AJCS 5(11):1441-1447 (211) ISSN:1835-277 Physiologil responses of soyen (Glyine mx L.) to zin pplition uner slinity stress Weri Weisny 1, Yousef Sohri 1*, Gholmrez Heiri 1, Ael Siosemreh 1, Kzem Ghssemi- Golezni 2 1 Deprtment of Agronomy n Plnt Breeing, Fulty of Agriulture, University of Kuristn, Snnj, Irn 2 Deprtment of Agronomy n Plnt Breeing, Fulty of Agriulture, University of Triz, Irn *Corresponing uthor: y.sohri@uok..ir Astrt A greenhouse reserh ws onute to evlute the meliortive effets of zin pplition on soyen photosyntheti prmeters, lef reltive wter ontent (RWC), reltive eletrolyti lekge (REL), hlorophyll ontents (Chl), n leves n roots lipi peroxition rte uner slinity stress (, 33, 66 n 99 mm NCl). The results revele tht zin pplition on plnts expose to slinity stress use notiele enhnement of photosynthesis (Pn) y 11%, wter use effiieny (WUE) y 54%, mesophyll effiieny (ME) y 98% n quntum yiel (Φ) y 12% ompre with plnts expose to slinity stress lone. The hlorophylls, n totl hlorophyll ontent n reltive wter ontent were signifintly reue with inresing NCl slinity. The highest REL n lipi peroxition were ourre t the highest slinity level. Keywors: Chlorophyll, photosynthesis, slinity stress, soyen, trnspirtion, zin. Arevitions: Ci: internl CO 2 onentrtion, Tr: trnspirtion rte, Pn: net photosyntheti rte, WUE: wter use effiieny, ME: mesophyll effiieny, Φ: quntum yiel, RWC: lef reltive wter ontent, REL: reltive eletrolyti lekge, Chl: hlorophyll. Introution Slinity is one of the mjor environmentl stresses ffeting the performne of mny rop plnts. Slinity hs vrious effets on plnt physiologil proesses suh s inrese respirtion rte n ion toxiity, erese lef net CO 2 ssimiltion rte (Hjloui et l., 26), effiieny of photosynthesis (Ashrf n Shhz, 23; Ko et l., 26; Sye, 23), n memrne isruption (Mrshner, 1986; Gupt et l., 22). Derese photosyntheti rtes my result from the losure of stomt n erese mesophyll onutne, inue y osmoti stress, or from slt-inue mge to the photosyntheti pprtus (Flexs et l., 24). The first step of photosyntheti CO 2 ssimiltion is tlyze y riulose-1,5-isphosphte roxylse/oxygense (RuBPCO) in C 3 plnts, n y phosphoenolpyruvte roxylse (PEPC) in C 4 plnts. Slinity enhnes the oxygense tivity of RuBPCO, while it urtils its roxylse tivity (Sivkumr et l., 2). Slinity often les to erese in hlorophyll ontents n photosyntheti rtes (Lee et l., 24; Ko et l., 26). It n seriously hnge the photosyntheti ron metolism, lefhlorophyll ontent, n photosyntheti effiieny (Seemn n Crithley, 1985; Shrkey et l., 1985). Zin supply oul mitigte the verse effets of NCl (Prker et l., 1992). Insie the hloroplsts proteolyti tivities re epenent on zin, for exmple, the repir proesses of photosystem II through turning over photo-mge protein (Biley et l., 22). The reution in hlorophyll level n the estrution of hloroplst ultr struture le to erese in photosynthesis in Zn-efiient plnts. Zin is onstituent of other enzymes involve in photosynthesis, inluing riulose-1,5- isphosphte roxylse (RuBPC), whih hs een foun to tlyse the initil step of ron ioxie fixtion in photosynthesis (Brown et l., 1993). Zin efiieny is now reognize s one of the most ritil mironutrient efiieny in plnts grown on lreous, sline, n soi soils with high ph vlues. It is well known tht zin is n importnt omponent of mny vitl enzymes, n struturl stilizer for proteins, memrne, n DNA-ining proteins (Arvin n Prs, 24). In ition, zin plys funmentl role in severl ritil ellulr funtions suh s protein metolism n IAA metolism (Mrshner, 1995). Soyen is mjor foo n oil rop in the most ountries where slinity prolems exist or might evelop. Lrge res of formerly rle ln re eing remove from rop proution every yer ue to inresing soil slinity. Therefore, it is neessry to evlute the physiologil responses of rop plnts to slt stress in orer to evelop pproprite strtegies to sustin foo proution uner verse environmentl onitions. Lef photosyntheti pity is suggeste to e key prmeter etermining rop yiel (Jing et l., 22; Zhng et l., 27). Furthermore, zin n notiely enhne photosynthesis prmeters n hlorophyll ontent uner sline onitions. However, the effets of zin pplition on physiologil performne of soyen re poorly unerstoo. Thus, this reserh ws ime to evlute this sujet with onsierle etils. Results n isussion Photosynthesis prmeters Aoring to the results of this stuy, net photosynthesis (Pn), internl CO 2 onentrtion (Ci), wter use effiieny (WUE), mesophyll effiieny (ME), n quntum yiel (Φ) signifintly erese with inresing slinity (Figure 1). Slinity lso signifintly reue trnspirtion rte (Tr), 1441
ompre with ontrol (Figure 1B). But, uring inresing slinity level, the ifferenes etween eh level ompre with the next one were mostly not signifint (Figure 1B). Similr results were reporte y Flexs et l. (24) for C 3 plnts. Slinity uses rnge of eleterious effets suh s inhiition of photosynthesis, pigment synthesis, mge to plsm memrne permeility, n other metoli isturnes (Sski et l., 1998; Krimi et l., 25). Reution in Pn my result from the restrition on CO 2 iffusion into the hloroplst, vi limittions on stomtl opening meite y shoot n root-generte hormones, n on the mesophyll trnsport of CO 2, to ltertions in lef photohemistry n ron metolism (Flexs et l., 24). Inhiition of photosyntheti pity my lso result from reue effiieny of riulose-1,5-isphosphte (RuBP) roxylse, or reution of RuBP regenertion pity, or from the sensitivity of PSII to NCl (Bll n Anerson, 1986). The Zn ition uner slt stress showe n ovious enhnement of Pn, WUE, ME, n Φ through inresing hlorophyll ontent of the soyen plnts. Reution of WUE uner slinity stress without zin pplition ws ue to eline in Pn (Figure 1E). The reution in Tr n Ci n e relte to stomt losure (Lee et l., 24). Reution in ME my e lso relte to eline in Pn (Figure 1A). Zn pplition on the plnts expose to slt stress use notiele enhnement of Pn, WUE, ME, n Φ ompre with the plnts expose to slt stress lone (Figure 1A, D, E n F). Zn, ting s n inhiitor on hypertive polriztion -tivte inwr nion/cl - hnnels, my e enefiil for reuing the Cl - sorption n enhning the - NO 3 uptke to plnts leves expose to slt stress (Ymguhi n Blumwl, 25). In photosynthesis, roni nhyrse (CA) is Zn-ontining enzyme tht tlyzes the reversile onversion of ron ioxie n wter into roni i, n requires Zn for its tlyti tivity. Therefore, roni nhyrse employs two-step mehnism: t in the first step, there is nuleophili ttk of zin-oun hyroxie ion on ron ioxie; t in the seon step, the tive site is regenerte y the ioniztion of the zin-oun wter moleule n the removl of proton from the tive site (Linskog, 1997). Zn enhnement n e very enefiil for plnts in orer to filitte the supply of CO 2 from the stomtl vity to the site of CO 2 fixtion (Sski et l., 1998). Furthermore, zin is onstituent of other enzymes involve in photosynthesis, inluing riulose-1, 5-iphosphte roxylse (RuBPC), whih hs een foun to tlyze the initil step of ron ioxie fixtion in photosynthesis n hs een foun in nvy ens, rley, rie, n perl millet (Brown et l., 1993). Lef hlorophyll ontent Chlorophylls,, n + ontent of leves were signifintly erese s NCl slinity inrese (Tle 2). Similr result ws reporte y Hsneen et l. (29) for Ltu stiv Plnt. This eution ws greter in tretments without Zn pplition. There were no signifint ifferenes mong the tretments in the rtio of Chl /. Slinity erese nitrogen vilility whih oul e one of the resons for erese hlorophyll ontent (Prshr n Verm, 1993). The reution of totl hlorophyll ontent ws proly relte to the enhne tivity of the enzyme hlorophyllse (Rey n Vor, 1986) n inuing the estrution of hloroplst struture n the instility of pigment protein omplex (Singh n Duey, 1995). Plnts trete with NCl n Zn h signifintly greter pigment ontents thn those expose to slt stress lone. Zn proly mintins hlorophyll synthesis through sulphyryl group protetion, funtion primrily ssoite with Zn (Ckmk, 2). Moreover, it prtiiptes in the synthesis of hlorophyll (Li et l., 26). Reltive wter ontent (RWC) RWC signifintly ws erese with inresing slinity. Nevertheless, when plnts were sujete to ifferent slt tretments long with zin, the reltive wter ontent signifintly improve (Tle 3). The reltive wter ontent of non-slinize plnts grown either in presene or in sene of zin remine reltively t high levels (Tle 3). The erese in lef RWC oul e relte to low wter vilility uner stress onitions (Shlhevet, 1993), or to root systems, whih re not le to ompenste for wter lost y trnspirtion through reution of the soring surfe (Gllh, 2). Slt stress inue reution in the reltive wter ontent of the leves, whih inites loss of turgor tht resulte in limite wter vilility for ell extension proess (Kterji et l., 1997). Zin my prtiipte in stomtl regultion ue to its role in mintining memrne integrity. Shrm et l., (1995) oserve erese in the K + ontent of gur ells in non-zin pplition plnts. This my e linke to enhne K + efflux reltive to influx, through leky ell memrnes, s sene zin reues memrne integrity. However, the speifi role of zin in stomt regultion requires further investigtion. Generlly, when stomtl losure is inue y slinity stress, there is ner onstny in lef wter use effiieny s the reution in trnspirtion is slightly greter thn reution in net photosynthesis (Figure 1A). However, no zin pplition use lower Pn n WUE. The t inite tht sene zin n slinity stress, plnts not only use less ville wter, ut lso the wter trnspire is use less effiiently. Reltive eletrolyti lekge (REL) n Lipi peroxition rte The REL of the lef tissue ws signifintly inrese s slinity inrese. The highest REL ws oserve uner 99 mm NCl onitions. REL ws reue with Zn pplition, ompre to no Zn pplition tretments (Tle 3). The oxitive mge ws oserve s MDA ontent, whih is prout of lipi peroxition inrese uring slinity tretment. Peroxition of memrne lipis is n inition of memrne mge n lekge uner slt stress onitions (Ktsuhr et l., 25). MDA is the eomposition prout of polyunsturte ftty is of memrnes uner stress. The rte of lipi peroxition level in terms of MDA n, therefore, e use s n inition to evlute the tolerne of plnts to oxitive stress s well s the sensitivity of plnts to slinity stress (Jin et l., 21). The results presente in Tle 3 lerly show tht in oth lef n root, MDA is influene y slt stress s lef n root MDA ws higher uner sline onitions, ompre to ontrol. Vritions in MDA ontents hve een foun in rie (Tijen n Ìsmil, 25), otton (Diego et l., 23) ultivrs iffering in slt tolerne, n in two lflf ultivrs uner slt stress (Wng et l., 25). Proly it ws onnete with the erese in wter potentil just from the eginning of the severe slt stress, whih might hve limite H 2 O 2 iffusion from the ple of its genertion. Together with higher hyrtion of 1442
Tle 1. Some physil n hemil properties of the soil use in the experiments. Texture ph EC (Sm -1 ) K P Mg Zn Mn Fe Cu (mg kg -1 soil) Sny ly lom 7.82.38 281 17.73 191.3.466 6.654 7.27.726 Tle 2. Totl hlorophyll onentrtion (T Chl ), Chlorophyll (Chl ), Chlorophyll (Chl ) (mg g 1 FM) n Chl /Chl rtio in soyen leves uner ifferent slinity levels with n without Zn pplition. Tretments Chl Chl Chl /Chl rtio T Chl NCl levels (mm) without Zin 1.13 ±.19.52 ±.11 2.19 ±.9 1.6 ±.3 33.36 ±.9.17 ±.4 2.11 ±.22.54±.13 66.28 ±.2.11 ±.1 2.38 ±.4.4 ±.3 99.22 ±.4.9 ±.8 2.31 ±.24.32 ±.4 e NCl levels (mm) long with Zin 1.29 ±.1.59 ±.7 2.18 ±.9 1.89 ±.17 33.85 ±.21.36 ±.4 2.37 ±.3 1.21 ±.3 66.91 ±.6.33 ±.4 2.85 ±.42 1.24 ±.4 99.86 ±.38 42 ±.23 2.31 ±.27 1.29 ±.62 Eh vlue is the men (± SE) of three replites (Dunn s test, P.5). tissues, H 2 O 2 migrtes more esily within ell n rets with some ell ompouns resulting in lipi peroxies formtion (Hlliwell n Gutterige 1999). However, MDA ws signifintly reue uner NCl+Zn tretments, ompre with NCl tretments without zin pplition. In present work, zin pplition ompenste Zn shortge in plnt (t re not shown) n reue the eleterious effets of slinity on Pn, WUE, ME, Φ, Chl, RWC, REL, n MDA in soyen (Figure 1n Tles 2, 3). The prinipl role of zin in preserving the integrity of ell memrnes ly in its ility to protet memrne proteins n lipis from the estrutive effets of superoxie rils n their erivtives proue y reox retions within the ell (Ckmk n Mrshner, 1988). Zn n lso interfere with retive oxitive speies (ROS) proue y the memrneoun NADPH oxise, n thus represents n exellent protetive ntioxint ginst the oxition of severl vitl ell omponents suh s hlorophyll, memrne lipis, n proteins (Ckmk 2). Mterils n methos Plnt mteril n growth onitions The experiments were onute in 29 t the greenhouse of the Fulty of Agriulture, University of Kuristn, Irn. Some physil n hemil properties of the soil re given in Tle 1. The soil smples were ir-rie, rushe to pss through 2-mm sieve, n mixe with sn t 2:1 rtio. Then zin ws omine thoroughly with soil t rte of 1 mgkg - 1 s ZnSO 4.7H 2 O. Eh 4-L plsti pot ws fille with 3.5 kg zin trete soil. The ertifie sees of soyen (v. Willims) were otine from Agriulturl Reserh Center of Kuristn, Irn. These sees were surfe-sterilize with.1% MgCl 2 solution for 5 min n wshe thoroughly five times with istille wter. The experiment ws rrie out using omplete rnomize esign with three replitions. Tretments pplie in four NCl levels (, 33, 66, n 99 mm) with n without zin pplition. The pots were kept uner nturl photoperio n wtere regulrly. Light urtion ws out 13 h. Temperture n reltive ir humiity were 27 ± 3ºС n 6 ± 5% respetively. The slinity tretments were pplie when plnts were 4 weeks ol (three noes on the min stem with fully evelope leves eginning with the unifolite noes) n mintine until finl hrvest. Ten leves on the ove one-hlf to onethir of the stem were hrveste for the evlution of the experimentl prmeters. Net photosynthesis rte Net photosynthesis (Pn) n trnspirtion (Tr) rtes n internl CO 2 onentrtion (Ci) were mesure on fully expne youngest lef of eh plnt using n open system LCA-4 ADC portle infrre gs nlyzer (Anlytil Development Compny, Hoeson, Herts, Engln), Mesurements were performe from 9:3 to 11:3 A.M. with the following speifitions n justments: lef hmer re ws fixe t 6.25 m 2, mient CO 2 onentrtion (C ref ) 295.35 µmol mol -1, temperture in lef hmer in the rnge of 28.67 3.24 C, lef hmer gs flow rte (V) of 4.2 4.26 m 3 s -1, molr flow of ir per unit lef re (Us) of 44.8 mmol m 2 s -1, mient pressure (p) of 99.9 kp n PAR t lef surfe (Q lef ) of 11-1453 µmol m -2 s -1. All the nlyses were rrie out using the mile trifolite of the thir expne trifolite lef from the pex. Wter use effiieny n mesophyll effiieny were lulte using the formul of Ashrf et l., (22). The vlue of quntum yiel (Φ) ws lulte oring to e Plm (1996). Lef hlorophyll ontent For hlorophyll etermintion, the fifth fully expne leves were ethe from the plnts fter the slinity tretment. Prior to extrtion, fresh lef smples were lene with eionize wter to remove ny surfe ontmintion. Fresh lef smples (1 g) were groun in 9% etone using pestle 1443 1442
16 14 A 3.5 3 B Pn (µmol (CO 2 )m -2 s -1 ) 12 1 8 6 4 2 Tr (m mol m -2 s -1 ) 2.5 2 1.5 1.5 Ci (µmol mol -1 ) 42 41 4 39 38 37 36 35 34 33 32 C Wter use effiierny (µmol CO 2 mmol -1 H 2 O 2 ) 6 5 4 3 2 1 D 31 3 Mesophyll effiieny (mol CO 2 m -2 s -1 ).35.3.25.2.15.1.5 E Quntum yiel.1.9.8.7.6.5.4.3.2.1 F Fig 1. Mens of A: photosynthesis rte (Pn), B: trnspirtion rte (Tr), C: internl CO 2 onentrtion (Ci), D: wter use effiieny (WUE), E: mesophyll effiieny (ME) n F: Quntum yiel (Ф) in leves of soyen uner NCl stress (, 33, 66, n 99 mm NCl) with n without Zn pplition. Eh vlue is the men (± SE) of three replites (Dunn s test, P.5). n mortr. The sorne ws mesure using UV/visile Shimzu 16 A spetrophotometer, n hlorophyll ontent were lulte using the eqution propose y Strin n Sve (1966). Reltive wter ontent (RWC) Reltive wter ontent (RWC) of leves ws mesure t stge of po formtion. Twenty helthy lef iss of 1 m imeter were ut from the plnts using lef punh. RWC ws lulte s: (FM - DM)/(TM - DM) 1, where FM is the fresh mss, TM is the mss fter rehyrting smples for 24 h y soking the leves in wter, n DM is the ry mss otine fter oven-rying t 7 C for 36 h. Reltive eletrolyti lekge (REL) Ten lef iss (5 mm 2 ) from the young fully expne leves were ple in 5 ml glss vils, rinse with istille wter to remove eletrolytes relese uring lef is exision. Vils were then fille with 3 ml of istille wter n llowe to stn in the rk for 24 h t room temperture. Eletril onutivity (EC1) of the thing solution ws etermine t the en of the inution perio. Vils were hete in temperture-ontrolle wter th t 95ºC for 2 min n then oole to room temperture n the eletril onutivity (EC2) ws gin mesure. The REL ws lulte s REL = (EC1/EC2) 1 (Shi et l., 26). 1444
Tle 3. Amounts of MDA in leves n roots, RWC, n REL of soyen sujete to ifferent NCl tretments (, 33, 66 n 99 mm) with n without Zn pplition. Tretments Lef MDA (nmol MDA g 1 FM) Root MDA (nmol MDA g 1 FM) RWC (%) REL (%) NCl levels (mm) without Zin 2.58 ± 1.21 2.7 ±.61 7.4 ± 1.56 16. ± 2.92 e 33 9.93 ± 2.42 8.9 ± 2.49 57.3 ± 1.56 32.4 ± 4.26 66 15.3 ±.11 1. ±.42 49.5 ± 5.48 e 58.2 ± 2.4 99 16. ±.89 12.1 ± 4.22 38.9 ± 6.94 e 65.5 ± 4.92 NCl levels (mm) long with Zin 3.72 ± 1.18 1.29 ±.41 76.4 ±.69 12.3 ±.47 f 33 6.3 ± 2.7 4.12 ±.85 69.1 ±.26 24.3 ± 1.15 66 19.1 ± 1.31 3.67 ±.25 68.8 ± 1.2 23.4 ± 2.91 99 11.8 ± 1.18 4.19 ±.836 63.9 ± 2.6 2.2 ± 5.69 e Eh vlue is the men (± SE) of three replites (Dunn s test, P.5). Lipi peroxition rte Oxitive mge to lef lipis, resulting from slt stress, ws estimte y the ontent of totl 2-thiorituri i retive sustnes (TBARS) expresse s equivlents of mlonilehye (MDA). TBARS ontent ws estimte using the metho of Ckmk n Horst (1991) with some moifitions. Fresh lef smples (.2 g) were groun in 5ml of.1% (w/v) trihloroeti i (TCA) t 4ºC. Following the entrifugtion t 12 g for 5 min, n liquot of 1ml from the superntnt ws e to 4 ml of.5% (w/v) thiorituri i (TBA) in 2% (w/v) TCA. Smples were hete t 9 C for 3 min. Therefter, the retion ws stoppe in ie th. Centrifugtion ws performe t 1 g for 5 min, n sorne of the superntnt ws reore t 532 nm on spetrophotometer (Moel Cmspe M33 UV/Vis) n orrete for non-speifi turiity y sutrting the sorne t 6 nm. The following formul ws pplie to lulte MDA ontent using its sorption oeffiient (ε) n expresse s nmol MDA g 1 fresh mss: MDA (nmol g -1 FM) = [(A532-A6) V 1/ε] W Where, ε is the speifi extintion oeffiient (=155mMm 1 ), V is the volume of rushing meium, W is the fresh weight of lef, A6 n A532 re the sorne t 6 nm n 532 nm wvelength respetively. Sttistil nlysis Anlysis of vrine ws performe using the SAS softwre (Ver. 9.1). The t were presente s the mens for eh tretment (n = 8). Mens were ompre using the Dunn test t the 5% proility level. Conlusion In summry, these results emonstrte ifferent roles of Zn in eresing the effets of slt -stress on soyen. Zn my not t s its own iret nutritionl funtion on soyen uner slinity stress, ut iniretly t s svenger of ROS for mitigting the injury on io-memrnes (inluing plsm memrne, hloroplst memrne, thylkoi memrne, n so on) (Ckmk 2). Referenes Arvin P, Prs MNV (24) Zin protets hloroplsts n ssoite photohemil funtions in mium expose Certophyllum emersum L., fresh wter mrophyte. Plnt Si 166: 1321 1327 Ashrf M, Krim F, Rsul E (22) Intertive effets of giereli i (GA 3 ) n slt stress on growth, ion umultion n photosyntheti pity of two spring whet (Tritium estivum L.) ultivrs iffering in slt tolerne. Plnt Growth Regul 36: 49 59 Ashrf M, Shhz M (23) Assessment of genotypi vrition in slt tolerne of erly CIMMYT hexploi whet germplsm using photosyntheti pity n wter reltions s seletion riteri. Photosyntheti 41: 273 28 Biley S, Thompson E, Nixon PJ, Horton P, Mullineux CW, Roinson C, Mnn NH (22) A ritil role for the Vr2 FtsH homologue of Ariopsis thlin in the photosystem II repir yle in vivo. J Biol Chem 277: 26 211 Bll MC, Anerson JM (1986) Sensitivity of photosystem II to NCl in reltion to slinity tolerne. Comprtive stuies with thylkois of the slt-tolernt mngrove, Avienni mrin, n the slt-sensitive pe, Pisum stivum. Aust J Plnt Physiol 13: 689 698 Brown PH, Ckmk I, Zhng Q (1993) Form n funtion of zin in plnts. In: Roson AD (e) Zin in Soils n Plnts, Kluwer Aemi Pulishers, Dorreht, Boston, Lonon, pp 9 16 Ckmk I (2) Possile roles of zin in proteting plnt ells from mge y retive oxygen speies. New Phytol 146: 185 25 Ckmk I, Horst J (1991) Effet of luminium on lipi peroxition, superoxie ismutse, tlse, n peroxise tivities in root tips of soyen (Glyine mx). Physiol Plnt 83: 463 468 Ckmk I, Mrshner H (1998) Enhne superoxie ril proution in roots of zin efiient plnts. J Exp Bot 39: 1449 146 e Plm L (1996) Photosyntheti hrteristis of six Pisthio ultivrs. Pper presente t the 1 th GREMPA Seminr, Meknes (Moroo), Instituto Agronómio Meiterráneo e Zrgoz, Spin, pp 45 49, 14-17 Ot 1996 1445
Diego AM, Mro AO, Crlos AM, José C (23) Photosynthesis n tivity of superoxie ismutse peroxise n glutthione reutse in otton uner slt stress. Environ Exp Bot 49: 69 76 Flexs J, Bot F, Loreto F, Corni G, Shrkey TD (24) Diffusive n metoli limittions to photosynthesis uner rought n slinity in C 3 plnts. Plnt Biol 6: 269 279 Gllh MAA (2) Effets of inole-3-eti i n zin on the growth, osmoti potentil n solule ron n nitrogen omponents of soyen plnts growing uner wter efiit. J Ari Environ 44: 451 467 Gupt NK, Meen SK, Gupt S, Khnelwl SK (22) Gs exhnge, memrne permeility, n ion uptke in two speies of Inin jujue iffering in slt tolerne. Photosyntheti 4: 535 539 Hjloui H, Denen M, Bouslm M (26) Effet u hlorure e soium sur les ritères morpho-physiologiques et proutifs u pois hihe (Cier rietinum L.). Institut Ntionl e Reherhes en Génie Rurl, Eux et Forêts 8: 171 187 Hlliwell B, Gutterige JMC (1999) Oxitive stress n ntioxint protetion: some speil ses. In: Hlliwell B, Gutterige JMC (e) Free rils in iology n meiine, 3r en. Oxfor, Clrenon Press, pp 53 533 Hsneen MNA, Younis ME, Tourky SMN (29) Plnt growth, metolism n pttion in reltion to stress onitions XXIII. Slinity-iofertility intertive effets on growth, rohyrtes n photosyntheti effiieny of Ltu stiv. Plnt Omis 2: 6 69 Jin M, Mthur G, Koul S, Srin NB (21) Ameliortive effets of proline on slt stress-inue lipi peroxition in ell lines of grounnut (Arhis hypoge L.). Plnt Cell Rep 2: 463 468 Jing H, Wng XH, Deng QY, Yun LP, Xu DQ (22) Comprison of some photosyntheti hrters etween two hyri rie omintions iffering in yiel potentil. Photosyntheti 4: 133 137 Ko WY, Tsi TT, Tsi HC, Shih CN (26) Response of three Glyine speies to slt stress. Environ Exp Bot 56: 12 125 Krimi G, Ghornli M, Heiri H, Khvri Nej RA, Assreh MH (25) The effets of NCl on growth, wter reltions, osmolytes n ion ontent in Kohi prostrt. Physiol Plnt 49: 31 34 Kterji N, Vnhoorn JW, Hmy A, Mstrorilli M, Mou Krzel E (1997) Osmoti justment of sugr eets in response to soil slinity n its influene on stomtl onutne, growth n yiel. Agri Wter Mnge 34: 57 69 Ktsuhr M, Otsuk T, Ezki B (25) Slt stress-inue lipi peroxition is reue y glutthione S-trnsferse, ut this reution of lipi peroxies is not enough for reovery of root growth in Ariopsis. Plnt Si 169: 369 373 Lee G, Crrow RN, Dunn RR (24) Photosyntheti responses to slinity stress of hlophyti seshore psplum eotypes. Plnt Si 166: 1417 1425 Li WYF, Wong FL, Tsi SN, Tsi SN, Phng TH, Sho GH, Lm HM (26) Tonoplst-lote GmCLC1 n GmNHX1 from soyen enhne NCl tolerne in trnsgeni right yellow (y)-2 Cells. Plnt Cell Environ 29: 1122 1137 Linskog S (1997) Struture n mehnism of roni nhyrse. Phrmol Ther 74: 1 2 Mrshner H (1986) Minerl nutrition in higher plnts. Aemi Press, Lonon, Orlno, Sn Diego, USA, pp 477 542 Mrshner H (1995) Minerl nutrition of higher plnts, 2r en. Aemi Press, Lonon, p 889 Prshr A, Verm SK (1993) Effet of gierelli i on hemil omposition of whet grown uner ifferent slinity levels. Pper presente t the interntionl onferene on the Plnt Physiology, Nrenr Dev University of Agriulture n Tehnology (NDUAT) Kumrgnj, Fiz, Ini, 22 25 Prker DR, Aguiler JJ, Thomson DN (1992) Zinphosporus intertion in two ultivrs of tomto (Lyipersion esulentum L.) grown in helto-uffere nutrient solution. Plnt Soil 193: 163 177 Rey MP, Vor AB (1986) Chnges in pigment omposition, hill retion tivity n shries metolism in Bjr leves uner NCl slinity. Photosyntheti 2: 331 334 Sski H, Hirose T, Wtne Y, Ohsugi R (1998) Croni nhyrse tivity n CO 2 -trnsfer resistne in Znefiient rie leves. Plnt Physiol 118: 929 934 Sye OH (23) Chlorophyll fluoresene s tool in erel rop reserh. Photosyntheti 41: 321 33 Seemn JR, Crithley C (1985) Effets of slt stress on the growth, ion ontent, stomtl ehviour n photosyntheti pity of slt-sensitive speies, Phseolus vulgris (L). Plnt 164: 151 62 Shlhevet J (1993) Plnts uner slt n wter stress. In: Fowen L, Mnsfiel T, Stort J (e) Plnt Apttion to Environmentl Stress, Chpmn n Hll, Lonon, Glsgow, New York, Tokyo, Melourne, Mrs, pp 133 154 Shrkey TD, Seemn JR, Berry JA (1985) Photosynthesis in intt leves of C 3 plnts: physis, physiology n rte limittions. Botni Review 51: 53 15 Shrm PN, Tripthi A, Bisht SS (1995) Zin requirement for stomtl opening in uliflower. Plnt Physiol 17: 751 756 Shi Q, Bo Z, Zhu Z, Ying Q, Qin Q (26) Effets of ifferent tretments of sliyli i on het tolerne, hlorophyll fluoresene, n ntioxint enzyme tivity in seelings of Cuumis stiv L. Plnt Growth Regul 48: 127 135 Singh AK, Duey RS (1995) Chnges in hlorophyll n ontents n tivities of photosystems 1 n 2 in rie seelings inue y NCl. Photosytheti 31: 489 499 Sivkumr P, Shrmil P, Prh Srhi P (2) Proline llevites slt-stress-inue enhnement in riulose-1,5 iphosphte oxygense tivity. Biohem iophys Res Commun 279: 512 515 Strin HH, Sve WA (1966) Extrtion, seprtion, estimtion n isoltion of hlorophylls. In: Vernon LP, Seely GR (e) The Chlorophylls, Aemi Press, New York, pp 21 66 Tijen D, Ìsmil T (25) Comprtive lipi peroxition, ntioxint efense systems n prline ontent in roots of two rie ultivrs iffering in slt tolerne. Environ Exp Bot 53: 247 257 Wng YJ, Wisniewski M, Melin R, Cui MG, We R, Fuhigmi L (25) Overexpression of ytosoli sorte peroxise in tomto onfers tolerne to hilling n slt stress. J Am So Horti Si 13: 167 173 1446
Ymguhi T, Blumwl E (25) Developing slt-tolernt rop plnts: hllenges n opportunities. Trens Plnt Si 1: 615 62 Zhng C, Chu H, Chen G, Shi D, Zuo M, Wng J, Lu C, Wng P, Chen L (27) Photosyntheti n iohemil tivities in flg leves of newly evelope superhighyiel hyri rie (Oryz stiv) n its prents uring the reproutive stge. J Plnt Res 12: 29 217 1447 1446