Review Article Salinity A plant is an organism exposed simultaneously to two environments, the soil and the atmosphere. The aerial part of the plant, the shoot, depends on the root for its supply of water, minerals, nitrogenous components, and possibly other substances that are absorbed from the soil or synthesized or transformed by the root and transported to the shoot. On the other hand, the root depends on the shoot for photosynthesis and probably other substances synthesized in the shoot and transported to the root. The soil is the environment of the root system, and the root is exposed directly to the changing conditions of the soil. It is through the root that the whole plant is affected by the changing soil conditions. The root may be considered the plant ‘s sensor in the soil (Poljakoff-Mayber and Lemer, 1994). Soil salinity is a worldwide problem in crop production, depending on specific conditions one or more of a number of ions (Na + , Cl - , HCO 3 - , Mg 2+ , SO 4 2- and borate) may be present within the root range in high concentrations thus affecting crop growth (Mengel and Kirkby, 1987).the degree of salinity is usually measured in the water extract of a soil as electrical conductivity. This is expressed in mmhos cm -1 whish is the reciprocal of the electrical resistance. The higher the salt concentrations of the soil extract the higher is the electrical conductivity. The detrimental effects of salinity are due to the influence of ions on the water activity of the external solution, which affects the water status of the plant, and/or to the direct effects of the ions on the physiological and biochemical functions of the cell. These effects can result in turgor reduction, inhibition of membrane function or enzyme activity, inhibition of photosynthesis, induction of ion deficiency due to inadequate transport/selectivity mechanisms, or increased use of metabolic energy for nongrowth processes involved in the maintenance of tolerance (Hasegawa et al., 1986). Osmotic Stress The total ion concentration of the soil solution of saline soils can reach levels which can bring about plasmolysis of plant root cells. The radicles of germinating seeds are particularly sensitive to high ion concentrations in the soil solution. A further drawback of the high ion concentration of the soil solution the resulting high osmotic pressure, which binds the soil water and renders it less available to plant roots (Mengel and Kirkby, 1987). A saline environment can impose osmotic stress on plants. The water potential of plant cells generally equilibrates with that of their environment. The water relations of plant cells and their environment are given by equation (1) (Salisbury, and Ross, 1992).
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Review ArticleSalinity
A plant is an organism exposed simultaneously to twoenvironments, the soil and the atmosphere. The aerial part of theplant, the shoot, depends on the root for its supply of water,minerals, nitrogenous components, and possibly other substancesthat are absorbed from the soil or synthesized or transformed bythe root and transported to the shoot. On the other hand, the rootdepends on the shoot for photosynthesis and probably othersubstances synthesized in the shoot and transported to the root.The soil is the environment of the root system, and the root isexposed directly to the changing conditions of the soil. It isthrough the root that the whole plant is affected by the changingsoil conditions. The root may be considered the plant ‘s sensor inthe soil (Poljakoff-Mayber and Lemer, 1994).
Soil salinity is a worldwide problem in crop production,depending on specific conditions one or more of a number of ions(Na+, Cl-, HCO3
-, Mg2+, SO42- and borate) may be present within the
root range in high concentrations thus affecting crop growth(Mengel and Kirkby, 1987).the degree of salinity is usuallymeasured in the water extract of a soil as electrical conductivity.This is expressed in mmhos cm-1 whish is the reciprocal of theelectrical resistance. The higher the salt concentrations of thesoil extract the higher is the electrical conductivity.
The detrimental effects of salinity are due to the influenceof ions on the water activity of the external solution, whichaffects the water status of the plant, and/or to the direct effectsof the ions on the physiological and biochemical functions of thecell. These effects can result in turgor reduction, inhibition ofmembrane function or enzyme activity, inhibition of photosynthesis,induction of ion deficiency due to inadequate transport/selectivitymechanisms, or increased use of metabolic energy for nongrowthprocesses involved in the maintenance of tolerance (Hasegawa et al.,1986).
Osmotic StressThe total ion concentration of the soil solution of saline
soils can reach levels which can bring about plasmolysis of plantroot cells. The radicles of germinating seeds are particularlysensitive to high ion concentrations in the soil solution. Afurther drawback of the high ion concentration of the soil solutionthe resulting high osmotic pressure, which binds the soil water andrenders it less available to plant roots (Mengel and Kirkby, 1987).
A saline environment can impose osmotic stress on plants. Thewater potential of plant cells generally equilibrates with that oftheir environment. The water relations of plant cells and theirenvironment are given by equation (1) (Salisbury, and Ross, 1992).
Ψw˚ = Ψwi = Ψπ
i + Ψpi (1)
Where Ψw = water potential, Ψπ = osmotic (or solute) potential,Ψp = turgor, ° = outside and i = inside. The water potential of thesaline environment Ψw ° is primarily determined by its saltconcentration (Ψπ°).
Exposure of wall-encased plant cells to the low Ψw ° of asaline environment results in equilibration of the Ψw
i by cell waterloss and accompanying decreases in Ψπ
i and turgor Ψp according toEquation (1). Turgor is a prerequisite for plant cell expansion andgrowth. A simplified description of the growth in relation toturgor is given in Equation (2) (Cossgrove, 1989).
G = m (Ψp - y) (2)
where G = growth rate, m = plasticity of cell walls, and y =threshold turgor for cell enlargement {the minimum pressure (force)required for the cell wall to extend}. In a saline environment,growth should thus cease if turgor is not regulated. Salt-resistantplants are able to regulate their turgor within the range of theirsalt resistance or are able to adjust cell wall plasticity andthreshold values (Jacopy, 1994).
Turgor Regulation in response to salinitv :Bisson and Gutknecht (1980) described the sequence of
events occurring in plant cells upon external salinization anddecrease in \jfwo (Figure 1): water exits from the cell, turgordecrease, and water potentials equilibrate. The turgordecrease is sensed by a "turgor sensor", apparently in theplasma membrane. The sensor emits an "error signals" that istransducted to the activation of some biochemical processes,such as increased solute accumulation or synthesis. Thisresults in an increase in the amount of solutes in the cells,a transient decrease in \jf; and \jf~ , water influx, andeventually recovery of the original (regular) turgor pressure.During the recovery phase \jf~ and \jf; do not change, but theamount of solutes in the cell and turgor increaseconcurrently.
When considering salinity effects, it should be kept inmind that during a brief exposure (hours) of the roots tosalinity, the stress imposed upon the shoot essentially mimicsdrought, although small differences between salt and mannitoltreatments have been found (Yeo et al., 1991). Longer termexposure to salinity is clearly different from exposure todrought (Munns and Termaat, 1986).
Figure (1) : Basic elements of turgor regulation systembased on solute and water transport is random fluctuations in
environmental water potential, and output is turgor pressure(Bisson and Gutknecht, 1980).
Yeo et al. (1991) investigated the short term effects ofsalinity on the leaf growth of rice and found that salinitycaused a rapid decline in leaf elongation, but no effects ofsalinity on \j/p (hydrostatic pressure or turgor) in the growingzone were detected. The precise mechanism for the rapiddecline in leaf elongation rate after exposure to salinityremains obscure, but the speed at which it occurs can pointonly to a hydraulic signal. Turgor is obviously involved, butit is questionable, whether it is reduced throughout thegrowing zone or in only a few cells adjacent to the xylem, asNonami and Boyer (1989) have pointed out. Reduction in \j/p inonly a few cells would be undetectable with bulk tissuemeasurements but could inhibit growth by blocking water flowto the rest of the growing tissue.
The effects of longer term exposures to salinity (a dayor longer) on growth and \jIp have also been investigated.Neumann et al. (1988) found that exposure of bean plants to 50and 100 mM NaCI, reduced leaf area expansion as well asdecreased the \jIp of the leaves from about 0.24 to about 0.13MPa. On the other hand, exposure of wheat and barley plants to100 mM NaCI for 10 days reduced the relative growth rates toabout 25 and 50% of control values, respectively, while, \jIp. inthe growing zone of the leaves was not affected. Also, Lauterand Munns (1987) treated chickpea with a relatively mildsalinity level (-0.115 MP a). Shoot growth was inhibited, but\jIp of the expanding leaves over a period of 8 days wasunaffected by salinity. However, no correlation between growthand \jIp was observed. Recently, Ayala and 0' Leary (1995) foundthat water and osmotic potentials of the shoots decreasedsignificantly with increasing salinity but turgor potentialsdid not differ significantly among treatments. Stomatalconductance decreased with increasing salinity, resulting in asignificantly higher transpiration rate at the lowest salinitythan at the other higher levels.
Signal transduction mechanismsThe pathways that warrant attention at the molecular
level are properties of the plasmalemma that control NaCIuptake in the roots and salt transport in the xylem; thenature and location of ion pumps in the plasmalemma andtonoplast and maintenance of ion selectivity and pH ; control-and pathways for synthesis of organic osmolytes; maintenanceof photosynthesis and energy charge; and maintenance ofgrowth, involving cell cycle control and the biosynthesis andregulation of cell wall components.
It is presumed that salt stress acts via a chain of
events: perception, signal transfer and gene expression.Recent experiments have shown that changes in turgor orextracellular osmotic stress bring about physical and chemicalchanges in the plasmalemma, which result in the rapidactivation of specific genes. It was believed that there is asignal transduction links between the perception of changes inturgor and the activation of these genes. Some evidence hasbeen provided for the types of signal transduction mechanismsthat may be operating when plants are exposed to salinitystress. In maize root protoplasts, it was demonstrated thatsalinity stress disturbs the intracellular Ca2+ content (Lynchand Lauchli, 1988). By measuring cytoplasmic Ca-activity witha fluorescent probe, Lynch et al. (1989) found that high NaCIconcentrations caused immediate elevation of intracellularcytoplasmic Ca2+ activity and presented evidence for theexistence of a phosphoinositol regulatory system.Hypothetically, such a system would be an integral part of aCa2+ based signal transduction pathway that would link stresssignals to the activation of gene expression via proteinphosphorylation. There is direct evidence thatinositoltriphosphate may serve as a second messenger for themobilization of intracellular Ca2+ in higher plants (Rincon etal., 1989). Phosphatidyl serine activation of a plant proteinkinase C (Elliot et al., 1988) strongly suggests that a Ca2+second messenger system operates in plant membranes and thatit is important to plant hormone action. Recently, Pardo et al.(1998) found that calcineurin (CaN) is a Ca2+ and calmodulin-dependent protein phosphatase (PP2B) [serine/threoninespecific protein phosphatase], in yeast. It is an integralintermediate of a salt-stress signal transduction pathway that~ffects NaCI tolerance through the regulation of Na+ influxand efflux. Calmodulin (CaM) is a 16 kDa, highly conservedacidic protein which is heat stable and participates intransducing signals from external stimuli (Botella and Arteca,1994). Moreover, Zhang WenHua et al. (1998) suggested that Ca mayplay a role in the increase of the vacuolar H+ pumps in barleyroots which may reflect an adaptation to salt stress, and thatthe stimulation of H+ -ATPase and H+ -transport activities byCa depended primarily on its effect in maintaining thestability of the membrane under salt stress.
In the salt-resistant characean Lamprothamnium (Okasaki etal., 1984), a hypertonic salt shock induced a hyperpolarizationof the plasma membrane potential. Concordantly, in red beettissue slices and some plant roots, a hypertonic mannitolshock enhanced plasma membrane and tonoplast ATPase activityas well as ~ uptake. The shock also induced a transientincrease in the 1, 4, 5-IP3 (inositol 1, 4, 5triphosphate)content in the cells and enhanced phosphorylation of somemembrane-bound proteins (Srivastava et al., 1989). It was
suggested that activation of the IP (inositol phosphate)cascade and formation of 1, 4, 5-IP3 and DG (diacylglycerol)may constituent the error signal. The presence of 1, 4, 5-IP3should in turn induce the release of Ca+ from intracellularcompartments; Ca+ as well as DG acts as a second messenger andaffect the activity of protein kinase and of other cellularprocesses (Berridge, 1987).
Salinitv effects on vield thresholdThe yield threshold increased proportionally with the
concentration of salinity (0-120 mM NaCI) and was responsiblefor the inhibition of leaf elongation rate (Cramer and Bowman,1991). In a subsequent study (Cramer, 1992), two maizecultivars differing in their salt tolerance were comparedatter 24 h of salinity stress. The yield threshold wasincreased by salinity in both cultivars. Turgor was notaffected by salinity. The more sensitive cultivar had agreater reduction in effective \lip (greater increase of Y) thanthe more tolerant cultivar.
Adiustment of Cell wall Characteristics:As previously mentioned, in equation 2, G = m (\lip - y)
shows that the growth rate of plant cells depends on theturgor above a threshold value. Hence, to maintain growthunder saline conditions plants may either increase the amountsof solutes in the cells and regulate turgor or adjustplasticity and/or threshold turgor. Bressan et al. (1990) foundin comparison between unadapted and 428 mM NaCI adaptedtobacco cells that NaCI adapted cells have a greatIy reducedability to gain fresh weight, although their dry weight growthrate is similar to unadapted cells. The rate of cell expansionand the final volume of adapted cells are reduced compared tounadapted cells. It appears that adapted cells lack a cellelongation phase during development. Also, the sequentialextraction of cell wall substances from the acetone. powdersyielded material corresponding to 70 and 42% in the unadaptedand NaCI adapted cells, respectively. The low recovery by theadapted cells was a result of the loss of low molecular weightmaterials, principally reducing sugars and amino acidsprecipitated by the acetone, during dialysis of the firstextract. cells. The lower proportion of cell wall proportionrecovery from NaCI adapted cells in the acetone powdersreflected an enhanced accumulation of solutes at the expenseof wall synthesis. Moreover, The adapted cells released about7 times as much protein into the medium.Solutes Emploved for Turgor Regulation in plants:
Various organic solutes as well as mineral ions, inparticular Na+, t< and cr are accumulated in plants during
turgor or volume regulation. Some halophytes, the native floraof saline environments, adjust their solute content mainlywith inorganic ions (Flower et al., 1986). In other plants, sodiumis excluded or excreted and KCI is the major soluteaccumulated for turgor regulation (Reed et al., 1981). In otherplants, a larger part of the solutes comprises organiccompounds (Gorham et al., 1985). A large part of the biomass ofplants would have to be diverted to turgor regulation iforganic solutes were the main compounds employed for this inhighly vacuolated plant cells. Greenway (1973) calculated thatfor adaptation to 100 mM external NaCI with hexoses, 20-30% ofthe total biomass would be needed. Raven (1985) analyzed thecost benefit of turgor regulation with different solutes.These calculations show that 2-4 mol photons of light energyis needed for the accumulation of 1 Osmol KCI or NaCI, but 68-78 mol photons is needed for the synthesis of 1 Osmol sorbitolor mannitol, 70-93 mol photons for 1 Osmol proline and 78-101mol photons for 1 Osmol glycine betaine. The exact amount ofphotons needed in each case depends on whether the solutes areaccumulated in the roots or shoots and, for proline andglycine betaine, also on The N source, NH/ or N03-. However,energy inexpensive turgor regulation with mineral ions seemsto be limited by the inhibitory effects of high saltconcentrations on various metabolic processes in thecytoplasm.
Photosynthesis in response to salinitv:Exactly how stresses affect photosynthesis, i.e., via
stomatal closure or some more direct effect in the mesophyll,is not always clear. Once mesophyll activity is decreased,stomata frequently close, and vice versa. The precise linksbetween stomatal function and CO2 assimilation rate in themesophyll are present unknown, but it seems clear that a linkexists (Morison, 1987). Which factor is affected first by asalinity stress? Does stomatal closure cause the observeddecrease in CO2 assimilation, or does non-stomatal inhibitionof photosynthesis give rise to stomatal closure?
Under severe salinity stress, the cytoplasm can beoverloaded with Na+ which can affect enzymes and organellespresent in the cytoplasm. Thus, Hecht-Buchholz et al. (1974)reported that isolated chloroplasts of Phaseolus vulgaris subjectedto a 25 mM solution of NaCI were found to suffer aconsiderable loss in fine structure. The damage wasaccompanied by an exchange of I< from the chloroplasts for Na+from the solution. Interestingly, chloroplasts of Beta vulgariswere not affected by this same procedure and the KlNa exchangedid not occur. As Phaseolus is known to be a salt-sensitivespecies, whereas Beta is a rather salt tolerant plant, it istempting to speculate that salt tolerance in some way relates
to the stability of chloroplasts to high Na concentrations.Transmission electron microscopy indicated that in tomato
leaves of NaCI-treated plants, the chloroplasts wereaggregated, the cell membranes were distorted and wrinkled,and there was no sign of grana and thylakoid structures inchloroplasts (Khavari-Nejad and Mostofi, 1998). In soybeanplants, salt stress reduced the ability of chloroplasts tosynthesize oleic and palmitic acid. Oleic and palmitic acidcontents in lipids of OEM (outer envelope membranes)increased. Overall, lipid biosynthesis in IEM (inner envelopemembranes) was more sensitive to salt stress than in OEM. Thissuggested that lipid biosynthesis in IEM might affectadaptation to a saline environment (Huang Chi Yang et al.,1997). Hernandez et al. (1995) suggested that in the cellulartoxicity of NaCI in pea plants, superoxideand H202 -mediatedoxidative damage in chloroplasts may play an important role.
Popova et al. (1995) found that NaCI stress imposed throughthe root medium of Hordeum vulgare for a period of 8 d decreasedthe rate of CO2 assimilation and the leaf chlorophyll andprotein content. Fedina et al. (1994) found that NaCI treatmentresulted in an increase in endogenous proline, CO2compensation point, photorespiration and glycolate oxidaseactivity. Photosynthesis was significantly inhibited. Thereduced CO2 fixation of protoplasts isolated from NaCI Pisumsativum stressed plants indicated a direct effect of NaCI on thephotosynthetic process, which was not dependent upon stomatalclosure. Banuls and Primo (1995) found that the reduction inleaf stomatal conductance was closely correlated with decreasein leaf water potential. Also, there was significantcorrelation between photosynthesis and stomatal conductance.Chartzoulakis et aJ. (1995) found in kiwifruit plants that leafexpansion rate, leaf size and number of leaves per plant werereduced by salinity. Sodium accumulated mainly in roots andincreased with increasing NaCI concentration, while chloridecontent in leaves and roots increased significantly with >10mM NaCI. Photosynthetic rate (Pn) decreased with increasedlevels of leaf chloride. The decrease in photosynthesis wasonly partially due to stomatal closure. Also, in cucumber cv.Pepinex exposure to higher salinities (25, 50, 120 and 190 mM)caused stomatal closure and a significant decrease inphotosynthetic rate. Leaf water potential, osmotic potentialand turgor potential were also lower with increasing salinity.Leaf expansion rate and final leaf size declined linearly withan increase in external NaCI. The results suggest thatsalinity influences cucumber growth through a reduction inphotosynthesis and photosynthesizing area (Chartzoulakis,1994). Meanwhile, Sudhakar et al. (1997) found that salinityshock caused decline in the activities of ribulosebisphosphate carboxylase, ribulose-5-phosphate kinase, ribose-
5-phosphate isomerase and NADPGly-3-P dehydrogenase. Ribulosebisphosphate carboxylase was more sensitive to salt shock thanthe other enzymes. Also, Shen et al. (1994) found jn barleythat the activity of ribulose 1,5 bisphosphate carboxylase inleaves- was in the order: low-salt> control> high-salt plants.Meanwhile, Ritambhara et al. (1995) suggested that there is animpairment of the pentose phosphate pathway under salinity.
However, most plants have evolved some mechanisms to copewith salinity, such as increases in carbohydrate accumulation(Cheeseman, 1988). The production and accumulation of polyols,such as glycerol or sucrose, provides nonstructural carbon inthe cytoplasm acting in osmotic adjustment and turgormaintenance. The provision of carbon to act as an osmoticumwill be a cost for the organism, however, since this carbon isnot available for anabolic reactions. One adaptation to saltstress is the use of alternate metabolic pathways that allowthe plant to gain some additional advantage in survivaleither through more efficient carbon gain processes such as C4photosynthesis, which allows greater CO2 fixation underconditions of high light and temperature (Nelson andLangsdale, 1989), or crassulacean acid metabolism (CAM), whichallows plants to fix CO2 at night when evaporative water lossis minimal. Both C4 and CAM plants switch the primary mode ofCO2 fixation to the enzyme phosphoenolpyruvate carboxylase,PEPCase, which ultimately results in the concentration carbondioxide. Crassulacean acid metabolism may hold importantimplications for the analysis of osmotic stress tolerance inthat it is a well characterized physiological adaptation towater stress found in plants of tropical origin that typicallygrow in warm, dry climates. A variety of plant species from aC3 mode of photosynthetic carbon metabolism to CAM in responseto salt stress. In M. crystallinum this metabolic transition isaccompanied by substantial increases in the activity of a setof carbon metabolism enzymes of the glycolytic and CAMpathways (Holtum and Winter, 1982). Ratajczak et al. (1994) foundin plants of the facultative halophyte and CAM species M.crystallinum, parameters of the tonoplast H+-ATPase werecorrelated with the application of salinity, the expression ofCAM. It was concluded that (i) a pronounced increase in theamount of tonoplast H+ -ATPase is related to salinity per se(ii) the induction of 2 new polypeptides with molecular massesof 32 and 28 kDa is correlated in time with the expression ofCAM and (iii) the 2 new polypeptides are part of the tonoplastH+-ATPase holoenzyme. Recently, Forsthoefel et al. (1995)reported that salinity stress in Mesembryanthemum crystallinum(ice plant) triggers significant changes in gene expression,including increased expression of mRNAs encoding enzymesinvolved with osmotic adaptation to water stress and thecrassulacean acid metabolism (CAM) photosynthetic pathway.
They added that the isolation of a salinity-induced geneencoding phosphoglycerate mutase (a basic enzyme of glycolysisand gluconeogenesis) indicates that adaptation to salt stressin the M. crystallinum plant involves adjustments in fundamentalpathways of carbon metabolism and that these adjustments arecontrolled at the level of gene expression. It is proposedthat the leaf-specific expression of Pgm1 (phosphoglyceratemutase) contributes to the maintenance of efficient carbonflux through glycolysis/gluconeogenesis in conjunction withthe stress-induced shift to CAM photosynthesis.
Finally, Lakshmi et al. (1996) reported that the tolerantcultivar of mulberry showed a lesser reduction in net CO2assimilation rate (PN), stomatal conductance (gs) and a betterwater use efficiency (WUE). On the other hand, Singh andDubey(1995) reported that salt sensitivity was associated withdecreased chlorophyll and carotenoid contents, PSII and Hillreaction activities, and fluorescence emission.
Abscisic acid in response to salinitv :Abscisic acid (ABA) is the primary hormone that mediates
plant responses to stresses such as cold, drought and salinity(Wu et al., 1997). Colorado et al. (1994) suggested that ABA levelcorrelates with the plant resistance to stress. Gong et al.(1990) found that during NaCI stress, ABA content in wheat andbarley leaves increased with duration and intensity of stress.Moreover, Maslenkova et al. (1993) found that endogenous level ofABA increased with salinity stress, and that this levelcorrelates with plant resistance to the stress. Nilson andOrcutt (1996) attributed this increase in the concentration ofABA in the tissue as a result of release from bound forms, anincrease in the rate of synthesis or a decrease in the rate ofdestruction. In this respect, Sagi et al. (1998b) reported thatsalinity-enhanced activities of xanthine dehydrogenase (XDH)and AO (aldehyde oxidase) were more pronounced in the rootsthan in the shoots of ryegrass. The increase in both enzymeswith salinity may constitute part of the mechanisms of plantadaptation to stress by enhancing the activity of AO, whichcatalyses the final step in biosynthesis of phytohormones suchas abscisic acid.
Mozer (1980) proposed that ABA could positively affectthe imbibition of the seeds under salinity by increasing thepermeability of the membrane and can also regulate thesynthesis of certain enzymes related to germination. Moreover,ABA accumulation could induce some characteristicdevelopmental changes i.e., restricted growth of shoots,stimulation of root extension, lateral root growth, and roothair development which can help the plant to cope withsalinity stress (Hartung and Davies, 1994). Reggiani et al.(1993) reported that accumulation of amino acids and 4-
aminobutyrate was induced by 50100 I-tM ABA treatment inwheat, through an increase in glutamate decarboxylaseactivity. It was suggested that the ABA-induced accumulationof 4-aminobutyrate is a mechanism involved in the tolerance ofplant tissues to stress conditions. Meanwhile, Eberhardt andWegmann (1989) and Naqvi et al. (1994) reported that addition ofABA did not increase proline content, but delayed thedeleterious effect of NaCI and improved the state of thecells. They added that the site of action of ABA is unknown,but the immediate response to NaCI injury indicates that ABAat certain concentrations could have stabilizing effect on theplasmamembrane. Maslenkova et al. (1993) working on barley,indicated that ABA may play a specific role in membranestabilization by inducing its own set of proteins as anadaptive response of plants to salinity. Montero et al. (1997)suggested that the increase in ABA, induced by the saltpretreatment, seems to play an important role in limiting theaccumulation of Na+ and CI- in the leaves, leading toadaptation of bush beans to salt stress.
The salt tolerant halophyte Suaeda maritima L. Dum wasexamined to see if ABA participates in its response tosalinity (Clipson et aI., 1988). The highest steady state levelsof ABA (GC-ECD) occurred in plants grown in the absence ofNaCI; however, shifting plants from moderate to higher NaCllevels resulted in a 2- to 5-fold increase in ABA levels. Theyspeculate that the rise in ABA in succulents exposed tofluctuating salinity is more related to the regulation of ionand water transport than to control of stomatal behaviorbecause of a prior determination that changes in salinity havegreater effects on ion uptake than on photosynthesis andtranspiration (Clipson, 1987).
In many cases a correlation between salt s-OOss responseand hormone metabolism has been observed. Pekic, et al. (1993),working on wheat, rice and maize, mentioned that during highsalinity, elevated ABA levels appear to provoke discretechanges in gene expression. They suggested that geneticmodification of endogenous ABA content produced in response tosalinity might be a way of optimizing beneficial effects ofABA and thereby improving crop tolerance under salinity stressconditions. Physiological studies have shown that endogenousABA levels increase in plant tissue subjected to NaCI (Jones etaI., 1987). Under salt stress condition, specific genes areinduced that may play roles in controlling intracellularosmolarity or other protective functions. Exposure of culturedtobacco cells to ABA, led the cells to synthesize a 26-kDprotein (Singh et al., 1987b). The expression pattern of this ABAinduced 26-kD protein is transient unless cells are alsoexposed to NaGI stress. The ABA induced protein isimmunologically cross-reactive to 26kD proteins of several
plants. It is assumed that ABA is involved in the normalinduction of the synthesis of the 26-kD protein and thepresence of NaGI is necessary for the protein to accumulate.The 26-kD protein has been termed osmotin because it issynthesized and accumulated in cells undergoing gradualosmotic adjustment to salt stress (Bressan et al., 1985). Osmotinis preferentially localized to the vacuolar inclusion bodies(Singh et al., 1989). An osmotin gene has also been isolated fromtomato, which encodes a protein having a predicted product of24 kD (King et al., 1988). The mRNA for this clone is induced bysalt in tomato suspension cells during the late-log growthphase and is considerably more abundant in the roots of saltstressed plants.
Mundy and Ghau (1988) isolated a gene that is induced inrice plants under ABA treatment or water stress. This genenamed Rab21 (Responsive to ABA), encodes a basic glycine richprotein with a predicted molecular weight of 16 kD.Transcripts for this gene can be induced in a variety oftissues upon treatment with 200 mM NaGI or 10 I-IM ABA orboth. The effects of these two different stimuli are notcumulative, suggesting that they Share a common responsepathway. Induction of Rab21 mRNA is rapid (less than 15 min)and does not depend on de novo protein synthesis, indicatingthat preformed nuclear cytosolic factors mediate itsresponsiveness. Such produced proteins, have been described asa plant's "primary immune response", contributing to theoverall defense of the plant. Likewise, osmotin may function asa means of adjusting turnover rates of stored carbon compounds(e.g., organic acids in the vacuole).
Other plant hormones in response to salinity:Roots are the first tissues exposed to salt, therefore,cytokinins levels may be directly affected by salt stress(Thomas et aI., 1992). Itai et al. (1968) found that salt stresslowers cytokinin-like activity. The decline in cytokinin-likeactivity was proportional to the concentration of osmoticum.Declining cytokinin would presumably complement the tendencyof ABA to cause stomatal closing. Also, Meiri and Shalhevet,(1973) reported that saline conditions restrict the synthesisof cytokinins in the roots and their translocation toupper ..plant parts can also be inhibited. Recently, Zeinaband Sallam (1996) rep~ted that Cytokinin activity decreasedwith increase in salt stress in barley plants. On the otherhand, Nilson and Orcutt (1996) indicated that under salinitystress, the endogenous levels of cytokinins in roots andleaves did not change or may have slightly decreased. However,maintenance of some cytokinin synthesis activity undersalinity was suggested to confer tolerance to salinity (Neeraet al., 1995).
Auxin activity was adversely correlated with increase inplant age and salt stress in barley plants, (Zeinab and Sallam1996). Stefl (1988), working on wheat, found that withIncreasing Na+ concentration, the tryptophan synthase a-monomers were gradually dissociated from the oligomersproducing less active isoenzyme. This reduced the biosynthesisof L-tryptophan and consequently that of IAA, so that plantgrowth was retarded or even stopped.
Meanwhile, Prakash and Prathapasenan (1990) reported thatwhen plants of rice were subjected to salt stress (12 dSm-1),the extension growth and dry weight of the shoot system aswell as GA-like substances were rDarkedly reduced. Zeinab andSallam (1996) reported that at higher salinity there was anaccumulation of gibberellin inhibitors and no gibberellinactivity was found in barley plants.
Saha and Gupta (1997) found in sunflower seedlings thatthe cessation of ethylene production was associated withincrease in aminocyclopropane-carboxylic acid (ACC) andconjugated -ACC level. This was also associated with membranedeterioration which was evidenced from higher malondialdehydecontent, which increased, along with peroxidase activity, withincreasing salinity levels. Also, Bhattacharjee and Mukherjee(1996) reported that salinity stress caused greater membranedeterioration by membrane lipid peroxidation,
evidenced bymalondialdehyde accumulation and higher lipoxygenase activity.
Protein synthesis bv plants in response to salinitv:The main idea underlying studies of stress-induced proteinsynthesis in plants is that stress conditions lead to thedifferential expression of genetic information, resulting inchanges in gene products, including mRNA and proteins. Suchnewly synthesized proteins are specific to the particular typeof stress and possibly give survival value to the plants.Plant metabolism and more specifically protein synthesis areadversely affected under salinity stress. The effect ofsalinity depends on the developmental stage of the plant aswell as the intensity and duration of the stress.
It is well documented that salinity promotes thesynthesis of salt stress-specific proteins (Ben-Hayyim et al.,1989), causes either decreases or increases in the level oftotal andlor soluble proteins, depending on the plant partsstudied and leads to increased activity and synthesis of manyenzymes (Mittal and Oubey, 1991). Most experiments to studysalinity-induced synthesis of proteins have been conductedusing plant cell cultures.
In salt-adapted tobacco cells, osmotin constitutes about10-12% of total protein in the cell (Singh et al., 1985). It isbelieved that the is in providing osmotic adjustment to the
cells either by facilitating the accumulation of solutes or byproviding certain metabolic alterations in the cell, which maybe helpful in osmotic adjustment (Singh et al., 1987a). Increasingaccumulation of osmotin protein was observed during 7 daysexposure to 50 mM NaG!. Upon treatment with NaGI, osmotin mRNAlevels increased in both root and leaf of tomato tissues, withan additional longer transcript induced in roots (Grillo et al.1995).
Synthesis of salt induced proteins has also been shown inmaize callus (Ramagopal, 1986) and barley roots (Hurkman andTanaka, 1987) as well as citrus and tomato cells (Ben-Hayyim etaI., 1989). Also, in salt tolerant rice plants, Rani (1988)found a 28 kO protein in shoots that is absent in saltsensitive genotypes. Similarly to rice in citrus, a 25 kOprotein has been associated with salt tolerance (Ben-Hayyim etaI., 1989). This protein appears to be a constitutive protein insalt-tolerant citrus cells and is present whether cells aregrown in the absence or presence of NaG!. It appears that thesalt tolerance trait is stable in these species. salt tolerantlines in these species show synthesis of such constitutiveproteins up to many generations when grown in either thepresence or absence of NaG!.
A comparison of protein profiles of nonadapted and NaGIadapted cell lines of citrus and I' tomato indicates that incitrus, the level of most proteins is suppressed, whereas intomato it is enhanced under salt stress (Ben-Hayyim et al., 1989).In tobacco cells, enhancement in the level of certain proteinsand a decrease in the level of others is observed when cellsare adapted to NaG!. This indicates that salt-induced changesin proteins are species specific and that different proteinsare associated with salt tolerance in different species.
Glose (1996) and (1997) reported that dehydrins (lateembryogenesis abundant (LEA) 0-11 proteins) accumulate inplants in response to osmotic stress. Oehydrins are composedof several typical domains joined together in a fewcharacteristic patterns, with numerous minor permutations.These domains include one or more putative amphipathic a-helixforming consensus regions, a phosphorylatable tract of Serresidues, and an N-terminal consensus sequence. It appearsthat these proteins associate with macromolecules ranging fromnucleoprotein complexes in the nucleus to an endomembranesheath in the cytoplasm. At present, all observations areconsistent with a hypothesis that dehydrins are surfactantscapable of inhibiting the coagulation of a range ofmacromolecules, thereby preserving structural integrity. It issuggested that dehydrins may be structure stabilizers withdetergent and chaperone-like properties and an array ofnuclear and cytoplasmic targets. Xu et al. (1996) found a directevidence supporting the hypothesis that LEA proteins play an
important role in the protection of plants under water- orsalt-stress conditions. Thus, LEA genes hold considerablepotential for use in improving stress tolerance.
When potatoes leaves cv. Haig were subjected to saltstress (150 or 300 mM NaCI), synthesis of the 32 kDa stromachloroplastic droughtinduced stress protein CDSP 34 increased(Pruvot et aI., 1996). Moreover, Murota et al. (1994) found withthe oxygen-evolving activities of thylakoid membranes fromNaCI-adapted cells that it was more tolerant of high NaCIconcentrations than those from unadapted cells. Examination ofthe dissociation of 23-kDa and 33-kDa polypeptides from thewater-splitting complex of PSII at high NaCI concentrationsindicated that the affinity with which the 23-kDa polypeptidewas bound to thylakoid membranes of salt-adapted cells hadbeen altered. On the other hand, Moons et al. (1997) reporteda novel cDNA clone OSR40c1, encoding a abscisic acid (ABA)-responsive 40-kDa protein previously associated with salttolerance, was isolated from roots of rice seedlings.They indicated that OSR40c1 plays a role in the adaptativeresponse of roots to an hyper-osmotic environment and belongsto a novel plantprotein family that most probably has structural functions.Moreover, cyclophilins (Cyp) are ubiquitous proteins withpeptidyl-prolyl cis-trans isomerase activity that catalysesrotation of X-Pro peptide bonds and facilitates the folding ofproteins; these enzymes are believed to play a role in ih vivoprotein folding (Marivet et al., 1994). These findings suggestthat cyclophilin might be a salt stress-related protein.
Salinity in the majority of cases lowers the level ofprotein in salt stressed plant parts as a result of thedecreased synthesis of protein as well as increased activitiesof protein hydrolyzing enzymes. In certain cases, however, anincreased protein level is noticed under salinization,possibly as a result of the increased synthesis of new saltinduced proteins or the decreased activities of proteolyticenzymes.
In subjected Morus alba plants to NaCI salinity, the totalprotein content of the shocked plants declined with aprogressive increase in accumulation of free amino acids.Concurrently, the protease [proteinase] activity in thetissues was also increased. Nitrate reductase activitydeclined under stress conditions. Ammonia was accumulatedsignificantly in the tissue under salt stress conditions. Theenhanced activities of NADH- and NADPH-dependent glutamatedehydrogenase coupled with increased activities of aspartateaminotransferase and alanine aminotransferase may be involvedin detoxifying the excess levels of ammonia (by assimilation)found under stress conditions. The increased activity ofglutamine synthetase [glutamate-ammonia ligase] during stress
conditions paralleled the elevated levels of glutamine in thetissue. The magnitude of these changes increased over time andwith stress intensity (Ramanjulu et al. 1994).
In various crop species, a decrease in the protein levelin salt stressed plant parts is attributed to a decrease inprotein synthesis, the decreased availability of amino acids,and the denaturation of the enzymes involved in amino acid andprotein synthesis (Levitt, 1972). In germinating Vigna sinensisseeds under salinization, decreased seedling vigor and lowlevel of proteins in seedlings is noticed that is due to theinhibition of translocation of hydrolyzed products fromcotyledons to embryoaxes as well as the decreased synthesis ofproteins in seedlings (Prisco and Vieira, 1976). On the otherhand, an apparent increase in protein level in the endospermsof germinating seeds is observed with an increase in salinity.This can be explained as a result of decreased proteolysiscaused by salinity leading to slower depletion of reserveproteins, not as a result of enhanced protein synthesis (Dubeyand Rani, 1987). Recently, Sher et al. (1994) found that crudproteins declined at both sites at times of stress fromdrought or salinity due to increased proteolysis and decreasedprotein synthesis.
Enzvmes in response to salinitv:Salinity induces changes in the activities of
proteolytic, amylolytic, nucleolytic, phosphorolytic andoxidative enzymes in germinating seeds and growing plantparts. Salinity causes either an increase or a decrease in theactivity of enzymes, depending on the nature of the enzymes,the plant parts studied and the genotype of plant speciesdiffering in salt tolerance.
In endosperms of germinating seeds, salinity causes adecrease in the activities of hydrolytic enzymes, including a-amylase, protease, RNase, phosphatase and phytase (Dubey andRani, 1987). The decrease is greater in salt sensitive thantolerant varieties. In leaves of plants or in the growingseedlings, salinity enhances the activities of nucleases,proteases (Dubey, 1985), peptidases, phosphatase (Dubey andSharma, 1989) and oxidases (Mittal and Dubey, 1991).
Isoenzyme profiles of many enzymes are influenced bysalinity. In certain cases some of the molecular forms ofenzymes present in nonsalinized plants disappear in stressedplants, whereas in other cases certain new molecular forms ofenzymes appear under salinization. In shoots of 15-day oldnonsalinized rice seedlings, four acid phosphatase isoenzymewere observed, whereas when seedlings were raised at asalinity level of 14 dSm-1 NaCI, only one isoenzyme remaineddetectable (Oubey and Sharma, 1989). The decreased number ofacid phosphatase isoenzymes at a higher level of salinization
paralleled the decreased activity of the enzyme under suchconditions. Moreover, specific activities and pattern ofperoxidase of isoenzymes are altered significantly in plantssubjected to salinity stress. In 15-day old seedlings of asalt tolerant rice, three isoenzymes were observed in theroots and five in shoots, whereas in a salt sensitive one, sixisoenzymes were observed in the roots as well as in the shoots(Mittal and Oubey, 1991). Like acid phosphatase andperoxidase, isoenzymes profiles of ribonucleases (Mittal andOubey, 1990) and a-amylases (Oubey, 1983) are also influencedunder salinization. These studies and other similar studiessuggest that isoenzymes can be useful markers in the analysisof gene functions and metabolic regulations, including salttolerance characteristics (Mittal and Oubey, 1991). However,the mechanism of the expression of intrinsic isoenzymesproteins that specifically appear under salinization remainsto be investigated.
In forty-five day old chickpea cv. G-235 plants, the H202scavenging enzymes studied. Peroxidase registered a 2.5- to 3-fold increase 7 OAT with 50 and 100 mM NaGI, respectively. The50 and 100 mM NaGI treatments induced declines in catalaseactivity. Glutathione reductase and ascorbate peroxidaseactivity also decreased under salt stress but to a lesserextent than that of catalase (Sheokand et aI., 1995). Also, insoyabean acclimatized plants, at each water potential (saltstress), had higher activities of glutathione reductase,ascorbate peroxidase and dehydroascorbate reductase thanplants transferred directly to the same water potentials. Theenzymes became concentrated in the cytosol in saltstressedconditions. Lipid peroxidation was increased in salt-stressedconditions, particularly in the non-acclimatized plants. It issuggested that higher activities of the H202-scavengingenzymes may protect the leaf cell plasma membranes from lipidperoxidation, and that glutathione reductase may enable plantsto tolerate salt stress by maintaining a high reducedglutathione:oxidized glutathione ratio (Huang GhiYing et aI.,1995). Moreover, Gossett et al. (1994) found in cotton pants thathigher catalase and peroxidase activities indicated that thesalt-tolerant cell line had an increased ability to decomposeH202. The higher ascorbate peroxidase (AP) and glutathionereductase (GR) activities were reflected in the ascorbate andglutathione concentrations. The salt-tolerant cell line had asignificantly lower reduced ascorbate:oxidized ascorbate ratioand a significantly higher reduced glutathione:oxidizedglutathione ratio. It is
concluded that the salt-tolerant cell line had a more activeascorbateglutathione cycle and that salt tolerance could, atleast in part, be due to the cell's ability to up-regulate
this cycle. The results of Banks et al. (1998) suggested that theupregulation of the activity of ascorbate reductase andglutathione reductase in response to salt stress is due to ade nova transcription of the genes encoding these two enzymesand is not due to the translation of existing transcripts ormobilization of existing enzyme pools. The activity of solubleascorbate peroxidase was enhanced by the salt treatment inboth leaves and roots of Raphanus sativus. The salt-inducedincrease in ascorbate peroxidase activity requires days tobecome significant and can be considered as a late response.The increase in activity, but not in mRNA level, suggests thanthe salt-induced ascorbate peroxidase expression may be theconsequence of post-transcriptional events (Lopez et aI., 1996).
The possible involvement of activated oxygen species inthe mechanism of damage by NaGI stress was studied in leavesof 4 varieties of rice exhibiting different sensitivities toNaGI. These results indicate that free radical-mediated damageof membrane may play an important role in the cellulartoxicity of NaGI in rice seedlings and that salt-tolerantvarieties exhibit protection mechanism against increasedradical production by maintaining the specific activity ofantioxidant enzymes (Dionisio Sese and Tobita, 1998). Gomba etal. (1998) suggested that under mild saline stress,. in soybeanroot nodules, the elevated levels of the antioxidantenzymes .and reduced glutathione protect nodules against theactivated oxygen species thus avoiding lipid and proteinperoxidation, and leghaemoglobin breakdown. The two mostimportant enzymes active in elimination of reactive oxygenspecies, namely, superoxide dismutase (SOD) and ascorbateperoxidase. Gueta Dahan et al. (1997) suggested that the excessof H202 interacts with lipids to form hydroperoxides.
Ascorbate peroxidase seems to be a key enzyme indetermining salt tolerance in citrus as its constitutiveactivity in salt-sensitive callus is far below the activityobserved in salt-tolerant callus, while the activities ofother enzymes involved in the defense against oxidativestress, namely SOD and glutathione reductase, are essentiallysimilar. Treatment of M. crystallinum for several days with 0.4kmol/m3 NaGI in the root medium, in parallel with an increasein the cell sap osmolarity, increased the activity ofantioxidative enzymes, such as superoxide dismutases (SODs).M. crystallinum had 3 SOD isoforms. Salt treatment increasedthe activity of this isoform earlier than that of the otherSODs (Miszalski et aI., 1998). Lechno et al. (1997) reported thatNaGI treatment increased the activities of the antioxidativeenzymes catalase and glutathione reductase, and the content ofthe antioxidants ascorbic acid and reduced glutathione, butdid not affect the activity of superoxide dismutase. Thedistribution of Na+ and K ions in the plant suggests that the
salt-derived injuries and the effects on antioxidative systemsreflect a response to osmotic stress.
Ferredoxin-dependent glutamate synthase (EC 1.4.7.1)catalyses an essential step in the pathway of glutamatebiosynthesis. Exposing detached tomato cv. HellfruchtFruhstamm leaves for 6 h to 12 g NaCl/litre resulted in asignificant 2-fold increase in the activity of ferredoxin-dependent glutamate synthase extracted from the leaves. Theinduction of ferredoxin-dependent glutamate synthase undersalt stress may provide the glutamate required for prolinesynthesis which is a common response to salt stress (Berteli etal., 1995). However, the activity of the proline degradingenzyme, proline oxidase, decreased under salt stress in Brassicajuncea (Shashi Madan et al., 1995). This was again confirmed byRoosens et al. (1998) in Arabidopsis thaliana plants. Un ChuanChi etal. (1996) found that NaCI decreased glutamine synthetase andglutamate synthase activities in roots of rice plants, butincreased glutamate dehydrogenase activity. The growthinhibition of roots by NaCI could be reversed by the additionof L-glutamic acid or L-glutamine.
In annual ryegrass, Phosphoenolpyruvate carboxylase(PEPc, EC 4.1.1.31 )activity in shoots and roots waspositively correlated with concentration of organic acids, butwhereas PEPc activity was higher in roots, organic acidconcentration was higher in shoots. This suggests that some ofthe organic acids produced in the roots were used as carbonskeleton for transamination reactions. It is suggested thatincreased nitrate reductase (EC 1.6.6.1), PEPc, and glutaminesynthetase [glutamate-ammonia ligase] (EC 6.3.1.2) activitiesin roots may be involved in adaptation to salinity (Sagi et al.,1998a).
Sagi et al. (1998b) reported that salinity enhancedactivities of xanthine dehydrogenase (XDH) and aldehydeoxidase (AO) which were more pronounced in the roots than inthe shoots of ryegrass plants. The concentration of ureides(allantoic acid and allantoin) increased with salinity,especially in the roots. The increase in both enzymes withsalinity may constitute part of the mechanisms of plantadaptation to stress by increased XDH activity and thesubsequent production of ureides allowing transport of organicnitrogen compounds with a low C/N ratio.
Thiyagarajah et al. (1996) found that the activity ofgalactosidase, glucosidase, peroxidase or xyloglucan endo-transglycosylase extracted from S. maritima of the cell wallcompartment are much more salt-tolerant than cytoplasmicenzymes of higher plants with up to 1 M NaCI. Renu Munjal et al.(1995) found that in cotton cotyledonary, salinity increasedcellulase and protease activities at all the growth stages.Kolupaev and Trunova (1994) reported that in wheat coleoptile,
moderate salt stress (0.5% NaCI) caused a sharp increase ininvertase activity, and an accumulation of reducing sugarsmost likely due to the enhanced oligasaccharide hydrolysis.Moreover, Kolupaev et al. (1991) concluded that the increase ininvertase activity and oligosaccharide hydrolysis under salineconditions were considered protective and adaptive on thebasis of data on the high rate of induction of the enzymeactivity under sublethal NaCI concentrations and thenonspecific protective functions of soluble carbohydratesunder stress condition.
Benavides et al. (1997) suggested that because Ornithinedecarboxylase (ODC) was not detected and argininedecarboxylase (ADC) activity followed a pattern similar tothat of putrescine, that the variation in putrescine contentcould be attributed entirely to the decrease in ADC activity.alpha-Difluoromethylarginine and alphadifluoromethylornithine(ADC and ODC inhibitors, respectively) did not inhibit butdelayed the onset of germination of seeds, and alpha-difluoromethylornithine increased the content of spermidineand spermine. It is concluded that polyamines may be involvedin the germination process of H. annuus seeds and in responseto salt stress. Also, Chattopadhyay et al. (1997) suggested thatin the salt-tolerant rice cultivar, arginine decarboxylaseactivity (ADC, EC 4.1.1.19), the first enzyme involved in thebiosynthesis of polyamines (PA) from arginine, increases andits transcripts also accumulate during the prolonged salinitystress; this mechanism is absent in the salt-sensitive ricecultivars.
Salt tolerance of plants
In general the presence of soluble salts in the nutrientmedium can affect plant growth in three ways. In the firstplace high concentrations of specific ions can be toxic andinduce physiological disorders (e.g. Na+, borate). Secondly,ionic imbalances can be caused by high salt concentration.Thirdly, soluble salts depress the water potential of thenutrient medium and hence restrict water uptake by plantroots. Plants can adapt to this kind of water stress byosmoregulation (osmotic adjustment) which is brought about bythe uptake of inorganic ions and the synthesis andaccumulation of organic solutes. The most important inorganicsolutes are K, Cl and N03-. Increased uptake of these ionspecies results in a decrease of the cell water potentialwhich promotes water uptake. Inorganic ions are mainlyaccumulated in the vacuole whereas organic solutes aresynthesized and accumulate in the cytoplasm. The mostimportant organic osmotica in this respect is glycinebetaine.
Tolerance mechanisms used by plants to adapt to salinitycan be separated into those that allow the growing cells ofthe plant to avoid high ion concentrations and those thatpermit the cells to cope with high ion concentrations uponexposure to salt. Salt avoidance mechanisms involve exclusionat the root, absorption by xylem parenchyma cells, xylem-phloem exchange systems, distribution of ion gradients betweennongrowing and growing portions of the plant and, in the caseof halophytes, sequestration of ions into salt glands ortrichomes. In general, exclusion mechanisms are effective atlow to moderate levels of salinity, while ion accumulation isthe primary mechanism used by halophytes at high salt levels,presumably in conjunction with the capacity tocompartmentalize ions in the vacuole. The capability toaccumulate and compartmentalize ions has been theorized to bethe result of changes in membrane permeability and iontransport properties that facilitate transport againstelectrochemical gradients and membrane transport selectivity(Hasegawa et al., 1986).
A variety of terms have been introduced to try todistinguish degrees of salt tolerance of plants. Glycophytesperform best at very low levels of salt. If increases in saltover a narrow range are tolerated without an immediate loss inproductivity, the plants are commonly termed salt tolerant. Incontrast, halophytes, which are often subdivided into severalmore categories, perform better when some salt (miohalophytes)or high amounts of salt (eu-halophytes) are present.
Considerable differences occur between crop species andcultivars in relation to salt tolerance. Table 1 shows theresponses of various field crops to salinity (Bernstein,1970).
Table (1): Salt tolerance of various field crops asconductivity at which the yield is reduced by 25% data ofBernstein, 1970 .
EC ECBarley 15.8 Rice (paddy) 6.2Sugar beet 13.0 Maize 6.2Cotton 12.0 Sesbania 5.8Sunflower 11.3 Broadbean (Vicia) 5.0Wheat 10.0 Flax 4.8Sorghum 9.0 Beans(Phaseolus) 2.5Soybean 7.2
Plant Strateqies for Sodium Avoidance:
Plants have apparently evolved two principal strategies foravoiding high sodium concentrations in the cytoplasm, namelycompartmentation and exclusion.
Compartmentation of Salt
New techniques such as X-ray microanalysis and compartmentalefflux methods have added new insight into how cells organizetheir ionic compositions and deal with osmotic burdens. In theplants studied, sodium is excluded from the cytoplasm and cellorganelles and is primarily sequestered in the vacuole. Otherforms of compartmentation, such as export into cell wall,appear to be of limited significance. The study of membranetransport processes by which Na+ is effectively sequestered isof utmost importance for the molecular description of salt
tolerance. Sodium first has to pass through the plasmamembrane. Maintaining high concentrations of sodium in thevacuole necessitates an additional transport system located inthe tonoplast membrane. Transport systems through bothmembranes are ATP-requiring Na+/H+ transporters or antiporters whose biochemistry is being studied by several groups(Wang et al., 1989). Genes for subunits of both the plasmamembrane and the tonoplast A TPases are being characterized(Pardo and Serrano, 1989). Bremberger et al. (1988) have shownthat activity increases of the tonoplast ATPase in M. crystallinumare due to de novo synthesis of proteins of the enzyme complexand structural changes of the ATPase molecule.
Various lines of evidence show that Na+ is occluded inthe cell vacuoles of many plants, particularly in halophytes,and is excluded from the cytoplasm of all plants. Indirectevidence for such compartmentation comes from measurements oflongitudinal profiles of Na+ and K concentrations in roots. Insuch experiments with Hordeum distichum grown in the presence of1.0 M NaCI (Jeschke and Stelter, 1976), Na+ concentration inmeristematic nonvacuolated cells in the root tip was 10 mM. Na+ concentration increased rapidly with distance from the roottip and with cell vacuolization, to 65 mM at 2.0 mm from thetip. Potassium concentration changed in the oppositedirection; that is, it decreased with distance from the roottip. Recently, Koyro (1997) found that NaCI concel")trationswere seen to increase and the K concentrations to decrease.during salt stress in the vacuoles of the epidermis and cortexcells. The salt-induced increase in vacuolar NaCIconcentrations of epidermis and cortex cells are in the region
2 cm behind the root tip, which is sufficient for an osmoticbalance towards the growth medium.
Mechanisms of Sodium Transport :
Sodium transport from the environment into the cytoplasmof plant cells is a passive process. It depends on theelectrochemical potential gradient of Na+ and the presence ofpermeable Na+ channels in the plasma membrane. In principalNa+ could accumulate in the cytoplasm to a few hundred timesits concentration in the environment. However, suchaccumulation is prevented in salt tolerant plants by controlof influx (channel gating) and/or by active export from thecytoplasm to the vacuoles and also back to the environment.
Active sodium transport in plant cells is performed by Na+ /H+ antiport, ordinarily driven by an ATPase activity-drivedproton-motive force (Poole, 1988). The presence of a Na+ /H+anti porter would be expected in the tonoplasts of plant cellsthat tolerate Na+ by its excretion to and occlusion in thevacuoles.
Huang GhiYing et al. (1998) mentioned that the level of Na +accumulation in root cells correlated with the inside-acid protongradient (change in pH) across the plasma membrane vesicles. The salt-acclimatized plants had higher antiport activity of Na+ influxlH+efflux and H+-pumping ATPase activity than that of control and non-acclimatized plants. It is concluded that higher H+-ATPase activityfavored salt-acclimatized plants growing under salinity stress. Wuand Seliskar (1998) found a significant increase (up to 2- to 3-fold) of PM H+-ATPase activity when callus was grown on mediacontaining NaGI. The incremental activation of PM H+ -ATPaseactivity would enable the cell to tolerate higher cytoplasmic NaGIconcentrations. The response of PM H+ -ATPase in S. patens callussuggests that this species has evolved mechanisms that can regulatethis important enzyme when cells are exposed to NaGI. Also,Ballesteros et al. (1997) found that Na+ transport across thetonoplast and its accumulation in the vacuoles is of crucialimportance for plant adaptation to salinity. Mild and severe saltstress increased both A TP- and PPj -dependent H+ transport intonoplast vesicles from sunflower cv. Alhama seedling roots,suggesting the possibility that a Na+/H+ anti port system could beoperating in such vesicles under salt conditions. Salt treatmentsinduced a Na+/H+ exchange activity, which displayed saturationkinetics for Na+ added to the assay medium. This activity waspartially inhibited by 125 ~M amiloride, a competitive inhibitor ofNa+/H+ anti ports. It is concluded that the existence of a specificNa+/H+ exchange activity in tonoplast-enriched vesicle fractions,induced by salt stress, could represent an adaptative response in
sunflower plants, moderately tolerant to salinity. Ayala et al. (1996)suggested that the ability to accumulate and compartmentalize Na+may result, in part, from stimulation of the H+ -A TPases on theplasma membrane (PM-ATPase) and vacuolar membranes (V-ATPase).
Lin et al. (1997) reported that sensitivity to highlevels of salt in plants is associated with an inability toeffectively remove Na+ ions from the cell cytoplasm. Theability to compartmentalize Na+ may result, in part, fromstimulation of the H+ -A TPases on the plasma membrane (PM-ATPase) and vacuolar membrane (V-ATPase). These H"-pumpingATPases may provide the driving force for Na+ transport viaNa+-H+ exchangers. Although the PM-ATPase responds toincreased Na+, activity of the transport proteins on theplasma membrane alone may be insufficient to regulateintracellular Na+ levels. In addition, the inability of the V-ATPase to respond to increased levels of Na+ indicates thatsalt sensitivity in cotton seedlings may result, in part, froma lack of effective driving force for compartmentalization ofNa+.
There was an increased accumulation of plasma membraneH+ATPase mRNA in roots and expanded leaves of plants treatedwith 400 mM NaGI. mRNA for the 70 kDa subunit of the tonoplastH+-ATPase only increased in the expanded leaves of salttreated plants (Binzel and Cherry, 1994). Meanwhile, Koyro(1997) reported that the number of mitochondria increased inthe epidermal and in the cortex cells after salt stress thusindicating an additional supply of energy for osmoticadaptation and for selective uptake and transport processes.
Barkla et al. (1994) found in sugar beet cell suspensionsthat the activity of the vacuolar Na+/H+ antiport increasedwith increasing NaCI concentrations in the growth medium. Thisincreased activity was correlated with the increased synthesisof a 170 kDa tonoplast polypeptide, suggesting the associationof this protein with the plant vacuolar Na+/H+antiport. Lacanand Durand (1996) found in the presence of NaCI, the transportsystems released K into the xylem sap and reabsorbed Na+ ofsoybean plants. The Na+-K exchange was energized by proton-translocating ATPases, enhanced by external K concentration,and dependent on the anion permeability. Evidence waspresented for the operation of H+ /Na + and H+ /K anti portersat the xylem/symplast interface. Fukuda et al. (1998) concludedthat this Na+/H+ anti porter functioned as a Na+ transporterin the vacuolar membranes. It is suggested that the amount ofanti porter in the vacuolar membranes may be one importantfactor determining salt tolerance.
Ion Channels and Sodium Exclusion:
The sodium permeability of biological membranes is 102-106 times higher than that of artificial phospholipidbilayers. This permeability is facilitated by intrinsicproteins that constitute ion channels in the phospholipidbilayers (Tester, 1990). Sodium specific channels havehitherto not been demonstrated in the plasma membranes ofplant cells. Sodium apparently moves through a general cationchannel, with different permeabilities for the various ions(Schachtman et al., 1991). Regulation of gating and selectivity ofsuch channels seem to be responsible for sodium exclusion inmany salt tolerant crop plants. The presence of K and Ca+ions, has been shown to decrease Na+ influx to plant cells andconsequently decrease Na + damage and yield reduction (Zidan etal., 1991).
The existence of two kinds of channels that allow Na +permeation has been reported for the plasma membrane of plantcells (Maathuis and Prins, 1991). One is an inward rectifiedchannel (closes upon membrane depolarization) with a PK /PNa(K/Na+ permeability ratio) of 5-10 and an outward rectifiedchannel (opens upon depolarization) with a PK/PNa of 20-60.Membrane potential dependent Na+ influx to corn root wasabolished in the presence of K (Jacopy and Hanson, 1985).Potassium thus seems to prevent Na+ movement across the inwardrectified channel.
Katsuhara and Tazawa (1986) showed that 0.1 M NaCIdepolarized the plasma membrane, increased itselectrical conductivity, increased the Na+ content ofthe cells, and decreased their K content. Schachtman etal. (1991) suggested that depolarization opens theoutward rectified channel, allowing Na+ influx and Kefflux under saline conditions. All these effects ofNaCI are prevented by the presence of Ca2+ in themedium. Cramer et al. (1985) speculated that displacementof Ca2+ by Na+ from the surface of the plasma membranemay be the primary event and that this is prevented byincreased external Ca2+ concentration. The authorsfurther suggested that the opening of K channels and Kleakage may be a direct result of either Ca2+displacement from membrane surfaces or membranedepolarization and a rise in intracellular Ca2+. Ineither case, K leakage should probably be preceded by achange in the direction of the electrochemical Kgradient. Such a change would be induced by membranedepolarization and should also open the outward-rectified K channel.
Sodium distribution in the plant:
Most plants, when grown in the presence of salt,accumulate some Na+ in their roots even when it isexcluded from the shoots. Collander (1941)distinguished between Na + accumulator plants andnonaccumulators. The former plants transport largeamounts of Na + to their shoot; the latter exclude. Na+from their shoots and retain it in their roots.Dicotyledonous halophytes are the most prominent Na+accumulators, but some salt resistant glycophytes, suchas barley, also belong to this group. Generally, saltsensitive plants, such as beans and corn, are the mostprominent Na+ excluders. Sodium recirculation is amechanism for Na+ exclusion from the shoots employed byrelatively salt sensitive plants. Cell membranes ofsodium nonaccumulator, such as bean, seems not tocomprise a Na+ IH+ anti porter (Mennen et al., 1990) andhence cannot excrete Na+ from the cytoplasm to thevacuoles.
Salt Secretion
The transpiration stream continuously carries salts to
plant shoots. Large amounts of salt should thus bedelivered to the leaves of plants growing in a salineenvironment if the salts are not excluded from theshoots. Even in halophytes that accumulate Na + and Clin their leaf cells, the amount of salt carried to theshoot is much in excess of that needed for turgorregulation. Secretion by special salt glands is oneimportant mechanisms for the removal of excess mineralions from the leaves (Fahn, 1988).
Compatible orqanic solutes
Most organisms counter increases in extracellularsalt concentration by intracellular increases in"compatible" osmolytes, which often accumulate to highconcentrations in the cytoplasm and serve to adjust theosmotic potential of cells. These osmolytes are lowmolecular weight compounds that are normal constituentsof cell metabolism and are usually found in smallamounts. Such accumulated compounds are amino acidssuch as proline and glutamine, modified amino acidssuch as glycine-betaine, and more complex biogenicamines (Csonka, 1989) and polyols, such as trehalose,glycerol, or inositol derivatives. However, therelationship between stress and the accumulation of anycompound is complex. It may be that the accumulatingcompound is the end product of a pathway fulfilling ametabolic need, such as maintaining energy charge,rather than the necessity of accumulating theparticular compound. The role of proline accumulationin adaptation to salt stress, for example, is thesubject of some dispute. While some researchers havefound that increased proline accumulation occurred inmore salt tolerant cell lines than in more sensitivelines (Handa et al., 1986), others have concluded thatthere is no correlation between proline accumulationand salt tolerance (Chandler and Thorpe, 1987).Recently, Gzik (1996) concluded that the accumulationof high levels of proline under stressed conditionsindicates the involvement of proline in osmoregulation.It is suggested that the stress signal induces a lossof feedback inhibition of the enzyme involved inproline biosynthesis and that genetic engineering forosmotolerance should be focused on the overproductionof this enzyme and the reduction of its sensitivity toendproduct inhibition. Moreover, Sanada et al. (1995)
suggested that proline has a bifunctional role in theacclimatization to high salt stress; an osmoregulantrole in the light and as a substrate for darkrespiration to supply energy to perform thecompartmentation of ions into the vacuole in the dark.
Compatible solutes are supposed to provide anenvironment compatible with macromolecular structureand function (Yancey et al., 1982). It was proposed thatthese solutes are preferentially excluded from thesurface of proteins and their immediate hydrationsphere. Thus, the addition of these solutes to aprotein suspension creates a thermodynamicallyfavorable situation, since the chemical potentia Is ofboth the protein and the additive are increased. Thissituation stabilizes the native conformation of theproteins (Crowe et aI., 1988). Stewart and Lee (1974)demonstrated the compatibility of proline withglutamate dehydrogenase extracted from the halophyteTriglochin maritima. The enzyme was not inhibited in vitro byproline to a concentration of 0.6 M. Similar resultswere obtained for barley leaf malate dehydrogenase andbarley embryo pyruvate kinase (Pollard and Wyn Jones,1979). These enzymes were not inhibited in vitro by up to0.5 M glycine betaine. In addition, glycine betaineand, to a lesser extent, dimethylglycine, partiallyrestored malate dehydrogenase activity in the presenceof 0.3 M NaCI alone. The inhibition decreased linearlywith addition of glycine betaine, to 50% at 0.5 Mglycine betaine.
Gilbert et al. (1998) reported that accumulation oflow molecular weight nitrogen-containing compounds inColeus leaves was observed, which peaked within thefirst 10 days of exposure to salinity, and thendeclined, but remained slightly elevated for theremainder of the study. A number of amino acidsaccumulated in both the sink and source tissues,including arginine, asparagine, and serine which mayact as an osmoregulant. It is suggested that some ofthe observed accumulation of amino acids and amidesobserved is due to de novo synthesis and not simply theresult of protein degradation.
Effect of salinitv on potassium contents in plants:
The deleterious effects of salt, reported for N.obtusa, included excess Na+ accumulation as well as I<
leakage (Katsuhara and Tazawa, 1986). Both areprevented by Ca2+. Thus, the presence of Ca2+ seems tobe necessary for I</Na+ selectivity and for themaintenance of an appropriate I< concentration in plantcells. The response of I< content in different plantsto external Na+ increments is not uniform. Many plants,in particular relatively salt tolerant glycophytes,such as Atylosia sericea maintain a constant I< content oreven increase it in the presence of salt. Moresensitive glycophytes fail to maintain I< content inthe presence of a high salt concentration. Such adecrease in I< content may indicate damage (Winter andKirst, 1991). On the other hand, halophytes, such asSimondsia chinensis as well as tolerant glycophytes thataccumulate Na+, such as Sorghum bicolor, decrease I<content with increasing external salt concentrationwithout concomitant damage. This decrease seems to berelated to the replacement of vacuolar I< with Na+(Leigh and Wyn-Jones, 1984). The maintenance ofadequate I< content under saline conditions seems todepend on selective I< uptake as well as selective I<and Na+ compartmentation in the cells and distributionin the shoots.
The response of 10-day-old seedlings of radish cv.Fakir to salt stress (100-200 mM NaCI) was investigatedBy Lopez et al. (1994). Three weeks after initiation ofsalt treatment, the FW of the shoots of salt-treatedplants was half that of untreated plants. The saltstress resulted in the accumulation of Na+, preferablyin the old leaves. The I< level was reduced by as muchas 50% in the old leaves of NaCI-treated plants,whereas this reduction was only 20-25% in the youngleaves. Also, Botella et al. (1997) found that NaCIreduced I< net uptake rates and to a greater extent I<translocation from root to shoot, which resulted in alower I< shoot content and a higher I< root content.The inhibitory effect of salinity on I< translocationwas stronger with low I< concentration in the nutrientsolution. Net uptake of I< was dependent on Kconcentration in the root medium and on K status of theroot. Cramer et al. (1995) found a lower stem Kconcentrations and leaf malate concentrations insalinized than in control tomato plants, indicatingreduced functioning of the K-shuttle in salinizedplants.
Adaptation to salinitv
A large part of research on salinity is carriedout with the attention of accommodating crop plants togrow in salinities outside the natural range oftolerance and nevertheless obtain appropriateagricultural yields. However, two types of plantresponses to salinity are distinguished, firstly, the"preexisting resistance mechanisms" that enable theplant to cope with salinity within its natural range oftolerance, and secondly, "adaptation" (Amazallag et al.,1990a). Adaptation is achieved during a specifictreatment and involves changes in the plant's behaviorand expression of properties that were not evidentbefore the treatment. A plant is considered "adapted"to salinity when at least one of the following casesoccur after the treatment that induces adaptation. 1-An increase in the mean relative growth rate of thesalt-treated plant occurs, so that the growth isrestored to a value more or less similar to that of thecontrol plant. 2- When the plant has acquired thecapacity to complete its life cycle in a salineenvironment in which the nonadapted plant is not ableto do so. In the following, there were a few examplesof adaptation.
Both the strategies employed by intact salt-resistant plants can be found in salt adapted celllines. Thus, in the presence of salt, tolerant celllines of potato (Sabbah and Tal, 1990) more efficientlyexcluded Na+ and prevented the decrease in K contentthan unadapted lines. On the other hand, in tobaccocell lines, salt tolerance was associated with adecrease in K content in concert with increasingsalinity and an increase in Na+ as well as er, asprinciple solutes for turgor regulation. Organiccompounds also accumulated with salinity, in particularproline and sucrose (Blinzel et al., 1987). Sodium and Clwere occluded in the vacuoles of adapted tobacco cells.In cells adapted to 428 mM NaCI, the vacuolar contentsof Na+ and Cl were 780 and 624 mM, respectively, butcytoplasmic concentrations were maintained at 96 mM(Blinzel et al., 1988). However, increased salt toleranceof cultured cells has rarely led to increased salttolerance in normal regenerated plants (Dracup, 1991).
On the other hand, the salt adaptation of Sorghumplants was accompanied by an increased capability toexclude Na+ (Amzallag et al., 1990a) and an increase inphosphoenolpyruvate carboxylase activity (Amzallag etaI., 1990b).
Today, great effort is being directed towards thedevelopment of salttolerant crop genotypes through theuse of plant breeding strategies involving theintrogression of the genetic background from saline-tolerant wild species into cultivated plants. Withrecent developments in biotechnology, there is also thepotential for obtaining salt-tolerant crop genotypes bythe use of somatic cell selection or protoplast fusionmethodologies or by gene transformation usingrecombinant DNA methodologies. For ex. glycinebetaine[betaine] is one of the compatible solutes thataccumulate in the chloroplasts of certain halotolerantplants Nhen these plants are exposed to salt stress.The codA gene for choline Jxidase, the enzyme thatconverts choline into glycinebetainG. The transformedplants of A. thaliana with codA gene allowed it toaccumulate gIycinebetaine enhanced its ability totolerate salt stress (Hayashi et al., 1997).
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