Nitrogen supply increases N, P, K and to some extent Ca and Mg uptake but decreases
Na and Cl concentrations. Consequently, all these mechanisms contribute to maintain the ionic
balance, leading to improved plant tolerance to salinity.
N-mediated osmotic adjustment

Osmotic adjustment is a principal mechanism in plants to maintain their water status under
different environmental stresses including salinity (Kamel 2012). Osmotic adjustment is ensured
by the accumulation/synthesis, translocation and redistribution of ions or organic substances that
Table 3. Nitrogen-mediated maintenance of nutrient balance in plants under salinity stress.

Cotton Ten treatments comprising of N, P, K and Zn with 100 mg N kg−1 soil as urea decreased leaf Na+ by N-induced improvement in ionic balance. Khan et al.
(Gossypium and without farm yard manure at 10 dS m−1 43% while improved K+ 32%, K+:Na+ 133%, P 21%, (2016)
hirsutum L.) electrical conductivity. Zn 33%, plant height 50%, bolls plant−1 60%
compared to salt stressed plants without
additional N.
Rice Plants were grown in saline soil having 20.5 dS m−1 Under salinity stress, N @ 70 kg fed−1 with 5 ton Maintenance of nutrient balance due to increased Zaki (2016)
(Oryza EC by adding compost at 5 and 10 tons fed−1 and fed−1 compost increased N by 31 and 40%, P 42 internal nutrient demand resulted from
sativa) N at 35, 50 and 70 kg N fed−1. and 53%, K 29 and 31%, Fe 30 and 41% and Mn 40 N-induced improved plant growth.
and 60% in straw and grain, respectively
compared to lower N level (35 kg N fed−1 with 5
ton fed−1 compost).
Cucumber Plants were grown for 84 days at 0, 4, 8 and 12 mM N addition caused an increase of 31, 59 and 76% in NO3− alleviated Cl− induced nutrient imbalance by Shawer
(Cucumis NO3− added as KNO3; and 0, 5, 10 and 15 mM Cl− shoot N content; 13 and 35% in shoot P content; reducing competition between nutrients for (2014)
sativus L.) added as KCl at (0.25) Hoagland nutrient solution 26, 54 and 68% in shoot K content with a specific absorption sites in roots.
using nutrient film technique. reduction of 6, 11 and 14% in shoot Cl− content by
4, 8 and 12 mM NO3–N, respectively compared to
15 mM Cl− without NO3–N.
Sugarcane Plants were grown till maturity at 4 salinity levels (1, At 8 dS m−1 salinity, N @ 400 kg urea ha−1 reduced N alleviated the salinity effects by reducing Na+ Nadian
(Saccharum 2, 4 and 8 dS m−1) and 3 N fertilizer rates (200, 300 leaf Na+ concentration by 92% while increased leaf and increasing K+ accumulation under salinity et al.
officinarum and 400 kg urea ha−1). K+ concentration 24% compared to lower N level stress. (2012)
L) (200 kg urea ha−1) at the same salinity.
Sweet Plants were grown for 3 months at 3 Na levels (158, N at 13.7, 27.4 and 41.1 g m−2 increased leaf P N nutrition mitigated nutrient disorders, increased Serrao
sorghum 1162 and 2166 g m−2 as NaCl) and 4 N levels (0, concentration by 37, 32 and 37% at 1162 and 11, the leaf contents of the various major elements et al.
(Sorghum 13.7, 27.4 and 41.1 g m−2 as NH4NO3). 16 and 16% at 2166 g m−2 Na while leaf Mg2+ 29, with the consequent improvement in plant (2012)
bicolor L.) 65 and 53% at 1162 and 11, 39 and 56% at 2166 g productivity under saline conditions.
m−2 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.
Canola 8-day-old plants were grown for 21 days in full At 120 mM NaCl, NO3–fed plants accumulated 19% Salinity-induced nutrient imbalance was corrected Bybordi
(Brassica strength Hoagland nutrient solution at 0, 50, 100 less Na+, 50% less Cl−, 19% more K+, 3% more N, by NO3− nutrition through inhibiting the uptake et al.
napus L.) and 150 mM NaCl, and 10 mM NO3− or NH4+ 58% more Ca2+ in shoots while 35% more Na+, 3% of Na+ and Cl− while improving K+ and Ca2+. (2010)
applied as KNO3 or (NH4)2SO4. less Cl−, 44% more K+, 2% more N and 53% more
Ca2+ in roots compared to NH4+-fed plants at same
salinity level.
Sorghum Saline water of EC 8 dS m−1 was used with 8 N levels; 160 kg N ha−1 at 8 dS m−1 EC increased N by 27 and N interacted with Na+ and Cl−, reduced their Esmaili
(Sorghum no N-fertilizers, basal fertilizer without N, urea and 30%; K+ 12 and 10%; Ca2+ 16 and 13%; Mg2+ 15 uptake, and alleviated salinity-induced et al.
bicolor L.) NH4NO3 treatments, each consisted of 3 levels and 10% with a subsequent reduction in Cl− by 10 nutritional disorders. (2008)
including 114, 137 and 160 kg N ha−1. and 15%; Na+ 24 and 28% with urea and NH4NO3,
respectively compared to salt treated plants
without N.
(Continued )
11
12
M. ASHRAF ET AL.
Ryegrass Plants were grown at 0 and 60 mM NaCl with 0, 5, 10 KNO3 at 60 mM NaCl increased leaf K+:Na+ by 22, 64 KNO3 either as foliar or soil application involved in Tabatabaei
(Lolium and 15 mM KNO3. KNO3 was applied either as soil and 39% in foliar; 24, 51 and 27% in soil, NO3− 14, alleviating salt-induced nutrient imbalance by &
perenne) application or foliar spray. 71% and no effect in foliar; 7, 80 and 7% in soil increasing K+:Na+ and NO3− while reducing Na+ Fakhrzad
with a reduction in Cl− by no effect, 14 and 159% and Cl− concentrations. (2008)
in foliar; 166, 366% and no effect in soil
application by 5, 10 and 15 mM KNO3, respectively
Pea Plants were grown at 0 or 90 mM NaCl and 5 mM After 60 days of salt exposure, leaf Na+ concentration NO3–fed plants were more efficient to inhibit Na+ Figueira &
(Pisum mineral N as NO3−, NH4+, or NH4NO3 or N by BNF was increased by 3.3, 5.5 and 4.7 folds, Cl− by 162, and Cl− uptake but enhanced K+ and thus Caldeira
sativum L.) (Rhizobium leguminosarum) for 15, 30, 45 and 60 625 and 225% while K+ was increased by 31% but mitigated salinity-induced nutrient imbalance. (2005)
− +
day after treatment completion. decreased by 47 and 62% with NO3 , NH4 and
NH4NO3-N, respectively compared to control.
Guava 11-month-old plants were grown for 10 weeks at 30 15 mM Ca(NO3)2 decreased Na+ concentration by 65 Enhanced supply of Ca2+ and NO3− restricted the Ebert et al.
(Psidium and 60 mM NaCl by supplying 0, 5, 10 and 15 mM and 76%, Cl− 32 and 33% while increased N by uptake of Na+ and Cl− and alleviated the (2002)
guajava L.) Ca(NO3)2. 246 and 114%, Ca2+ 88 and 220% and K+ 213 and salinity-induced nutrient imbalance.
118% in new leaves at 30 and 60 mM NaCl,
respectively compared to NaCl treated plants
without Ca(NO3)2.
serve as osmprotectants, enabling the plants to extract water from soil under stressed conditions
(Rontein et al. 2002). These osmoprotectants are non-charged, highly water soluble, low-weight
molecules which are non-toxic at higher concentration to plant metabolism and help the plants to
balance the salinity-induced external osmotic pressure for the absorption of water in stressed
environment (Munns 2002). Nitrogen plays a pivotal role in osmotic adjustment through ionic
accumulation as well as by inducing the synthesis of organic osmolytes which help the plants to
extract water when plants are growing under salinity stress (Heidari et al. 2011). When NO3− uptake
is greater than its reduction, NO3− compartmentalizes in the vacuole and functions to adjust
osmotic stress under saline conditions. Nitrogen is involved in the synthesis of osmolytes including
proline, asparagine, GB, proteins and polyamines which function to maintain plant turgor under
salinity stress (Mansour 2000). Many studies, for example, Carillo et al. (2005) Triticum durum,
Heidari et al. (2007) Triticum aestivum L., Tattersall et al. (2009) Thellungiella salsuginea, Heidari
et al. (2011) Plantago ovata F., Kamel (2012) Vicia faba L., Nasab et al. (2014) Pistacia vera L. have
reported the involvement of N in improving salt tolerance through 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 N availability exceeds the
need for plant growth. Therefore, N application rate in saline environment should be exceeded that
considered optimum under non-saline conditions because a greater proportion of the plant N pool
should be allocated to the synthesis of compatible nitrogenous osmolytes. Moreover, plants have
to use energy for the synthesis of these organic solutes. The ATP requirement is 52 mol ATP mol−1
for sucrose, 50 mol ATP mol−1 for GB, 41 mol ATP mol−1 for proline and 34 mol ATP mole−1 for
mannitol as compared to 3.5 mol ATP mol−1 for Na+ accumulation when N is supplied in the form
of NO3− (Munns 2002). Thus, adequate supply of essential plant nutrients including N is vital for
sustaining the productivity of salt affected soils. Some other studies have demonstrated that N
supplementation under saline conditions regulates the opening and closing of stomata and
improves plant water use efficiency, photosynthesis and many other metabolic process, leading
to improved salt tolerance (Akram & Ashraf 2009). In conclusion, N being an integral component of
different osmolytes is involved in osmotic adjustment, enabling the plants to extract water from
saline soil for the maintenance of sufficient turgor which is vital for salt tolerance. Moreover, when
N availability exceeds the plant requirements, the excess N is accumulated in vacuole as NO3−
which serves not only as N source for plant structural growth but also helps to improve plant
tolerance to salinity through osmotic adjustment.
N effects on oxidative damage

Metabolic acclimation by accumulating/synthesizing different osmolytes provides protection to
plants against salinity-induced oxidative stress (Polesskaya et al. 2006). Many of these osmolytes are
nitrogenous compounds enabling the plants to overcome oxidative stress by protecting photo-
synthetic pigments and photosystem II, stabilizing the protein and enzyme structure against
denaturation, improving membrane stability and ROS scavenging (Cuin & Shabala 2007). Many
studies, for example, Jeong-Jin and Yeon-Sik (2006), Ashraf and Foolad (2007), Xiao-Hua et al.
(2008), Gimeno et al. (2009), Siddiqui et al. (2010), Bybordi et al. (2010), Aragão et al. (2012), Rais
et al. (2013), Fayez and Bazaid (2014) have demonstrated that plants tend to accumulate N
containing compatible solutes including GB, proline, asparagine, sucrose, glucose, dimethyl sul-
phoniopropionate etc. in response to N supplementation under salinity stress (Table 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 (Koca et al.
2007). Proline is extremely soluble in water and binds with water molecules to forms clusters which
are attached to macromolecules, and protect them against salinity-induced oxidative damage
(Mittal et al. 2012). Proline being involved in stabilization of membrane structure can enable the
plants to maintain plant water status and ionic balance (Gimeno et al. 2009), and help to mitigate
Table 4. Nitrogen-mediated adjustment of osmotic stress in plants under salinity stress.

14
Pistachio Plants were grown at 0, 800, 1600 and 2400 mg NaCl At 2400 mg NaCl kg−1 soil, N @ 180 mg kg−1 soil N-induced increase in proline, reducing Nasab
(Pistacia kg−1 soil with 0, 60, 120, and 180 mg N kg−1 soil as increased proline by 15%, reducing sugar 10%, shoot sugars and Ca2+ improved the osmotic et al.
vera L.) urea. Ca2+ 47%, root Ca2+ 14%, shoot Mg2+ 25% and root adaptation. (2014)
Mg2+ 18% compared to 0 N at same salinity level.
Faba beans Plants were irrigated with mixture of tap and sea water Plants irrigated with 20% seawater + N, accumulated 63 N-induced osmotic readjustment under Kamel
(Vicia faba at 5, 10, 15 and 20% seawater (v:v) and treated with and 23% more Ca2+, 14% more soluble sugars, 22 and seawater irrigation was mainly attributed (2012)
L.) 5 mM KNO3 or 5mM (NH4)2SO4. Plants were grown till 3% more water content with KNO3 and (NH4)2SO4, to changes in ion fluxes than the synthesis
flowering stage. respectively, while 17% more K+ with KNO3, 174% of compatible solutes.
more Na+ and 25% more SO4− with (NH4)2SO4 in
M. ASHRAF ET AL.
shoots as compared to 20% seawater without N.

Psyllium Seedlings were grown for 30 days in solution containing Application of N in mixed form at 200 mM NaCl Osmotic adjustment through N-induced Heidari
(Plantago N as (NH4)2SO4 and Ca(NO3)2 or 1/2 NH4+ and 1/2 increased soluble carbohydrates by 112%, proline by synthesis of proline and soluble et al.
ovata F.) NO3− with 0, 100 and 200 mM NaCl. 6-folds while soluble proteins were decreased by 18% carbohydrates. (2011)
compared to salt treated plants without N.
Catharanthus Plant were grown for two weeks with 6 mM N either in The combined N forms under saline conditions Osmotic adjustment, reduction in ion Zhonghua
roseus the form of NO3− or NH4+, or 3 mM NO3− + 3 mM decreased leaf Na+ by 34%, increased NH4+ by 20%, toxicity, decreased transpiration rates and et al.
NH4+ with and without 200 mM NaCl. relative water content 9%, gas exchange 383%, leaf well-kept water relations. (2011)
photosynthesis 183%, glucose 102%, sucrose 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 NaCl Optimum level of KNO3 to alleviate adverse effects of Foliarly applied KNO3 involved in osmotic Akram &
(Helianthus with different KNO3 levels (no spray, spray of water + salinity was found to be 1% K+ and 1.6% NO3− which adjustment and stomatal regulation, Ashraf
annuus L.) 0.1% Tween 20 solution, 0.5% K+ + 0.8% NO3−, 1% K+ improved net CO2 assimilation by 78%, stomatal thereby maintaining high tissue water (2009)
+ 1.6% NO3−, 1.5% K+ + 2.4% NO3− and 2% K+ + conductance 33%, leaf osmotic potential 25%, leaf content in stressful environments.
3.2% NO3− in 0.1% Tween 20 solution). turgor potential 11%, water use efficiency 62%, leaf
K+ 16% and leaf K+:Na+ ratio 21% as compared to salt
treatment without KNO3.
Thellungiella Seedlings were grown for 1–2 weeks at 0 and 100 mM Plants at 1.0 mM N + 100 mM NaCl had a higher content N-induced synthesis of proline helped to Tattersall
salsuginea NaCI supplied with 0.1 or 1.0 mM N. of nitrogenous solutes, particularly proline by 6.3- restore cellular osmotic balance in saline et al.
folds than in seedlings grown with low N (0.1 mM) at environment. (2009)
the same salinity level.
Durum wheat Plants were grown in hydroponics at 0 and 100 mM 10 mM NO3− increased proline by 74% and 10.8-folds, N containing compounds could serve as Carillo
(Triticum NaCl with 0, 0.1, 1 or 10 mM NO3− as KNO3. serine 2.2- and 2.18-folds, asparagine 13- and 11- osmolytes to balance water potential et al.
durum folds, soluble proteins 2.02- and 1.46-fold, glycine within the cell. (2005)
Desf.) betaine 3.75- and 2.63-folds in shoot and root,
respectively at 100 mM NaCl compared to NaCl
stressed plants without NO3−.
Mungbean Plants were grown in soil with 13.3, 40 and 60 kg N N application @ 60 kg ha−1 at 75 mM NaCl caused a N-induced accumulation of inorganic ions Kabir et al.
(Vigna ha−1. 100 ml of 75 mM NaCl solution was applied at reduction of 31% in leaf Na+ with an increase of 15% and soluble proteins in leaves contributed (2005)
radiata L.) 3-day intervals and continued till maturity. in leaf Ca2+ and 19% in K+, 3.82% in relative water to osmotic adjustment under saline
Measurements were made 30 days after treatment. content, 16% in exudation rate and 23% in leaf water conditions.
potential compared to lower N levels at same salinity
level.
Table 5. Nitrogen-mediated amelioration of oxidative damage in plants under salinity stress.

Barley Plants were grown at 50, 100 and 150 mM NaCl, with KNO3 at 150 mM NaCl caused a decrease of 20% in leaf Protection against oxidative stress through Fayez &
(Hordeum 10 mM KNO3 for 2 weeks. Na+, 58% in leaf Na+:K+, 20% in malondialdehyde synthesizing N containing compounds. Bazaid
vulgare L.) and 6% in total antioxidant activity with a (2014)
subsequent increase of 71% and 64% in chlorophyll
a and b, 84% in carotenoids, 89% in leaf K+
compared to salt stressed plants without KNO3.
Mustard Plants were grown for 30 days in soil consisting of peat Combined use of N and S caused 30–44% more N and S regulated the formation of osmolytes Rais et al.
(Brassica and compost (4:1, w/w) and mixed with sand (3:1, proline, 38–81% higher chlorophyll fluorescence, which involved in osmotic adjustment and (2013)
juncea L.) w/w). Plants were treated with 100 mM NaCl with 157–290% higher chlorophyll content, 105–127% protected plants against oxidative damage.
−1
and without N or/and S at 100 mg kg soil. more N accumulation, 156–200% more nitrate
reductase activity and 225–275% greater dry mass
compared to salt stressed plants without N or S.
−
Barbados nut 23-day-old plants were grown at 2 NO3 levels; 1 and N-NO3− supply under salt stress increased net NO3− NO3− assimilatory reduction and NH4+ Aragão
(Jatropha 10 mM as KNO3 and Ca(NO3)2 and 2 NaCl levels (0 uptake by 250%, leaf CO2 assimilation rate 57%, assimilation in chloroplast provide a sink for et al.
curcas) and 100 mM). Measurements were taken 10 days stomatal conductance 43%, carboxylation electrons, leading to reduced photo-damage (2012)
after treatments completion. instantaneous efficiency 104%, total free amino acid
10% while decreased electrolyte leakage by 12%
Canola Plants were grown at 0 and 200 mM NaCl with 0:100, At 75:25 NH4+:NO3− ratios, plants showed 33% and NH4+ ion may represent a stress signal that Bybordi
(Brassica 75:25, 50:50 and 25:75 ratios of NO3− and NH4+. 28% higher catalase, 22% and 92% higher triggers the activation of antioxidant et al.
napus L.) glutathione reductase and 133% and 48% higher enzymes. (2010)
glutathione S-Transferase activities in leaves and
roots, respectively as compared to 0:100 NH4+:NO3−
ratios.
Mustard 14-day-old seedlings differing in salinity tolerance were The synthesis of proline and glycine betaine was N-containing compounds help to stabilize sub- Siddiqui
(Brassica grown at 2 NaCl levels (0 and 90 mM) and 5 N increased by 128 and 106%, in sensitive while 135 cellular structures against oxidative damage. et al.
juncea L.) concentrations (0, 30, 60, 90 and 120 mg kg−1 sand). and 109% in tolerant genotypes at 90 mmol L−1 (2010)
NaCl + 60 mg N kg−1 sand as compared to
respective control.
Fino lemon 2-year-old plants grafted on salt tolerant and salt N fertilization via soil solution had beneficial effects on N-induced accumulation of proline, quaternary Gimeno
(Citrus sensitive rootstocks were irrigated for 12 weeks with salinity tolerance, particularly in salt sensitive ammonium compounds and K+ contributed et al.
limon complete nutrient solution containing 0 or 50 mM rootstocks where N decreased leaf Na+ by 59%, leaf to minimizing oxidative and/or osmotic (2009)
Burm.) NaCl with 10 mM KNO3, or 1% KNO3 foliar spray. Cl− 54% but improved leaf K+ 16%, proline 27% and stress.
quaternary ammonium compounds 23% compared
to NaCl stress without additional N.
(Continued )
15
16
M. ASHRAF ET AL.
Indian Plants were grown for 50 days at control, 100 mM Combined application of N and GA3 had maximum N-containing compounds lowered the Siddiqui
mustard NaCl, 40 mg N kg−1 sand (in 2 splits), 10–5 M GA3 alleviating effect on salt stress by increasing proline generation of free radicals and reduced lipid et al.
(Brassica (spray), 100 mM NaCl + 40 mg N kg−1 sand, 100 mM 57%, glycine betaine 44%, K+ 74% with a decrease peroxidation linked membrane damage (2008)
–5 −1
juncea L.) NaCl + 10 M GA3, 100 mM NaCl + 40 mg N kg of 50% in malondialdehyde, 42% in electrolyte under salt stress.
sand + 10–5 M GA3. leakage and 35% in Na+ accumulation compared to
NaCl without N and/or GA3.
Jerusalem At 3rd leaf, uniform sized slices were exposed to 0, 10 N with 25% seawater decreased Na+ by 24%, Cl− 15%, N-induced activation of antioxidant enzymes Xiao-Hua
Artichoke and 25% seawater with and without 7.5 mmol N L−1 malondialdehyde 12%, electrolyte leakage 8% while and increased synthesis of osmolytes under et al.
(Helianthus as NaNO3. Measurements were made after 4, 8 and increased K+ 18%, proline 32%, soluble sugar 45%, seawater irrigation. (2008)
tuberosus) 12 days of treatment completion. catalase 23%, superoxide dismutase 33% and
peroxidase 21% in aerial plant parts compared to
25% seawater without N.
Soybean Seedlings were transferred into N-free (control) and At 100 mM NaCl, superoxide dismutase (SOD)/ NH4NO3-supplied plants were better able to Jeong-Jin
(Glycine N-treatment group (NH4NO3-N, KNO3-N @ 5 and ascorbate peroxidase (APX) ratio was increased by effective removal of oxidative products & Yeon-
max) 10 mM) and received modified McKnight’s solution 212 and 35% with 5 and 10 mM KNO3 while through increasing the balanced activity of Sik
of 100 ml having 0, 50, 100 or 150 mM NaCl daily. decreased by 16 and 28% with 5 and 10 mM SOD and APX in salt environment. (2006)
Measurements were taken 12 days after treatment. NH4NO3. At 150 mM NaCl, SOD/APX ratio was
decreased by 26% and 27% with 5 and 10 mM KNO3,
while decreased by 34% and 8% with 5 and 10 mM
NH4NO3, respectively.
Wheat 17-day-old seedlings were grown in 0.2 strength NO3− or NH4+ nutrition produced 4–50% more N-induced plant tolerance to salinity was Polesskaya
(Triticum Hoagland solution salinized with 300 mM NaCl with chlorophyll-a, 12–55% more chlorophyll-b, 2–30% correlated with the activation of antioxidant et al.
aestivum L.) N-deficient, 3 mM NO3− or 3 mM NH4+. Plants were more carotenoids, 13–19% more glutathione enzymes, accumulation of chlorophyll and (2006)
harvested 3 days after treatment completion. reductase activity while a reduction of 34–41% in carotenoids.
SOD, 5–10% peroxidase and 7.6–27% in catalase
activities compared to salt stressed N-deficient
plants.
oxidative damage by scavenging ROS (Ashraf & Foolad 2007). Proline metabolism might also affect
the redox potential of plant cells associated with signaling development and leading to plant
tolerance to salinity (Heidari et al. 2011). Similarly, N-induced GB synthesis contributes to maintain
the integrity of thylakoid and plasma membranes, protects the protein, chlorophyll and photo-
systems against salinity stress (Tattersall et al. 2009), and thus frequently reverses the damaging
effects of salinity on plant metabolism (Rais et al. 2013). Some other studies, for example, Aroiee
et al. (2005), Shabala and Cuin (2006), Ehlting et al. (2007), Gimeno et al. (2009), Nadian et al. (2012)
have demonstrated that application of N fertilizer to saline environment might help to mitigate the
harmful effects of salts on plant growth by enhancing the accumulation of osmolytes which are
responsible for the detoxification of ROS and alleviate the oxidative damage.
Accumulation of malondialdehyde (MDA) in plant body increases with salinity which indicates
the level of lipid peroxidation, and is used as an important criterion for determining plant
adaptation to saline environment (Giannakoula et al. 2008). N nutrition under saline conditions
increases the synthesis of osmoprotectants which improves plant tolerance to salinity as measured
by reduction in MDA concentration. Siddiqui et al. (2008) have shown that plants fed with
additional N under saline conditions generally have decreased MDA accumulation. N-induced
decline in MDA results from the increased accumulation of N containing compounds which
subsequently improves plant adaptation to saline environment by stabilizing the macromolecules,
maintaining ROS balance, and resisting a change in redox potential of plant cells. In conclusion, N
induced an accumulation of osmolytes contributes to plant tolerance to salinity by maintaining
membrane integrity, improvement in photosynthetic efficiency, reduction in protein and enzyme
denaturation, stimulation of antioxidant defense system and protection of plant macromolecules
against ROS.
Nitrogen forms and salinity tolerance

Plants absorb N principally as NH4+ and/or NO3− (Zhonghua et al. 2011). Plant response to N
application under salinity stress varies greatly depending on whether NH4+ and/or NO3− are added
to growth medium (Crawford & Forde 2002). There may be a higher sensitivity to salinity in NH4+-
fed plants (Leidi et al. 1991), no effect of N form on plant response to salinity stress (Ashraf &
Sultana 2000), or more sensitivity in case of NO3–N (Arghavani et al. 2017). These differences in
plant response to N nutrition in saline environment have been explained on the basis of absorption
and metabolism of NO3− and NH4+ that require different ionic equilibria in which organic and
inorganic cations and anions have a part. Certain plant species such as Pisum sativum L. (Frechilla
et al. 2001), Helianthus annuus L. and Zea mays L. (Rios-Gonzalez et al. 2002), have shown more salt
tolerance with NO3− nutrition in saline environment, other plant species such as Solanum lycoper-
sicum L. (Flores et al. 2001), Catharanthus roseus (Zhonghua et al. 2011), Vicia faba L. (Kamel 2012),
Sorghum bicolor L. (de Souza-Miranda et al. 2014) have performed better when growth medium is
containing NH4+ plus NO3− in equal concentration while Helianthus annuus L. (Ashraf 1999),
Hordeum vulgare L. (Kant et al. 2007), Sorghum bicolor (de Souza Miranda et al. 2016) and many
others exhibited greater response to NH4+ application. In general, plants response to N forms under
salinity stress differs greatly depending upon plant species, salt concentration and composition as
well as rate of N application (Table 6, Figure 3).
NH4+-N and salinity interactions

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 NH4+
assimilation in the roots. As roots are in immediate contact with the salt containing growth
medium, it is possible that N assimilation in NH4+-fed plants is dislocated by salt ionic effects
which would not interfere with shoot-based NO3–N assimilation; (b) in NO3–fed plants, a malate-
18
Table 6. Nitrogen forms and plant adaptation to saline environment.

Kentucky Three salinity levels (0, 40 and 80 mM NaCl) and 80 mM NaCl caused a reduction of 48, 57 and 63% in Effects of increasing NH4+ on the Arghavani et al.
bluegrass three NO3−/NH4+ ratios (6/0.5, 6/1 and 6/2) were dry weight; 35, 50 and 57% in turf quality; 20, 30 decreased K+ content and lower K+:Na+ (2017)
(Poa pratensis applied in nutrient solutions. and 45% in K+ concentration while an increase of ratio.
L.) 800, 850 and 1050% in Na+ concentration with 6/
0.5, 6/1 and 6/2 NO3−:NH4+ ratios compared to
control.
Rice Two N forms – NH4NO3 and urea with three N levels In Cuom cultivar, urea produced 400 and 100% Urea required less energy for assimilation Nhung et al.
M. ASHRAF ET AL.
(Oryza sativa 1.4, 2.1 and 2.8 mM were applied to Yoshida higher dry weight, 290 and 60% root length, 84 than nitrate which firstly reduced to (2017)
L.) solution salinized with 113 mM NaCl. and 71% SPAD value, 85 and 64% leaf area, 475 ammonium.
and 67% N use efficiency at 1.4 and 2.1 mM N,
respectively than NH4NO3.
Sorghum Plants were grown at 75 mM NaCl with 5 NO3−:NH4+ Decrease in leaf area and shoot dry mass of 0:100 Improved plant photosynthetic de Souza Miranda
(Sorghum ratios (100:0, 75:25, 50:50, 25:75 and 0:100) for N-fed stressed plants was minimum (40 and 17%) performance, which reflected an et al. (2016)
bicolor L.) 10 days. compared to 25:75 (72 and 50%), 50:50 (88 and alleviated Na+ toxic effects by NH4+.
67%), 75:25 (66 and 51%) and 100:0 (65 and 47%)
treatments.
Populus simonii Plants were grown in hydroponics at 75 mM NaCl NH4+-fed plants were less tolerant to salinity; root Increased Na+:NH4+ ratio and competitive Meng et al.
supplemented with 1 mM NH4Cl or KNO3 as the N biomass was decreased by 18 and 14%, root inhibition of Na+ and NH4+ (2016)
source length 32 and 17%, stem height 23 and 16%,
chlorophyll content 63 and 50%, photosynthetic
rate 59 and 29% 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 N with 50:50 ratio of NO3−:NH4+ protects de Souza-Miranda
(Sorghum solution salinized with 75 mM NaCl and enriched 34 and 22%, anthocyanins 12 and 23% compared photosynthetic pigments from et al. (2013)
bicolor L.) with 5 mM N in NO3−:NH4+ ratios of 100:0, 75:25, to NO3−:NH4+ of 100:0 and 0:100, respectively. degradation and allows higher PSII
50:50, 25:75 and 0:100. Photosynthetic efficiency was also increased by efficiency under salt stress.
50:50 ratio but non-significantly.
Barley 5-day-old seedlings were grown at 6 mM N in the Mixed NH4+:NO3-N supply produced higher leaf Energy savings associated with N Kant et al. (2007)
(Hordeum form of NO3− or NO3− + NH4+ in the ratio of 75:25 number 42%, shoot and root fresh weights 75% assimilation and more energy allocation
vulgare L.) with 2 NaCl levels (0 and 120 mM) for 25 days. and 60%, total N 11–17% in leaves, glutamine towards salt tolerance mechanisms with
synthetase activity 23%, glutamate dehydrogenase mixed supply.
55% while 11–15% lowered Na+ than NO3− alone
at the same salinity level.
Tomato Plants were grown with 14 mM N at NO3−:NH4+ At 60 mM NaCl, leaf Cl− was increased by 122 and Reduced accumulation of Na+ and Cl− and Flores et al.
(Lycopersicon ratios of 14:0, 12:2 and 10:4. NaCl levels of 0, 30 97%, leaf Na+ 5.6- and 3.5-folds, compared to increased reducing sugars in leaves at (2001)
esculentum and 60 mM were imposed 28 days after control, at NO3−:NH4+ ratio of 14:0 and 10:4, NO3−:NH4+ ratio of 10:4 contributed to
Mill.) transplanting and plants were harvested 42 days respectively. NO3−:NH4+ ratio of 10:4 increased higher salt tolerance than 14:0.
after transplanting. glucose by 40%, fructose 31%, Chl a + b 18% and
leaf Fe 65% compared NO3−:NH4+ ratio of 14:0 at
60 mM NaCl.
(Continued )
Pea Seedlings were grown in hydroponics for 21 days NH4+-fed plants were less tolerant to salinity as Specific Na+ toxicity, low soil water Frechilla et al.
(Pisum with 5 mM N either as Ca(NO3)2, or (NH4)2SO4. shown by a reduction in total soluble sugars of potential or inhibition of the uptake of (2001)
sativum L.) Saline treatments consisted of 1 and 30 mM NaCl. 21% in shoot, 20% in root; organic acids 48% in essential nutrients causing nutrient
shoot; anions 102% in shoot, 269% in root; cations imbalances in the plant.
40% in shoot, 383% in root while an increase of 5-
+ –
fold in plant Na than NO3 fed plants.
Sunflower 8-day-old seedling were grown in Hoagland solution At 120 mM NaCl, N-forms have no effect on shoot NH4+-induced inhibition in cations uptake. Ashraf & Sultana
+ − +
(Helianthus salinized with 0, 60 and 120 mM NaCl and Na and Cl while shoot K was decreased by 93% (2000)
annuus L.) supplied with 8 mM N either as KNO3 or NH4Cl for and Ca2+ 100% with NH4+ compared to NO3–N. In
+ −
21 days. roots, Na was increased by 11%, Cl 33%, while
K+ was decreased by 196% and Ca2+ 97% with
NH4+ compared to NO3–N.
Maize 7-day-old plants were exposed to 20, 50 and 80 mM At 80 mM NaCl, NH4+-fed plants exhibited a NH4+ assimilation in roots, absence of ion Lewis et al.
(Zea mays L.) NaCl with 4 mM NH4+ or NO3−. reduction of 54% in fresh biomass, 59% in translocatory shuttle, higher osmotic (1989)
stomatal conductance, 58% in net photosynthesis effects in NH4+-fed plants.
and 30% in transpiration rate compared to NO3–
fed plants at same salinity.
19
20 M. ASHRAF ET AL.
Figure 3. Nitrogen forms (NH4+ and NO3−) effects on plant adaptation to saline environment.
nitrate shuttle is operative between root and shoot (Lewis et al. 1989). The absence of this shuttle
in NH4+-fed plants could bring about ion translocatory problems which are exacerbated by the
uptake of NaCl; (c) in NH4+-fed plants, carbon utilization during N assimilation resulting 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 al. 2007).
Generally, two processes are competing for the energy utilization in roots of NH4+-fed plants, NH4+
assimilation and Na+ exclusion which could be responsible, at least in part, for low tolerance of
NH4+-fed plants to salinity. High concentration of NH4+ in the growth medium may result in NH4+
toxicity which leads to leaf chlorosis, reduced crop yield, nutrient imbalance, rhizosphere acidifica-
tion and alteration in plant metabolism. Some other studies, for example Lewis et al. (1989),
Frechilla et al. (2001), Rios-Gonzalez et al. (2002) have observed that NH4+-fed plants operated
the metabolic pathways which generated more ROS and produced little beneficial effects on plant
tolerance than NO3–fed plants. Ashraf and Sultana (2000) also observed NH4-treated Helianthus
annuus L. plants accumulated more Cl− while less K+, Ca2+ and Mg2+ than NO3–fed plants, and are
less tolerant to salinity.

On the other hand, Fernández-Crespo et al. (2012) have shown that NH4+ supplementation can
enhance salt tolerance in Citrus sinensis L. because NH4+ toxicity causes mild stress, leading to
stress-induced morphogenetic responses (SIMRs). These responses produce an acclimation stage
which provides better protection to plants against succeeding salinity stress. SIMRs initially
increases H2O2 generation which serve as a modulator of stress signal and enhances plant
adaptation to salinity stress. Another protective mechanism induced by NH4+ against salinity stress
is the maintenance of higher K+:Na+ which could result from restricted uptake and translocation of
Na+ and/or increased Na+ exclusion (de Souza Miranda et al. 2013). 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 (Alvarez-Pizarro et al. 2011). Moreover,
NH4+ nutrition enhances the synthesis of osmolytes which improves salt tolerance through osmotic
adjustment and stimulation of antioxidant defense system. Hessini et al. (2013) reported that NH4+
nutrition is more beneficial to improve plant tolerance to salinity by coordinating the activities of
H2O2-producing enzymes such as superoxide dismutase and H2O2-detoxifying enzymes including
guaiacol peroxidase, glutathione reductase, catalase and ascorbate peroxidase. In conclusion,
NH4+-induced salt tolerance in plants might be attributed to low energy cost of N assimilation,
reduced Na+ uptake, higher synthesis of organic osmolytes, stimulation of antioxidant enzymes
activities and regulation of K+/Na+ homeostasis (Figure 3(a)).
NO3–N and salinity interactions

NO3− is the principal form of N used by plants in aerobic growth medium/soil environment.
However, NO3− has to be reduced to NH4+ prior to its incorporation into organic N compounds
using energy. NO3− assimilation uses 20 mole ATP mole−1, whereas 5 mole ATP mole−1 are required
for NH4+ assimilation (Salsac et al. 1987). In spite of high energy requirements, plants use N mostly
in the form of NO3− because NH4+ accumulation at higher concentration within the plant body
often leads to ion toxicity in plants (Meng et al. 2016). While, NO3− can accumulate in vacuoles that
can play a key role in plant nutrition and osmotic adjustment, conferring more salt tolerance than
NH4+ (Irshad et al. 2002). Furthermore, NO3−assimilation is less restricted by salinity because it
occurs in shoots as compared to NH4+ assimilation that occurs in roots which are in direct contact
with rhizosphere salts. Another mechanism for higher plant tolerance to salinity by NO3–N is its
rapid translocation and accumulation in shoot that serves as a signal for the efficient regulation of
shoot-root allocation (Crawford 1995). In some studies, however, NO3–grown plants have been
found relatively less tolerant to salinity than NH4+-grown plants because Cl− might reduce the NO3−
uptake by plants due to antagonistic effect (Kant et al. 2007), NO3− might favor the Na+ uptake and
22 M. ASHRAF ET AL.
accumulation within the plant cells (Zhonghua et al. 2011), or due to reduction in water use
efficiency and carbon assimilation rate (Ashraf 1999) (Figure 3(b)).
Combination of NH4+ and NO3–N and salinity interactions

The protective role of N against salinity stress is often more effective when both NH4+ and NO3− are
applied in combination to saline environment compared to their sole application. N application
with same amounts of NO3− and NH4+ protects the photosynthetic pigments against salinity stress,
leading to high PSII efficiency under saline conditions. The better performance of 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, reduced ROS
generation, decreased specific ion toxicity, balanced ionic accumulation and better osmotic adjust-
ment (de Souza-Miranda et al. 2014). Some other studies, for example, Lu and Zhang (2000), Miller
et al. (2010) assigned it to the regulation of photosynthetic electron transport with minimum
generation of ROS under salinity stress. Even, the partial substitution of NO3− with NH4+ in the
growth medium can improve plant adaptation to salinity stress because of improved N assimila-
tion, particularly via alternative NH4+ assimilation pathway which reduces the requirement of
energy for N assimilation than the sole application of NO3–N (Kant et al. 2007). Better plant
performance with combined use of NH4+ and NO3− under salinity stress might 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 reported that
underlying mechanisms for improved plant growth with combined N forms might be: (a) improved
water absorption through osmotic adjustment; (b) antagonism between NH4+ and Na+ or NO3− and
Cl−, leading to reduced uptake and translocation of salt ions; (c) enhanced synthesis/accumulation
of osmolytes and (d) maintenance of ion homeostasis. However, the response of N forms to salinity
stress varies widely depending upon many plant as well as soil factors, and the selection of an
appropriate N form should be a major concern in N-salinity interaction studies. In summary, NH4+-N
is energetically inexpensive but it causes ion toxicity at higher concentration and inhibits the
uptake of other ions such as K+, Ca2+ and Mg2+, while NO3− has incremental effect on these ions
but it is energetically expensive. It is believed that for most plant species, NO3− is preferred form of
N under saline conditions, while a small number of plants prefer NH4+, however mixtures of NH4+
and NO3− at ratio of 50:50 can exert consistent beneficial effects on plant growth and metabolism
in saline environment (Figure 3(c)).
Conclusion and future prospects

Salinity stress causes several metabolic alterations in plants such as reduction in water uptake,
disturbance in nutrient balance, specific ion toxicity, increase in ROS generation, disruption of
hormonal balance, inactivation of enzymes, peroxidation of lipids, reduction in chlorophyll synth-
esis and the damage of photosystems which lead to reduced plant productivity. Plant adaptation
to salinity is the result of different ionic, physiological and biochemical mechanisms such as
regulation of ion uptake, translocation and compartmentation, maintenance of plant water status
and ionic balance, biosynthesis of osmolytes, and enzyme activation. Exposure of plants to elevated
salinity levels reduces the N uptake and assimilation, probably due to direct interaction between
salinity and the processes involved in N uptake, utilization or translocation within the plant or via a
salinity-induced reduction of the relative growth rate resulting in a lower N demand. A wide
discrepancy has been found in plant growth behavior to N nutrition under saline conditions
depending upon salt nature and concentration in the root zone, N form applied and plant type.
At low to moderate salinity level, increasing supply of N can efficiently reverse the salinity effects
on plant growth. At higher level of soil salinization, adequate N nutrition partly alleviates the
salinity effects but over N fertilization may aggravate the deleterious effects of salinity. Nitrogen is
contributed to salt tolerance by regulating ion uptake, translocation and distribution, stimulating
plant growth and reducing leaf abscission, activating enzymes, maintaining hormonal balance and
synthesizing N containing compounds which can contribute to osmotic adjustment, stabilize the
cellular structures and scavenging ROS under saline conditions. The understanding of the N
metabolism under salinity stress might be crucial for salt tolerance research, and will be an
important research direction for salt stress physiology in future. Since, plant response to N nutrition
in saline environment changes with stage of plant growth, emphasizing that such interactions
should be studied during the entire life cycle of a plant to find alleviative effect of N against salinity
stress at a specific stage of plant development as well as over time.
Disclosure statement
No potential conflict of interest was reported by the authors.
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00.0 Nitrogen Nutrition and Adaptation of Glycophytes

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Archives of Agronomy and Soil Science

ISSN: 0365-0340 (Print) 1476-3567 (Online) Journal homepage: http://www.tandfonline.com/loi/gags20

Nitrogen nutrition and adaptation of glycophytes

Muhammad Ashraf, Sher Muhammad Shahzad, Muhammad Imtiaz,

To link to this article: https://doi.org/10.1080/03650340.2017.1419571

Published online: 04 Jan 2018.

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Download by: [University of Cambridge] Date: 08 January 2018, At: 23:08

Nitrogen nutrition and adaptation of glycophytes to saline

ABSTRACT ARTICLE HISTORY

N accumulation by plants, particularly glycophytes is severely restricted by salt ions in saline

Plant growth in saline environment

Figure 1. Schematic summary of major salinity stress mechanisms of plants.

Table 1. Salinity stress eﬀects and mechanisms in plants.

Nitrogen eﬀects on plant growth in saline environment

N-induced adaptation mechanisms against salinity stress

N-mediated mitigation of speciﬁc ion toxicity

N-mediated maintenance of nutrient balance

N-mediated osmotic adjustment

Table 3. Nitrogen-mediated maintenance of nutrient balance in plants under salinity stress.

N eﬀects on oxidative damage

Table 4. Nitrogen-mediated adjustment of osmotic stress in plants under salinity stress.

shoots as compared to 20% seawater without N.

Table 5. Nitrogen-mediated amelioration of oxidative damage in plants under salinity stress.

Nitrogen forms and salinity tolerance

NH4+-N and salinity interactions

Table 6. Nitrogen forms and plant adaptation to saline environment.

less tolerant to salinity.

NO3–N and salinity interactions

Combination of NH4+ and NO3–N and salinity interactions

Conclusion and future prospects

maize under saline conditions. J Plant Nutr. 25:189–200.

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