Phytohormones and plant responses to salinity stress: a review

Plant Growth Regul (2015) 75:391–404 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 / Published online: 24 December 2014 Ó 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: [email protected] 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 123 392 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), 123 Plant Growth Regul (2015) 75:391–404 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 Inzé 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 (2015) 75:391–404 Table 1 Regional distribution of salt-affected soils (million hectares) Source: FAO land and plant nutrition management service Regions 393 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 7 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 5 0.2 15 0.8 12,781 397 3.1 436 3.4 World’s 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 plant’s 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 plant’s 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 123 394 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). Zörb 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- 123 Plant Growth Regul (2015) 75:391–404 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 (2015) 75:391–404 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 395 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 123 396 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 Plant Growth Regul (2015) 75:391–404 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 source–sink 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 (2015) 75:391–404 Root of control maize plant 397 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 carbohydrate’s 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 (Horváth 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 salinity—a pragmatic approach and step forward to accelerate our potential crop yields. However, a lot of work still 123 398 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 et al. 2000; Özdemir et al. 2004; Hayat et al. 2010; Fahad 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 studying on rice, Özdemir et al. (2004) found that 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 and Rao 2001; Özdemir et al. 2004). Exogenous applications of BRs resulted in modulation of both enzymatic and non-enzymatic antioxidants in plants subjected to 123 Plant Growth Regul (2015) 75:391–404 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, source–sink 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 (2015) 75:391–404 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 399 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 400 Plant Growth Regul (2015) 75:391–404 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. 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