THE LEGUME-RHIZOBIA SYMBIOSIS UNDER SALT STRESS - A …a broad range of crops (Lauchli and Epstein, 1990; Serrano and Gaxiola, 1994). ... Progress towards achieving salinity tolerance

THE LEGUME-RHIZOBIA SYMBIOSIS UNDERSALT STRESS - A REVIEW

Ranju Singla and Neera Garg

Department of Botany,Panjab University, Chandigarh - 160 014, India

ABSTRACTSalinity is one of the severe problems in worldwide agricultural production. Soil salinity limits

the productions of both forage and grain legumes. Adverse effects of salinity are mediated throughdetrimental effects on the rhizobium - legume interactions that lead to the establishment of thenitrogen fixing symbiosis. Salt stress inhibits the initial steps of the rhizobia - legume symbiosis. Forimprovement of nodulation and symbiotic nitrogen fixation under saline environments, the answerlies in selecting and developing salt tolerant cultivars of legumes as well as rhizobium for effectivesymbiosis under salinity. This review focuses on the effect of salt stress on nodulation and symbioticnitrogen fixation in legumes and to suggest future lines for alleviation of salinity effects on theseprocesses.

Soil salinity is a major agriculturalproblem, significantly reducing productivity ofa broad range of crops (Lauchli and Epstein,1990; Serrano and Gaxiola, 1994).Worldwide, about one third of the irrigatedarable land is already salt affected and thatportion is still expanding (Lazof and Bernstein,1999). Each year approximately 10 x 106 haof the all agricultural land is abandoned becauseof salinisation (Flowers and Yeo, 1995). InIndia, 7.04 million ha land is affected by salinity(Abrol and Bhumbla, 1971). The decline inthe productivity of crops, in salt affected soils,is mainly caused by salt induced osmotic effects,ion toxicity and mineral perturbations in plants(Hu and Schmidhatter 1997; Volkmar et al.,1998; Lazof and Bernstein 1999; Lauchli,1999; Hasegawa et al., 2000; Muhling andLauchli, 2002). In fact, all major agronomiccrops are relatively salt intolerant (Ashraf andO’Leary, 1994; Lutts et al., 1995; Garg andGupta, 1997; Garg and Gupta, 2001). Highsalinity causes both hyperionic andhyperosmotic stress effects, and theconsequences of these can be plant demise(Yeo, 1998; Glenn et al., 1999; Hernandezet al., 2000, 2001; Rout and Shaw, 2001).

Long time back, in the year 1953Bernstein and Hayward wrote, “An

understanding of the physiology of salttolerance of plants is important for an effectiveapproach to the salinity problem, which is ofincreasingly widespread occurrence.” Couplingand understanding of the genetic control ofsalt tolerance with this physiological approachadds further dimension of promising to lead tothe development of salt tolerant crops.Tolerance to stress varies with the growthstage, climatic conditions as well as for differentgenotypes/cultivars of a crop within the samespecies. Different strategies have been adoptedby soil scientists to solve the problem of salinity.The major strategy to overcome it includesreclamation of salt affected soils by usingpreventive and curative measures; but the costin terms of money and energy is high. Apossible alternative, the biotic approach, is tolay emphasis on the selection and developmentof varieties which give minimum depressionin yield when grown under saline conditions.Selection of high salt tolerant genotypes withina species, in comparison to relatively saltsensitive ones, highlights the prospects forimprovement through conventional selectionand breeding technique. A prerequisite inselection and breeding for salt tolerance is thepresence of genetic variations for tolerance ingene pool of the species. Interspecific, intra-

Agric. Rev., 27 (1) : 1 - 21, 2006

specific and intra-cultivar variations for acharacter provide scope for their improvement(Johnsen et al., 1990; Ashraf, 1994).

Legumes belonging to familyFabaceae, the third largest family ofangiosperms, with three subfamiliescomprising 650 genera and more than 18,000species (Polhill, 1994), rank next to cereals inimportance as food for human beings andanimals. In addition to their nutritive values,legumes have considerable importance inagriculture for their ability to improve soilfertility by fixing large amounts of atmosphericnitrogen. Legumes have long been recognizedto be very sensitive to salinity (Lauchli, 1984).Amongst grain legumes lentil, chickpea,mungbean, pigeonpea etc, widely grown in thesubcontinent because of their importance aspulse crops, are considered to be relatively saltsensitive crops as compared to soybean.Despite their great importance, very little workhas been done on the improvement of salttolerance in legume crops. Differences in salttolerance, at the cultivar and genotypic levels,have been reported in several leguminous crops(Lauchlii, 1984; Dua et al.,1998; Subbaraoand Johansen, 1994; Serraj et al., 1998,2001) and exploitation of genetic variabilityin cultivated species offers the possibility ofdeveloping salt tolerant crops (Epstein et al.,1980). However this variation has not beenevaluated thoroughly and systematically formost of the leguminous crops.

Physiological responses of plants tosalinity are one of the most studied subjects inplant physiology (Flowers et al., 1977; WynJones, 1981; Greenway and Munns, 1980;Flowers, 1985; Munns and Termaat, 1986;Epstein and Rains, 1987; Cheeseman, 1988;Munns, 1993; Hasegawa et al., 2000).Progress towards achieving salinity tolerancein crops can be made only when physiologicaland biochemical processes for tolerance areunderstood (Shannon, 1985; Yeo and Flowers,

1989; Shannon and Noble, 1990; Cuarteroet al., 1992; Munns, 1993) Inter-specific, intra-specific and intra-cultivar variation is of primeimportance for the improvement of salttolerance through selection and breeding. Theexistence of genetic variability in the sensitivityof N

2 fixation and to salt among legume species

and cultivars may be useful to further elucidatethe NaCl inhibition symbiotic nitrogen fixationto select optimal Rhizobium-legume symbiosisfor agricultural production in soils subjected tosalinity (Serraj et al., 2001; Serraj, 2002).During the last two decades, a number ofworkers like Lauter and Munns, 1982; Olmosand Hellin, 1996; Adb El Samad et al., 1997;Dua and Sharma, 1997; Dua, 1998; Soussiet al., 1999; Sleime et al., 1999 have tried toidentify the traits attributing towards salinityresistance amongst the different legumespecies. However, no consistent and specificcorrelations were identifiable. In order to havea better understanding of the influence ofsalinity stress and the mechanism of salinityresistance, it is needed to study themorphophysiological and biochemical behaviourof different cultivars/genotypes of a speciesand to visualize the traits associated with salinitytolerance or susceptibility with the help ofexperimental evidence. In the light of mostrecent literature available, the effect of saltstress on various metabolic activities of legumeshas been reviewed under the following heads:

1. Effects of salt stress on germination,growth and metabolic biology.2. Effects of salinity on nitrogen metabolism.3. Ameliorative measures to salt stress.

1. Effects of salt stress on the germination,growth and metabolic biology of legumes

Salt accumulation in the soil of aridregions and irrigated fields often described assalinity, impairs plant growth. Salinity stressinfluences plants at every stage of the lifecycleand stimulates water stress in many ways. Themain inhibitory effect of salt stress is osmotic.

2 AGRICULTURAL REVIEWS

Sodium chloride is usually present in the soiland, although rather innocuous in its inorganicconstituents, influences many membranefunctions and induces membrane ultrastructural changes. Growth of plants in thepresence of sodium chloride may impaircellular ion homeostasis, characterized by highK+ and low Na+ cytoplasmic content.Increased salinity can affect plant growth by :the imposition of water stress throughincreased osmotic potential of the rootingmaterial (Levitt,1980; Yeo,1983; Hale andOrcutt, 1987) or the accumulation of ions orother possible toxins in the soil or in the planttissue (Flowers,1985; Munns, 1988, 1993;Jacoby, 1994).

1.1 Cellular water relations:Legumes have long been recognized as eithersensitive or only moderately resistant to salinity(Delgado et al., 1994). At cellular level manyof the physiological effects of salinity on shootand leaf growth are typical of a water stresswhich necessitates a corresponding adjustmentin the osmotic potential of the plant cells tosustain water uptake. According to Neumannet al. (1988) salt stress initially inhibits leafexpansion through reduced turgor, and mayinfact eventually result in increased cell wallextensibility, which counteracts the negativeeffects of low turgor. In the presence of salt,cell wall extensibility of the growing region maydecrease (Cramer, 1992; Nonomi et al.,1995). Wu et al. (1997) suggested that ABAmodulated the expression of enzymes affectingplasticity of the cell wall. These results suggestthat the hormonal balance is able to controlthe cell wall expansion. Crop plants show somedegree of tissue osmotic adjustment in responseto either salinity or drought (Mastuda and Riazi,1981). Accumulation of compatible solutes inresponse to stress is a metabolic adaptationfound in a number of stress tolerant, oftenunrelated taxa, suggesting convergentevolution for this trait (Yancey et al., 1982).

The osmoprotectants are synthesized inresponse to stress and are localized in thecytoplasm (McCue and Hanson, 1990;Delauney and Verma, 1993; Louis andGalinski, 1997; Glenn et al., 1999) and leadto turgor maintenance for the cell underosmotic stress. A variety of osmoprotectivecompounds such as proline, glycine betaine,various sugars (sucrose and fructose), sugaralcohols (glycerol, methylated ionsitols) andcomplex sugars (trehalose, raffinose, fructose)accumulate in response to osmotic stress andact as “compatible” solutes i.e. they do notinhibit normal metabolic reactions (Pharret al., 1995; Piqueras et al., 1996; Hasegawaet al., 2000).

1.2 Ionic Relations: Theaccumulation of toxic salts in tissues hasfrequently been postulated as another limitingfactor for growth under salt stress. Althoughmany biochemical functions require specificinorganic ions, increasing the concentrationsof these ions above normal intracellularconcentrations may lead to disruption ofmetabolic functions by reducing the activitiesof enzymes (Yancey et al., 1982). Leopold andWilling (1984) suggested that NaCl could causeleakage of solutes from soybean leaf tissuewhich could interact with cellular membranes.According to Greenways and Munns (1980)older leaves tend to have higher levels of Na+

and Cl- than younger leaves because ofcontinuous accumulation of these ions overtime due to transpiration. Salt accumulationin the plants leads to reduced longevity ofmature leaf tissue. Dale (1986) explainedreduced leaf size due to salt stress on the basisof limited assimilate supply. Munns (1993)argue that salt concentrations in older leavesaccelerated their death leading to reducedassimilate or hormone export to the rest ofthe plant. Nonami et al. (1995) suggested directeffect of Na+ on cell expansion. Volkmar et al.(1998) explained reduced production in leaves

Vol. 27, No. 1, 2006 3

on the basis of reduced storage capacity in theshoots in the form of cell vacuoles toaccommodate salts arriving from the roots,leading to further salt toxicity. Lauchli (1999),Santa- Maria and Epstein (2001) reported theimportance of maintenance of adequate netuptake of K+ by plants at high Na+ and thissustained Na+/K+ selectivity as a physiologicalmarker for the ionic component of salt stress.Hasegawa et al. (2000) suggested that signalingcascades presumably function in intercellularcoordination or regulation of effectors genesin a cell-/tissue-specific context required fortolerance of plants. Zhu (2002) has proposedthat salt stress signal transduction consists ofionic and osmotic homeostasis signalingpathways detoxification (i.e. damage controland repair) response pathways, and pathwaysfor growth regulation. He further states thatosmotic stress activates several protein kinasesincluding mitogen-activated kinases which maymediate osmotic homeostasis and/ordetoxification responses. A number ofphospholipid systems are activated by osmoticstress, generating a diverse array of messengermolecules, some of which may functionupstream of the osmotic stress activatedprotein kinases. Munns (1993) has proposedanother biphasic model of growth response tosalinity. In the first phase toxic ions increaseespecially in the mature leaves. These fullyexpanded leaves often show necrotic leaftissue, while in younger expanding leaves saltinduced water deficit leads to Ca2+ deficiencysymptoms (Fortmeier and Schubert, 1995).Therefore Na+ accumulation in leaves,particularly in the leaf apoplast, could beresponsible for Na+ toxicity in leaves (Volkmaret al., 1998). Oertli (1968) originally proposedthat salt lead to the death of leaves bydehydration of leaf cells and turgor loss. Na+

accumulation in the leaf apolast may also occurbecause of stimulation of the plasmamembrane ATPase under salt stress (Niu et al.,1995), which may lead to an increased Na+

efflux from the cytoplasm into the apoplast orby incoming salt from the root which couldno longer be sequestered into the cell vacuoles(Munns, 1993).Muhling and Lauchli (2002)also supported the hypothesis that saltaccumulation in the leaf apoplast could beresponsible for the death of leaves in plantsexposed to salinity.

1.3 Mineral Composition and IonUptake: The simultaneous presence of saltsand nutrients elements in the root can influencenutrient uptake by plants and thereby affecttheir chemical composition. Murumkar andChavan (1986) found increased concentrationsof Na, Cl, P in pods and seeds of chickpeawith a decrease in the concentrations of Ca inpods and Fe, Mn, Mg in seeds under increasingsalt. Increasing levels of salinity significantlyreduced the uptake of P, Zn, Fe in chickpea(Dravid and Goswami, 1987). Concentrationsof Ca, Mg, Na increased and that of K and Bdecreased with increasing salinity (0.4-8.5dSm-1) (Yadav et al., 1989). Elshiekh and Wood(1989) while working on specific ion effects inchickpea found chloride ions of Na, K, Mg tobe more toxic than the corresponding sulphateions. According to Dhingra et al. (1994) salinitycaused accumulation of Na+ and Cl- in the seedsof chickpea but did not affect K+ content.Cordovilla et al. (1995) reported higher saltsensitivity of faba bean and pea, whichaccumulated more Mg2+, Ca2+ in shoots andNa+, K+ in roots as compared to common beanand soybean showing the direct relationshipbetween accumulation of Na+ in shoots andplant salt sensitivity. Mamo et al. (1996) foundchloride concentration (mg/g) in chickpeaplant parts at salt levels (0-8 dSm-1) 2-5 timesthat of Na with significant reduction in K+

concentration. Zayed and Zeid (1997-1998)reported reduced mineral uptake in mungbeanunder salt stress rather than PEG induced waterstress due to maintenance of higher succulenceunder salt stress. Khan et al. (1997-1998)


studied the physiological responses of alfalfa(Medicago sativa L.) to salinity (100 mM NaCl)and some inorganic nutrients (K+,Ca2+, N asNO3-) and reported that inclusion of thesenutrients in plant nutrient medium incombination or alone brought the markedstimulation in control plants and moderatedthe salinity caused reductions in NaCl treatedplants. On the basis of their study on fourchickpea genotypes belonging to the tolerantand susceptible groups (salt stress). Singh andSingh (1999a) reported lower Na and higherK in the shoots of tolerant genotypes ascompared to the susceptible genotypes.Sekeroglu et al. (1999) also found that salinitycaused decreased K content while increasedNa content of chickpea seedlings. Baalbakiet al. ( 2000) while working on ionic relationsin chickpea cultivars found that salinity affectedshoot Na+ and Cl- contents but nodulatingplants had higher shoot to root ratio and higherlevels of Na+ and K+ than plants supplied withmineral nitrogen. Na concentration increasedsignificantly in all plant parts in alfalfa(Medicago sativa L.) as the level of salinitytreatments increased (0-12.2 dSm-1) while P,K, Ca, Mg concentration decreased; the rootsaccumulated significantly more Na than otherplant parts (Esechie et al., 2002).

1.4 Germination: Soil salinity cansignificantly inhibit seed germination andseedling growth, not only in glycophytes, butalso of halophytes, due to combined effects ofhigh osmotic potential and specific ion toxicity.The reduction in germination under salineconditions could be attributed to the increasedosmotic pressure of soil solution which reducesthe water absorption rate, leading to moisturestress in the seeds and reduced mobilization offood reserves. This inhibition of reservesmobilization could be because of the effects ofsalts on the enzyme responsible for hydrolysisand effects on the translocation of reservehydrolysis products from the storage organs

to the embryo axis (Garg and Gupta, 1998).

Mehta and Bharti (1983) observedthat chloride and sulphate salinity (4 to 12 dSm-1)affected seed germination in gram anddecreased the fresh and dry weight of theembryo axis. Sheoran and Garg (1983) foundthat Na

2SO

4 significantly decreased

germination in gram while NaCl, KCl, K2SO

4

only delayed it. Siddiqui and Krishnamoorthy(1986) observed decreased length and freshand dry weights of the embryo axis of cowpeaand chickpea with increasing salinity. Saxenaet al. (1989) found relatively higher degree ofsalt tolerance with a mixture of salts in termsof germination in alfalfa and the relative orderof salt tolerance was; NaCl > CaCl

2> Na

2SO

4>

Na2CO

3> NaHCO

3. Dua (1992) while working

on 20 genotypes of chickpea observed thatsensitivity of all genotypes increased with plantgrowth and higher salinity levels. Further,chlorides were found to be more toxic thansulphates. Mamo et al. (1996), while workingon chickpea and lentil observed differencesamongst different varieties in response to NaCl(0-8 dSm-1) application, with lentil showingrelatively higher percentage emergence ascompared to chickpea. Zurayk et al. (1998)also observed significant reduction in thegermination of 18 cultivars of chickpea,calculated as speed of germination index (SGI)as well as early seedling growth but theresponse varied with the type of cultivars aswell as the salinity levels. Sekeroglu et al.(1999) and Khalid et al. (2001) observeddecreased germination, freshweight, radicleand plumule length and K content with aconcomitant increase in the Na content undersalinity in chickpea. Similar effects werereported by Dash and Panda (2001) in blackgram (Phaseolus vulgaris L.). The relativeeffects of salinity on germination and earlyseedling growth in four legume species namelypigeonpea, chickpea, mungbean and soybeanvaried under saline conditions with chickpea

Vol. 27, No. 1, 2006 5

proving to be most salt susceptible andsoybean most salt tolerant (Garg and Dua,2000). Promila and Kumar (2000) observedreduced seed germination in mung bean undersalinity. With an increase in salinity (NaCl)concentrations, there was correspondingdecrease in imbibitions and germination ofbean cultivars and the variability amongst thesecultivars gave scope for selection of cultivarstolerant to salinity (Moreno et al., 2000).Similar varietal variability’s in salinity toleranceof seven alfalfa varieties and two chickpeacultivars at the germination stage have beenreported by Maiti et al. (2002) and Esechieet al. (2002), respectively. Soltani et al. (2002)studied the interactive effects of seed size andsalinity on germination and seedling growthin chickpea and found that larger seed did nothave any advantage in producing morevigorous seedlings under saline condition.Demir and Kocacalinian (2002) reporteddecreased seedling growth under NaCltreatment and application of proline helpedalleviate salinity stress in bean (Phaseolusvulgaris L.) seedlings. The salt tolerance atgermination and early seedling growth isimportant because the initial stand determinesthe ultimate production to a large extent.

1.5 Growth And Development:Salinity is a major constraint in agriculture andadversely affects germination of seeds, plantgrowth and metabolism (Dua, 1992; Zurayket al., 1998). In legumes, salt stress imposes asignificant limitation on productivity. Not onlythe varying concentration of salts but thedifferent types of salinity have different aspectson plant growth. Manchanda and Sharma(1989) reported that chickpea growth wasreduced by sodium salts at very lowconcentration but sensitivity was high whenthe saline soil has a high concentration ofsulphate and/or low concentration of chloride.Hafeez et al. (1988) found that increasing NaClsalinity decreased the dry matter yield of Vigna

radiata L. irrespective of the stages of plantgrowth. Sharma et al. (1990a, b) investigatedthe effect of chloride and sulphate salinity inchickpea and found chloride salinity to be moredeleterious than sulphate salinity. Wignrajah(1990) found that low salinity stress (48 mMNaCl) resulted in delayed development of leavesas well as plant growth with higher negativeeffects on shoot growth than root growth inPhaseolus vulgaris L. Increased leaf area ratio(LAR) and net assimilate rate (NAR) wereidentified as major physiological traits forsalinity tolerance. Similar negative effects onroot and shoot growth has been reported inchickpea by Elsheikh and Wood (1990) and inmaize and soybean by Shalhevet et al. (1995).Delgado et al. (1994) and Cordovilla et al.(1995) compared the effect of salinity ongrowth and productivity and found pea,fababean to be significantly affected andsoybean and common bean to be moderatelyeffected. Zaidi and Singh (1995) reported thatsalinity inhibited leaf growths as well as netassimilate rate and relative growth rate of thesoybean plants. Dua and Sharma (1995)studied the relative salt tolerance of desi andkabuli genotypes of chickpea and found kabuligenotypes to be more salt tolerant than desi.Mamo et al. (1996) observed significantdifferences among different varieties ofchickpea and lentil in their response to NaClapplication with few varieties showing somedegree of superiority in terms of mean relativeshoot and root dry weights, and grain yieldover the others. Salinity (100 mM NaCl) causedsubstantial reduction in leaf area, relativegrowth rate in alfalfa (Khan et al., 1997-1998).Rogers et al. (1998) found lucerene to bemoderately tolerant to Na

2SO

4 predominated

salinity that to NaCl dominated salinity andthe dry matter production was negativelycorrelated with shoot concentration of specificions like Na+, C- and S2-. Zurayk et al. (1998)reported significant reduction in the dry weightof above ground biomass in chickpea on


treatment with NaCl+, Na2SO

4 salts (0.5

dSm-1, 3dSm-1, 6dSm-1, 9dSm-1). Similarly,Soussi et al. (1998, 1999) reported decline inplant growth of Cicer arietinum L. by 100 mMsalt concentration. Cordovilla et al. (1996,1999) also reported the decline in shoot androot weight on treatment with salt and salinityaffected root growth more than shoots in fababean, thus increasing the root to shootbiomass. Growth inhibition by salt in commonbean plants proved significant in theexperiments carried out by Ferri et al. (2000).The effect of salt was more pronounced inthe second sampling, taken during thereproductive period, which could be explainedby the excessive salt accumulation. Al-Khanjariet al. (2002) observed variation in dry matteryields of alfalfa (Medicago sativa L.) cultivarsto salt tolerance. Salinity significantly reducedboth shoot dry matter and root volume.

1.6 Metabolic alterations: A numberof investigators have studied metabolic changesinduced by salt stress in legumes with a viewto understand the physiological andbiochemical basis of salt tolerance.

1.6 a. Amino acid, Protein andCarbohydrate Metabolism: Salinity is knownfor its depressive effects on metabolic pathwaysand energy generating normal growthprocesses. Mehta and Bharti (1983) found thatboth chloride and sulphate salinity increasedthe soluble carbohydrates in germinating seedsof chickpea but free aminoacids were reduced.A NaCl tolerant callus line of chickpeaaccumulated free proline in response toincreasing NaCl concentrations and its contentsmarkedly suppressed upon substituting KCl forNaCl (Pandey and Ganapathy, 1985).Murmukar and Chavan (1986) reported thatincreasing NaCl salinity decreased the proteinand starch content of the seeds while the sugarand free proline contents increased the podshell in chickpea followed by a reduction inphotosynthetic carbon assimilation. In chickpea

cultivars, both chloride and sulphate salinityreduced carbohydrates, starch and proteincontent of leaves, however, aminoacids andproline increased with increasing conductivity(Sharma et al., 1990a,b). Dhingra and Sharma(1993) on the basis of their analysis on twodistinct types of seeds of mungbean healthyand shriveled found that total soluble sugars(including reducing sugars), proteins, freeamino acids and proline were much lower inshriveled seeds than the healthy ones undersaline conditions. Dhingra et al. (1994)observed that seeds of three promisinggenotypes of chickpea (ICCV 88102, H82-2and C-235) differed in accumulation of solublesugars and starch. With salinity, starch andprotein content decreased in the chickpeaseeds with no effect in the sugar content(Dhingra et al., 1995). Singh and Singh (1995)reported a continuous decline in reducing, non-reducing, total saccharides, total proteincontents with increasing sodicity, though thefree proline content was enhanced in all threegenotypes of pea. Durgaparsad et al. (1996)reported that soybean seedlings germinatedunder different NaCl salinity increasedprotease activity, aminoacids and prolineaccumulation though it decreased the utilizationof reserve protein of the cotyledons. Inchickpea cv. ICCV 88102, lower salinity atsowing increased protein content marginallywhereas higher salinity decreased itsubstantially (Dhingra et al., 1996) Zaidi andSingh (1995) reported proline accumulationin soybean plants under salinity. The chloridesalinity declined starch content in the chickpeacalli (Sangwan et al., 1997). Garg et al. (1998)reported that salinity induced changes in levelsof certain leaf metabolites (starch, reducingsugars, total chlorophyll, soluble protein, freeamino acids and free proline) in clusterbeanand increasing salinity led to significantly highermetabolic derangements which wereparticularly more pronounced at the floweringstage, as compared with other stages of

Vol. 27, No. 1, 2006 7

growth. Salt reportedly boosted proline, aminoacid and carbohydrates in the leaves ofchickpea. (Soussi et al., 1998). Singh andSingh (1999a) found that tolerant genotypesof chickpea had higher proline content inshoots under salinity as compared to thesusceptible genotypes. Paneerselvam et al.(1998) reported that NaCl stress causedaccumulation of proline and aminoacids anddecreased protein and nucleic acid contentin soybean seedlings, but addition oftriadimefon restored the growth and increasedthe protein, amino acid and nucleic acidcontent. Bean (Vicia faba) plants whensubjected to salinity had decreased soluble andhydrolysable sugars, soluble proteins andenhanced total free amino acids (Gadallah,1999). Promila and Kumar (2000) reportedthat amylase activity in the cotyledons of Vignaradiata was progressively reduced withincreasing NaCl concentration but theincreased soluble sugar content in thecotyledons indicated that sugars were notlimiting for mungbean seeding growth undersalinity. Mansour (2000) observedaccumulation of nitrogen containingcompounds like amino acids, amides,proteins, quaternary ammonium compounds(QAC) and polyamines in legume plantsexposed to salinity stress. Dash and Panda(2001) and Rai (2002) reported increasedproline content in legume plants on subjectionto salinity stress. Demir and Kocacalikan(2002) reported that NaCl decreased seedinggrowth in bean seedlings cultured invitro , whileproline added to control seedling did notchange seedling growth but decreasedchlorophyll and increased protein content.Soybean showed higher tolerance towardssaline condition as compared to gram andindex for salt tolerance seemed to be directlyrelated with higher levels of sugars, aminoacids, proteins and nucleic acid (Garg, 2002).

1.6b. Carbon Metabolism and

Carbon Catabolism: The effect of salt stresson carbon metabolism is related to the saltconcentration in the photosynthetic tissues andresponse of enzymes like ribulose 1-5bisphosphate carboxylase oxygenase andphosphoenolpyruate carboxylase. Salinity mayaffect the overall process of photosynthesis atdifferent points, either inhibiting enzymeactivity or by altering it. The effects of salinityon photosynthesis can be both stomatal(Brugnoli and Lauteri, 1991) and non-stomatal(Seeman and Chritchley, 1985). Salinity mayresult in decreased quantum efficiency ofcarbon dioxide uptake (Seeman and Chritchley,1985), change in the ionic relations of thechloroplast (Long and Baker, 1986) or changein photochemical reactions (Reddy et al.,1992).

Seeman and Critichley (1985)reported inhibition of Rubisco activity by thesalt stress in Phaseolus vulgaris, which may bedue to sensitivity of this enzyme to chlorideions. Bekki et al. (1987) reported diminshedrespiratory capacity of the Medicago nodulesunder sodium chloride stress. Plaut (1990) alsoreported decline in both photosynthesis andRubisco activity when salt concentrationexceeded 65 mM in bean. Wignarajah (1990)found that low salinity stress resulted in delayeddevelopment of the leaves and, further,increased leaf area ratio (LAR) and netassimilate rate (NAR) were identified as majorphysiological traits for salinity tolerance.Brugnoli and Lauteri (1990) observed reductionin leaf area development and stomotalconductance under salinity. NaCl reducedphotosynthesis by 170 mol m-3 in the salttolerant cultivar (Kapulink and Hever, 1991).Irigoyen et al. (1992) reported inhibition ofelectron transport and photophosphorylationsunder saline conditions in alfalfa. Malateconcentration reportedly diminished with saltstress, but under these conditions nodulecytosolic phosphoenolpyruvate carboxylase


activity and bacteroid malate dehydrogenaseincreased in the nodules of pea (Delgadoet al., 1993). Khan et al. (1994) studied theinteraction between salinity and nitrogen formsin alfalfa (Medicago sativa) and observed thatphotosynthesis was more significantly reducedin ammonium than in nitrate fed plants.Further, the promotive effect of nitrogen onphotosynthesis in saline as well as in non-salineconditions could be attributed to enhancedsynthesis and availability of carbon assimilatoryenzymes and cofactors required for optimalphotosynthesis. Awada et al. (1995) alsoreported reduced photosynthetic rate by alllevels and types of sodium salts in Phaseolusvulgaris L. Zaidi and Singh (1995) reportedreduction in total chlorophyll, chlorophyll a/bratios, as well as NAR under salinity in soybeanplants. Fernandez-Pascual et al. (1996)observed increased oxygen diffusion resistancewith 100 mol m-3 NaCl in white lupin. Fiveday old Vigna radiata seedlings exposed to200mM NaCl significantly increased the levelof NADH, H+ with marked decrease in the e-

transport activities than control (Sarandhiet al., 1996). Sudhakar et al. (1997) observedsalinity shock caused decline in the activitiesof Ribulose bisphosphate carboxylase andfurther, NaCl was more toxic to the enzymeactivity as compared to Na

2SO

4. Reduced

photosynthesis rate was reported in twochickpea genotypes under increasing salinitylevel (Sharma, 1997). Zayed and Zeid (1997-98) and Garg et al. (1998) observed significantreduction in chlorophyll content in Vignaradiata and Cyamaposis under salt stress,respectively. Singh and Singh (1999b) reportedan increase in carotenoids in tolerantgenotypes of chickpea whereas a decrease wasobserved in the susceptible ones under saltstress when analysed at the seedling stage.Soussi et al. (1998) while working in the Dept.of Biologia Vegetal , Univ. of Granada, Spainreported that photosynthetic carbonassimilation process, leaf chlorophyll content

in chickpea was greatly depressed by the highlevels of salt. Moreover, the activity of leafribulose, 1, 5 biphosphate carboxylase declinedwith an increase in the nodulephosphoenolpyruvate carboxylase and malatedehydrogenase activity under salinity at thefirst harvest, and a decrease at the later stage.Gadalladh (1999) observed reduced chlorophyllcontent in Vicia faba under salinity whichincreased upon application of proline andglycinebetaine. Soussi et al. (1999) reportedthat photosynthesis was more affected by saltin Pedrosillano (sensitive) cultivar of chickpeathan in ILC 1919 (tolerant) andphosphoenolpyruvate carboxylase(PEPC),alcohol dehydrogenase (ADH), malatedehydrogenase (MDH) activity in the nodulescytosol was higher in the tolerant cultivar undersaline conditions which could improveregulation of oxygen diffusion. A significantincrease in net photosynthetic rate (P

N) at

low salinity and reduction at higher salinitieswas observed in alfalfa genotypes (Anandet al., 2000) which was primarily due toreduction of stomatal conductance. Ferri et al.(2000) observed decline in PEPC, MDH, ADH,ICDH (isocitrate dehydrogenase) activities inthe nodule cytosol by the salt treatments, whilein bacteroid cytosol, the enzyme activitiesincreased at high salt concentrations. Moreoverthe respiratory capacity of bacteroids wasdepressed by salt which diminished further withplant age. Al-Khanjari et al. (2002) studied thevariabilities amongst alfalfa cultivars on thebasis of chlorophyll content to salinity andreported that magnitude of decreases inchlorophyll concentration in cultivars was inline with their tolerance to salinity. Reducedchlorophyll content under NaCl was alsoreported in Phaseolus vulgaris by Demir andKocacalikan (2002).

Respiration and nitrogen fixation inlegume root nodules is limited by the rate atwhich oxygen (O

2) from atmosphere enter

Vol. 27, No. 1, 2006 9

nodules. A number of workers have reportedlowered nitrogenase activity of legume rootnodules due to limitation of O

2 supply to

bacteroids (Witty et al., 1984; Minchin et al.,1986; Caroll et al., 1987; Atkins et al., 1988).

Dakora and Atkins (1990), reporteddecrease in nitrogen fixation at PO

2 below 5%

in Vigna unguiculata nodules which may bedue to lower nodulation and nodule mass andat pO

2 above 60%, to a fall in specific nitrogen

fixing activity of nodules. For nitrogenaseactivity, regulation of O

2 supply to infected cells

was necessary and there existed a variablediffusion barrier within the inner cortex (Huntand Layzell, 1993). Iannetta et al. (1995)studied time course of changes involved in theoperation of the O

2 diffusion barrier in Lupinus

albus L. (white lupin) nodules and foundincreased glycoproteins within the cell wallsfollowing exposure to 50% O

2 for 30 min.

Suganuma and LaRue (1995) reporteddecrease in acetylene reduction activity insoybean plants on exposure of roots to 100%O2 and, further, there was accumulation of

succinate, malate, alanine in nodules ontreatment with O

2. Bergersen (1997) observed

from studies on soybean bacteroids thatnitrogenase is converted to less active butrobust form, in the presence of O

2 (in excess

of about 70 nM), protecting from inactivationby excess O

2. He further observed that,

respiration by large numbers of hostmitochondria in the periphery of infectednodule cells, adjacent to gas - filled intercellularspaces, plays an important role in maintaininga steep gradient of O

2 concentration in this

zone. Rao (1999) studied the effect of elevatedCO

2 levels and temperature on Arachis

hypogaea L. and reported stimulated plantgrowth and biomass production under elevatedCO

2 (1660+30ppm) + elevated temperature

(40oC) than ambient CO2 (330+30 ppm) +

control temperature (350C). Lundquist (2000)on the basis of interactive effect of oxygen and

short term nitrogen deprivation in Alnus incanaroot nodules, reported decline in nitrogenaseactivity. Shrivastva et al. (2001) repeatedincreased nodulation, nitrogense activity androot growth under elevated carbon dioxide(600+50ppm) in Phaseolus radiatus.

1.6c. Enzyme Activities: Plantgrowth is the result of many integrated andregulated physiological processes. Salinity, atthe whole plant level, effects changes inphotosynthesis and in carbon, and nitrogenmetabolism and increase and decrease invarious enzyme activities which alter the growthand development of the plant (Alam, 1990;Yang et al., 1990).

Khatri et al. (1985) reported decreasein starch degradation and its utilization in theembryo axis of Cicer arietinum L. under saltstress which was closely correlated withdecrease in soluble sugars and α -amylaseactivity in chickpea genotypes differing in salttolerance. Dhingra (1994) reported highersuccinate dehydrogenase activity which impliedthat major fraction of soluble sugars produceddue to higher hydrolytic activities in responseto salinity was utilized as a substrate forrespiration and this extra metabolic energy waslikely to be consumed in the process of osmoticadjustment and survival under adverseconditions. Filho Eneas et al. (1995) observednegative effect on the activities of α and βglatcosidases under 100 mM NaCl treatmentin cotyledons of Vigna unguiculata. Olmos andHellin (1996) reported higher presence ofenzymes related to sugar metabolism(glucokinase, fructokinase and acid invertase)in pea response to NaCl salinity. Lower activityof polyphenol oxidase (PPO) enzyme in theembryos and food tissue of bean under salinitywas reported by Kabar et al. (1997). Sangwanet al. (1997) observed continuous declensionin alpha-amylase in two genotypes of gramon subjection to salt. Zayed and Zeid (1997-1998) reported decline in the activity of α-


amylase and protease in germinating Vignaradiata seeds during 3-d salt stress and increasein the activity of hydrolytic enzymes during 10day stress. Guerrier et al. (1997-1998) studiesthe relationship between proline contents andactivities of proline biosynthesis [ornithinetransaminase; NAD(P)H-pyroline - 5 -carboxylase reductase], of proline catabolism[NAD(P) proline dehydrogenase] and of NADkinase, and reported that these enzymes wereclearly NaCl-regulated which resulted in prolineaccumulation in soybean calli. Arachishypogaea L. were able to grow at highconcentration of NaCl due to alteration in geneexpression and induction of nine differentesterase isoenzymes in the embryos of seedsgerminated in 105 mM NaCl (Hassanein,1998). Soussi et al. (1999) reported inhibitionsof enzymes of sucrose breakdown by NaCl inchickpea cv. Pedrosillano but in cv. ILC 1919a rise in alkaline invertase was observed, whichcould compensate for the lack of the sucrosesynthase hydrolytic activity. Malatedehydrogenase and alcohol dehydrogenaseactivity was inhibited by salinity in the nodulecytosol of Phaseolus vulgaris L. (Ferri et al.,2000). Promila and Kumar (2000) reportedreduced amylase activity in Vigna radiata seedswith increasing NaCl concentration. Dash andPanda (2001) observed that with the increasein NaCl concentration and duration of stress,catalase (CAT), peroxidase (POX) andpolyphenol oxidase (PPO) activities decreased,while proline increased. Singh et al. (2001)studied variability in the four chickpeagenotypes under salinity and found higheractivities of amylase, protease, peroxidase andcatalase in the tolerant genotypes. Similarvariabilities were reported in lentil (Lensculinaris) genotypes by Singh et al. (2001).Panda (2001) reported increase in the activityof antioxidative enzymes like catalase, guaiacolperoxidase and superoxide dimutase in rootand shoot tissues of Vigna radiata L. undersalinity stress. Malencic et al. (2003) also

studied stress tolerance parameters in thedifferent genotypes of soybean and reportedhigh superoxide dimutase activity and low lipidperoxidation in the tolerant genotypes.

Kaur et al. (2003) reported higheramylase activity, increased activities of sucrosesynthase (SS) and sucrose phosphate synthase(S PS) in the cotyledons and shoots of Kinetintreated salt stressed chickpea seedlings whichcould be responsible for an increase in sucroseturnover in the shoots of stressed seedlings.

2. Effects of salinity on Nitrogen metabolismLegumes have the innate ability to

form symbiotic association with soil bacteriaand rhizobia and to fix atmospheric nitrogen.But symbiotic nitrogen fixation is particularlysensitive to environmental stresses like salinitywhose effects are mediated throughdetrimental effects on nodulation and symbioticnitrogen fixation. Salinity may differentiallyaffect various phase of legume - Rhizobuimsymbiosis namely: Rhizobium survival andinfection of the host, nodule initiation anddevelopment, nodule functioning or nitrogenfixation process as well as growth of the hostlegume and its ability to maintain a constantsupply of photosynthates and nutrients to theroot nodule.

2.1 Nodulation and NitrogenFixation: The adverse effect of salinity onlegume - Rhizobium symbiosis includedecreased nodulation, nodule mass anddecreased nitrogen fixation.

Campbell et al. (1986) observedsubstantial reduction in nitrogen fixation as wellas total nitrogen content in snap bean plantsgrown under saline conditions. Hafeez et al.(1988) also observed that salinity reducednodule formation in Vigna radiata, but whenthe nodules were formed salinity did not affecttheir functioning provided the plantsmaintained reasonable photosynthetic activity.Salinity induced depressive effects on

Vol. 27, No. 1, 2006 11

nodulation, leghemoglobin (Lb) content,nitrogenase and peroxidase activities whichwere metabolically regulated and operatedthrough the intervention of some keyregulatory substances in mungbean (Garget al., 1988). Pessarakli and Zhou (1990)studied variabilities in three cultivars (TenderImproved, Slim green, Dentucky Wonder) ofgreen bean (Phaseolus vulgaris) for nitrogenfixation under salt stress and found that saltstress significantly decreased total N content,per cent of N fixed and amount of total Nfixed by plants in slim green. Sharma et al.(1990 b) reported that both chloride andsulphate salinities reduced nodule dry weight,nitrogenase activity, nitrogen percentage intwo cultivars of chickpea and magnitude ofdeclension enhanced under Cl- salinity as wellas with the rise in the salinity level. Elsheikhand Wood (1990) reported that in chickpeacultivar inoculated with salt tolerantRhizobium strain Ch 191, salinity decreasedtotal nodule number/plant nodule weight andaverage nodule weight. Further Rhizobium wasable to form an infective and effective symbiosisunder saline and non-saline conditionssuggesting more salt sensitivity of host chickpeaas compared to the Rhizobium. Subbaraoet al. (1990), Subbarao and Johansen (1994)observed significant differences among Cajanuscajan L. and different Rhizobium strains in theirability to nodulate and fix nitrogen under salineconditions, and observed that the early stagesof establishment of symbiotic system wassensitive to salinity which became efficient infixing nitrogen after the establishment ofsymbiosis. In alfalfa, on subjection to NaClstress, total organic acid concentration innodules was depressed, while it induced a largeincrease in the amino acids and carbohydratepools (Fougere et al., 1991). It was furtherobserved that within the amino acids; prolineand amongst carbohydrates; pinitolconcentration increased significantly thussuggesting their contribution to salt stress. Qifu

and Murray (1993) observed negative effectsof SO

2 concentrations on nodule number/dry

weights, nitrogenase activity and reduced shootand root nitrogen contents which could beameliorated by NaCl salinity probably due todecreasing SO

2 uptake through stomatal

closure. Reduced nodule weight and N2-ase

activity was reported in snapbeans (Phaseolusvulgaris ) under NaCl salinity (Akhavan -Kharazian et al ., 1991) However, addition ofcalcium to NaCl treatment increased theseparameters and positive effect of calcium onnitrogen fixation was attributed to maintenanceof selective permeability of membranes.Delgado et al. (1993) observed reduced ARAand leghemoglobin (Lb) content in the nodulesof pea along with decreased malateconcentration in bacteroids and cytosol of peaunder NaCl stress with an increase in totalsoluble sugars due to inhibition in the utilizationof the carbohydrates within the nodules. Thisdecrease in leghemoglobin (Lb), respiratorycapacity of bacteroids and malateconcentration in nodules, induced by salt stress,were identified as some of the importantmechanisms involved in inhibitory effect ofsalinity on nitrogen fixation. Delgado et al.(1994) reported depressive effect of salinestress on dry weight and ARA of nodules aswell as the respiratory capacity of bacteroidsin pea, fababean, bean, soybean, which weredirectly related to the salt induced decline indry weight and N content of shoots. Further,faba bean and pea was severely affected bysalinity while soybean was least affectedindicating better adaptation of soybean nodulesto salinity.

Serraj et al. (1994) also reportedreduced ARA and nodule respiration insoybean with NaCl salinity. Velagaleti andSchweitzer (1994) reported diversity insoybean cultivars for salt tolerance, with salttolerant one showing better N fixation andphotosynthetic efficiency, when grown in


nutrient media containing 7.8 dSm-1 NaClsalinity. Ikeda (1994) reported that in Trifoliumrepens early stage of nodulation was moresensitive to NaCl stress than the later stages;probably due to the inhibition of root haircurling. Garg et al. (1995) studied the inter-relationship between the relative sensitivity, ofsoybean and chickpea, to salinity and theendogenous levels of cytokinins. They observedmarked varibations in the two crops withsoybean having higher dry weight, nitrogenaseactivity, nitrogen content. Similar observationshave also been recorded in pigeonpea by Gargand Dua (1996). Nitrogenase activity andleghemoglobin content decreased with salinestress (100 mol m-3 NaCl) in Lupinus albus andfurther, nodular starch content decreased andsucrose content increased suggesting anosmotic regulation (Fernandez-Pascual ,1996).Cordovilla et al. (1996) reported decline insoluble protein content of nodules and increasein proline content within nodule cytosol of Viciafaba under salinity. Further exogenousapplication of KNO

3 to the growth medium

increased plant tolerance to salinity. Serraj andDrevon (1998) studied the interactive effectsof nitrate and NaCl in alfalfa and found highereffect of NaCl on the percent N content andnitrogenase activity of N

2 fixing plants,

compared to NO3- fed plants indicating that

N2 fixation was more sensitive to NaCl than

nitrate nutrition or other functions supportingplant growth. Serraj et al. (1998) observedintraspecific variation amongst commonbean,soybean and alfalfa with common bean to bemore sensitive than soybean and alfalfa undersalinity in terms of nodule growth andnitrogenase activity which could be correlatedto regulation of oxygen diffusion anddistribution of ions in nodules. Zurayk et al.(1998) reported reduction in nodule dry weightand N-fixation in chickpea cultivars undersalinity and found that symbiosis was more saltsensitive than both Rhizobium and the hostplant. NaCl significantly inhibited nitrogenase

activity, nodule number and dry matteraccumulation per plant in all four cultivars ofsoybean On the basis of grafting experimentsAbd-Alla et al. (1998) confirmed a shoot rolein the autoregulatioin of nodule number as wellas in determining salt tolerance of a genotype.Soussi et al. (1998) reported inhibition ofnodulation and nitrogen fixation in Cicerarietinum cv. ILC 1919 even at lowest NaClconcentration (50 mM) while Cordovilla et al.(1999) found that nodulation and nitrogenfixation in Vicia faba was affected only by highconcentrations of salinity (100 mM). FurtherARA activity declined even with low salt stressin both. Soussi et al. (1999) compared the twocvs. of chickpea with differential tolerance tosalinity and found the effect of salt onnodulation and nitrogen fixation morepronounced in Pedrosillano (sensitive) andreported that increase in nodular mass in ILC1919 (tolerant) partially counteracted theinhibition of nitrogenase activity. Ferri et al.(2000) also reported inhibition in dry weightand ARA in the Phaseolus vulgaris. Nandwalet al. (2000) observed sharp decline in theleghemoglobin content and ARA of the nodulesof mungbean under salinity and reportedgenotypic variability, with K-851 more affectedthan the mutant. Babber et al. (2000) reporteddecreased leghemoglobin, reduced ARA ofnodules in chickpea plants under salinity whichcould be directly associated with structuralchanges in nodules under salt stress namelyreduction in size of the nodules, decreasedmeristematic zone, reduced number anddegradation of symbiosomes, reducedintracellular spaces and deposition of electrondense material in the intercellular spaces inthe cortex of the nodules. Rao et al. (2002)studied the effect of salinity on genotypicvariability amongst small seeded desi, mediumseeded desi and kabuli chickpea genotypes andfound kabuli genotype, CSG 8927, to be moresalt tolerant with better nodulation and higherrates of nitrogen fixation than the sensitive

Vol. 27, No. 1, 2006 13

genotypes (desi). Chakrabati and Mukherji(2003) reported that application of NaClinhibited total nitrogen content in Vigna radiataleaves, roots, nodules as well as the nitrogenaseactivity.

2.2 Enzymes of NitrogenAssimilation: Salinity responses of variousenzymes depend on the intensity, duration andtypes of ions, stages of plant growth and assayconditions employed. The enzymes glutaminesynthetase (GS) and glutamate synthase(GOGAT), which forms the major route ofammonia assimilation in plants are markedlyaffected under saline stress (Katiyar, 1990;Chaillou et al., 1992; Singh and Dubey, 1994).

Sharma and Gupta, (1986) observeddeclined nitrate reductase (NR) activity withaccumulation of nitrate under NaCl salinity inpea seedlings. On the contrary, Misra andDwivedi (1990) reported higher NR activity inthe roots of germinating Phaseolus aureusseeds in the presence of NaCl. Lentil (Lensesculanta) plants showed continuous decreasein NR as well as nitrite reductase (NiR) activitiesunder increasing levels of Na+ in the soil (Tewariand Singh, 1991) and the possible reason forthe decreased NR activity under salinizationappeared to be due to inhibition of enzymeinduction under these conditions. In roots of28 day soybean plants, NR activity increaseddue to NaCl in the growth medium (Chaillouet al., 1992) and higher NR activity in plantsunder salinisation showed their betteradaptability to saline conditions due to efficientnitrate reduction (Katiyar and Dubey, 1992).Khan (1996) observed reduced nitratereductase (NR) and nitrite reductase (NiR)activities in leaves and roots of two soybeangenotypes grown under NaCl and Na

2CO

3

salts. Khan et al. (1997-1998) and Garg et al.(1997) observed substantial reduction in thenitrate reductase activity of alfalfa andclusterbean under salinity, respectively.

In pea (Pisum sativum) and soybean

(Glycine max) plants grown under salinizedconditions, decreased GS activity was observedin the roots (Sharma and Gupta, 1986;Chaillou et al., 1992). Billard and Boucaud(1980) reported that salt treatment substantiallyinhibited the glutamate synthase cycleenzymes. Further NADH-GOGAT was moreadversely affected than GS in the Vicia fabacv. Alborea. Cullimore and Bennett (1988),Bouregeais-Chaillou et al. (1992) reportedreduced GS and NADH-GOGAT activitiesunder salt stress in faba bean and soybean,respectively. Misra and Dwivedi (1990)observed increased GOGAT activity inresponse to salt stress in germinating Phaseolusvulgaris L. seeds while Reddy et al. (1993)observed insensitive nature of GS activity tosalinity in horsegram seedlings. According toYamaya and Oaks (1988), increased glutaminesynthetase activity in response to salinity mightbe helping plants in providing more glutaminerequired for biosynthetic reactions. Even,Dubey and Rani (1989) suggested that higherglutamine synthetase in plants growing undersaline conditions might be a useful adaptationfor such plants in saline environments indetoxifying and assimilating more ammonia bythis pathway, leading to increase accumulationof soluble nitrogenous compounds, which actas compatible cytoplasmic solutes under salinestress. Increased glutamate dehydrogenase(GDH) activity in horsegram seedlings whensubjected to NaCl or Na

2SO

4 salinity was

reported by Reddy et al. (1993). Dubey andPessarkali (1995) observed that GDH activityremains maintained as control or getsdecreased in plants under sodium chloridesalinity. According to Shrivastva and Singh(1987), Dubey and Pessarkali (1995), whenGS/GOGAT pathway of ammonia assimilationgets impaired under saline condition, thenglutamate dehydrogenase pathway is thealternative/adaptive one to plants inassimilating more ammonia. Gulati and Jaiwal(1996) reported that when NaCl non-adapted


as well as NaCl adapted callus cultures of Vignaradiata were grown in the presence of NaCl,GOGAT activity decreased while GDHincreased throughout as compared to thecontrols. Cordovilla (1993) and Cordovillaet al. (1994) observed inhibition in GS andNADH-GOGAT activities in the Vicia fabagenotypes under salt stress. Cordovilla et al.(1996) analyzed the effect of salt on faba beanin response to nitrate levels and found thatactivity of enzymes mediating ammoniumassimilation in nodules (GS, NADH-GOGAT,NAD-GDH) decreased by high nitrate levels.Further, NADH-GOGAT activity was moremarkedly inhibited than GS activity by salinity,suggesting that NADH-GOGAT limits theammonium assimilation by nodules under saltstress. Soussi et al. (1998) observed that inCicer arietinium L. plants, GS and GOGATactivities in nodules increased at low saltconcentration (50 mM NaCl) but high saltdosages (100 mM NaCl) strongly inhibited theenzyme activities at all harvests. Cordovillaet al. (1999) reported inhibition in ammoniumassimilating enzyme activities in Vicia fabanodules under salinity and glutamine synthetaseto be tolerant to salinity than glutamatesynthase and hence limiting ammoniumassimilation under saline stress. Chakrabati andMukherji (2003) observed that application ofNaCl (4.0 mScm-1) in Vigna radiata L. resultedin reduced GS, GOGAT and GDH activity.Further, the decline was least significant inGDH while most significant in GOGAT.

3. Ameliorative measures to salt stressThe growing plant requires the

mobilization and translocation of variety ofsubstances to regulate various metabolicprocesses. Plant growth regulators (PGRs), inrecent years, have largely been used toregulate plant growth and development inseveral crop plants (Malik et al., 1985).Legumes are major source of proteins,improves soil fertility through nitrogen fixation

and bioregulators are known to improve theyield and quality contributing characters oflegumes. Upadhyay et al. (1993) observed thatapplication of kinetin improved the chlorophyllcontent of leaves, KNO

3application increased

nitrogen content while naphathlene acetic acid(NAA) improved the sugar content and yieldof chickpea. Foliar applications of NAA to lentilplants increased total plant dry matter,partitioning coefficients, harvest index (Setiaet al., 1993). Further seeds harvested fromNAA treated plants showed increased aminoacid content , decreased total soluble sugarand starch levels, better germinability, morewater imbibitions capacity and decreased seedcoat thickness. Chakrabarti and Mukherji(1994) highlighted the importance ofphytohormones as possible inducers ofresistance to saline stress and reported theefficiency of indole 3- acetic acid, gibberellicacid and Kinetin in restoring the metabolicalterations relating to total chlorophyll content,chlorophyllase activity, photosynthetic non-cyclic electron transport and CO

2 uptake as

imposed by NaCl stress in Vigna radiata.Bhatia et al. (1994) reported thatphotosynthogen {2-(3,4-dichlorophenoxy)triethyl amine}, a PGR stimulated themobilization during groundnut seedgermination, by decreasing the quantity ofdifferent metabolites (soluble sugars, starch,lipids, free amino acids and total protein) inthe cotyledons with a corresponding increasein the axis. Dhingra et al. (1995, 1996)reported that the foliar application of NAA andbenzylaminopurine (BAP) increased thelifespan of leaves along with improvement inseed yield in chickpea under salinity. Chhabraet al. (1995) also observed that applicationof NAA and BAP improved germination andpollen tube growth in chickpea plants exposedto salinity while no effect was seen in plantsraised under non- salinized conditions. Pateland Saxena (1995) reported that applicationof 6 PGRs, viz., gibberellic acid (GA

3), Kinetin

Vol. 27, No. 1, 2006 15

(KIN) napthylene acetic acid (ETH), indoleacetic acid (IBA), abscisic acid (ABA) in Vignaradiata L. seeds improved protein, starch,amino acids contents along with increase inper seed germination and fresh and dryweights. Garg et al. (1995) reported declineendogenous distribution of cytokinins andnitrogen fixation in soybean and chickpea andpostulated that the endogenous status ofcytokinins played a vital role in impartinghigher salt resistance to soybean themchickpea. Increased nodulation, leaf growthand reduced senescence in cowpea werereported on the application of IAA, GA

3 and

KIN (Ragahava et al., 1996). Wasnik andBagga (1996) reported that mepiquat chloride(MC) (1-1- dimethyl piperidinium chloride) aPGR spray on two chickpea varieties increasedthe leaf chlorophyll content branching podnumber/weight seed weight per plant andyield in BG 384 due to higher production ofphotosynthesis in chickpea. Exogenousapplication of KNO

3 to the growth medium

increased plant tolerance to salinity in Viciafaba (Cordovilla et al., 1996).Vardhini and Rao(1997) reported that brassinosteroids(brassinolide, 24- epibrassinolide, 28-homobrassinolide) application was able toreverse the growth inhibitory effects of salinitystress in Arachis hypogaea L. Khan et al.(1997-98) observed that inclusion of K+, Ca2+

and N as NO3- in plant nutrient medium incombination or alone moderated the salinitytreated alfalfa plants. Panneerselvam et al.(1998) reported that triadimefon couldameliorate the effect of NaCl stress in soybean.In salt stressed bean (Vicia faba) plants,application of proline and glycinebetainereduced membrane injury, improved K+ uptakeand growth and increased chlorophyll content(Gadallah et al., 1999). Zurayk et al. (1998)suggested that application of sufficient amounts

of mineral nitrogen could improve the salinitytolerance and hence alleviate the growth andyield of chickpea. Ferri et al. (2000) reportedthat addition of proline or lactate to theincubation medium raised oxygen consumptionin the bacteroids isolated from Phaseolusvulgaris plants treated with salt. Shrivastavaet al. (2001) reported that application of PGRslike triacontanols increased growth yield andnutrient uptake by chickpea plants. Patil et al.(2001) highlighted the importance of soilconditioner, halophiles and PGRs in restoringfertility and productivity of saline soils. Demirand Kocacalikan (2002) reported that additionof proline to NaCl treated Phaseolus vulgarisL. increased growth in comparison with NaCltreated only. Garg (2002) reported higherdecline in sugars (reducing, non-reducing andtotal), total free amino acids, proteins andnucleic acids in chickpea as compared tosoybean and these salinity stressed inducedchanges in key metabolites seemed to bedirectly associated with availability of PGRswhose exogenous application could counteractthe harmful effects of salinity. Thepretreatment with IAA, GA

3, and KIN was

helpful in restoring the metabolic alterationsimposed by NaCl salinity in Vigna radiata(Chakrabati and Mukherji, 2003).

S U M M A R YIt may be concluded that selection for

improved nitrogen fixation should proceed byfirst screening legume germplasm to identifygenotypes with the best available nodulationand nitrogen fixation characteristics under saltstress. It is becoming evident that combinedtools of the plant physiologist, geneticist andbreeder must be brought to bear on theincreasing salinity problems confrontingirrigation agriculture on a world wide scale.


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Documents

THE LEGUME-RHIZOBIA SYMBIOSIS UNDER SALT STRESS - A …a broad range of crops (Lauchli and Epstein, 1990; Serrano and Gaxiola, 1994). ... Progress towards achieving salinity tolerance