Physiological responses of NaCl stressed cowpea plants grown in nutrient solution supplemented with CaCl 2
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1 AND NCl STRESS IN COWPEA PLANTS R E S E A R C H A R T I C L E 99 Physiologicl responses of NCl stressed cowpe plnts grown in nutrient solution supplemented with CCl 2 José Vieir Silv 1, Cludivn Feitos de Lcerd 1,2, Pulo Henrique Alves d Cost 1, Joquim Enés Filho 1, Enés Gomes Filho 1 nd José Trquínio Prisco 1, * 1 Lbortório de Fisiologi Vegetl, Deprtmento de Bioquímic e Biologi Moleculr, CC/UFC, CP 6039, , Fortlez, CE, Brsil; 2 C F L present ddress: Deprtmento de Engenhri Agrícol CCA/UFC; * Corresponding uthor: prisco@ultrnetcombr Received: 05/02/2003, Accepted: 01/04/2003 Pitiub cowpe (Vign unguicult (L) Wlp) plnts were grown in nutrient solution nd kept in greenhouse up to preflowering stge They were subjected to four different tretments: nutrient solution; nutrient solution contining 75 mmoll -1 NCl; nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 CCl 2 ; nd nutrient solution contining 75 mmoll -1 NCl nd 10 mmoll -1 CCl 2 Slt stress strongly inhibited plnt growth, cused disturbnce in plnt-wter blnce, nd incresed the totl content of inorgnic solutes in the different plnt prts, due minly to ccumultion of N + nd Cl - It lso incresed lef nd root soluble crbohydrtes, reduced soluble mino nitrogen both in root tips nd in the youngest trifolite leves, nd reduced proline levels in root tips Although the ddition of CCl 2 to the root environment of slt stressed plnts cused reduction in N + content, specilly in roots, it did not meliorte the slt stress effects on plnt-wter reltions nd growth Therefore, the results obtined do not support the hypothesis tht supplementl clcium would meliorte the inhibitory effects of NCl-stress Key words: clcium, growth, slt stress, solutes ccumultion, Vign unguicult, wter reltions Resposts fisiológics de plnts de feijão-de-cord estressds com NCl e cultivds em solução nutritiv suplementd com CCl 2 : Plnts de feijão-de-cord (Vign unguicult (L) Wlp) Pitiúb form cultivds em solução nutritiv e conservds em cs de vegetção té o estádio de pré-florção, e form submetids qutro trtmentos, sber: solução nutritiv; solução nutritiv contendo NCl 75 mmoll -1 ; solução nutritiv contendo NCl 75 mmoll -1 e CCl 2 5 e 10 mmoll -1 O estresse slino inibiu fortemente o crescimento, provocou distúrbios no blnço hídrico ds plnts e elevou o teor totl de solutos inorgânicos ns diferentes prtes ds plnts, em vist, principlmente, do cúmulo de N + e Cl - Além disso, umentou o teor de crboidrtos solúveis ns folhs e rízes, reduziu o teor de nitrogênio mino-solúvel, tnto ns extremiddes ds rízes como ns folhs trifoliolds mis jovens, e diminuiu os níveis de prolin ns extremiddes ds rízes Embor dição de CCl 2 o mbiente rdiculr de plnts estressds tenh provocdo redução no teor de N +, especilmente ns rízes, não minorou os efeitos do estresse ns relções hídrics e no crescimento ds plnts Os resultdos obtidos, portnto, não dão suporte à hipótese de que o cálcio suplementr minorri os efeitos inibitórios do estresse induzido por NCl Plvrs-chve: cálcio, crescimento, estresse slino, cúmulo de solutos, Vign unguicult (L) Wlp, relções hídrics INTRODUCTION The ddition of supplementl C 2+ to the root environment hs been suggested s men of enhncing plnt tolernce to slt stress (Rengel, 1992; Epstein, 1998) Under slt stress conditions there is decrese in the clcium/sodium rtio in the root environment which ffects membrne properties, due to displcement of membrne-ssocited C 2+ by N +, leding to disruption of membrne integrity nd selectivity (Crmer et l, 1985; Kinride, 1998) This fvors the increse of N + inside the cells tht could: chnge enzyme ctivity resulting in cell metbolicl ltertions; disturbnce in K + uptke nd prtitioning in the cells nd throughout the plnt, tht my even ffect stomtl opening (Epstein, 1998) Therefore, impiring the bility of the plnt to growth The
2 100 JV SILVA et l ddition of C 2+ to the root environment of slt stressed plnts mintins or enhnces the selective bsorption of potssium t high sodium concentrtions, tht will prevent the deleterious effects of the excess of N + (Epstein, 1998) Another role ttributed to supplementl C 2+ ddition is its help in osmotic djustment nd growth vi the enhncement of comptible orgnic solutes ccumultion (Colmer et l, 1996; Girij et l, 2002) The mechnism of ction of C 2+ -enhnced tolernce of NCl-stressed plnts hs been studied both t cell-tissueorgn nd t moleculr level, using in vitro cell cultures nd Arbidopsis thlin mutnts (Liu nd Zhu, 1997) However, there is not consensus bout the effectiveness of the use of supplementl C 2+ for the enhncement of plnt slt tolernce specilly when pplied s CCl 2 While some uthors hve obtined results tht fvor its protective role on growth of slt stressed plnts (Rengel, 1992; Song nd Fujiym, 1996), others hve observed conflicting results (Lcerd et l, 1995; Kinride, 1999; Reid nd Smith, 2000) Therefore, in this pper the effects of supplementl CCl 2 on growth, inorgnic nd orgnic solutes composition nd plntwter reltions were studied in NCl-stressed cowpe plnts iming to clrify this discrepncy MATERIAL AND METHODS Seed germintion nd growth conditions: Pitiub cowpe (Vign unguicult (L) Wlp) seeds were germinted on pper towels under lbortory conditions s described previously (Prisco nd Vieir, 1976) Five dys fter plnting seedlings were selected nd trnsferred to plstic trys contining diluted (1/4 strength) nd erted Hoglnd nutrient solution, nd plced in greenhouse The seedlings were grown under these conditions for 5 dys nd then were trnsferred to 55 L plstic pots contining erted hlf strength Hoglnd nutrient solution Slt dditions into the nutrient solution (25 mmoll -1 NCl nd/or 5 mmoll -1 CCl 2 per ddition) were mde every other dy strting 24 h fter the plnts were trnsferred to the plstic pots After these dditions it were estblished 4 tretments: nutrient solution (C); nutrient solution contining 75 mmoll -1 NCl (S); nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 CCl 2 (SC1); nd nutrient solution contining 75 mmoll -1 NCl nd 10 mmoll -1 CCl 2 (SC2) At the lst slt ddition the strength of nutrient solution chnged from hlf to full Nutrient solution level ws mintined constnt throughout the experimentl period by dding distilled wter, nd its ph ws kept t 55 by dding 01 moll -1 KOH or HCl Chnges in nutrient solution were mde every 5 dys, nd ech time the mount of slt dded ws restored to ech pot in the slt stressed tretments During the experimentl period photosyntheticlly ctive rdition vried from minimum of 120 t sunset to mximl of 1,600 µmolm -2 s -1 t middy, nd men ir temperture nd reltive humidity inside the greenhouse were 311 C nd 668 %, respectively Growth mesurements: At the twenty-first dy from the strt of slt dditions four plnts from ech tretment were hrvested Ech plnt ws divided into lef bldes, stem nd petioles, nd roots After determining lef re using Li- Cor re meter LI-3000 (Li-Cor, Inc, Lincoln, Nebrsk, USA) nd the fresh mss of the different prts they were dried in forced ir circultion oven t 60 o C for 72 h Mesurement of plnt-wter reltions: The fifth trifolite strting from the youngest lef ws used for wter potentil (Ψ w ) determintion The mesurements were mde in 4 different plnts from ech tretment t predwn of the lst dy of the experimentl period using pressure chmber (Soilmoisture Equipment Corp, Snt Brbr, CA, USA) Stomtl conductnce (g s ) nd trnspirtion rte (E) were determined long different dys of the experimentl period using LI-1600 Stedy Stte Porometer (Li-Cor, Inc, Lincoln, Nebrsk, USA) The mesurements were mde on the centrl leflet of the third trifolite strting from the youngest lef of four different plnts from ech tretment Totl wter trnspired by the plnts during the experimentl period ws determined for four different plnts from ech tretment by clculting the mount of distilled wter used to mintin the nutrient solution level in ech pot Trnspirtion rtio (mss of wter consumed for the production of 1 grm of plnt dry mss) nd lef succulence (lef fresh mss/lef re) were lso determined Determintions of inorgnic nd orgnic solutes: Smples of 500 mg of oven-dried nd ground mteril were shed t 550 o C for 4 h, nd weighed for determintion the % of sh in the oven-dried mteril The shed mteril ws dissolved in 2 ml of 6 moll -1 HCl, filtered into volumetric flsk, nd the volume completed to 50 ml of deminerlized wter This extrct ws used for N, K, C, Mg nd P determintions (Mlvolt et l, 1989) Chloride ws determined by titrtion fter smples of 50 mg of oven-dried nd ground mteril were extrcted in 25 ml of deminerlized wter for 30 min
3 AND NCl STRESS IN COWPEA PLANTS 101 (Mlvolt et l, 1989) Root tips (1 cm) nd the youngest trifolite leves, fter being frozen, were lyophilized, ground nd smples of this mteril were used for orgnic solutes extrction nd determintions Smples of 2 mg of the freezedried mteril were suspended in 10 ml of distilled wter, centrifuged t 3,000 g for 5 min, nd the superntnt used for soluble crbohydrtes determintion (Dubois et l, 1956) Proline ws extrcted nd determined ccording to Btes et l (1973) Soluble mino nitrogen ws extrcted ccording to Ainouz (1970) nd determined ccording to Cocking nd Yemm (1954) Experimentl design nd sttisticl nlysis: The experimentl design ws completely rndomized with four replictes per tretment The dt were subjected to nlysis of vrince, nd the mens were compred by Tukey s test (p < 005) RESULTS Plnt growth: Plnt growth mesured both on dry mss nd on lef re (tble 1) bsis ws strongly inhibited by slt stress Totl plnt biomss production suffered men reduction of 604%, being the reduction of shoot growth (618 %) greter thn tht of root growth (476 %) As result of this there ws decrese in shoot/root rtio of bout 38 % (dt not shown), typicl of slt nd wter stressed plnts The ddition of CCl 2 (SC1 nd SC2) to the nutrient solution contining 75 mmoll -1 NCl did not overcome the inhibitory effect of slt stress (S) Lef growth ws lso strongly inhibited (662 %) by slt stress, nd the ddition of CCl 2 to the nutrient solution contining 75 mmoll -1 NCl did not overcome this effect On the contrry, the ddition of 10 mmoll -1 CCl 2 enhnced lef re inhibition from 662 to 778 % Plnt-wter reltions: The dt on plnt-wter reltions re shown in tble 2 nd figure 1 Slt stress cused reduction of bout 37 % in lef wter potentil (Ψ w ), nd this reduction ws not reversed by the ddition of 5 or 10 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl Slt stress reduced totl wter trnspired during the experimentl period by bout 68 % This reduction ws not ltered when plnts were grown in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 CCl 2 (SC1) However, the ddition of 10 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl (SC2) cused greter decrese in wter trnspired Trnspirtion rtio ws lso reduced (bout 13 %) by slt stress, nd the ddition of 5 or 10 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl did not reverse this reduction When lef succulence ws nlyzed it ws observed tht it incresed in bout 30 % in the slt stressed plnts (S), nd the ddition of 5 or 10 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl did not overcome this effect The dily vritions of stomtl conductnce (g s ) nd trnspirtion rte (E) hve demonstrted tht the curves for control plnts (C), slt stress (S), slt stressed contining 5 (SC1) or 10 mmoll -1 CCl 2 (SC2) showed the sme generl tendency (figure 1), tht is, lower vlues in the morning tending to increse towrd middy nd decresing towrd the end of the fternoon However, the rte vlues obtined t ech hour of the dy hve shown tht slt stress decresed both g s nd E, nd tht this decrese is greter in the tretments SC1 nd SC2 None of the tretments showed middy drop in trnspirtion, nd the mximl trnspirtion rte occurred between 11:00 nd 13:00 h for ll tretments Inorgnic nd orgnic solutes: Although slt stress cused n increse in totl inorgnic solutes (Ash) in the different plnt prts, this ws not observed for ll ions nlyzed (tble 3) Slt stress induced n increse in sh content in roots, stem + petioles, nd leves resulting minly from N + nd Tble 1 Dry mss (DM) production nd lef re of cowpe plnts grown in nutrient solution (C), in nutrient solution contining 75 mmoll -1 NCl (S), nd in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 (SC1) or 10 mmoll -1 (SC2) CCl 2 Tretments Dry Mss (g) Root Shoot Totl Lef re (cm 2 ) C ,532 S 206 b (476) 1412 b (618) 1618 b (604) 2,880 b (662) SC1 151 c (615) 1328 b (641) 1479 b (638) 2,698 b (684) SC2 097 d (753) 782 c (788) 879 c (785) 1,893 c (778) Vlues followed by the sme letter within the sme column re not sttisticlly different t p < 005 (Tukey test); vlues between prenthesis represent the percentge of reduction in reltion to control tretment
4 102 JV SILVA et l Cl - ccumultion It induced increses in root N + (930 %) nd Cl - (196 %), nd decreses in ll other ions studied There were increses in N + (880 %), Cl - (576 %) nd phosphorus (25 %) in stem + petiole, decrese in K + (19 %), nd the contents of C 2+ nd Mg 2+ were not ffected Slt stress (S) lso cused increses in lef N + (233 %), Cl - (117%), phosphorus (555 %) nd K + (193 %), nd t the sme time induced decreses in C 2+ (238 %) nd Mg 2+ (15 %) The ddition of 5 or 10 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl cused enhncement in totl inorgnic solutes (Ash) in ll plnt prts This could be due bsiclly to the ccumultion of Cl - in ll plnt prts nd of C 2+ in the shoot (stem + petiole + leves) The dditions of CCl 2 to the nutrient solution of slt stressed plnts induced decrese in N + content, specilly in roots However, this decrese ws not sufficient to rech the N + content of the control tretment (C) in ny of the plnt prts It ws lso observed tht the CCl 2 dditions (SC1 nd SC2) were not sufficient to lter the K + decrese in roots nd stem + petiole induced by slt stress, lthough in the leves SC2 brought K + content to the control tretment (C) level As expected, the CCl 2 dditions prtilly overcme the slt stressed induced decreses in C 2+ nd Mg 2+, specilly in the roots, but did not hve ny effect on slt induced chnges in phosphorus contents Slt stress cused significnt increse in soluble crbohydrtes both in roots (371 %) nd in leves (574 %), decreses in soluble mino nitrogen in roots (428 %) nd in leves (178 %), nd lso in root-proline (217 %), but lefproline content ws not ffected (tble 4) Although the dditions of CCl 2 to the nutrient solution of slt stressed plnts brought the root-crbohydrtes content to the control tretment (C) level, the sme did not hppen with lefcrbohydrtes, ie they cused decreses in crbohydrtes content, which did not rech the control tretment level CCl 2 dditions did not reverse the slt stressed induced decrese in both root nd lef soluble mino-n nor in root-proline content Finlly, clcium dditions contributed to n increse in lef-proline content g s (mmolm- 2 s- 1 ) E s (mmolm- 2 s- 1 ) Hours of the dy Figure 1 Stomtl conductnce (g s ) nd trnspirtion (E) of cowpe plnts grown in nutrient solution (C), in nutrient solution contining 75 mmoll -1 NCl (S), nd in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 (SC1) or 10 mmoll -1 (SC2) CCl 2, t 9 ( ), 15 ( ) nd 21 ( ) dys fter strting NCl dditions Tble 2 Wter potentil (Ψ w ), totl wter trnspired (WT), trnspirtion rtio (TR) nd lef succulence (LFM/LA) of cowpe plnts grown in nutrient solution (C), in nutrient solution contining 75 mmoll -1 NCl (S), nd in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 (SC1) or 10 mmoll -1 (SC2) CCl 2 Tretments Ψ w (MP) WT (L) TR (g H 2 Og -1 DM) LFM/LA (mgcm -2 ) C b S b 476 b b 2545 Sc1-028 b 439 b b 2521 Sc2-029 b 285 c b 2559 LFM = lef fresh mss; LA = lef re; vlues followed by the sme letter within the sme column re not sttisticlly different t p < 005 (Tukey test)
5 AND NCl STRESS IN COWPEA PLANTS 103 Tble 3 Inorgnic solutes contents of cowpe plnts grown in nutrient solution (C), in nutrient solution contining 75 mmoll -1 NCl (S), nd in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 (SC1) or 10 mmoll -1 (SC2) CCl 2 Tretment Solutes (molkg -1 DM) N C Cl K P Mg Ash (%) Roots C 0100 c c c S c 1109 b 1110 b 0119 b 0038 c 1540 b SC b 0148 b 1017 b 1207 b 0116 b 0046 b 1741 b SC b 0155 b b 0113 b 0050 b 1863 Stem + Petioles C 0087 c 0293 b 0143 c c d S b 0966 b 1115 b 0048 b c SC b b 1146 b 0052 b b SC b b Leves C 0052 c 0653 c 0394 c 1061 c 0058 b c S d 0857 b b 1482 b SC b 0948 b 1189 b c 1578 b SC bc c 1744 Vlues followed by the sme letter within the sme column nd for ech plnt prt re not sttisticlly different t p < 005 (Tukey test) DISCUSSION Slt stress reduced plnt growth, but contrry to wht ws observed by others (Epstein, 1998; Ky et l, 2002), the ddition of 5 mmoll -1 CCl 2 to the nutrient solution contining 75 mmoll -1 NCl did not meliorte the slt stressed induced growth inhibition, nd 10 mmoll -1 CCl 2 even incresed growth inhibition (tble 1) These discrepncies could be due to severl fctors, such s: use of different concentrtions nd sources of clcium slts, different NCl concentrtions (Reid nd Smith, 2000; Munns, 2002), nd environmentl conditions under which the plnts were grown (Yeo, 1999) The ltter seems to be relevnt becuse this sme cowpe cultivr hs responded differently to supplementl clcium, depending upon the evportive demnd of the environment under which they were grown (Lcerd et l, 1995) Another interesting spect of the response of slt-stressed plnts to supplementl clcium is the durtion of the tretment For instnce, slt-stressed plnts grown under high evportive demnd of the ir nd supplemented with clcium during their entire life cycle, despite hving their vegettive growth inhibited, hd their pod production meliorted (Lcerd et l, 1995) The beneficil effects of clcium dditions to the root environment of NCl-stressed plnts re ssocited with the mintennce of cell membrne integrity, reducing N + nd fvoring K + bsorption in slt stressed plnts (Epstein, 1998) Although the ddition of clcium to the nutrient solution did not fvor K + bsorption in slt-stressed plnts it reduced N + bsorption by the roots nd contributed to its reduction in the shoot On the other hnd, Cl - contents were the highest in plnts subjected to tretment contining higher clcium concentrtion in nutrient solution (tble 3) It should be lso noted tht lef succulence in this tretment (SC2) ws similr to those of S nd SC1 (tble 2) even though its Cl - content ws considerbly higher The fct tht the Cl - concentrtion, expressed on wter content bsis (dt not shown), ws considerbly higher in the SC2 tretment could prtilly explin the greter growth reduction in this tretment, due to toxic effects of this ion (Zekri nd Prsons, 1990) In ddition to this, the totl slt concentrtion in nutrient solution ws the highest in this tretment (SC2), which could hve contributed to this higher growth reduction (Song nd Fujiym, 1996; Reid nd Smith, 2000) Therefore, lthough there ws beneficil effect of CCl 2 ddition on the decrese of N + ccumultion in the shoot, this ppered to be counterblnced by the deleterious effects of tissue Cl - ccumultion nd by the lowering of the Ψ w in the root environment, due to the increse in totl slt concentrtion in the nutrient solution (Zekri nd Prsons, 1990)
6 104 JV SILVA et l Tble 4 Orgnic solutes contents of cowpe plnts grown in nutrient solution (C), in nutrient solution contining 75 mmoll -1 NCl (S), nd in nutrient solution contining 75 mmoll -1 NCl nd 5 mmoll -1 (SC1) or 10 mmoll -1 (SC2) CCl 2 Tretments Soluble crbohydrtes Solutes (molkg -1 DM) N-mino soluble Proline Root tips C 0398 b S b 0009 b Sc b 0010 b Sc b 0348 b 0009 b Youngest trifolite lef C 0535 c b S b 0021 b Sc b 0412 c 0024 Sc b 0532 b 0026 Vlues followed by the sme letter within the sme column re not sttisticlly different t p < 005 (Tukey test) It ws lso suggested tht the ddition of clcium to the root environment of NCl-stressed plnts would help orgnic solute ccumultion in the roots, which could contribute to root osmotic djustment, fvoring the mintennce of plntwter blnce nd growth (Colmer et l, 1996; Girij et l, 2002) Slt-stressed cowpe plnts ccumulted soluble crbohydrtes s well s ions both in roots nd in leves At the sme time, proline nd soluble mino-nitrogen were either not ffected or decresed s result of slt-stress (tble 4) Therefore, the ccumultion of ions nd crbohydrtes could be ccounted for by the osmotic djustment tht could hve contributed to the mintennce of their wter blnce under stress conditions (tble 2) The ddition of clcium to the nutrient solution of the slt stressed plnts (SC1 nd SC2 tretments) reduced soluble crbohydrte contents nd did not lter or incresed proline content, when compred to plnts of the S tretment (tble 4) The decrese in crbohydrtes content could be explined by their deversion to other nbolic nd ctbolic pthwys, nd could ccount for the lower productive cpcity s well s for the enhncement of mture lef senescence observed by Munns (2002) The increse in lef proline content s result of clcium ddition could be ssocited to lef dehydrtion (Lcerd et l, 2003) or to higher ion ccumultion (Weimberg et l, 1984) Although proline content incresed s result of slt stress, its concentrtion ws not high enough to explin their contribution to osmotic djustment The increse in proline content ws more conspicuous in plnts tht showed the gretest growth reduction, reinforcing the ide tht increse in proline concentrtion is the result of stress dmge nd it is not ssocited with stress tolernce (Ferreir et l, 1979; Lcerd et l, 2003) Proline content in root tips did not differ between S nd SC1 or SC2 tretments, nd they were lower in slt-stressed thn in the control tretment (tble 4) These results do not support the hypothesis tht clcium promotes orgnic solute ccumultion, minly proline, in root tips fvoring osmotic djustment nd root growth under slt stress conditions (Frnco et l, 1999) The reductions in stomtl conductnce nd in trnspirtion rtes were, in generl, higher in plnts supplemented with clcium thn in plnts subjected only to NCl stress (figure 1), these results being prtilly relted to the increses in tissue ions ccumultion (tble 3) nd plnt growth reduction (tble 1) Although these mechnisms could be beneficil becuse they reduce plnt wter loss, they lso reduce net CO 2 ssimiltion nd consequently plnt productivity (Seemnn nd Critchley, 1985) So, the dditions of CCl 2, despite hving some beneficil effects on decresing N + bsorption, were not sufficient to mintin plnt-wter blnce (figure 1) nd meliorte the growth of slt stressed plnts Therefore, the results obtined reinforce the ide tht the beneficil effects of clcium on growth of NCl-stressed plnts will only pper if they supplnt the deleterious effects ssocited with the increse in totl slt concentrtion of the root environment, ie, osmotic effects resulting from the decrese in osmotic potentil of the nutrient solution (Reid nd Smith, 2000) nd toxic effects due to tissue ions ccumultion, especilly those of the compnion nion, such s Cl - (Zekri nd Prsons, 1990) Acknowledgements: We thnk Dr Michel Richrdson for reviewing the English text, nd cknowledge the finncil support given by Conselho Ncionl de Desenvolvimento Científico e Tecnológico (CNPq) nd Fundção Coordenção de Aperfeiçomento de Pessol de Nível Superior (CAPES) REFERENCES Ainouz TL (1970) Preliminry studies on proteins of Vign sinensis An Acd Brs Cienc 42: Btes LS, Wldren RP, Tere JD (1973) Rpid determintion of free proline for wter-stress studies Plnt Soil 39: Cocking EC, Yemm EW (1954) Estimtion of mino cids by ninhydrin Biochem J 58:12-13
7 AND NCl STRESS IN COWPEA PLANTS 105 Colmer TD, Fn TW-M, Higshi RM, Läuchli A (1996) Interctive effects of C 2+ nd NCl slinity on the ionic reltions nd proline ccumultion in the primry root tip of Sorghum bicolor Physiol Plnt 97: Crmer GR, Läuchli A, Polito VS (1985) Displcement of C 2+ by N + from the plsmlemm of root cells A primry response to slt stress? Plnt Physiol 79: Dubois M, Gilles KA, Hmilton JK, Rebers PA, Smith F (1956) Colorimetric method for determintion of sugrs nd relted substnces Anl Chem 28: Epstein E (1998) How clcium enhnces plnt slt tolernce Science 40: Ferreir LGR, Souz JG, Prisco JT (1979) Effects of wter deficit on proline ccumultion nd growth of two cotton genotypes of different drought resistnces Z Pflnzenphysiol 93: Frnco OL, Enés Filho J, Prisco JT, Gomes Filho E (1999) Effects of CCl 2 on growth nd osmoregultor ccumultion in NCl stressed cowpe seedlings Rev Brs Fisiol Veg 11: Girij C, Smith BN, Swmy PM (2002) Interctive effects of sodium chloride nd clcium chloride on the ccumultion of proline nd glycinebetine in penut (Archis hypoge L) Environ Exp Bot 47:1-10 Ky C, Kirnk H, Higgs D, Sltli K (2002) Supplementry clcium enhnces plnt growth nd fruit yield in strwberry cultivrs grown t high (NCl) slinity Sci Hort 93:65-74 Kinride TB (1999) Interctions mong C 2+, N + nd K + in slinity toxicity: quntittive resolution of multiple toxic nd meliortive effects J ExpBot 50: Kinride TB (1998) Three mechnisms for the clcium llevitions of minerl toxicities Plnt Physiol 118: Lcerd CF, Silv JV, Prisco JT (1995) Efeitos do C 2+ e do meio mbiente n composição minerl d prte ére de plnts de feijão-de-cord submetids estresse slino In: Anis do XXV Congresso Brsileiro de Ciênci do Solo Viços, Brsil volii pp Lcerd CF, Cmbri J, Cno MAO, Ruiz HA, Prisco JT (2003) Solute ccumultion nd distribution during shoot nd lef development in two sorghum genotypes under slt stress Environ Exp Bot 49: Liu J, Zhu J-K (1997) Proline ccumultion nd slt-stressinduced gene expression in slt-hypersensitive mutnt ofarbidopsis Plnt Physiol 114: Mlvolt E, Vitti GC, Oliveir SA (1989) Avlição do estdo nutricionl ds plnts: Princípios e Aplicções Associção Brsileir pr Pesquis d Potss e do Fosfto, Pircicb Munns R (2002) Comprtive physiology of slt nd wter stress Plnt, Cell Environ 28: Prisco JT, Vieir GH (1976) Effects of NCl slinity on nitrogenous compounds nd proteses during germintion of Vign sinensis seeds Physiol Plnt 36: Reid RJ, Smith A (2000) The limits of sodium/clcium interctions in plnt growth Aust J Plnt Physiol 27: Rengel Z (1992) The role of clcium in slt toxicity Plnt Cell Environ 15: Seemnn JR, Critchley C (1985) Effects of slt stress on the growth, ion content, stomtl behviour nd photosynthetic cpcity of slt-sensitive species, Phseolus vulgries L Plnt, 164: Song JQ, Fujyim H (1996) Difference in response of rice nd tomto subjected to sodium sliniztion to the ddition of clcium Soil Sci Plnt Nutr 42: Weimberg R, Lerner HR, Poljkoff-Meyber A (1984) Chnges in growth nd wter-soluble solute concentrtions in Sorghum bicolor stressed with sodium nd potssium slts Physiol Plnt 62: Yeo A (1999) Predicting the interction between the effects of slinity nd climte chnge on crop plnts Sci Hort 78: Zekri M, Prsons LR (1990) Clcium influences growth nd lef minerl concentrtion of citrus under sline conditions HortScience 25:
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