Journal of Plant Nutrition

ISSN: 0190-4167 (Print) 1532-4087 (Online) Journal homepage: http://www.tandfonline.com/loi/lpla20

Salinity effects on nitrogen metabolism in plants –

focusing on the activities of nitrogen metabolizing
enzymes: A review

Muhammad Ashraf, Sher Muhammad Shahzad, Muhammad Imtiaz &

Muhammad Shahid Rizwan

To cite this article: Muhammad Ashraf, Sher Muhammad Shahzad, Muhammad Imtiaz &
Muhammad Shahid Rizwan (2018): Salinity effects on nitrogen metabolism in plants – focusing
on the activities of nitrogen metabolizing enzymes: A review, Journal of Plant Nutrition, DOI:
10.1080/01904167.2018.1431670

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Published online: 23 Feb 2018.

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JOURNAL OF PLANT NUTRITION
https://doi.org/10.1080/01904167.2018.1431670

Salinity effects on nitrogen metabolism in plants – focusing on the

activities of nitrogen metabolizing enzymes: A review
Muhammad Ashrafa, Sher Muhammad Shahzada, Muhammad Imtiazb, and
Muhammad Shahid Rizwanb
a
Department of Soil and Environmental Sciences, University College of Agriculture, University of Sargodha, Sargodha,
Pakistan; bMicroelement Research Center, College of Resources and Environment, Huazhong Agricultural University,
Wuhan, PR China

ABSTRACT ARTICLE HISTORY

Nitrogen (N) metabolism is of great economic importance because it provides Received 12 November 2016
proteins and nucleic acids which in turn control many cellular activities in Accepted 5 September 2017
plants. Salinity affects different steps of N metabolism including N uptake, KEYWORDS
NO3¡ reduction, and NH4C assimilation, leading to a severe decline in crop GDH; GS/GOGAT; N
yield. Major mechanisms of salinity effects on N metabolism are salinity- metabolism; NH4C
induced reductions in water availability and absorption, disruption of root assimilation; NO3¡ reduction;
membrane integrity, an inhibition of NO3¡ uptake by Cl¡, low NO3¡ loading NR; salinity
into root xylem, alteration in the activities of N assimilating enzymes,
decrease in transpiration, and reduction in relative growth rate which results
in a lower N demand. However, the effects of salinity on N metabolism are
multifaceted and may vary depending on many plant and soil factors. The
present review deals with salinity effects on N metabolism in plants,
emphasizing on the activities of N metabolizing enzymes in a saline
environment.

Introduction
Soil salinity as a major environmental stress factor induces several metabolic changes in plants, for
example, reduced water absorption, specific ion toxicity, altered nutrient uptake and metabolism,
reduction in chlorophyll content and photosynthesis, an increase in the production of reactive oxygen
species (ROS), and all such alterations subsequently lead to decreased plant growth and development
(Monteiro et al. 2011; Ahmad et al. 2013; Khan et al. 2014; Acosta-Motos et al. 2017). Salinity generally
depresses nutrient uptake and causes nutrient deficiency or disorders in plants (Ashraf et al. 2017).
Among plant nutrients, nitrogen (N) is perhaps the most important to influence plant growth because
N is a vital component of many compounds including amino acids, amides and proteins, quaternary
ammonium compounds, and polyamines which are involved in plant salt tolerance through different
mechanisms (Kamel 2012; Rais et al. 2013; Zaki 2016; Arghavani et al. 2017). Adequate regulation of N
metabolism is of great significance for plant tolerance to salinity; however, the relationship between
salinity and N metabolism is a very complex network depending on the degree and duration of the salt
stress, the plant species, the plant growth stage, amount, type and form of N in the rhizosphere (Munns
and Tester 2008; Chen et al. 2010; Dai et al. 2015; Teh et al. 2016). Salinity disrupts N metabolism
mainly due to decreased N uptake, altered activities of nitrate (NO3¡) and ammonium (NH4C)-assimi-
lating enzymes, decreased amino acid synthesis, increased activity of hydrolyzing enzymes such as

CONTACT Muhammad Ashraf mashraf_1972@yahoo.com Department of Soil and Environmental Sciences, University Col-
lege of Agriculture, University of Sargodha, Lahore-Khushab Main Bypass, Sargodha 40100, Pakistan.
© 2018 Taylor & Francis Group, LLC
2 M. ASHRAF ET AL.

RNase, DNase, protease and several others (Nathawat et al. 2005, Debouba et al. 2007; Massa et al.
2009; de Souza et al. 2016).
In the saline environment, chloride (Cl¡) is the dominant anion and generally known to compete
with NO3¡ uptake (Abdelgadir et al. 2005) and subsequently diminishes the N accumulation within
plant parts. Many studies demonstrated that salinity-induced increase in Cl¡ uptake is often accompa-
nied by a decrease in plant-NO3¡ concentration. Examples of such an effect have been found in Gos-
sypium hirsutum L. (Chen et al. 2010); Oryza sativa L. (Wang et al. 2012); Sesbania karadge L. (Sadale
and Karadge 2013); Ipomoea batatas L. (Yu et al. 2015); Zea mays L. (Hasan and Miyake 2017); Sesa-
mum indicum L. (Kanagaraj and Desingh 2017). In addition to antagonistic effect of Cl¡ with NO3¡,
NO3¡ uptake may also be inhibited due to inactivation of NO3¡ transporters by the excessive accumu-
lation of salt ions (Balliu et al. 2015), reduction in water absorption due to change in soil water poten-
tial (Ehlting et al. 2007), or the interference of the Cl¡ ion with certain systems of membrane transport
which leads to lower N assimilation and consequently synthesis of amino acids (Queiroz et al. 2012).
Besides limiting the acquisition of NO3¡ by plant roots, salinity also restricts the ability of plants to
reduce and assimilate N by inhibiting the synthesis and activities of N assimilation enzymes including
nitrate reductase (NR), nitrite reductase (NiR), glutamine synthetase (GS), and glutamate synthase
(GOGAT) (Hossain et al. 2012). Salt ions generally affect the activities of NR and NiR either due to
direct inhibition or reduced synthesis (Debouba et al. 2006) while GS due to low availability of gluta-
mate (Kawakami et al. 2013), which are subsequently responsible for decreased N assimilation under
salinity stress. The inhibition of the N assimilation enzyme activities under saline conditions may also
be related to salinity-induced osmotic changes (Debouba et al. 2007) as well as a reduction in NO3¡
uptake (de Souza et al. 2016). Moreover, NR activity is dependent on several internal signals, and
NO3¡ is the first signal that induces the transcription of NR genes (Kaiser et al. 2002). Salinity may
incite the decrease in NO3¡ reduction process, which supplies NH3 for the synthesis of new amino
acids mainly via GS/GOGAT pathway (Wang et al. 2012). The decrease in GS enzyme activity under
salinity stress is mainly associated with low accessibility of glutamate for the GS enzyme because of the
high deviation of glutamate to the synthesis of osmolytes such as proline.
Salinity stress generally results in the elevated level of NH4C content in plants due to rapid proteoly-
sis (Wang et al. 2007). Excessive NH4C has been found to induce the aminating glutamate dehydroge-
nase (GDH), shifting NH4C assimilation from GS/GOGAT to GDH pathway in the saline
environment (Khadri et al. 2001). The activation of aminating GDH pathway by NaCl suggested that
GDH may be involved in vivo in the NH4C detoxification and in the replenishment of glutamate pool,
which is largely required to produce protective metabolites (proline, phytochelatines, etc.). Interest-
ingly, N assimilating enzyme responses to salinity stress often differed greatly depending on plant spe-
cies, cultivars, and analyzed tissues (Zhou et al. 2004).
The findings on the relations between salinity and N metabolism in plants are limited and contro-
versial which highlight the need to compile such information. The salinity–N relations are significantly
different in field experiments with those of greenhouse; soil with solution culture; using simple salts or
a mixture of salts or in long-term studies over the short term. However, for evaluating the effect of
salinity on N metabolism, it is imperative to understand the involvement of salinity in different steps
of N metabolism. The present review deals with salinity effects on N metabolism with a major focus on
salinity interference with N uptake, N assimilation, and N assimilating enzymes activities.

N uptake in saline environment

The process of N uptake by plants is mostly inhibited in saline environment probably due to antagonis-
tic effect of salt ions with NO3¡ and NH4C (Parida and Das 2004), disturbance in N ions loading into
root xylem (Abd-El-Baki et al. 2000), reduced water absorption due to osmotic changes in the root
zone (Gessler et al. 2005), reduction in transpiration rate (da Silveira et al. 1999), damage in root mem-
brane structure (Debouba et al. 2007), and/or lower N demand due to the reduced growth rate of plants
(Ullrich 2001). Many other studies, for example, Abdelgadir et al. (2005), Albassam (2005), Debouba
et al. (2007), Massa et al. (2009), Chen et al. (2010), Balliu et al. (2015), Dai et al. (2015), de Souza et al.
 JOURNAL OF PLANT NUTRITION 3

(2016), Teh et al. (2016), Kanagaraj and Desingh (2017) have also demonstrated the effects of salinity
on N uptake (Table 1).
In the saline environment, Cl¡ is known to compete with NO3¡ during uptake and translocation to
aerial plant parts (Abdelgadir et al. 2005), and thus may decrease N accumulation in plants. Examples
of such effects have been reported in Solanum melongena L. (Savvas and Lenz 2000); Lycopersicon escu-
lentum Mill (Arshad and Rashid 2001); Citrus sinensis (Iglesias et al. 2004); Medicago sativa L. (Albas-
sam 2005); Olea europaea L. (Tabatabaei 2006); Gossypium hirsutum L. (Chen et al. 2007); Zea mays L.
(Hutsch et al. 2016); Triticum durum (Annunziata et al. 2017). Kafkafi et al. (1992) evaluated the differ-
ent sources of Cl¡ and found that Cl¡ from CaCl2 but not KCl, could inhibit NO3¡ uptake in Cucumis
melo and Solanum lycopersicum L. in a range to which the plants would likely be exposed under field
conditions (up to 60 mol/m3). It was only in the higher concentration range (100–200 mol/m3) that
Cl¡ from KCl could inhibit NO3¡ uptake. The authors concluded that the effects of NaCl and KCl
were almost similar; however, NO3¡ inhibition by Cl¡ was much more prominent at the lower salinity
level if the counter ion was Ca2C rather than a monovalent cation. NaC also has antagonistic effect
with NH4C and could cause a significant reduction in NH4C uptake rate under saline conditions (Dluz-
niewska et al. 2007). Reduction in NH4C uptake with increasing NaC concentration in soil solution has
also been observed in Sorghum bicolor L. (Camberato and Bock 1989), Spartina alterniflora (Bradley
and Morris 1991), Triticum aestivum L. (Hawkins and Lewis 1993), Tageta patula (Bahmanzadegan
and Aboutalebi 2013), Gossypium hirsutum L. (Dai et al. 2015).
In addition to the ionic antagonism, salinity can also impair N uptake in plants by reducing plant
water absorption due to changes in soil water potential. Many studies, for example, Lea-Cox and
Syvertsen (1993), Grattan and Grieve (1998), da Silveira et al. (1999), Halperin et al. (2003), Abdelgadir
et al. (2005), Ehlting et al. (2007), Zakery-Asl et al. (2014) have reported that osmotic effects of salt ions
in soil solution decreased water absorption and mass flow of nutrients including N to the roots, and
subsequently caused a marked reduction in the uptake by plants. Besides limiting the N uptake via
ionic antagonism and reduced water availability and absorption, salinity can also restrict N uptake by
reducing plant N demand due to a marked reduction in the relative growth rate (Kafkafi and Bernstein
1996). Some other studies, for example, Touraine et al. (1994) and Van Hoorn et al. (2001) have found
that salinity-induced changes in relative growth rate of plants due to a reduction in photosynthesis
influenced the internal N demand of plants and thereby determined the rate at which N is taken up by
plant roots. N contribution of the soil to plants has also been decreased under salinity stress indicating
the salinity effects on the mineral N production in soil by biological activity through N fixation and
transformation of organic N. In summary, salt ions, particularly NaC and Cl¡ interact with N, reduce
its uptake via ion antagonism, transporter inactivation, restricted water absorption, and/ or reduction
in internal N demand.

N assimilation in saline environment

Assimilation of N into carbon skeletons is of great significance for plant growth and development, par-
ticularly in stress environment (Lea and Mifflin 2003). N assimilation is required not only for the gen-
eral plant growth but also some of its metabolite derivatives are involved in osmotic adjustment and
scavenging of ROS in the salt stressed environment (Gimeno et al. 2009). In higher plants, inorganic N
is first reduced to NH4C prior to its incorporation into organic form by the involvement of NR and
NiR (Zhang et al. 2014). NH4C is toxic to plant cells causing proton extrusion associated with NH4C
uptake, cytosolic pH disturbance, and uncoupling of photophosphorylation. To avoid NH4C toxicity
within the plant body, it must rapidly be assimilated into non-toxic organic N compounds. This can be
achieved by the concerted action of two highly regulated pathways: GS/GOGAT pathway, where NH4C
is incorporated into glutamine (Gln) by GS which is then converted with 2-oxoglutarate to glutamate
(Glu) by GOGAT; and GDH pathway which synthesizes Glu from 2-oxoglutarate and NH4C (Lancien
et al. 2000). NH4C and/or NO3¡ assimilation is inhibited seriously during salinity stress causing a
marked influence on plant N status under saline conditions (Hoai et al. 2005). The high plant sensitiv-
ity to salinity-induced changes in N assimilation leads to more severe deleterious effects on plant
4 M. ASHRAF ET AL.
Table 1. Salinity effects on N uptake by plants.
Plant species Treatment
Sesame (Sesamum Seedlings were salinized by
indicum L.) irrigation daily (500 ml/d)
with the nutrient solution
containing 40 mM, 80 mM
and 120 mM NaCl for 45 d.
Sorghum Plants were grown for 33 d at 5 2 M saline concentration at 0
(Sorghum silicon levels (0, 50, 100, 150,
bicolor) and 200 mM) and 3 saline
concentrations (0, 1.5, and
2.0 M).
Rice Cultivars MR 220 and MR 253
(Oryza sativa) were grown under non-
saline and 150 mM NaCl
using 5 and 10 mM proline
for 30 d.
Tomato (Solanum 30-d-old seedlings (non-
lycopersicum L.) inoculated and inoculated
with Arbuscular mycorrhizal
fungi) were separately
transplanted to plastic pots
filled with nutrient-saturated
vermiculite and exposed to
0, 50, and 100 mM NaCl for
37 d.
Cotton At 2-true leaf stage, seedlings Salinity decreased N
(Gossypium were transplanted to aerated
hirsutum L.) nutrient solution containing
1 mM each of Ca(NO3)2 and
KNO3; for NH4C-N treatment
1.5 mM NH4(SO4)2, with and
without 150 mM NaCl.
Measurements were made
14 d after treatment.
Cotton (Gossypium Four salinity levels 2.4, 7.7, 12.5, N uptake was decreased by
hirsutum L. and 17.1 dS/m, referred to as
non-saline, low, medium,
and high salinity were
created with applying NaCl
and CaCl2 (1:1 weight ratio)
in clay loam soil before
planting. Plants were grown
for 150 d.
Rose (Rosa spp.) 1-year-old plants were
transplanted to nutrient
solution containing 0, 5, 15,
25, 35, 45, 55, 65 mol/m3
NaCl and 7 mol/m3 NO3¡.
¡
NO3 uptake was measured
during first 24 hr.
Tomato Seedlings at 5-leaf stage were In tomato, salinity decreased N
(Lycopersicon transplanted to nutrient
esculentum Mill) solution. After 2 weeks,
Rice (Oryza plants were treated with 0.7
sativa L.) (low N), 7 (medium N), and
14 (high N) mmol/L of N, and
Effect Mechanism Reference
At 45 d after treatment An increase in Cl¡ uptake Kanagaraj
completion, 120 mM NaCl and accumulation was and
reduced N uptake by 53%, accompanied by a Desingh
41%, 23%, 27%, 42%, 48%, decrease in N (2017)
and 31% in variety PAIYUR, concentration.
SVPR-1, TMV-3, TMV-4, TMV-
5, VIR-1, and VIR-2,
respectively, compared to
control.
Direct competition between de Souza
mM of silicon reduced NO3¡ Cl¡ and NO3¡ ions for et al.
concentration by 61% in the same carrier and/or (2016)
roots and 79% in leaves alterations in membrane
compared to 0 salinity level. integrity.
150 mM NaCl reduced shoot Salinity-induced reduction in Teh et al.
NO3¡ content by 7- and 17- plant growth and hence (2016)
folds in MR 220 and MR 253, N demand, and Cl¡
respectively, compared to antagonism.
non-stressed plants.
Salinity caused a reduction of Interference of salt ions with Balliu et al.
40% and 38% in leaf N N uptake and (2015)
concentration, 49% and 43% transportation within the
in relative N uptake rate in plant body.
non-inoculated while 34%
and 111% in N
concentration, 27% and 50%
in relative N uptake rate in
inoculated plants at 50 and
100 mM NaCl, respectively,
compared with the control.
Antagonistic effect of NaC Dai et al.
accumulation whether in with NH4C and Cl¡ with (2015)
NO3¡-N or NH4C-N solution, NO3¡ in saline
but the N levels in NO3¡-fed environment.
plants were higher than
those in NH4C-fed plants;
NO3¡-N was decreased by
about 31% while NH4-N by
35% at 150 mmol NaCl
compared with the 0 NaCl.
Competition between Cl¡ Chen et al.
12.2%, 35.7%, and 16% in and NO3¡ for uptake (2010)
leaves; 12.5%, 37.5%, and sites diminished N
76.1% in bur; 45.2%, 35.7%, uptake in plant parts.
and 9.5% in shed; 21.2, 27.3,
and 42.4 in roots while total
N by 16.1%, 37.7%, and
46.7% at low, medium, and
high salinity, respectively,
compared with non-saline.
NO3¡ uptake was severely Antagonistic action exerted Massa et al.
inhibited by the presence of by Cl¡ inhibited NO3¡ (2009)
NaCl in the nutrient solution. absorption.
It was decreased by 23%,
38%, and 50% at 25, 45, and
65 mol/m3 NaCl compared
with the 5 mol/m3 NaCl.
Reduced water uptake in Abdelgadir
uptake by about 82%, 64%, tomato while Cl¡ et al.
and 65% with Cl¡ and 83%, ¡
antagonism with NO3 in (2005)
50%, and 45% with SO4¡ rice were responsible for
while in rice the decrease low N uptake under
was 86%, 89%, and 91% salinity stress.
(Continued on next page)
 JOURNAL OF PLANT NUTRITION 5

Table 1. (Continued ).
Plant species Treatment Effect Mechanism Reference

7 (control) and 100 mmol/L
Cl¡ or SO42¡ salinity for 16 d.
Alfalfa (Medicago 10-d-old seedlings were
sativa L.) transferred to aerated
modified half strength
nutrient solution. After 5 d,
NaCl were applied at 0, 50,
100, and 150 mM NaCl by
50 mM NaCl at 2 d intervals.
Measurements were made
45 d after sowing.
Tomato 80-d-old plants were grown in
(Lycopersicon sand at 0.3, 4, and 8 bars
esculentum Mill) osmotic pressure by adding
NaCl in nutrient solution. 15N
was applied as 10 mg/pot on
day 1, 11, and 21 of 15N
treatment. N was measured
at 5, 10, 15, 20, 25, 30 d after
treatment.
with Cl¡ and 75%, 86%, and
85% with SO4¡ at low,
medium, and high N levels,
respectively, compared with
the control (non-saline).
The shoot NO3¡ uptake was Antagonistic effect of Cl¡ Albassam
decreased by 29.2% in with NO3¡ and/or (2005)
¡
Siriver, 8.1% CUF-101, 17.7% inhibition of NO3
Hasawi, and 31% Sewa while reductase activity.
root NO3¡ uptake was
decreased by 24.6% in
Siriver, 21.8% CUF-101, 22%
Hasawi, and 36.2% Sewa at
150 mM NaCl compared with
the control.
At 8 bar osmotic pressure, total Direct toxicity of Cl¡ and/or Arshad and
N uptake was decreased by NaC and an antagonistic Rashid
35.45%, 34.44%, 42.68%, effect of Cl¡ on NO3¡ (2001)
66.39%, 66.14%, and 66.56% uptake.
15
while N uptake was
decreased by 43.88%,
52.76%, 60.98%, 74.01%,
77%, and 75.61% at 5, 10,
15, 20, 25, and 30 d after
treatment application,
respectively, compared with
the control (0.3 bar).

growth since several nitrogenous compounds derived from N assimilation such as proteins, amines,
and amino acids are believed to be important for plant tolerance to salinity and other environmental
stresses (Yu et al. 2015). Salinity stress inhibits NO3¡ reduction and NH4C assimilation by reducing
the uptake and transport of N (Khadri et al. 2001), altering the activities of enzymes involved in N
assimilation (Zhou et al. 2004) and changing the pool of amino acids (Ashraf and Bashir 2003), all of
these seem to be highly implicated in the regulation of plant growth in the saline environment. Many
studies, for example, da Silveira et al. (2001), Khadri et al. (2001), Maighany and Ebrahimzadeh
(2004), Kwinta and Cal (2005), Debouba et al. (2006), Iqbal et al. (2006), Hossain et al. (2012), Queiroz
et al. (2012), Wang et al. (2012), Kawakami et al. (2013), Yu et al. (2015) have reported the effects of
salinity stress on N assimilation in plants (Table 2).

NO3¡ reduction in saline environment

NO3¡ is the main source of N for the higher plants and about 99% of the organic N in the biosphere is
derived from NO3¡ assimilation (Heldt 1997; Yao et al. 2008). On transportation into root cells, NO3¡ is
stored in the vacuole, reduced in the cytoplasm, or transported to the leaves where it can be stored or
reduced (Crawford 1995). NO3¡ is reduced to NH4C by the NO3¡ assimilatory pathway (Sadale and Kar-
adge 2013) which takes place in two successive enzymatic steps; NO3¡ is first reduced to NO2¡ by NR, a
cytoplasmic enzyme, using pyridine nucleotide as the source of reductant (Cao et al. 2008). Since this
NO2¡ is highly reactive, plant cells immediately transport the NO2¡ from the cytosol into chloroplasts in
leaves and plastids in roots where it is further reduced to NH4C by NiR (Rosales et al. 2011). Finally, NH4C
is incorporated into amino acids by the GS/GOGAT pathway (Hirel and Lea 2002). NO3¡ assimilation is
appeared to be very sensitive to salinity. Salinity interferes with the uptake, transportation, and reduction of
NO3¡ in a wide variety of crops including Vigna unguiculata (da Silveira et al. 2001), Anacardium occiden-
tale (da Silveira et al. 2003), Triticum durum (Carillo et al. 2005), Morus alba L. (Surabhi et al. 2008),
Arabidopsis thaliana (Maaroufi-Dguimi et al. 2011), Glycine max L. (Queiroz et al. 2012). When plants are
exposed to a moderate level of salinity, roots often contain higher concentration of NO3¡, while NO3¡ in
 6

Table 2. Salinity effects on N assimilation in plants.

Plant species Treatment Effect Mechanism Reference

Sweet potato Uniform seedlings of salt-sensitive and salt-tolerant In salt-sensitive cultivar, GS and NADH-GOGAT NaCl-induced NH4C efflux could deplete cellular Yu et al. (2015)
(Ipomoea cultivars at 5–6 functional leaves were subjected activities were decreased by 50% and 40% in roots NH4C pool and disrupt NH4C assimilation.
batatas L.) to 100 mM NaCl for 6 d. while 40% and 60% in leaves, respectively,
compared to control after 6 d of NaCl treatment.
However, in salt-tolerant cultivar, GS and NADH-
M. ASHRAF ET AL.

GOGAT activities were not significantly affected.

Cotton Plants were grown in untreated control, High salinity caused 2.06- and 1.67-fold decrease in Reduced NR activity (due to direct inhibition of NR Kawakami et al.
(Gossypium recommended N, 80% of recommended N, 80% of leaf NO3¡ reduction compared with the low and activity and/or low NR synthesis) and GS activity (2013)
hirsutum L.) recommended NCNBPT and 80% of moderate salinity levels, respectively. Leaf NH4C (due to low availability of glutamate) which are
recommended NCNBPT and DCD. Low (0.45), assimilation was decreased 18% by high salinity the main enzymes responsible for N assimilation.
moderate (8), and high (16) dS/m salinity levels compared with moderate salinity, while 20% by
were used. moderate salinity compared with low-salinity. Leaf
protein content was 15% lower at high salinity
than low salinity.
Tomato 10-d-old seedlings were transplanted to half-strength NO3¡ reduction was decreased by 15.50% and 33.35% Cl¡ ions inhibited NO3¡ uptake resulted in the low Hossain et al.
(Lycopersicon Hoagland’s nutrient solution at 0 (control), 60, and in leaves, 16.27% and 37.20% in roots; NO2¡ NO3¡ content in plant tissues and subsequently (2012)
esculentum) 120 mM NaCl by adding 30 mM per day. Plants reduction was decreased by 6.7% and 9.32% in decreased N reduction under salinity stress.
were harvested at day 7 after treatment. leaves, 27.25% and 47.27% in roots while soluble
protein content was decreased 25.64% and 42.75%
at 60 and 120 mM NaCl, respectively, compared
with the control.
Soybean (Glycine 45-d-old plants were irrigated with 250 mL of A strong decline in the root NO3¡ and amino acids Inhibition of NO3¡ uptake by Cl¡ ion leading to lower Queiroz et al.
max L.) complete nutrient solution twice a week. NaCl was was found in the presence of NaCl. Root NO3¡ N assimilation and subsequently synthesis of (2012)
added to nutrient solution gradually until the final contents were decreased by 72%, 80%, and 83% amino acids under salinity stress.
concentrations of 50, 100, and 200 mM were while root amino acids were decreased by 58.91%,
reached. 70.93%, and 62% with 50, 100 and 200 mM NaCl,
respectively, compared to control.
Rice (Oryza sativa 7-d-old seedlings were transferred to hydroponics. When seedlings were subjected to salt stress for 5 d, Salinity-induced NO3¡ deficiency caused Wang et al. (2012)
L.) After 12 d, plants were subjected to 0 (control) most of genes involved in NH4C assimilation were downregulation of genes involved in NH4C
and 100 mmol/L NaCl. The solutions were downregulated by salt stress. In shoot, OsNR1 was assimilation (OsGS1;2, OsGS2, OsNR1, and OsFd-
replaced daily. Measurements were made after downregulated by 72.18%, OsGS1;1 27.15, OsGS2 GOGAT).
4 hr and 5 d. 87.74 and OsFd-GOGAT by 78.67% while OsGDH2
activity was upregulated by 54.85%.
Tomato Plant seedlings were grown in hydroponics for 10 d NO3¡ reduction was decreased in leaves by 30% and Inhibition of NO3¡ reduction in leaves was associated Debouba et al.
(Lycopersicon without NaCl, and then exposed to 25, 50, 37% at 50 and 100 mM NaCl, respectively, while in with low availability of NO3¡ to NR, or NR (2006)
esculentum) 100 mM NaCl for 10 d. 100 mM NaCl was achieved roots it was increased by 60% at 25 mM but not inactivation by NaC and Cl¡ in the cytosol under
by a daily increase of 50 mM. Plants were changed at 50 and 100 mM NaCl. NO2¡ reduction salinity stress. Reduction in NH4C assimilation in
harvested 6 hr after the beginning of the was decreased by 30% at 50 mM NaCl in leaves leaves was due to low accessibility of glutamate
photoperiod and sorted immediately into leaves while it was decreased by 32%, 39%, and 78% in for the GS enzyme.
and roots for enzymatic experiments. roots at 25, 50, and 100 mM NaCl, respectively.

Wheat (Triticum Plants of 3 cultivars were grown in pots having sandy Salt stress reduced NO3¡ reduction rate in all cultivars. Inhibition of NR activity and/or reduced rate of
aestivum L.) loam soil at 5 and 10 dS/m salinity by adding
Na2SO4, CaCl2, MgCl2, and NaCl at the ratio of
70:35:10:23, respectively. N reduction was
measured at vegetative and reproductive growth
stages.
Wheat (Triticum Plants of salt sensitive and tolerant cultivars grown in In salt sensitive cultivar, 300 mM NaCl reduced NO3¡ NaCl-induced reduction in xylem transport rate of
aestivum L.) 3-kg mixture of medium textured soil, sand, and
manure in a ratio of 2:1:1, respectively, were
treated with 0, 50, 100, 200, and 300 mM NaCl at
22, 45, 58, and 69 d after sowing (DAS) and grown was increased by 150% in leaves but decreased
for a week after treatment completion.
Common bean The seeds were planted in modified Leonard jar
(Phaseolus assemblies containing vermiculite, and nutrient
vulgaris) solution with 1 mM KNO3. Solution was changed
after 3 d. After 18 d, plants were treated with 0,
25, 50, and 100 mM NaCl and harvested at 3, 6, 9
and 12 d after treatments (DAT).
Cowpea (Vigna 8-d-old plants were pre-acclimated at 0 and 50 mol/ NO3¡ uptake and its assimilation from leaf-NR activity NaCl-osmotic shock reduced NO3¡ uptake as well as
3
unguiculata L.) m NaCl in nutrient solution during 8 d.
Subsequently, pre-acclimated and non-acclimated
plants were subjected to NaCl-osmotic shock
(100 mol/m3) in the nutrient solution for 4 d.
Plants were harvested at day 0, 1, 2, 3, and 4 after
treatment completion.
NH4C assimilation was decreased by 18% at
100 mM NaCl in leaves while it was increased in
roots by 50, 30, and 19% at 25, 50, and 100 mM
NaCl, respectively.
Iqbal et al. (2006)
At the vegetative stage of plants, N reduction was enzyme synthesis under salinity stress.
decreased by 35% in wheat cultivar LU-26S, 39% in
Sarsabaz, and 44% in Pasban-90 at 10 dS/m
compared with control. At the reproductive stage,
N reduction was decreased by 42% in LU-26S, 53%
in Sarsabaz, and 42% in Pasban-90 at 10 dS/m
compared with control.
Maighany and
reduction by 44% and 50% at 22 DAS, 41% and NO3¡ from root to shoot or from vacuole to Ebrahimzadeh
70% at 45 DAS; 30% and 59% at 58 DAS in leaves cytoplasm (2004)
and roots, respectively. In salt tolerant cultivar, it
50% in roots at 22 DAS; decreased 66% in leaves
and 70% in roots at 45 DAS; decreased by 57% in
leaves and 64% in roots at 58 DAS.
Plants subjected to salt stress could utilize the GDH Salinity-induced inhibition in GS/GOGAT cycle led to Khadri et al. (2001)
pathway instead of the GS/GOGAT cycle for NH4C NH4C accumulation in plants which triggered
assimilation. Plant exposure to 50 and 100 mM NH4C assimilation pathway from GS/GOGAT to
NaCl reduced GS and GOGAT activities between 30 GDH.
and 50% from 9 DAT. The AAT was inhibited by
between 20% and 40% by 50 and 100 mM NaCl in
the third and fourth harvests, while almost no
effect appeared at 25 mM in any of the harvests.
da Silveira et al.
were more limiting to N assimilation under NaCl– loading into the root xylem and consequently (2001)
salinity than NH4C assimilation from GS activity. reduced NR activity and NO3¡ reduction.
100 mol m¡3 NaCl caused a decline in leaf NO3¡
accumulation (100–70% of initial value) in non-
acclimated and 50–35% in pre-acclimated plants,
NR activity 100–45% non-acclimated and 70–43%
in pre-acclimated plants while NO3¡ reduction
100–45% in non-acclimated and 80–36% in pre-
acclimated plants compared with control.
JOURNAL OF PLANT NUTRITION
7
8 M. ASHRAF ET AL.

shoot becomes very low, suggesting that loading of NO3¡ into root xylem is especially a salt-sensitive step
(Debouba et al. 2007). This may have severe consequences for whole-plant NO3¡ assimilation because
NO3¡ is a major signal affecting NR expression and activity under salinity stress. Some other studies, for
example, Iqbal et al. (2006), Hossain et al. (2012), Ahanger and Agarwal (2017) reported that salinity stress
caused an alteration in the uptake and transport of NO3¡ that influenced the N assimilation with the conse-
quent inhibition of amino acid and protein metabolism. They found that decrease in NR activities due to
either direct inhibition or reduced rate of enzyme synthesis under salinity stress could be responsible for
reduction in NO3¡ assimilation. Hossain et al. (2012) have demonstrated that during N assimilation in a
saline environment, major inhibitory effects of high salinity are on NO3¡ uptake rather than NO3¡ reduc-
tion. They found that salinity largely influenced the activity of NO3¡ transporter rather than its induction.
So, susceptibility of the NO3¡ transporter to salinity injury rather than that of the NO3¡ reduction system
might be a critical factor to plant survival during salt stress. Furthermore, salinity-induced decline in NO3¡
uptake and flux into the stem has been found to decrease leaf NR activity and hence NO3¡ assimilation
(Parida and Das 2004), whereas inhibition of root NR activity is less frequently reported under salinity
stress (Meloni et al. 2004). Salinity-induced higher inhibition of NR activity in leaves is mainly due to the
decreased xylem transport rate of NO3¡ from root to shoot or from vacuole to cytoplasm (Maighany and
Ebrahimzadeh 2004). In conclusion, salinity-induced decline in NO3¡ reduction could mainly be attributed
to inhibition of NO3¡ uptake by roots, restricted NO3¡ loading into root xylem, and alterations in NR
activities either due to direct inhibition or reduced rate of enzyme synthesis under salinity stress.

NH4C assimilation in saline environment

All inorganic N is generally first reduced to NH4C because it is the only reduced form of N available to
plants for assimilation into N-carrying compounds such as amino acids (Ruiz et al. 2007). The first
step is catalyzed by GS which forms glutamine, and subsequently glutamine is changed to glutamate by
GOGAT. It has been reported that NH4C originating from either direct absorption, NR activity, photo-
respiration, dinitrogen fixation, or deamination of nitrogenous compounds is assimilated into organic
N compounds by the GS and the GOGAT which are the major enzymes involved in NH4C assimilation
(Frechilla et al. 2002; Esposito et al. 2005; Wickert et al. 2007). A number of studies have shown that
the process of NH4C incorporation into plant metabolism is inhibited by salinity stress to varying
degree depending on many plant- and soil-related factors (da Silveira et al. 2003; Debouba et al. 2006;
Queiroz et al. 2012; Yu et al. 2015). Salinity-induced decline in NH4C production in plants might be
associated with downregulation of genes (OsGS1; 2, OsGS2, OsNR1, and OsFd-GOGAT) involved in
NH4C assimilation due to NO3¡ deficiency which subsequently led to the inhibition of N assimilation
under salinity stress (Wang et al. 2012). According to Meng et al. (2016), the GS and GOGAT activities
are responsible for NH4C absorption, and generally the GS activity is higher than GOGAT under nor-
mal conditions. However, salinity stress inhibits the activities of both enzymes and GOGAT is found
to be more sensitive to salt effects, particularly at higher salt concentration suggesting that the latter
enzyme is the more limiting factor in NH4C assimilation under salinity stress. Some other studies, for
example, Khadri et al. 2001 and Kawakami et al. (2013) have also reported that salinity-induced inhibi-
tion of NADH-GOGAT is more responsible for limiting the NH4C assimilation in plants.
It is commonly believed that the GS/GOGAT pathway is the major mechanism for NH4C assimila-
tion under normal growth conditions. However, decline in GS/GOGAT activities under salinity stress
limits the production of glutamine and amino acid while increases NH4C accumulation which activates
GDH pathway, an alternative pathway for NH4C assimilation in a saline environment. An example of
such effects has been found in Phaseolus vulgaris (Khadri et al. 2001), Oryza sativa L. (Wei et al. 2004),
Triticale hexaploide Lart (Kwinta and Cal 2005), Solanum lycopersicum (Zhang et al. 2014), leading to
the accumulation of NH4C ions in plant cells which in turn triggered GDH aminating activity in plants.
Hence, plants subjected to abiotic stress including salt stress could utilize the GDH pathway instead of
the GS/GOGAT cycle for NH4C assimilation. Kumar et al. (2000) reported that the increasing deami-
nating GDH activity in Oryza sativa L. plants growing under salinity stress indicated that the enzyme,
through glutamic acid breakdown into 2-oxoglutarate, sustained carbohydrate metabolism by
 JOURNAL OF PLANT NUTRITION 9

supplying an intermediate to the tricarboxylic acid cycle. GDH deaminating activity is also a source of
reduction force in the shape of NAD (P) H, which plays an important role in many metabolic processes
(Lasa et al. 2002). On the other hand, salinity stress may also lead to an increase in leaf protein catabo-
lism, yielding high amounts of NH3 and free amino acids. There are two ways of metabolic detoxifica-
tion of NH3 in tissues of higher plants: (i) detoxification of excessive NH3 by simple acceleration rate
of N assimilation via usual pathway (GS/GOGOAT pathway) or (ii) supplementing the normal path-
way by additional NH3 utilizing reactions, initiated only at times when there is an excessive level of
NH3 in tissues (GDH pathway) (Wang et al. 2012). Both of these mechanisms seem to be operative
during certain environmental conditions with the “additional NH3 utilizing reactions” which are par-
ticularly important during accumulation of the N-containing compounds (Rabe 1994). It is summa-
rized that salinity stress could result in elevated levels of NH3 either due to inhibition of NH4C
assimilation or enhanced proteolysis. The accumulation of NH3 is paralleled by a sharp rise in GDH
activity, which is primarily involved in the catabolism of glutamate to oxoglutarate, thus providing car-
bon skeleton for tricarboxylic acid (TCA) cycle, with the concomitant release of NH3. The excess of
NaC and Cl¡ might change the pathway of NH4C assimilation by inactivation of GS/GOGAT pathway
and stimulation of GDH pathway.

Activities of N metabolizing enzymes under salinity stress

The activities of various enzymes involved in N metabolism are influenced to varying degree by the
excessive concentration of salts in the growth medium depending on plant species, cultivars, analyzed
tissues, type, and concentration of salts and duration of stress. Such effects have been extensively stud-
ied in various plant species including Zea mays L. (Abd-El Baki et al. 2000), Oryza sativa L. (Wei et al.
2004), Triticale hexaploide Lart. (Kwinta and Cal 2005), Olea europaea L. (Tabatabaei 2006), Solanum
lycopersicum L. (Debouba et al. 2007), Brassica napus L. (Bybordi 2010), Triticum aestivum (Abd-El
Baki 2014), Populus simonii (Meng et al. 2016) (Table 3). On the basis of changes in the enzyme activi-
ties under salinity stress, two types of responses have generally been distinguished: (a) early responding
enzymes, which are changed as early as 24 hr after adding salts to the growth medium, i.e., NR and
deaminating GDH in leaves, and Fd-GOGAT in the leaves and roots; and (b) late responding enzymes,
which are affected at least 4 d after the salt treatment, i.e., NADH-GOGAT in leaves, NAD-GDH in
roots, and NiR, GS and aminating GDH in both leaves and roots. The prime enzyme of NO3¡ assimila-
tion is NR, which catalyzes the conversion of NO3¡ to NO2¡, known to play a major role in the uptake
of NO3¡ by serving as NO3¡ transporter (Marschner 1995). It is localized mainly in the cytoplasm of
plant cells and can be found in the roots and leaves of most plant species (Oaks and Hirel 1985). NR
activity is associated with protein synthesis and plant growth, both of which are influenced by salinity
stress (Iqbal et al. 2006). This enzyme has been studied extensively by various groups of investigators
for its behavior in different plant species under salinity stress (Nathawat et al. 2005; Carillo et al. 2005;
Debouba et al. 2006). It has been found that NR activity was greatly depressed in shoots and roots of
different plant species including Phaseolus vulgaris L. and Gossypium hirsutum L. (Gouia et al. 1994),
Zea mays L. (Abd-El Baki et al. 2000), Olea europaea L. (Tabatabaei 2006) in the presence of excessive
salts. Salinity-induced decline in NR activity has generally been attributed to three distinct mecha-
nisms: direct inhibition of the enzyme activity by salt ions (Plaza et al. 2009), reduced NO3¡ uptake
and translocation, and low NR enzyme synthesis (Carillo et al. 2005). The decline in NR activities in
the saline environment may be related to osmotic changes and/or low NO3¡ availability (Debouba
et al. 2007). Plants exposed to salinity stress often exhibit high restriction in acquisition of NO3¡ from
the nutrient solution. As a direct consequence, these plants have a lower NO3¡ accumulation in their
tissues, particularly in stems and leaves which subsequently leads to a proportional decrease in leaf NR
activity (Klobus et al. 1988) and in situ NO3¡ reduction (Aslam et al. 1984). Some other studies, for
example, Foyer et al. (1998), Forde (2000), Parida and Das (2004), Wang et al. (2004) have reported
that a salinity-induced decrease of NO3¡ uptake and flux into the stem has been found to reduce leaf
NR activity whereas inhibition of root NR activity is less frequently reported. Under the conditions of
restricted NO3¡ flux induces by salinity stress or water deficit, NR activity may be lowered initially on
10 M. ASHRAF ET AL.

account of enzyme degradation/inactivation, reduction in gene expression and NR protein synthesis

(Carillo et al. 2005). Reduction in NO3¡ content in plant leaves and roots under saline conditions
causes a restrictive effect of salinity on the NO3¡ uptake and assimilation processes (da Silveira et al.
2001). However, NR activity has been less affected in the roots than in the leaves, despite the large
decrease in NO3¡ concentrations due to NaCl in both organs, suggesting that NR is regulated differ-
ently by NO3¡ availability in different plant organs. Different assimilates such as sugars and amino
acids may also be involved in the control of NR expression in plants under salinity stress (Matt et al.
2001). Indeed, NO3¡ regulates NR transcription, translation, and activation in higher plants. A positive
correlation between NR activity and NO3¡ concentrations has been found in plant leaves and roots. In
this sense, cytosolic NO3¡ seems to protect the NR enzyme against the action of proteases and/or
inhibitors besides triggering the de novo synthesis of NR protein by the induction of NR gene
expression.
The inhibition of NR activities under salinity stress can reduce the activities of NiR in plants. Ogawa
et al. (2000) have confirmed the hypothesis of a co-regulation between NR and NiR which is indispens-
able to prevent NO2¡ toxicity and to avoid the waste of electrons by NR and NiR activities. Salinity has
been found to decrease the upregulation of NO3¡ uptake, NO3¡ influx, and NO3¡ reduction which
consequently inhibit the NR and NiR activities (Flores et al. 2004). However, compared to NR activity,
NiR activity is relatively less affected which may be related to more stable nature of NiR proteins in
plants (Bray 1997). Debouba et al. (2006) conducted an experiment with Lycopersicon esculentum using
25, 50, and 100 mM NaCl and found that NiR activity was much higher than NR in saline environment
indicating more stable nature of NiR under saline conditions. This imbalance assured that toxic levels
of NO2¡ are not reached in the cytosol.
GS has an important role in the assimilation of toxic NH3 derived from direct NH4C root uptake, N2
fixation, NO3¡ reduction, and photorespiration (Blevins 1989). GS is the main enzyme of NH3 assimi-
lation with energy provision by ATP. The enzyme catalyzes the combination of NH3 and glutamate
into glutamine and transfers inorganic N into organic N. The circle reaction consisting of GS and
GOGAT is the main pathway of NH4C assimilation in plants (Lam et al. 1996). GS/GOGAT activities
are decreased under salinity stress (Wang et al. 2007) which may be attributed to either direct inhibi-
tion of the enzyme (Wei et al. 2008), low GS enzyme synthesis (Kawakami et al. 2013), or low availabil-
ity of glutamate (Debouba et al. 2006). In the saline environment, reduced GS/GOGAT activities or
increased proteolysis generally accumulated NH4C which stimulated GDH activities and shifted NH4C
assimilation from GS/GOGAT to GDH pathway. The essential function of GDH enzyme is the deami-
nation of glutamate to provide carbon skeletons and reducing power for plant cells (Robinson et al.
1991). Kwinta and Cal (2005) have observed an increase in the aminating and deaminating GDH activ-
ities in both shoots and roots of Triticale hexaploide Lart. seedlings grown in the presence of 100 mM
NaCl. They found that NaCl inhibited NH4C assimilation, leading to the accumulation of NH4C ions
in plant cells, which in turn stimulated GDH aminating activity. The activation of GDH pathway by
salinity stress suggests that GDH may be involved in the NH4C detoxification and in the replenishment
of glutamate pool, which is highly required to produce protective metabolites under salinity stress. Salt-
induced increase in the aminating GDH activity may be considered as an alternative N assimilation
pathway involved in the NH4C detoxification and glutamate synthesis (Surabhi et al. 2008). Therefore,
plant tolerance to salinity may be attributed, at least in part, to the ability to shift the metabolic rate;
greater accumulation of amino acids coupled with a lesser accumulation of ammonia, largely by re-
assimilation by relatively greater activities of GDH in the tissue (Bielawski 1993; da Silveira et al. 1998;
Zhang et al. 2015). Taken all together, it may be concluded that activities of N assimilating enzymes
are influenced differently by salinity stress. Increasing NaCl concentration generally causes a marked
decrease in the activities of NR, NiR, GS, GOGAT while there is an increase in the activities of GDH.

Conclusions and future prospects

N uptake and transport within the plant body have been found to be sensitive to salinity, and this
might have severe consequences for N metabolism in the plants under salinity stress. In the saline
Table 3. Salinity effects on the activities of N metabolizing enzymes in plants.
Plant species Treatment
Populus simonii Plants were grown in hydroponics at 75 mM NaCl
supplemented with 1 mM NH4Cl or KNO3 as the N
source.
Wheat (Triticum 21-d-old plants in sand clay soil were treated with 0 Shoot NR activity was decreased by 16.4% in Bani suief 1, Osmotic changes and reduced NO3¡ transport from Abd-El Baki
aestivum) (control), 50, 100,150, and 200 mM NaCl by top
irrigation and then grown further for 79 d.
Tomato (Solanum Seedlings at 3rd leaf stage were transplanted to
lycopersicum) modified half strength Hogland solution. At 6th true
leaf stage, they were exposed to 0 (control);
75 mmol/L saline-alkaline solution of NaCl: Na2SO4:
NaHCO3:Na2CO3 (1:9:9:1) for 4 d.
Canola (Brassica Plants were grown for 12 months in pots filled with
napus L.) sand and perlite mixture (1:1), irrigated with half
strength Hoagland solution having 0, 50, 100,
150 mM NaCl and 100, 200, 300 mg L¡1 N.
Tomato (Solanum Plants were grown for 10 d in control medium, and
lycopersicum L.) then for 10 d in the presence of 100 mM NaCl. NaCl
concentration was increased to 50 mM on the first
day and then to 100 mM on the second day to avoid
osmotic shock.
Olive (Olea Plants were grown in pots filled with sand and perlite NR activity in 150 mM NaCl treated plants was decreased Reduced NO3¡ uptake or translocation to leaves
europaea L.) mixture (1:1) for 12 months at 0, 50, 100, and
150 mM NaCl.
Triticale (Triticale Seedlings were grown for 14 d in nutrient solution
hexaploide containing 5 mM NO3¡ and then treated with
Lart.) 100 mM NaCl. Measurements were made after 7 d of whereas NADPH-dependant GDH activity was
salt treatment.
Effect Mechanism Reference
Salt stress had only minor effects on NR and NiR activities NaCl caused a reduction in NH4C production from Meng et al.
in both NH4C and NO3¡-fed plants. However GS photorespiration, which immediately (2016)
activity was reduced by 75% (roots) and 65% (leaves) downregulated the OsGS2 and OsFd-GOGAT
in NH4C-fed, whereas 52% (roots) and 46% (leaves) in and weakened the GS/GOGAT pathway.
NO3¡-fed plants. Root GOGAT activity was reduced by
C ¡
74% in NH4 -fed and 56% in NO3 -fed plants. No
change in leaf GOGAT activity was observed after salt
exposure.
13.5% in Bani suief 3, 26.4% in Seds6 but increased by roots to shoots impaired the NR activity in (2014)
41% in Seds1 at 200 mM NaCl compared to control. shoots.
Salinity-alkalinity stress decreased NR activity by 26 and Reduced NO3¡ but enhanced NH4C uptake, Zhang et al.
78%, NiR 11 and 8%, GS 29 and 38% while GDH was increased proteolysis decreased NR, NiR, GS/ (2014)
increased by 42 and 100% in cvs Jinpeng chaoguan GOGAT but increased GDH activities.
and Zhongza No. 9, respectively. GOGAT was
increased by 6% in Jinpeng chaoguan but decreased
by 13% in Zhongza No. 9 compared with the control.
150 mM NaCl caused a decrease in NR activity by 57%, Reduced uptake or translocation of NO3¡ leads to Bybordi
69%, and 62% at N100; 18%, 41%, and 55% at N200 lower NO3¡ concentration in leaves, (2010)
in SLM046, Licord and Okapi, respectively, while 91% subsequently reducing NR activity under salinity
at N300 in SLM046. Plants of Okapi and Licord at stress.
NaCl150 and N300 were completely died at the end
of the experiment.
Leaf NR activity was decreased to 60% in only 24 hr by Inhibition in N assimilation enzyme activities under Debouba
the NaCl treatment and then it gradually increased saline conditions might be related to NaCl- et al.
after 7th day, and reached 50% of the control value at induced osmotic changes and/or low NO3¡ (2007)
the end of treatment. Leaf NiR activity was decreased availability.
by 25% at 10th day. GS activity was lowered by 20–
25% with respect to control leaves. NADH-GOGAT
decreased by 30% and 40% compared with control at
7th and 10th day after treatment, respectively.
Tabatabaei
by 27%, 58%, and 52% in cvs Mission, Manzanillo and under salinity stress. (2006)
Zard, respectively, compared with the control.
GS activity in roots of salt-stressed plants was increased Salinity-induced reduction in GS activity caused Kwinta and
by 16% but in shoots, it was decreased by 27% NH4C accumulation in leaves which stimulated Cal (2005)
GDH pathway.
JOURNAL OF PLANT NUTRITION
increased by 200% in roots and 290% in shoots
compared to control plants.
(Continued on next page)
11
 12

Table 3. (Continued ).
Plant species Treatment Effect Mechanism Reference

Maize (Zea mays L.) Seedlings were transplanted to modified Knop solution Leaf NR activity was decreased by about 30% in Cyrkon Antagonistic effect of Cl¡ with NO3¡ and/or Sacala et al.
cvs Limko and and exposed to 60 mmol dm¡3 NaCl or 60 mmol and 60% in Limko under NaCl while 62% in Cyrkon inhibition of activity or synthesis of NR under (2005)
¡3 ¡3
Cyrkon dm NaCl C 5 mmol dm CaCl2 for 7 d. and 47% in Limko under NaClCCaCl2 treatment salinity stress.
compared with the control.
Rice (Oryza sativa 7-d-old seedlings were sown on the nylon net floating 150 mM NaCl caused a decrease of 15%, 31.2%, and Reduced NO3¡ reduction decreased GS and NADH- Wei et al.
M. ASHRAF ET AL.

L.) on nutrient solution and exposed for 72 hr to 0, 50, 43.4% in GS, 1%, 30%, and 31% in NADH-GOGAT GOGAT activity while increased proteolysis (2004)
100, and 150 mmol/L NaCl. while an increase of 6%, 42%, and 50% in NADH-GDH caused accumulation of NH4C which stimulated
in the roots of Jindao 779, Jin-zhu-1 and Zao-hua-2, GDH activity.
respectively, compared with the control.
Maize (Zea mays L.) After 12 d growth in nutrient solution, seedlings were NaCl caused considerable reduction in leaf NR activity Reduced leaf NO3¡ accumulation due to restricted Abd-El Baki
exposed for 1 d to 150 mM NaCl by adding 50 mM (about 50% of the control plants) while root NR NO3¡ loading into root xylem. et al.
NaCl daily. activity was slightly increased under saline conditions. (2000)
 JOURNAL OF PLANT NUTRITION 13

environment, N uptake is markedly inhibited due to antagonistic effects of salt ions, reduced water
absorption, restricted plant growth, and damaged membrane integrity. The NO3¡ reduction to NO2¡
and then NH4C by NR and NiR, respectively, is known to be negatively influenced by salinity-induced
enzyme degradation/inactivation and the reduction in gene expression and protein synthesis, with
greater reduction in NR compared to NiR activity. The NH4C assimilation by GS/GOGAT is also
restricted by salinity stress either due to enzyme inactivation or reduced activities of NR and NiR.
Salinity might cause accumulation of NH4C ions in plant cells due to inhibition in the activities of
main NH4C assimilation enzymes (GS/GOGAT) or enhanced proteolysis, stimulating GDH aminating
activity, alternative enzymes for GS/GOGAT cycles in plants. Furthermore, the NO3¡ reduction and
NH4C assimilation are increased in the roots when these processes are inhibited by salt stress in the
leaves. It seems that NaCl stress can shift N metabolism from leaves to roots in an attempt to sustain
plant growth in a saline environment. However, the effects of salinity on N metabolism are highly com-
plicated and involve complex regulatory mechanisms. The understanding of the N metabolism in
response to salinity stress, therefore, might be crucial for salt tolerance research and would be an
important research direction for salt stress physiology in future. Moreover, research work at the molec-
ular level will improve the understanding of N enzyme expressions and activities under salinity stress,
in order to discern whether salt effects on plant growth are due to mineral disturbances and/or to meta-
bolic changes.

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