Plant Growth Regul

DOI 10.1007/s10725-014-0013-y

REVIEW PAPER

Phytohormones and plant responses to salinity stress: a review

Shah Fahad Saddam Hussain Amar Matloob Faheem Ahmed Khan
Abdul Khaliq Shah Saud Shah Hassan Darakh Shan Fahad Khan
Najeeb Ullah Muhammad Faiq Muhammad Rafiullah Khan
Afrasiab Khan Tareen Aziz Khan Abid Ullah Nasr Ullah
Jianliang Huang

Received: 18 August 2014 / Accepted: 12 December 2014

Springer Science+Business Media Dordrecht 2014

Abstract Plants are exposed to a variety of abiotic

stresses in nature and exhibit unique and complex
responses to these stresses depending on their degree of
plasticity involving many morphological, cellular, anatomical, and physiological changes. Phytohormones are
known to play vital roles in the ability of plants to acclimatize to varying environments, by mediating growth,
development, source/sink transitions and nutrient allocation. These signal molecules are produced within the plant,
and also referred as plant growth regulators. Although plant
response to salinity depends on several factors; nevertheless, phytohormones are thought to be the most important
endogenous substances that are critical in modulating
physiological responses that eventually lead to adaptation
to salinity. Response usually involves fluctuations in the
levels of several phytohormones, which relates with

changes in expression of genes involved in their biosynthesis and the responses they regulate. Present review
described the potential role of different phytohormones and
their balances against salinity stress and summarized the
research progress regarding plant responses towards
salinity at physiological and molecular levels. We
emphasized the role of abscisic acid, indole acetic acid,
cytokinins, gibberellic acid, salicylic acid, brassinosteroids,
jasmonates, ethylene and triazoles in mediating plant
responses and discussed their crosstalk at various baseline
pathways transduced by these phytohormones under
salinity. Current progress is exemplified by the identification and validation of several significant genes that
enhanced crops tolerance to salinity, while missing links on
different aspects of phytohormone related salinity tolerance
are pointed out. Deciphering mechanisms by which plant

S. Fahad
S. Hussain
F. Khan
A. Khan
A. Ullah

J. Huang (&)
National Key Laboratory of Crop Genetic Improvement, MOA
Key Laboratory of Crop Ecophysiology and Farming System in
the Middle Reaches of the Yangtze River, College of Plant
Science and Technology, Huazhong Agricultural University,
Wuhan 430070, Hubei, China
e-mail: jhuang@mail.hzau.edu.cn

S. Hassan
Khyber Pakhtunkhwa Agricultural University, Peshawar 25000,
Pakistan

A. Matloob
A. Khaliq
Department of Agronomy, University of Agriculture, Faisalabad,
Punjab 38040, Pakistan
F. A. Khan
Key Laboratory of Agricultural Animal Genetics, Breeding and
Reproduction, Huazhong Agricultural University,
Wuhan 430070, Hubei, China

D. Shan
Women Institute of Learning, Abbottabad, Pakistan
N. Ullah
Department of Plant and Food Sciences, The University
of Sydney, Sydney, Australia
M. Faiq
M. R. Khan
A. K. Tareen
Kasetsart University, Bangkok 10900, Thailand
N. Ullah
Department of Plant Biology and Ecology, Nankai University,
Tianjin, China

S. Saud
Department of Horticultural, Northeast Agricultural University,
Harbin 150030, China

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Plant Growth Regul

perceives salinity and trigger the signal transduction cascades via phytohormones is vital to devise salinity related
breeding and transgenic approaches.
Keywords Abiotic stress
Climate change
Plant growth
regulators
Phytohormones
Salinity
Stress tolerance

Introduction
World population is envisaged to increase by 34 % in 2050
reaching about 9.1 billion, thus necessitating 70 % more food
production (FAO 2009). Fulfilling food requirement of a
burgeoning population remains a challenging task as climate
changes have endangered the sustainability and productivity
of the agricultural production systems (Hussain et al. 2014).
Plants are exposed to a variety of abiotic stresses under field
conditions. Modern agriculture too faces several abiotic
stresses, such as sub-optimal levels of salinity, drought,
chilling and heat as major constraint affecting crop yields
(Tardieu and Tuberosa 2010; Saud et al. 2013). More than
50 % reduction in average yield of major crops has been
attributed to the abiotic stresses (Wang et al. 2001). Crop
plants elicit a complex and unique cellular and molecular
response in response to various stresses in order to prevent the
damage and ensure survival (Fahad et al. 2015). Although the
underlying mechanisms of abiotic stresses may vary
depending upon the specific nature and extent of stress, stage
and duration of plant exposure, yet the ultimate outcome of
exposure to stress is the reduction in germination, growth and
final yield of crops (Parida and Das 2005; Munns and Tester
2008). Plants employ many strategies in response to abiotic
stresses that ultimately enhance the plant growth and productivity in stressful environments. These phenomena include
change in morphological and developmental pattern (growth
plasticity) as well as physiological nd biochemical processes
against several stresses (Tuteja 2007; Saud et al. 2014).
Adaptation to all these stresses is accompanied with metabolic
adjustments that lead to the accumulation of several organic
solutes like sugars, polyols, betaines and proline, protection of
cellular machinery, maintenance of ionic homeostasis, scavenging of free radicals, expression of certain proteins and upregulation of their genes and induction of phytohormones
(Parida and Das 2005; Tuteja 2007; Munns and Tester 2008).
Phytohormones, often regarded as plant growth regulators
in literature refer to the compounds derived from plant biosynthetic pathways that can act either locally (at the site of
their synthesis) or transported to some other site within plant
body to mediate growth and development responses of both
under ambient and stressful conditions (Peleg and Blumwald
2011). Growth and development in the sessile plants is regulated in a coordinated fashion by the activity of several
phytohormones like abscisic acid (ABA), gibberellins (GA),

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ethylene (ETHY), auxins (IAA), cytokinins (CKs), and

brassinosteroids (BRs), which control many physiological
and bio-chemical processes (Iqbal et al. 2014). However, in
recent years, new compounds like polyamines, nitric oxide
(NO) and strigolactone have also been added to this list (Gray
2004). These hormones may act either close to or remote
from their sites of synthesis to regulate responses to environmental stimuli or genetically programmed developmental changes (Davies 2004). Phytohormones thus have a vital
role in mediating plant response to abiotic stress, by which
the plant may attempt to escape or survive the stressful
conditions and may result in reduced growth so that the plant
can focus its resources on withstanding the stress (Skirycz
and Inze 2010). Abiotic stresses often lead to alterations in
production, distribution or signal transductions of growth as
well as stress hormones, which may promote specific protective mechanisms (Eyidogan et al. 2012). Indeed, perception of a stress signal triggers the signal transduction
cascades in plants with phytohormones acting as the base
line transducers (Harrison 2012).
Worldwide, soil salinity has adversely affected about 30 %
of the irrigated and 6 % of total land area (Chaves et al. 2009)
with a resultant monetary loss of 12 billion US$ in agricultural
production (Shabala 2013). Soil salinization is one of major
stress affecting more than 831 million hectares of the agricultural lands worldwide (Table 1; FAO 2005). Increased
incidence of salinity on arable lands suggests the need of a
better understanding of the plant tolerance mechanisms in
order to sustain crop productivity by modulating growth
conditions to the best possible extent. Inhibition of growth and
development, reduction in photosynthesis, respiration and
protein synthesis in sensitive species have been reported under
salinity (Parida and Das 2005; Tuteja 2007; Munns and Tester
2008; Hussain et al. 2013; Mustafa et al. 2014). Excessive
generation of reactive oxygen species (ROS) such as superoxide anion, hydrogen peroxide and the hydroxyl radicals,
particularly in chloroplasts and mitochondria is an important
indication of salinity induced oxidative damage in plants
(Masood et al. 2006). To rectify damaging effects of ROS,
plants employ antioxidant enzymes to protect nucleic acid,
proteins and membrane lipids (Prochazkova and Wilhelmova
2007; Munns and Tester 2008). Disruption of membrane
structure and permeability, metabolic toxicity and damage to
ultrastructures due to ROS, and attenuated nutrients are the
factors that initiate more catastrophic events in plants subjected to salinity stress (Zhu 2000; Cost et al. 2005).
Recent studies mainly focused on understanding the
mechanisms of salt tolerance in plant along with general
consequences of its harmful effects (Parida and Das 2005;
Chinnusamy et al. 2005; Tuteja 2007; Munns and Tester
2008), and control of ionic homeostasis and osmotic shock.
The influence of phytohormones in modulating biochemical events and physiological processes of plants under

Plant Growth Regul

Table 1 Regional distribution
of salt-affected soils (million
hectares)

Source: FAO land and plant

nutrition management service

Regions

Total area (Mha)

Saline soils

Sodic soils

Mha

Mha

%
1.8

Africa

1,899

39

2.0

34

Asia, the Pacific and Australia

3,107

195

6.3

249

8.0

Europe

2,011

0.3

73

3.6

Latin America

2,039

61

3.0

51

2.5

Near East

1,802

92

5.1

14

0.8

North America

1,924

0.2

15

0.8

12,781

397

3.1

436

3.4

Worlds total

salinity is now widely acknowledged (Fatma et al. 2013).

Although plant response to salinity depends on several
factors and their relative importance can vary in time and
space, still phytohormones are thought to be the most
important endogenous substances that are critical in modulating physiological responses that eventually lead to
adaptation to an unfavorable environment, as is the case
under salinity (Khan and Khan 2013). Endogenous level of
these compounds could help predict the mechanisms of
tolerance or susceptibility of plants (Velitcukova and Fedina 1998) as many proteins expressed by plants under
stress are induced by phytohormones (Hamayun et al.
2010). Meager plant growth under salt stress could be an
outcome of altered hormonal balance (Iqbal et al. 2012),
and reduced emergence and diminished growth has been
attributed to decreased endogenous levels of phytohormones (Jackson 1997). Exogenous application of phytohormones has been proposed as a pragmatic approach to
cope with salt stress (Iqbal et al. 2012) and implicated in a
number of studies with a fair degree of success in alleviating adverse effect of salinity (Sharma et al. 2013; Iqbal
and Ashraf 2013a, b; Amjad et al. 2014). Plants treated
exogenously with phytohormones revealed prompt and
transitory variations in genome-wide transcript profiles
(Chapman and Estelle 2009). Thus, understanding the role
of individual phytohormone or its crosstalk with other
phytohormones would yield crucial information on
molecular mechanisms conferring adaption to saline soils.
In present review, we discussed the potential role of
phytohormones in alleviating adverse effect of salinity on
plants. We also summarized the recent progress in engineering of hormone-associated genes aimed at improving
the stress tolerance in plant.

Phytohormones and abiotic stresses

Abscisic acid (ABA)
Abscisic acid has been proposed to play an important role
in stress responses and/or adaptation (Sharma et al. 2005)

as ABA mediated signaling is known to regulate the

expression of salt-responsive-genes under salinity (Narusaka et al. 2003). It plays a significant role during many
stages of the plant life cycle, including seed development
and dormancy, and mediates plant responses to various
environmental stresses (Eyidogan et al. 2012; Devinar et al.
2013). The ABA is often regarded as the stress hormone as
it acts as the major internal signal enabling plants to survive adverse environmental conditions (Keskin et al.
2010). It is now well thought-out as a plant stress hormone
because different stresses tend to induce ABA synthesis
(Mahajan and Tuteja 2005). It acts as an endogenous
messenger to regulate the plants water status. It plays an
important role in regulating plant water status and growth,
through guard cells as well as by induction of genes (Zhu
2002). Zhang et al. (2006) reported that plants exposure to
salinity is known to make a proportional increase in ABA
concentration that is usually associated with leaf or soil
water potential. Concentration of ABA increases in roots,
when root continues their growth, which suggests that these
tissues may have different responses to the restricted ABA
concentration either in endogenous form, or when exogenously applied (Jia et al. 2002). Hartung et al. (2002)
argued that pH changes play a key role in the ABA
redistribution in leaf tissues and control the stomata at
times when no significant changes in ABA concentration
are detected in the xylem.
ABA in conjunction with other phytohormones regulates control of root growth, stress perception triggered
expression of responsive genes and proteins (dehydrins and
late embryogenesis abundant proteins) as well accumulation of compatible solutes under stress (Zhu 2002; Sharp
et al. 2004; Verslues et al. 2006; Fahad et al. 2015). Rapid
and significant accumulation of ABA under salinity is
pivotal to plant protective mechanisms (Shakirova et al.
2010) and synchronizes with expression of early saltinduced genes in roots (Parida and Das 2005). The facilitating role of salt-induced ABA in restricting Na? and Cl-1
in leaves and mediating leaf expansion is also documented
elsewhere (Cabot et al. 2009). The ABA can limit transpiration and resulting water loss by regulating stomatal

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closure (Wilkinson and Davies 2010). This stomatal closure upon exposure to salinity is presumably because of
ABA-induced increased concentration of Ca?? in cytoplasm. Succeeding activation of ion channels in plasma
lemma, and turgor losses by guard cells are also related to
ABA-induced augmentation of H2O2 production that
serves as an intermediate signal of ABA in stomatal closure
process (Kim and Wang 2010). This phytohormone is also
crucial regarding synthesis and accumulation of osmoprotectants like proline (Iqbal et al. 2014) and dehydrins in
response to ROS generation under salt-stress-induced
dehydration (Szabados and Savoure 2009; Hara 2010). The
ABA-mediated accumulation of H2O2 causes generation of
NO that in turn activates mitogen-activated protein kinase
(MAPK) thus upregulating genes for antioxidant enzymes
to scavenge ROS (Zhang et al. 2007a; Lu et al. 2009). The
positive influence of ABA in conferring salinity adaptation,
manifested in the form of reduced Na? concentration and
its shoot translocation has been documented (Khadri et al.
2007). The presence of ABA caused significant increase in
vacuolar contents of Na? while discouraging its xylem
transport and plasmalemma influx in barley (Hordeum
vulgare L.) roots (Behl and Jeschke 1981). Exogenous
application of ABA was helpful in averting accumulation
of toxic Cl-1 ions in citrus leaves thereby limiting ETHY
release and leaf abscission under salinity (Gomez et al.
2002). Increase in K?/Na? in response to exogenous
application of ABA was conducive to salinity tolerance in
rice (Bohra et al. 1995). Recently, Gurmani et al. (2013)
documented that exogenous application of ABA was
effective in averting ionic content of Na? and Cl- and
Na?/K? ratio in rice. These authors further concluded that
ABA increased rice grain yield by increasing accumulation
of proline, soluble sugars and K? and Ca?? homeostasis.
There is strong experimental evidence that supports the
notion of increased membrane stability owing to greater
Ca?? uptake as the ABA contents increased under salt
stress (Parida and Das 2005). Zorb et al. (2014) found
significant increase in ABA concentration in leaves of salt
resistant maize hybrids under salinity. They argued that
such an increase is indispensable for acidifying the apoplast as a growth prerequisite. Similar findings are also
reported for salt resistant genotype of tomato that recorded
higher ABA concentration in xylem sap under salinity
(Amjad et al. 2014).
Application of ABA exogenously at 100 lM to Indica
rice seedlings improved survival rate by 20 % and provoked accumulation of proline via expression of OsP5CS1
gene in rice. Salt-stress-induced expression of OsP5CS1
gene required increase in endogenous ABA level (Sripinyowanich et al. 2013); (Mahajan and Tuteja 2005) stated
that various transcription factors regulate the ABAresponsive gene expression. Salinity stress is known to up-

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regulate the generic stress hormone ABA and induce genes

involved in salt and osmotic alleviation (Wang et al. 2001).
Shi and Zhu (2002) also reported the regulations of AtNHX1 expression and tissue distribution by ABA and salt
stress. Effects of ABA on expression of two genes such as
HVP1 and HVP10 for vacuolar H?-inorganic pyrophosphatase and one HvVHA-A for the catalytic subunit (subunit A) of vacuolar H? ATPase have been discussed by
Fukuda and Tanaka (2006). Quantification of the transcript
levels revealed the hormones liable for adaptable expression of these genes in barley in reaction to salt stress.
Keskin et al. (2010) reported faster induction of MAPK4like genes (TIP1 and GLP1) in wheat crop due to ABA
treatment. The substantive support of this finding is supported by the role of these genes in the ABA-induced
pathways (Javid et al. 2011). For a better understanding,
the mechanisms that upregulates ABA biosynthesis genes
under salinity stress are still need to be elucidated and
further research is inevitable to understand the functions of
all the different types of ABA-responsive genes.
Auxins (IAA)
The IAA is the first identified plant hormone; nevertheless,
its biosynthetic pathway at the genetic level has remained
unclear (Fahad et al. 2014). The IAA plays a key role in
regulating plant growth related processes like cell elongation, vascular tissue development and apical dominance
(Wang et al. 2001). Although IAA has widely been
acknowledged for its implications in plant growth and
development; yet, it can govern plant growth response to
stress or coordinate growth under stressed conditions
(Eyidogan et al. 2012). IAA also responds to salinity in
crop plants (Iqbal et al. 2014) and a link between auxin
signaling and salt stress has been established (Jung and
Park 2011). They suggested that under salinity, seed germination is modulated by a membrane bound transcription
factor (NTM2) that incorporates auxin signal in seed germination. Adding further, Park et al. (2011) reported that
salt signaling pathway is mediated by overexpression of
IAA30 gene of NTM2. Nevertheless, little information is
available on the relationship between IAA levels in plants
under salinity, and the role of IAA in mitigating salt stress
(Javid et al. 2011). Abiotic stresses, like salinity can
influence IAA homeostasis due to alterations in IAA
metabolism and distribution. Moreover, generation of ROS
in response to abiotic stresses may also influence auxin
response (Schopfer et al. 2002). Under salinity, the variations in IAA content appeared to be similar to those of
ABA. According to Ribaut and Pilet (1994), the increased
level of IAA has reportedly been correlated with reduced
growth suggesting alterations in plant hormonal balance
under stress conditions. Hence, to counter this situation,

Plant Growth Regul

exogenous application of IAA provides an attractive

approach. Nilsen and Orcutt (1996) concluded that exposure of rice plants to salinity stress significantly reduced
IAA levels over an incubation period of 5 days. Recent
work of Iqbal and Ashraf (2013a) reported a non-consistent
effect of GA3 priming (150 mg L-1) on auxin concentration in salt-tolerant and -intolerant wheat genotypes. Seed
priming with different sources of auxins (IAA, IBA and
tryptophane) effectively diminished the negative implications of salt stress on endogenous ABA concentration in
salt-intolerant wheat cultivar (Iqbal and Ashraf 2013b).
Moreover, grain yield was also positively associated with
endogenous IAA concentration.
Seed priming with IAA was effective in mitigating the
inhibitory effects of salt stress on germination and growth
of wheat via regulation of ionic homeostasis and auxininduced biosynthesis of free salicylic acid in leaves (Iqbal
and Ashraf 2007). Fahad and Bano (2012) noted that
salinity significantly reduced the IAA levels in maize
plants; nonetheless, salicylic acid application was effective
in increasing the same to a significant extent as compared
to saline control with no salicylic acid application. These
results suggest that hormonal balance and their cross talk is
critical regarding signal perception, transduction and
mediation of stress response. Transcriptions of a large
number of genes are stimulated by auxin called primary
auxin-response-genes. From different plant species, a large
number of auxin-responsive-genes have been identified and
characterized, including soybean, Arabidopsis and rice
(Hagen and Guilfoyle 2002). These responsive genes have
been separated into three gene families: auxin/indoleacetic
acid (Aux/IAA), GH3 and small auxin-up RNA (SAUR)
gene families. Auxin restricts the outgrowth of tiller buds
in rice by down regulating OsIPT expression and cytokinin
biosynthesis in nodes (Liu et al. 2011). However, the novel
genes identification involved in salt stress responses provides the basis for researchers to devise genetic engineering strategies for greater stress tolerance (Zhu 2002).
Further researches should be conducted to understand the
biosynthetic pathway of IAA at the genetic level in future.
Cytokinins (CKs)
Naturally occurring CKs are N6-substituted adenine
derivatives containing either aromatic or isoprenoid side
chain. This phytohormone play a significant role during
several plant growth and developmental processes including cell division, chloroplast biogenesis, apical dominance,
leaf senescence, vascular differentiation nutrient mobilization, shoot differentiation, anthocyanin production, and
photo-morphogenic development (Davies 2004; Fahad
et al. 2014). The CKs are also known to alleviate the
adverse effects of salinity on plant growth (Barciszewski

et al. 2000; Fahad et al. 2014). Seed priming with CKs was
reported to increase plant tolerance to salinity stress (Iqbal
et al. 2006). These authors inferred that decreased concentration of ABA in plants developing from kinetin
primed seeds was possibly responsible for alleviation of
salt stress in wheat. Application of CKs can reverse leaf
and fruit abscission that are induced by ABA or water
stress. Contrary to ABA that inhibits germination; CKs
release seed dormancy. They act as ABA antagonists and
IAA antagonists/synergists in various plant processes (Iqbal et al. 2006) and help alleviating salinity stress (Iqbal
et al. 2014). Decrease in CKs level has been suggested as
an early response to salt stress; nevertheless, influence of
salinity on salt-sensitive variety of tomato was not mediated by Cks since reduction in growth preceded any decline
in Cks (Walker and Dumbroff 1981). During plant growth
and development, CKs are master regulators, and were
recently shown to control plant adaptation to salt stress
(Hadiarto and Tran 2011). Wu et al. (2013) reported
increased salinity tolerance via increased proline contents
in egg plant under exogenous application of CKs. Under
salinity, CKs play an important role by acting as an
intermediate in the demonstration of protective role of
epibrassinolide and methyl jasmonate in wheat (Shakirova
et al. 2010). Inhibition of K-shuttle activity limits CKs
transport under salinity (Cruz et al. 1995) and decreased
level of CKs have been reported in root and shoot of
resistant barley plants just after addition of 65 mM NaCl to
the nutrient solution. Nevertheless, adverse influence of
salinity on growth of salt-sensitive plants preceded the
lowering of CKs in levels suggesting genotypic specificity
(Kuiper et al. 1989). The concentrations of zeatin (Z),
zeatin riboside (ZR), isopentenyl adenine (iP), and isopentenyl adenine (iPA) in shoots and roots of barley cultivars decreased significantly after exposure to salinity
(Kuiper et al. 1990). In salt-sensitive variety of barley,
addition of benzyl adenin inhibited its growth, but in a salttolerant variety it overcame the negative impact on growth
rate, shoot/root ratio and internal CKs content (Kuiper et al.
1990). Chakrabarti and Mukherji (2003) reported that Kinetin acts as a direct free radical scavenger or it may also
involve in the antioxidative mechanism that are related to
the safety of purine breakdown. In stress responses, a
possible involvement of genes is often inferred from
changes in the transcript abundance in response to a given
stress trigger. In stress-response assays functional analyses
of CKs receptor mutants exhibited that all three CKs
receptors of Arabidopsis act as negative regulators in ABA
signaling and in the osmotic stress responses. CKs dependence of this activity was demonstrated for CRE1/AHK4
(Tran et al. 2007). Expression of a great number of stressinduced genes is regulated by plant hormones, including
CKs. Merchan et al. (2007) reported that CKs receptor

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Plant Growth Regul

genes of other species are regulated by changes in the

osmotic conditions as well, demonstrating that in the
osmotic stress response their function might be common
although mechanistically not well understood. Despite their
established role in plant/crop development, feeble information is available regarding how CKs are reduced under
saline conditions. The reduction in the CKs level raises the
question whether the hormones biological activity was
minimized by enhancing temporary storage or whether it
was metabolized and this aspect needs to be explored in
future studies for a better insight.
Gibberellic acid (GA)
The GA is known to be actively involved in regulating
plant responses to the external environment (Chakrabarti
and Mukherji 2003). It is an important phytohormone that
can impart stress tolerance including salinity, in many crop
plants (Hoque and Haque 2002). Rapid accumulation of
GA is a characteristic of plants exposed to abiotic stresses.
Under abiotic stress specific concentration GA3 can be
beneficial for the physiology and metabolism of many
plants, since it regulates the metabolic process as a function
of sugar signaling and antioxidative enzymes (Iqbal et al.
2011). The GA greatly influence the processes of seed
germination, leaf expansion, stem elongation, flower and
trichome initiation, and fruit development (Yamaguchi
2008). Through their influence on photosynthetic enzymes,
GAs are known to improve the photosynthetic efficiency of
plants, leaf-area index, light interception, enhanced efficiency of nutrients and play an important role in modulating diverse processes throughout plant development
(Khan et al. 2007). The integrated mechanisms induced by
GA enhance the source potential and redistribution of
photosynthates thus increasing sink strength (Khan et al.
2007). It has been verified that the morphological and stress
protective effects of triazoles (TR) are reversed by GA3
(Gilley and Flecher 2007), thereby indicating an intimate
relationship between GA3 and plant stress protection.
Reduced level of bioactive GAs in salt-treated Arabidopsis
plants suggested that salt-induced reduction in growth was
presumably because of modulation of GA metabolism
pathway (Achard et al. 2006).
The GA has been reported to alleviate the adverse
effects of salinity stress on plant water relations and water
use efficiency (Yamaguchi 2008). Maggio et al. (2010)
reported that in tomato plants, application of GA decreased
stomatal resistance and improved efficiency of plant water
use at lower salinity level. Treatment with GA may
increase crop growth and yield under saline condition.
Therefore, to return metabolic activities to their normal
levels, exogenous application of growth hormones may
benefit under stressful environments (Iqbal et al. 2011). GA

123

improved growth of soybean by regulating the level of

other phytohormones under salinity (Hamayun et al. 2010).
Such improvement was attributed due to increased level of
bioactive GA1 and GA4 with a concurrent decrease in level
of ABA and SA in soybean treated with GA3. In brassica,
application of GA in conjunction with nitrogen was helpful
in alleviating salinity stress (Siddiqui et al. 2008). The
positive influence of GA under salinity was attributed to
increased water level and in part to maintenance of protein
and RNA levels. Increasing levels of salinity diminished
wheat growth; nevertheless, seed treatment with GA was
quite effective in averting negative implications of salinity
on wheat growth (Kumar and Singh 1996). Signaling of
GA was required for adjustment to adverse environmental
conditions and helped maintain sourcesink relationship
(Iqbal et al. 2011) as salinity caused a reduction in sink
enzyme activities. This usually leads to increased sucrose
contents in source leaves due to reduced photosynthetic
rate as a consequence of feedback inhibition (Iqbal et al.
2011). GA increased nitrogen and magnesium in leaves and
roots under salinity (Tuna et al. 2008). The positive influence of GA3 on salt stressed mung bean seedlings was
manifested due to multiple effects like increased reducing
sugars, activity of enzymatic antioxidants, protein synthesis and decreased activity of ribonuclease and polyphenol
oxidase (Mohammed 2007).
The GA3-priming-induced modulation of ions uptake
and partitioning (within shoots and roots) and hormonal
homeostasis under salinity; nevertheless, homeostasis of
this hormone itself is still unclear (Iqbal et al. 2011; Iqbal
and Ashraf 2013a, b; Fahad et al. 2014). Radi et al. (2006)
stated that pre-soaking wheat seeds in GA enhanced the
germination potential especially at moderate salinization
levels. Under stressful conditions, reduced plant growth
could result from an altered hormonal balance and application of phytohormone provides an attractive approach to
cope with stress (Vettakkorumakankav 1999). The acquisition of stress protection in barley was intimately related
to the GA levels (Vettakkorumakankav 1999). There is a
correlation among the survival of salt toxicity and the
function of DELLA proteins (Achard et al. 2006). These
results advocate that the salt-inducible DDF1 (dwarf and
delayed flowering 1) gene is involved in growth responses
under high salinity conditions in part through altered GA
levels and improves seed germination. Results from different species revealed that IAA promotes GA biosynthesis
(Wolbang et al. 2004). On the other hand, catabolism of
ABA is enhanced by GA application (Gonai et al. 2004).
Moreover, GA increases ETHY on one hand while on the
other; its own signaling mechanism is affected by ETHY
suggesting a cross talk to occur between these phytohormones. Conclusively, modulation of GA is an attractive
approach for conferring protection against salt stress.

Plant Growth Regul

Root of control maize plant

Root of maize plant affected

by salinity stress

Root of Maize plant enhanced

by Salicylic acid application
during saline condition

Fig. 1 Effect of salicylic acid on root length of maize under salinity stress. Salicylic acid application improved the growth of maize root under
saline condition as compared to stress conditions without salicylic acid application

Different approaches to modulate GA levels in plants can

be integrated to form the basis for novel crop protection
strategies with global implications.
Salicylic acid (SA)
The SA play a critical role in the regulation of plant
growth, development, and interaction with other organisms
and defense responses to environmental stresses (Senaratna
et al. 2000; Devinar et al. 2013; Bastam et al. 2013). Its
role is evident in seed germination, glycolysis, flowering,
fruit yield, ion uptake and transport, photosynthetic rate,
stomatal conductance, transpiration, thermo-tolerance,
senescence and nodulation (Khan et al. 2003).
Major role of SA in plant is thought to be the regulation
of responses to biotic stresses; however, a large body of
literature now suggests that SA is also involved in responses
to several abiotic stresses including salt stress (Khodary
2004; Javid et al. 2011; Fahad and Bano 2012; Bastam et al.
2013; Iqbal et al. 2014; Fahad et al. 2014). Dela-Rosa and
Maiti (1995) found an inhibition in the chlorophyll biosynthesis in sorghum plants because of salt stress. Positive
effects of SA on photosynthetic capacity could be attributed
to its stimulation of Rubisco activity and pigment contents.
Plants treated with SA exhibited higher values of pigment
concentration than those of control or salinity-treated
samples. Soybean plants treatment with SA, increased
pigments content as well as the rate of photosynthesis (Zhao
et al. 1995). In another study, SA treatment of salt stressed
maize was found to stimulate their salt tolerance via
accelerating their photosynthesis performance and carbohydrates metabolism (Khodary 2004). Fahad and Bano
(2012) observed that SA increased the level of IAA and
decreased the ABA contents in maize plants under salinity.

Similarly under stress conditions, SA treatment showed an

increase in root growth (Fig. 1), superoxide dismutase,
peroxidase and ascorbate peroxidase activities of maize as
compared to salt treatment while decreased the catalase
activity. SA has been reported to exert a differential influence on the activities of antioxidative enzymes. Recently,
Bastam et al. (2013) also found that exogenous application
of SA led to increased salt tolerance in seedlings of pistachio. Salt ameliorative effects of SA has been well documented for crops like bean (Azooz 2009), wheat
(Sakhabutdinova et al. 2003), barley (El-Tayeb 2005),
mung bean (Khan et al. 2010; Nazar et al. 2011) and mustard (Syeed et al. 2011). Besides exogenous application of
SA, its addition to the soil also manifested salt ameliorative
effects in maize and mustard by decreasing accumulation of
toxic ions (Gunes et al. 2007). The salinity tolerance under
SA treatments has been ascribed to the accumulation of
compatible solutes like proline and glycine betaine (Palma
et al. 2009) and upregulation of antioxidative systems
(Nazar et al. 2011). Plants treated with SA also exhibited
lower lipid peroxidation and membrane permeability that
otherwise was quite higher under salinity (Horvath et al.
2007). Salt-induced decline in photosynthetic rate of mustard was rectified by SA application due to induced activity
of nitrate reductase and ATP-sulfurylase and antioxidant
metabolism (Nazar et al. 2011). Pre-treatment of Arabidopsis with SA suppressed salt-induced membrane depolarization and loss of K? via guard cell outward rectifying
channel (Jayakannan et al. 2013).
In future, exploitation of this phytohormone as a stress
management tool will be a subject of interest as it can
impart tolerance to our agricultural crops against the
salinitya pragmatic approach and step forward to accelerate our potential crop yields. However, a lot of work still

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Plant Growth Regul

need to be done to unravel the exact pathway of SA biosynthesis, whether major or minor, important regulatory
point of its biosynthesis, mode of action and other key and
mutual regulatory roles performed by SA that have
remained elusive up to date. Exploring interaction of SA
with other phytohormones also remains a germane issue to
be addressed in the current context as the SA is excessively
involved in crosstalk with other phytohormones or can alter
their biosynthesis (Pieterse et al. 2009).
Brassinosteroids (BRs)
The BRs are a group of naturally occurring novel steroidal
phytohormones comprising of brassiniloide (BL), castasetrone (CS) and their various derivatives that regulate
plant growth and development by producing an array of
physiological changes (Khripach et al. 2000; Kartal et al.
2009). They can occur either freely or conjugated to
sugars or fatty acids. BRs are involved in a wide range of
activities including seed germination, vascular differentiation, pollen tube growth, epinasty and leaf bending,
activation of proton pump, ETHY, nucleic acids and
protein biosynthesis and photosynthesis, reproductive
growth, and production of flowers and fruit (Khripach
zdemir et al. 2004; Hayat et al. 2010; Fahad
et al. 2000; O
et al. 2015). They are also known to ameliorate the ill
effects of salinity on plant growth performance (Zhu 2002;
Krishna 2003; Zhang et al. 2007b; Kartal et al. 2009;
Wang et al. 2011). Exogenous application of BRs ameliorated the adverse effects of salt stress on seed germination, root elongation and subsequent growth of rice by
restoring pigment levels and increasing nitrate reductase
activity (Anuradha and Rao 2001). Krishna (2003) found
that pre-incubation of barley leaf segments with BRs
before exposure to salinity (0.5 M NaCl) was effective in
reducing salt-stress-induced damage to cell ultrastructures
like nuclei and chloroplast. BRs are known to play a vital
role in the regulation of ion uptake (Khripach et al. 2000).
Seed treatment with BL significantly increased the dry
mass accumulation and activities of antioxidant enzymes
in lucerne under salinity (Zhang et al. 2007b). While
zdemir et al. (2004) found that
studying on rice, O
24-epibrassinolide treatment considerably improved seed
germination, seedling growth, antioxidative system, proline content; while reduced the lipid peroxidation under
salinity stress. The positive mediation of developmental
aspects by BRs under salinity is well supported by the
findings of studies that focused on 24-epibassinolide (24EBL) treatment to counter salinity in brassica (Kagale
et al. 2007), Arabidopsis (Divi et al. 2010), rice (Anuradha
zdemir et al. 2004). Exogenous appliand Rao 2001; O
cations of BRs resulted in modulation of both enzymatic
and non-enzymatic antioxidants in plants subjected to

123

salinity in these studies. Recently, Sharma et al. (2013)

showed that EBL resulted in enhanced proline contents in
salt stressed rice seedlings. Moreover, BRs-mediated
stress tolerance in Arabidopsis was linked with ABA, SA,
and ETHY pathways (Divi et al. 2010). The BRs act as
synergists to GA and IAA during hypocotyl elongation of
Arabidobsis (Tanaka et al. 2003). Nevertheless, ABA acts
as an antagonist as ABA treatment repressed the BR
enhanced expression (BEE1, BEE2 and BEE3) proteins
(Friedrichsen et al. 2002).
There are many core areas where research focus should be
on the sites, pathways and enzymology of BRs biosynthesis,
sourcesink relationships, developmental and stress physiology, interactions with micro-organisms, fungi and animals, and the realization of their application potential.
Another important and critical assignment is to integrate
knowledge of the effects and vital roles of BRs into our
general models of plant growth and development.
Jasmonates (JA)
The JA are vital cellular regulators involved in diverse
plant developmental processes, including seed germination,
callus growth, primary root growth, flowering, formation of
gum and bulb, and senescence (Cheong and Choi 2003;
Pedranzani et al. 2003; Tani et al. 2008). Biosynthesis of
JA occurs in leaves and there is proof of a similar pathway
in roots. As well, cellular organelles such as chloroplasts
and peroxisomes are considered to be the main sites of JA
biosynthesis (Cheong and Choi 2003). These are known to
activate the plant defense responses to various biotic and
abiotic stresses (Mei et al. 2006). Exogenous application of
JA to plants resulted in induction of pathogenesis- or
stress-related genes (Moons et al. 1997; Mei et al. 2006).
Levels of JA were enhanced in tomato (Pedranzani et al.
2003) and Iris hexagona (Wang et al. 2001) upon exposure
to high salinity. In rice leaves and roots, high salinity
increased levels of JA, resulting in the induction of stressrelated proteins and JA biosynthetic genes (Tani et al.
2008). These stress-induced increases in JA levels were
studied only in vegetative tissues. Whether saline conditions augment JA levels in reproductive organs, remains
yet to be answered. The concentration of JA was considerably higher in salt-tolerant rice cultivar than in salt-sensitive cultivar (Kang et al. 2005). Exogenous application of
JA improved recovery of salt-stressed rice seedlings.
Induction of JA-responsive genes was considered as a
crucial aspect of barley response to salinity (Walia et al.
2006). Adding further, Walia et al. (2007) suggested that
three JA-regulated genes ribulose 1, 5-bisphosphate carboxylase/oxygenase (Rubisco) activase, arginine decarboxylase, and apoplastic invertase were possibly involved
in salinity tolerance mediated by JA. Barley leaf segments

Plant Growth Regul

exposed to osmotic stress of sorbitol or manitol exhibited a

sharp increase in endogenous JA contents (Kramell et al.
2000). However, such effect was not observed for high
NaCl concentration (Kramell et al. 1995). Also, methyl
jasmonate (MeJA) levels in rice roots were significantly
enhanced in response to 200 mM NaCl (Moons et al.
1997). Therefore, in salt-tolerant plants high levels of ABA
accumulated after salt treatments can be an effective protection against high salinity. The JA are shown to alleviate
the inhibitory effect of salinity on the rate of CO2 fixation,
and proteins in peas (Velitcukova and Fedina 1998).
There seems to be little knowledge available about how
salinity affects endogenous JA levels in plants. Kang et al.
(2005) pointed out that post-application of exogenously
applied JA can ameliorate salt-stressed rice seedlings,
particularly those of the salt-sensitive rather than the salttolerant cultivar. In addition, exogenous JA application
dramatically decreased sodium concentration. After salt
treatment exogenous application of jasmonates (JA) may
change the endogenous hormones balance, such as ABA,
which provides a significant hint for understanding the
protection mechanisms against salt stress (Kang et al.
2005). These results undoubtedly show that exogenous JA
may be engaged in the defense against salt stress and their
role in manifesting salt tolerance has recently been
acknowledged (Khan and Khan 2013). Under salinity,
exogenous JA application may change the balance of
endogenous plants hormones, which provides an important
clue for understanding the protection mechanisms against
salt stress.
Ethylene (ETHY)
ETHY is a gaseous hormone that regulates plant growth
and development. It has been considered as a stress hormone and is induced by many stresses, however, in salt
stress its role is equivocal (Wang et al. 2011). El-Iklil et al.
(2000) reported that lesser ETHY production was related
with salt tolerance. Contrarily, higher production of ETHY
was regarded as an indicator of salt tolerance in rice (Khan
et al. 1987). According to Pierik et al. (2006), ETHY has
long been known as a growth inhibitor, but it can also
promote growth. Achard et al. (2006) suggest that in
Arabidopsis, ETHY signaling promotes salt tolerance. An
experiment conducted by Cao et al. (2007) suggests that
ETHY receptor function leads to salt sensitivity and ACC
appears to suppress this salt sensitivity, inferring that for
salt tolerance needs ETHY signaling.
Response of plant to salt stress may depend on the
balance and/or interaction between receptor and ETHY.
When receptor signaling is prevalent, the plant is susceptible to salt stress but shows large rosette and late flowering. When ETHY signaling is prevalent, the plant is

tolerant to salt stress but has small rosette and early flowering. Between these two extreme situations the plant needs
to make adjustment (Cao et al. 2007). At various levels
fine-tuning may make plants in an active homeostasis, and
then under stress condition the plants can survive better and
have relatively normal growth.
Based on the mutant analysis of triple responses of etiolated seedlings treated with ETHY, a signal transduction
pathway of ETHY has been put forward in Arabidopsis that
involves ETHY receptors, CTR1, EIN2, and EIN3, and
other components (Guo and Ecker 2004). In Arabidopsis
five receptor genes have been found, and based on structural features they are categorized into two subfamilies.
Subfamily I includes ETR1 and ERS1. Subfamily II
includes ETR2, EIN4, and ERS2. All these receptors of
ETHY can bind ETHY, and ETR1 has his kinase activity
(Hall et al. 2000).
ETHY signaling is significant in regulating plant growth
and stress responses, and ETHY functions through its
receptors. Plants responses to abiotic stresses are mediated
by changes by variation in the expression level of ETHY
receptors and salinity reduced the expression of ETHY
receptor ETR1 in Arabidopsis. Glycine betaine mediated
salt tolerance in wheat showed involvement of ETHY
(Khan et al. 2013). Though it is usually believed that
ETHY signaling functions in multiple stress responses, it is
not clear that under salt stress what specific roles the
receptors can play. Cao et al. (2007) transformed a tobacco
type II ETHY receptor homolog gene NTHK1 into Arabidopsis and observed that the resulting transgenic plants,
with NTHK1 mRNA and protein expression, were salt
sensitive as can be seen from high electrolyte leakage, and
decreased root growth under salt stress. Over expression of
NTHK1 in the transgenic plants seems to represent gain of
function of ETHY receptor suggesting the receptor functioning as the basis of salt-sensitive responses. The high
electrolyte leakage can be entirely or partly suppressed by
1-aminocyclopropane-1-carboxylic acid treatment, recommending that a negative effect exerts by ETHY on its
receptors. In sum, Plants have evolved various specific
mechanisms to adapt themselves to the changing environment. ETHY signaling is one of these pathways that plants
have adopted for regulation of salt stress responses. However, many enigmas inside in the ETHY signaling pathway
remain to be elucidated.
Triazoles (TR)
These are a group of compounds that can be exploited as
either plant growth regulators or fungicides; nevertheless,
in different degrees they manifest both properties. Their
protective role in various biotic and abiotic stresses has
been reported in plants (Fletcher et al. 2000). Among

123

Plant Growth Regul

different TR developed, uniconazole was most effective in

alleviating stresses in plants; although, its practical use for
combating salinity in agriculture is impeded by its residual
effect in both plant tissues and soil. In NaCl stressed plants
of radish (Panneerselvam et al. 1997) and pigeon pea
(Karikalan et al. 1999), TR augmented the plant dry mass.
Generally, TR are known to enhance the photosynthesis
rate due to enhanced chlorophyll content and more wellpacked chloroplasts within a smaller leaf area (Fletcher
et al. 2000). Addition of TR to radish raised the net photosynthetic rate and intercellular CO2 concentration in spite
of being stressed by NaCl (Panneerselvam et al. 1997).
Paclobutrazol treated wheat plants accumulated more water
soluble carbohydrates and reducing sugars under salt stress.
This treatment was also effective in limiting Na? ions in
wheat roots (Hajihashemi et al. 2009). Under stressful
conditions, TR application stimulates the nitrate reductase
activity and protease activity. Furthermore, antioxidant
enzymes activities like peroxidase, superoxide dismutase
and polyphenol oxidase were also enhanced by TR (Karikalan et al. 1999). Soil application of propiconazole (a
triazole compound) ameliorated the NaCl stress on Madagascar periwinkle plants by improving root growth (length
and biomass) and activities of enzymatic antioxidants (Jaleel et al. 2008). Though, there is considerable evidence
about the TR effect on plants (Fletcher et al. 2000), yet
very few studies are available on the role of TR in alleviating salt stress in different crops and this aspect needs to
be consider in future studies.

with these phytohormones or their exogenous application

ameliorated the adverse effects of salinity in a variety of
plant species. For example, low concentrations of SA and
JA are more effective under stress by enhancing physiological processes and improving tolerance by their effect
on biochemical and molecular mechanisms as compared to
higher doses. Plant genes and phytohormones are strongly
interlinked with each other, as some plant genes, which are
necessary for the activity of plant hormones and the other
plant genes, are activated by phytohormones. As research
on the biosynthesis and activity of plant hormones progresses, it is becoming apparent that a large diversity of
metabolites related to different phytohormones play a role
in plant defense and plant-environment interactions. Controlling dose/response ratio of phytohormone remains an
uphill task, since the hormone levels attained should be
moderate in order to sustain a balance between the positive
effects of plant hormones on different abiotic stress tolerance and the negative effects on growth and development.
The use of conditional promoters driving gene expression
at specific developmental stages, in specific tissues/organs
and/or in response to specific environmental cues circumvents this problem and will make possible the generation of
transgenic crops able to grow under various abiotic stresses
with minimal yield losses. The molecular pathways, recognized by molecular biology and proteomic analyses
regarding the perception of plant hormones, may elucidate
more details related to the effects of phytohormones on
plant responses to salt stress.

Conclusions and future perspectives

Acknowledgments We thank the funding provided by the Key

Technology Program R&D of China (Project No. 2012BAD04B12)
and MOA Special Fund for Agro-scientific Research in the Public
Interest of China (No. 201103003).

Crop production is challenged by increasing food demands

of a burgeoning population, fatigued natural resource base
and uncertainty of climatic optima. Besides these factors,
abiotic stresses are also important constraint limiting crop
productivity worldwide. Salinity is an important abiotic
stress that denotes dwindling land use for agriculture due to
deterioration in soil quality. During the past few years the
molecular mechanisms regulating hormonal synthesis,
signaling, and action have been illuminated, and the roles
of phytohormones in regulating responses to adverse
environmental condition have been extensively documented. In present article we summarized the regulatory
circuits of different phytohormones and cross talks
amongst ABA, indole ABA, CKs, GA, SA, BRs, JA,
ETHY and TR at physiological and molecular levels on
exposure to salinity. We found that all these phytohormones are directly or indirectly are involved in modulating
plant responses to salt stress and their relative balances
changes in response to salinity due to crosstalk between
these phytohormones. In many cases, seed pre-treatment

123

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