Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L.
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- Todd Jackson
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1 Kong t l. Botnil Stuis 214, 55:9 RESEARCH Opn Ass Effts of folir pplition of sliyli i n nitri oxi in llviting iron fiiny inu hlorosis of Arhis hypog L. Jing Kong, Yunji Dong *, Linlin Xu, Shung Liu n Xioying Bi Astrt Bkgroun: Th im of this xprimnt ws to nlyz th llvition mhnism of xognous sliyli i (SA) n soium nitroprussi (SNP, nitri oxi onor) on pnut slings unr F fiiny. Th ffts of SA n SNP on iron uptk n vilility, ions ln n oxint mg wr stui with folir pplition of xognous 1. mm SA (SA) or 2.5 mm SNP (SNP) or.5 mm SA+1.25 mm SNP [1/2(SA+SNP)] or 1. mm SA+2.5 mm SNP (SA+SNP). Rsults: Th rsults show tht ftr 21 ys trtmnt, th pnut slings growing unr iron fiiny onitions xhiit lf intrvinl hlorosis, n this iron-fiiny inu symptom ws prvnt y folir pplition of SA, SNP, 1/2 (SA+SNP), spilly SA+SNP. Th inrs ontnts of hlorophyll n tiv iron, n inrs F umultion in ll orgnlls wr osrv in SA+SNP trt young lvs, suggsting tht n improvmnt of iron vilility in plnts. Morovr, th improv nutrint solution ph, inrs H + -ATPs tivity n inrs iron onntrtion in roots in SA+SNP trt plnts, suggsting tht SA+SNP is fftiv in moulting iron uptk. Furthrmor, th inrs lium (C), mgnsium (Mg) n zin (Zn) onntrtions n rs mngns (Mn) n oppr (Cu) onntrtions in th lvs n roots of pnut init tht SA+SNP stimult th mintnn of ions istur y F fiiny. In ition, SA+SNP llvit th inrs umultion of suproxi nion (O 2 ) gnrtion rt n mlonilhy (MDA), n moult th ntioxint nzyms. Conlusions: Ths rsults init tht th intrtion of SA n SNP promot F uptk, trnslotion n tivtion; moult th ln of minrl lmnts; n prott F fiiny inu oxitiv strss. Thrfor, SA n SNP h synrgisti ffts in llviting hlorosis inu y F fiiny. Kywors: Ativ iron; Antioxint nzyms; Arhis hypog L.; Minrl lmnts; SA; SNP Bkgroun Iron (F) is n ssntil minrl nutrint for plnts. It ts s o-ftor for mny nzyms n protins. F is involv in hlorophyll iosynthsis, thylkoi synthsis, n hloroplst vlopmnt (Buhnn t l. 2). Thrfor, F fiiny impirs hlorophyll iosynthsis n hloroplst vlopmnt in oth iotylonous n monootylonous spis (Grzino t l. 22). Aitionlly, in highr plnts, it is wll known tht th rtrnslotion of F from ol lvs to young lvs is iffiult. Thrfor, whn th plnts suffr from F fiiny, th nwly forming lvs vlop hlorosis * Corrsponn: yjong@su.u.n Collg of Rsours n Environmnt, Shnong Agriulturl Univrsity, Ti n 27118, P.R. Chin symptoms (Jin t l. 27). Pnuts long to Strtgy I plnts, n it rspons to F fiiny y soring iron in thr sussiv stps. First, thy iify th rhizosphr to inrs th soluility of F(III) (Snti n Shmit 29). Nxt, thy ru solul F(III) to F(II) y th frri-hlt ruts FRO2 (Ding t l. 29). Finlly, plnts trnsport F(II) ross th root plsm mmrn y th mtl trnsportr IRT1 (Ding t l. 21). Howvr, th ftors tht inu Ffiiny hlorosis of pnut wr vry omplit in th fil, n th st pritor of F ffiiny in pnut ws not vry lr (Go n Shi 27). Sliyli i (SA) is n nognous growth rgultor of phnoli ntur, whih prtiipts in th rgultion of physiologil prosss n plnt rsistn to ioti n ioti strss (Krlig t l. 29). For xmpl, 214 Kong t l.; lins Springr. This is n Opn Ass rtil istriut unr th trms of th Crtiv Commons Attriution Lins ( whih prmits unrstrit us, istriution, n rproution in ny mium, provi th originl work is proprly it.
2 Kong t l. Botnil Stuis 214, 55:9 Pg 2 of 12 it improvs grmintion, plnt growth, trnspirtion rt, stomtl rgultion n photosynthsis, ion uptk n trnsport (Khn t l. 23; Mtwlly t l. 23; Khory 24; H t l. 21). Furthrmor, it is now lr tht SA provis prottion ginst numr of ioti strss s ht strss in strwrry (Krlig t l. 29), hvy mtl strss suh s mium (Mtwlly t l. 23; H t l. 21), oppr (Khory 24; El-Ty 26) n mngns (Shi n Zhu 28), n slt strss (El-Ty 25; Khory 24). In ition, it is oming lr tht SA intrts oth ngtivly n positivly with othr mjor signling pthwys, inluing thos rgult y jsmoni i n thyln (Rskin 1992). Furthrmor, it is monstrt tht SA is l to triggr nitri oxi synthsis in Ariopsis slings. Stuying th kintis of umultion of nitri oxi, lr rspons ws osrv tht ws pnnt on th onntrtion of SA (Zottini t l. 27). Nitri oxi (NO) is nothr signling molul, whih plys n importnt rol in mny physiologil prosss in plnts, suh s growth, vlopmnt, snsn n ptiv rsponss to multipl strsss (Hu t l. 27; Frooq t l. 29; Kzmi t l. 21). Rntly, it hs n shown tht trtmnt with NO or its onor n mit hlorophyll inrs, F vilility n ntioxint nzyms (Zhng t l. 212). Svrl mols suggst tht rox signlling through NO n ROS is nhn y SA in slf-mplifying pross. Howvr, th rltionship twn NO, SA, n ROS in th tivtion of fn gns n/or inution of host ll th is not lrly fin (Zottini t l. 27). Iron fiiny hs n wispr prolm in pnut (Arhis hypog L.) grown on lrous soils of northrn Chin n hs rsult in signifint yil losss (Go n Shi 27). Prvious rsrhs monstrt tht th intrtion of SA with SNP oul ountrt th ltrious ffts inu y NCl (Simi t l. 211). Bs on th ov stuis, w suppos tht SA n NO prtiipts in F fiiny tolrn ws importnt in pnut slings n th intrtion of SA with NO oul mliort F fiiny inu hlorosis. Thrfor, th purpos of th prsnt stuy ws to xmin whthr folir pplition of SA n SNP oul (i) improv F uptk, trnsporttion n tivtion; (ii) moult th ions ln; (iii) prott F fiiny inu oxitiv strss. Mthos Plnt mtrils n xprimntl sign Th slt ss of pnut (Arhis hypog L.) wr surf striliz with 5% H 2 O 2 for 3 min, wsh svrl tims with stril ioniz wtr, n grmint on wt stril sn t 25 C in th rknss. Aftr grmintion, uniform slings trnsfrr into rt on-hlf strngth Hogln solution for 3 ys. Thn, th solution ws rpl with stnr Hogln solution (Hogln n Arnon 195). Whn th thir lf xpn fully, th slings wr trnsfrr into hyroponi systms (Hogln nutrint solution whih sustituting.1 mm FSO 4 for.1 mm EDTA-F) n rmov otylons. Six trtmnts wr stlish s follows: (1) hyroponi systms (CK); (2) Hogln nutrint solution ontining.1 mm EDTA-F (EDTA-F); (3) hyroponi systms n folir pplition of 1. mm SA (SA); (4) hyroponi systms n folir pplition of 2.5 mm SNP (SNP); (5) hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP (SA+SNP); (6) hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP [1/2(SA+SNP)]. Th trtmnts r rrng in rnomiz lok sign with thr rplits. Trtmnts of sprying SA n/or SNP solution on lvs wr prform in th vning vry y with 1 ml vry tim. Eh pot h 2.5 L of rt nutrint solution n ontin four plnts. Nutrint solutions wr rpl vry thr ys n initil ph vlu ws just to 6.3 with 1. mm NOH. Plnts wr grown in growth hmr t 25 ± 1 C/2 ± 1 C (y/night) tmprturs with 16 h photoprio t light intnsity of 3 ± 1 μem -2 s -1 provi y rfltor sunlight ysprosium lmp. Rltiv humiity rng from 65 to 7%. Dtrmintion of Chlorophyll ontnt, photosynthti prmtrs n fluorsnt prmtrs Th hlorophyll ontnt ws trmin oring to th mtho of Knuson t l. (1977)..5 g frsh pnut lvs wr xtrt in 2 ml 95% (v/v) thnol for 24 h in th rk, n th xtrt solution ws nlyz. Th mounts of hlorophyll, n rotnoi wr trmin sptrophotomtrilly (SHIMADZU UV-245, Kyoto, Jpn), y ring th sorn t 665, 649 n 47 nm. C = 13.95*A *A649; C = 24.96*A *A665; C rotnoi = (1*A47-2.5*C *C )/245. Th hlorophyll ontnt rsults r xprss s unit s mg pr grm-frsh wight (mg g -1 FW). Th young lvs wr slt to msur photosynthti n fluorsnt prmtrs twn 9: 1: AM y using th photosynthsis systm (CIRAS-2, UK) n th puls mplitu moult systm (mol FMS2. Hnsth Instrumnts. UK). Dtrmintion of th nutrint solution ph Th nutrint solution ph ws trmin with MVpH mtr (DMP-2), n h trtmnt ws rplit for thr tims. From th nintn y ftr stlishing F fiiny onition, in othr wors, from th lst tim hng nutrint solutions, th nutrint solution ph
3 Kong t l. Botnil Stuis 214, 55:9 Pg 3 of 12 ws msur from 8.m. to 6 p.m. for vry two hours in th first y (nintn-y-ol pnut slings), n msur t 2 p.m. in th son (twnty-y-ol pnut slings) n thir y (twnty on-y ol slings). During th msuring prio, th nutrint solution ws not rpl, n only istill wtr ws to rplnish tht lost y vportion. Isoltion of plsm mmrn n th msurmnt of H + -ATPs n C 2+ -ATPs tivitis in PMs A mmrn frtion nrih in plsm mmrn vsils ws prpr s sri y Briskin t l. (1987) with minor hngs. Exis roots wr homogniz (1/2, w/v) with mortr n pstl in ol grining mium ontining: 25 mm HEPES-Tris (ph 7.2), 25 mm mnnitol, 5 mm EDTA, 5 mm EGTA, 1 mm DTT n 1.5% (w/v) PVP. Th whol isoltion prours wr rri out t 4 C. Th homognt ws filtr through four lyrs of hsloth n ntrifug t 56 g for 12 min, thn th suprntnt ws ntrifug t 1, g for 15 min, n th suprntnt ws ntrifug t 6, g for 3 min to yil ru mmrn frtion. Th rsulting pllt ws rsuspn with 1 ml in grint uffr ontining: 2 mm HEPES-Tris (ph 7.5), 5 mm EDTA,.5 mm EGTA. Th suprntnt ws lyr on top of stp grint onsisting of 1 ml 45%, 33%, n 15% (w/w) suros, rsptivly, n thn ntrifug for 2 h t 7, g. ATP hyrolysis ssys wr prform s sri y Briskin t l. (1987) in.5 ml th rtion mium ontining: 36 mm Tris-Ms (ph 6.5), 3 mm ATP- N 2,3mMMgSO 4,1mMNN 3,5mMKNO 3,1mM N 2 MoO 4,.2% (w/v) Triton A-1, in th prsn or sn of 2.5 mm N 3 VO 4. Th rtion ws strt y ing 5 μl PM vsils. Aftr 3 min inution t 37 C, th rtion ws qunh y th ition of 5 μl 55%(w/v)TCA.ThH + -ATPs tivity ws trmin y msuring th rls of Pi (Ohinishi t l. 1975). Aitionlly, ATP hyrolysis ssys wr prform s sri y Briskin t l. (1987) in.5 ml th rtion mium ontining: 5 mm Tris-M (ph 7.6), 25 mm suros, 1. mm DTT, 2. mm ATP-N 2,.1 mm (NH 4 ) 2 MoO 4,.2% TritonX-1 (v/v), 3 Mm NNO 3, 1. mm NN 3, in th prsn or sn of 2. mm C(NO 3 ) 2. Th rtion ws strt y ing 5 μlpm vsils. Aftr 3 min inution t 37 C, th rtion ws qunh y th ition of 5 μl 55% (w/v) TCA. Th C 2+ -ATPs tivity ws trmin y msuring th rls of Pi (Ohinishi t l. 1975). Solul protin ontnt ws msur y th Coomssi Brillint Blu G-25 mtho (Brfor, 1976). Solul protin ontnt ws xprss s mg g -1 FW. Assy of F(III)-Chlt Ruts (FCR) Plnts roots wr immrs in sturt CSO 4 solution for 5 min, wsh with ioniz wtr, n thn trnsfrr to th nutrint solution mntion ov, whih ontin.1 mm F-EDTA n.4 mm 2, 2-ipyriyl, ph 5.. Th nvironmntl onitions uring th msurmnt wr th sm s for plnt growth. Aftr 2 h, F-rution pity y th roots ws trmin y msuring th onntrtion of F 2+ -ipyriyl omplx form t A 523 in sptrophotomtr (Shimzm UV- 221) (Go n Shi 27). Dtrmintion of tiv F ontnt Frsh young lvs wr ut into pis n 2. g ws wigh n xtrt with 2 ml 1 N HCl (in 1:1 tissu: xtrtnt), shkn for 5 h n filtr, n th susqunt F onntrtion in th filtrt ws msur with tomi sorption sptrophotomtr (PE-21B, Prkin Elmr Co. Lt., MA, USA) (Go n Shi 27). Dtrmintion of th istriution of F in sullulr strutur of pnut plnts Aftr 21 ys of trtmnt, roots of ll th pnut plnts wr immrs in 2 mm isoium thylnimin ttrti i (N 2 -EDTA) for 15 min n wr thn rins thr tims with ioniz wtr. Eh 25 g smpl ws homogniz in 5 ml of hill xtrtion uffr ontining 5 mm Hps (ph 7.5), 5 mm suros, 1 mm DTT, 5 mm sort n 1% polyvinylpolypyrrolion (PVPP). Th homognt ws ntrifug t 5 g for 5 min to isolt th ll wll frtion. Th suprntnt from this ntrifugtion stp ws thn ntrifug t 2, g for 45 min to simnt ll orgnlls, n th rsultnt suprntnt solution ws rfrr to s th solul frtion. All stps wr prform t 4 C. Th frtions of th smpls wr igst in mixtur of HNO 3 n HClO 4 (4:1, v/v) t 12 C for t lst 3 h. F ws thn quntifi using n tomi sorption sptromtr (AA-68, Shimzu, Tokyo, Jpn). Antioxint nzyms n MDA xtrtion n ssy For trmintion ntioxint nzyms,.5 g powr of frz-ri pnut lvs wr homogniz with 5 mm N 2 HPO 4 -NH 2 PO 4 uffr (ph 7.8) ontining.2 mm EDTA n 2% insolul polyvinylpyrrolion in hill pstl n mortr. Th slurry ws ntrifug t 12, g for 2 minuts n th suprntnt ws us for nzym tivitis ssy. Th xprimnt ws rri out t 4 C. Totl SOD tivity ws ssy y th photohmil mtho (Ro n Srsty 2). Th 3 ml rtion mixtur ontin 5 mm phospht uffr (ph 7.8), 13 mm mthionin, 75 μm nitrolu ttrzolium, 2 mm rioflvin, 1 mm EDTA n.1 ml nzym xtrt.
4 Kong t l. Botnil Stuis 214, 55:9 Pg 4 of 12 On unit of th nzym tivity ws fin s th mount of nzym rquir to rsult in 5% inhiition of th rt of nitro lu ttrzolium (NBT) rution msur t 56 nm. SOD tivity ws xprss s U g -1 FW min -1. Guiol proxis (POD) tivity ws stimt ftr Nikl n Cunninghm (1969) mtho. Ativity ws msur y th inrs in sorn t 47 nm u to guiol oxition. Th tivity ws xprss s U g -1 FW min -1. CAT tivity ws trmin y following th onsumption of H 2 O 2 t 24 nm oring to th mtho of Ckmk n Mrshnr (1992). CAT tivity ws xprss s nmol H 2 O 2 mg -1 FW min -1.Th lvl of lipi proxition in frsh lf ws msur in trms of mlonilhy (MDA) ontnt y th thiorituri i rtion mtho (Hth n Pkr 1968). MDA ontnt ws xprss s nmol g -1 FW. Dtrmintion of th O 2 gnrtion rt For th msurmnt of O 2 grmintion rt,.3 g frsh lvs wr groun in liqui N 2 n xtrt in 3 ml of i ol 5 mm soium phospht uffr (PBS) (ph 7.). On millilitr suprntnt of frsh lvs xtrtion ws to.9 ml 65 mm phospht uffr solution (ph 7.8) n.1 ml 1 mm hyroxylmmoniumhlori. Th rtion ws inut t 25 C for 35 min..5 ml solution from th ov rtion mixtur ws thn in.5 ml 17 mm sulfni i n.5 ml 7.8 mm ɑ-nphthylmin solution. Aftr 2 min of rtion, 2 ml of thr ws into th ov solution, n thn mix wll. Th solution ws ntrifug t 15 g t 4 C for 5 min. Th sorn of th pink suprntnt ws msur t 53 nm with th sptrophotomtr. Asorn vlus wr lirt to stnr urv gnrt with known onntrtions of HNO 2 (Shi n Zhu 28). Dtrmintion of plnt growth inx n minrl lmnt onntrtions Aftr 21 ys trtmnt, th pnut plnts wr hrvst. Roots wr sok in 2 mm N 2 -EDTA for 15 min to rmov mtl ions hring to root surfs, n rins with ioniz wtr svrl tims. Th pnut plnts wr ivi into roots n shoots n msur plnt hight, root lngth n frsh wight. Th root volum ws trmin y th wtr. Th smpls wr ri t 7 C to onstnt wight n wight. 5 mg of ri plnt tissus wr groun up n igst in 1 ml of onntrt nitri i for 2 3 t room tmprtur. Smpls wr thn oil for 1 2 h until ompltly igst. Aftr ing 4 ml of millipor-filtr ioniz wtr n rifly ntrifuging, th minrl lmnt onntrtions of h smpl wr trmin y tomi sorption sptrophotomtr (SHIMADZU AA-63) (Zhng t l. 211). Sttistil nlysis Th tuky s tst ws us to tst th fft of iffrnt trtmnt, n th lst signifint iffrn (LSD) ws lult to ompr th iffrn twn mns in h trtmnt. Sttistil nlyss wr prform y nlysis of vrin (ANOVA) using th SAS softwr n orrltiv nlysis us th SPSS softwr (SPSS 11.5). Rsults Plnt growth Tl 1 shows tht plnt growth hrtristis of pnut wr grtly influn y F fiiny n folir pplition of SA n/or SNP. F fiiny rmtilly rs th shoot hight, frsh wight n root/shoot rtio. Howvr, ition of SA, SNP, spilly SA+SNP llvit th F fiiny ffts. Whn pnut plnts wr trt with SA or SNP unr F fiiny, th shoot hight, root lngth n root volum in SA trtmnt inrs y 18.2%, 29.3% n 19.4% ompr with ontrol, n th frsh wight n root/shoot rtio in SNP trtmnt inrs y 28.4% n 33.3% ompr with ontrol. In ition, th llvition fft of SA+SNP ws tt st ompr with SA, SNP or 1/2 (SA+SNP) trtmnt. Chlorophyll ontnt As shown in Tl 2, thr ws signifint rs on hlorophyll ontnt of pnut plnts unr F fiiny. Howvr, folir pplition of SA, SNP, 1/2(SA+SNP), spilly SA+SNP, th inhiitory ffts of F fiiny on hl n hl wr signifintly mliort. Aitionlly, folir pplition of SA+SNP rmtilly inrs th hl +, rnhl/ rtio y 19.1%, 26.3% n 3.6% ompr with ontrol, rsptivly. Photosynthti n fluorsnt prmtrs Pnut plnts sujt to F fiiny xhiit rmti rs in nt photosynthti (Pn) n trnspirtion rts (Tr) y 32.9% n 23.5% ompr with EDTA-F trtmnt, whrs Fo, Fv/Fm n ΦPSII lso signifintly rs in pnut lvs (Tl 3). Howvr, whn pnut plnts trt with SA, SNP, 1/2(SA+SNP), prtiulrly SA+SNP, th inhiition of photosynthti systm inu y F fiiny rmrkly llvit. In ition, th Fo, Fv/Fm n ΦPSII of SA+SNP trtmnt, intrstingly inrs y 26.55%, 8.6% n 26.9% ompr with ontrol, n th Fv/Fm n ΦPSII wr similr to EDTA-F trt ons. Th ph of nutrint solution n th tivitis of H + -ATPs n C 2+ -ATPs Th H + -ATPs trnsports protons out of th ll ross th plsm mmrn, thus stlishing th proton ltrohmil grint tht ontriuts to th mintnn
5 Kong t l. Botnil Stuis 214, 55:9 Pg 5 of 12 Tl 1 Effts of xognous SA n NO on plnt growth of pnut t 21 ys trtmnt Trtmnts Shoot hight (m/plnt) Root lngth (m/plnt) Root volum (ml/plnt) Frsh wight (g/plnt) Root/Shoot rtio CK 28.6 ± ±.6.98 ± ±.8.18 ±.1 EDTA-F 33.9 ± ± ± ±.7.21 ±.1 SA 33.8 ± ± ± ± ±.1 SNP ± ± ± ± ±.1 SA+SNP ± ± ± ± ±.1 1/2(SA+SNP) 34.5 ± ± ± ± ±.1 CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Dt r mns ± SD of thr rplit smpls pr trtmnt. of th intrllulr n xtrllulr ph n plys mjor rol in th tivtion of ion n nutrint trnsport (Frééri t l. 27). Thrfor, w trmin th tivitis of H + -ATPs n C 2+ -ATPs in plsm mmrn n ph of nutrint solution. As shown in Figur 1, unr F fiiny, th tivity of H + -ATPs ws onsirly stimult. Compr with th ontrol, SA+SNP n 1/2 (SA+SNP) trtmnts furthr inrs th tivity of H + -ATPs y 24.39% n 13.88%, rsptivly. F fiiny inhiit th tivity of C 2+ -ATPs. Howvr, th C 2+ -ATPs tivity ws signifintly inrs y folir pplition of SA, SNP, or 1/2(SA+SNP), spilly SA+SNP. In ition, s shown in Figur 1C n D, on th whol, th nutrint solution ph of ll trtmnts xhiit lin from 8.m. to 14 p.m. in th first y, lthough it ppr to flutut in th lin. Unr Ffiiny strss, ph vlu in nutrint solution ws signifintly lowr thn EDTA-F trtmnt. SA+SNP trtmnt, in prtiulr, show th lowst ph t 14 p.m. in th first y. Furthrmor, on th whol, th nutrint solution ph of ll trtmnts xhiit lin from th first y to th son y, n n inrs from th son y to th thir y (Figur 1B). Totl F, tiv F n FCR tivity As shown in Tl 4, F fiiny inhiit F sorption n trnsporttion of pnut slings, prouing 38.4% (roots), 31.3% (stms) n 19.5% (lvs) rs in th F onntrtions ompr with EDTA- F trtmnt. Morovr, it mrkly rs th tiv F ontnt. Howvr, it strikingly inrs FCR tivity ompr with EDTA-F trtmnt. Folir pplition of SA, SNP or 1/2(SA+SNP), prtiulrly SA+SNP show positiv influn on F onntrtions, tiv F ontnt, n FCR tivity. SA+SNP signifintly inrs th F onntrtions in roots, stms n lvs y 37.68%, 55.4% n %, n rmtilly inrs th tiv F ontnt n FCR tivity y 91.5% n 28.2%, rsptivly, ompr with ontrol. Th istriution of F in sullulr strutur of pnut plnts In orr to invstigt th mhnisms of xognous SA n SNP in llviting hlorosis inu y F fiiny, F istriutions in ll wll, solul frtion n ll orgnlls wr xmin rfully. In th roots, mjority of F umult in th ll wll. Howvr, F umult in th solul frtion ws lss thn in th ll wll, n only minority of F umultion ws in ll orgnlls (Figur 2A). In ontrst, in th lvs, th mount of F umult in th solul frtion ws mor thn th mount of F umult in th ll wll, n th ll orgnlls umult th lst F Tl 2 Effts of xognous SA n NO on hl, hl, r, hl + n hl / of pnut Trtmnts Chl (mg g -1 FW) Chl (mg g -1 FW) Crotnois x. (mg g -1 FW) Chl + (mg g -1 FW) Chl / CK 1.15 ±.1f.46 ±.3.19 ± ±.1f 2.49 ±.22 EDTA-F 1.22 ±.3.48 ±.2.2 ± ± ±.8 SA 1.26 ±.1.5 ±.4.2 ± ± ±.18 SNP 1.29 ± ±.2.21 ± ± ±.98 SA+SNP 1.39 ±.6.54 ±.4.24 ± ± ±.31 1/2(SA+SNP) 1.35 ±.5.53 ±.3.22 ± ± ±.23 CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Dt r mns ± SD of thr rplit smpls pr trtmnt.
6 Kong t l. Botnil Stuis 214, 55:9 Pg 6 of 12 Tl 3 Effts of xognous SA n NO on th nt photosynthti (Pn), trnspirtion rt (Tr), Fo, Fv/Fm n ΦPSII of lvs Trtmnts Pn [μmol m -2 s -1 ] Tr [mmol m -2 s- 1 ] Fo Fv/Fm ΦPSII CK 1.78 ± ± ± ± ±.2 EDTA-F 16.7 ± ± ± ± ±.2 SA ± ± ± ± ±.1 SNP ± ± ± ± ±.2 SA+SNP ± ± ± ± ±.2 1/2(SA+SNP) ± ± ± ± ±.1 CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Dt r mns ± SD of thr rplit smpls pr trtmnt. (Figur 2B). Th rsults wr quit iffrnt in th plnts trt with F fiiny n folir pplition of SA+SNP. Unr F fiiny, F onntrtions wr signifintly inrs in th ll wll, ut rmtilly rs in th ll orgnll n solul frtion in th roots n lvs of pnut. Folir pplition of SA+SNP, F onntrtions in th roots n lvs wr intrstingly inrs in th ll orgnll n solul frtion, ut rs in th ll wll. In ition, th fft of SA+SNP ws ttr thn 1/2(SA+SNP). Antioxint nzyms, MDA n O 2 gnrtion rt Rsults in Tl 5 monstrt tht F fiiny l to th MDA ontnt n O 2 gnrtion rt inrs rmtilly in th lls of pnut lvs. Folir pplition of SA n/or SNP, th oxitiv mg inu y F fiiny ws signifintly llvit. As w ll know, SOD, POD n CAT r ll importnt ntioxint nzyms. Folir pplition of SA, SNP, or 1/2(SA+SNP), spilly SA+SNP, signifintly inrs th tivitis of ths nzyms. Folir pplition of SA+SNP signifintly inrs th tivitis of SOD, POD n CAT y 9.32%, 113.3% n 22.41%, rsptivly, ompr with ontrol. Minrl lmnt ontnts As shown in Figur 3, F fiiny rmtilly istur th ioni homostsis, ling to th onntrtions of mngns (Mn), oppr (Cu) n zin (Zn) signifintly inrs, n th onntrtion of mgnsium (Mg) intrstingly rs in roots. Folir pplition of SA n/or SNP, th onntrtions of Cu n Mn signifintly rs, howvr, th onntrtions of Zn n Mg rmtilly inrs in th roots n lvs ompr with ontrol. SA+SNP inrs th onntrtions of potssium (K), Mg, lium (C) n Zn y 11.4%, 85.9%, 3.6% n 19.%, n rs th onntrtions of Cu n Mn y 53.1% n 34.9% ompr with ontrol in th lvs of pnut. Disussion Symptoms of F fiiny in pnut hv n prviously sri y Zuo t l. (2). For xmpl, F fiiny n us rs growth, ltr photosynthti rts n us morphologil hngs in th lvs (Sun t l. 27; Zhng t l. 212). In this xprimnt, F fiiny-inu hlorophyll n rotnois fiiny ws losly orrlt with visul osrvtions of hlorosis of pnut lvs (Tl 2), n similr rsults hv n otin in mny othr rop plnts, suh s pr (Morls t l. 2), ph (Molssiotis t l. 25), miz (Sun t l. 27), n Chins g (Ding t l. 28). Th hlorosis n sri to th rol of F in th formtion of δ-minolvulini i n protohlorophylli, th prursors of th hlorophyll iosynthsis. In ition, F fiiny l to n inhiitory fft on plnt growth (Tl 1). Th inhiition of growth in pnut might rsult from F fiiny-inu ltrtion of funmntl mtoli pross, photosynthsis, tiv F ontnt n uptk of nutrint lmnts. SA n NO r prtiipting in th rgultion of multipl physiologil prosss n plnt rsistn to ioti n ioti strss. Rntly, it ws stlish tht NO lvts th ontnt of SA known s omponnt of signling pthwys uring ioti strsss (Klssig t l. 2) n SA my in turn stimult synthsis of NO in Ariopsis thlin, ting vi th nzym with NO synthsizing tivity (Zottini t l. 27). Th ffts of SA n NO on llviting nvironmnt toxiity in plnts, suh s nikl n slt strss, hs n rport y Kzmi t l. (21) n Simi t l. (211). Thrfor, in th xprimnt, w nlyz th possil rol of folir pplition of SA n/or SNP in moultion of th photosynthti prformn n th ntioxint fns systm ginst F fiiny inu hlorosis in pnut slings. Rsults from this xprimnt lrly init tht SA, SNP, prtiulrly SA+SNP, fftivly llvit hlorosis inu y F fiiny, sri s SA n
7 Kong t l. Botnil Stuis 214, 55:9 Pg 7 of 12 (A) (B) Th tivity of H + -ATPs (µmol Pi mg -1 protin h -1 ) CK EDTA-F SA SNP SA+SNP 1/2(SA+SNP) Trtmnts Th tivity of C 2+ -ATPs (µmol Pi mg -1 protin h -1 ) CK EDTA-F SA SNP Trtmnts SA+SNP 1/2(SA+SNP) (C) CK SA SA+SNP EDTA-F SNP 1/2(SA+SNP) (D) CK SA SA+SNP EDTA-F SNP 1/2(SA+SNP) ph Tim (h) ph Tim () Figur 1 Effts of xognous SA n NO on th tivitis of plsm mmrn H + -ATPs (A) n C 2+ -ATPs (B) in roots of pnut slings n hngs of ph in ultur mium (C n D). Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Th vlus r mns ± SD of thr rplit smpls pr trtmnt. CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. SNP inrs th uptk n trnslotion of F, promot th tivtion of F in th lvs of pnut n prott F fiiny inu oxitiv strss, rsulting in inrs hlorophyll ontnt n improv sling growth. A notl rution of hlorophyll prmtrs ws tt in pnut slings xpos to F fiiny strss (Tl 2; Zhng t l. 212). Th rs in hlorophyll ontnt might ttriut to F fiiny ru tiv F ontnt (Tl 4), whr tiv F prtiipts in vrious physiologil tions insi th plnts, suh s th ltron trnsport, hlorophyll iosynthsis (Hkn n Vhp 27; Zhng t l. 211). Folir pplition of SA, SNP, or 1/2(SA+SNP), spilly SA+SNP to plnts signifintly nhn th hlorophyll ontnt in young lvs (Tl 2; Kzmi t l. 21). This phnomnon my ttriut to th ft tht folir pplition of SA n/or SNP rs
8 Kong t l. Botnil Stuis 214, 55:9 Pg 8 of 12 Tl 4 Effts of xognous SA n NO on th F onntrtion, tiv F ontnt n F (III)- hlt ruts tivity Trtmnts F onntrtion (mg kg -1 DW) Ativ F ontnt (mg kg -1 FW) Roots Stms Lvs F(III)- hlt ruts tiity (μmol g -1 2h -1 FW) CK ± ± ± ± 1.1f 3.12 ±.9 EDTA-F ± ± ± ± ±.9 SA ± ± ± ± ±.2 SNP ± ± ± ± ±.7 SA+SNP ± ± ± ± ±.12 1/2(SA+SNP) ± ± ± ± ±.6 CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Dt r mns ± SD of thr rplit smpls pr trtmnt. hlorophyll grtion us y snsn n nvironmntl strss. In ition, folir pplition of SA+SNP, th tiv F ontnt ws rmtilly inrs in lvs (Tl 4) n th F onntrtion in th ll orgnll in lvs ws lso signifintly inrs (Figur 2). It init tht SA+SNP n improv F ntr into ll n promot th tivtion of F in th lvs of pnut. Th proution of NO hs n onsir s n rly rspons to iron privtion n is mintin whil th plnt is xpos to low-iron onitions (Grzino n Lmttin 27). Chn t l. (21) furthr monstrt tht NO ts s signl ownstrm of th uxin unr F fiiny tht ls to th ultimt inution of FCR vi FIT-mit trnsriptionl rgultion. Pnuts long to Strtgy I plnts rspon to F fiiny y inuing th frri hlt ruts m in root pirml ll plsm mmrn n lso vi stimultion of th plsm mmrn proton pump, thus inrsing proton xution (Vrt t l. 22; Jin t l. 26). Thrfor, th inrs tiv F ontnt my us SA+SNP nhn xrtion of protons n inrs tivity of FCR to soluiliz F III oxis to F II hlts. Th xport of protons from th plnt lls is mit y th plsm mmrn H + -ATPs (Lig t l. 24; Osss n Gooy 26). On of th min funtions of plsmlmm H + -ATPs is H + xtrusion from ll ytosol to ll wll r n loosning of ll wll mirofirils ling to ll growth y longtion (Hgr 23). Ths prosss n ontroll y IAA n fusioin n (A) CK EDTA-F 1/2(SA+SNP) SA+SNP (B) CK EDTA-F 1/2(SA+SNP) SA+SNP Root F onntrtion (mg kg -1 FW) f Cll wll Cll orgnll Solul ftion f h g f Cll wll Cll orgnll Solul ftion Figur 2 Effts of iffrnt trtmnts on tissu istriution of F in pnut roots (A) or lvs (B). Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Th vlus r mns ± SD of thr rplit smpls pr trtmnt. CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Lf F onntrtion (mg kg -1 FW) g
9 Kong t l. Botnil Stuis 214, 55:9 Pg 9 of 12 Tl 5 Effts of xognous SA n NO on SOD, POD n CAT tivitis n MDA ontnt n suproxi prou rt of pnut lvs Trtmnts SOD tivity (Unit mg -1 protin) POD tivity (Unit mg -1 protin) CAT tivity (Unit g -1 protin) MDA ontnt (nmol g -1 FW) O 2 - gnrtion rt (μmol g -1 h -1 FW) CK 2.36 ±.8.3 ±.4.58 ± ± ±.52 EDTA-F 2.34 ±.7.41 ±.3.67 ± ± ±.47 SA 2.52 ±.6.47 ±.1.69 ± ± ±.6 SNP 2.52 ±.16.5 ±.9.68 ± ± ± 1.31 SA+SNP 2.58 ±.3.64 ±.4.71 ± ± ±.32 1/2(SA+SNP) 2.52 ±.5.57 ±.6.69 ± ± ± 1.53 CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Dt r mns ± SD of thr rplit smpls pr trtmnt. possily rvl th lst phss of hormon ontroll growth rliztion. In th xprimnt, th tivitis of H + -ATPs n FCR wr signifintly inrs in roots y folir pplition of SA n/or SNP, ling to th nutrint solution ph ru n totl F onntrtions inrs in roots. Morovr, th F onntrtion in th ll wll in roots ws rs n th F onntrtions in th solul frtion n ll orgnlls in roots wr inrs y folir pplition of SA+SNP. In ition, folir pplition of SA+SNP lso rmtilly inrs th F onntrtions in th roots, stms n lvs of pnut ompr with ontrol. Thrfor, w n infr tht SA+SNP improv th uptk n trnslotion of F. Sin th monoropp pnut suffrs from lss F vilility, pnut unr monoropping hngs th xprssion of F-rsponsiv gns, suh s AhIRT1, noing n iron-uptk trnsportr (Ding t l. 21), n AhFRO1, noing frrihlt ruts (Ding t l. 29). Pnut unr F fiiny my lso hng AhIRT1 n AhFRO1 to improv F sorption n trnsporttion in th xprimnt. Howvr, whn F vilility is unr thrshol lvl, thos r not suffiint to support th F rquirmnt for plnt vlopmnt, n th strss symptoms om vint. Exognous pplition of SA+SNP inrs th F onntrtions in pnut roots, stms n lvs ompr with F fiiny trtmnt. Whthr this is us SA+SNP hng AhIRT1 n AhFRO1 improving F sorption n trnsporttion or not is n furthr rsrh. F fiiny signifintly rs th nt photosynthsis (Tl 3; Zhng t l. 212). Th ftors minly inlu stomtl limittion us y stomtl losur n non-stomtl limittion. Th formr my us y svrl ftors, inluing th lin of ssntil nutrint lmnts ontnt, spilly K, n th inrs proution of ROS in hloroplsts. Th lttr my us y F fiiny rs tiv F ontnt. Unr our xprimntl onitions, th ioni homostsis ws grtly istur (Figur 3) n tiv F ontnt ws rmtilly rs (Tl 4) y F fiiny. In ition, hlorophyll ontnt n hlorophyll fluorsn r onsir s initors of mgs to photosynthti systm inu y nvironmntl strssors (Mxwll n Johnson 2; Shi t l. 29). As w ll know, F is involv in hlorophyll iosynthsis. Thrfor, F fiiny impirs hlorophyll iosynthsis n hloroplst vlopmnt, whr th photosynthsis in plnts prominntly rlis on th grn lf, n its proutivity irtly pns upon th hlorophyll ring surf r, irrin n its potntil to utiliz CO 2. Howvr, folir pplition of SA n/or SNP stimult th mintnn of ions istur y F fiiny. Bush (1993) hs lrly stlish tht C 2+ ts s n intrllulr mssngr in oupling wi rng of xtrllulr signls to spifi rsponss. In th prsnt stuy, SA n/or SNP inrs C 2+ -ATPs tivity in roots n signifintly inrs C 2+ onntrtion in lvs (Figur 3D). Erlir stuis init tht xognous SA trtmnt stimult root formtion n inrs minrl uptk y plnts (Khn t l. 23; Yilirim t l. 28). In ition, SA hs long n known s signl molul in th inution of fns mhnisms in plnts (Horvth t l. 27) n proly moult th totl myls tivity n -myls tivity y hormonl rgultion (H t l. 21). This is why th rol of SA on mmrn lkg, lipi proxition, n minrl uptk unr strss onitions is importnt (Guns t l. 27). This positiv fft of SA n SNP oul ttriut to nhn CO 2 ssimiltion, tiv F ontnt, hlorophyll onntrtion, n photosynthti rt, whih prott photosynthsis systm. In plnts, thr r svrl rports whih show mtlinu ltrtions in oth th tivitis of ntioxitiv
10 Kong t l. Botnil Stuis 214, 55:9 CK SNP 4 K ontnt (g kg-1 ) 35 EDTA-F SA+SNP 3 25 (B) Roots Stms Lvs 45 2 Stms (D) Cu ontnt (mg kg-1 DW) C ontnt (g kg-1 DW) Roots Stms Lvs Roots (F) Mn ontnt (mg kg-1 DW) Lvs 4 1 Stms Lvs 6 5 Roots Stms Zn ontnt (mg kg-1 DW) Roots Lvs 4 (E) (C) 6 SA 1/2(SA+SNP) Mg ontnt (g kg-1 DW) (A) Pg 1 of 12 Roots Stms Lvs Figur 3 Effts of xognous SA n NO on th onntrtions of K (A), Mg (B), C (C), Cu (D), Zn (E), n Mn (F) of pnut. Diffrnt lowr s lttrs in th sm lin init signifint iffrn (P <.5) twn iffrnt trtmnts. Th vlus r mns ± SD of thr rplit smpls pr trtmnt. CK: hyroponi systms; EDTA-F: Hogln nutrint solution ontining.1 mm EDTA-F; SA: hyroponi systms n folir pplition of 1. mm SA; SNP: hyroponi systms n folir pplition of 2.5 mm SNP; SA+SNP: hyroponi systms n folir pplition of 1. mm SA n 2.5 mm SNP; 1/2(SA+SNP): hyroponi systms n folir pplition of.5 mm SA n 1.25 mm SNP. nzyms n th lvl of solul ntioxints (Ckmk n Mrshnr 1992; Guo t l. 27), ompni y n nhnmnt of lipi proxition (Shi n Zhu 28; Shi t l. 29). Dpning on its onntrtion, F fiiny n impir th ltron trnsport n my l to th proution of ROS (Grzino n Lmttin 25). Th ovrproution of ROS n l to oxitiv injury suh s mmrn lipi proxition, protin
11 Kong t l. Botnil Stuis 214, 55:9 Pg 11 of 12 oxition, nzym inhiition n DNA n RNA mg (Mittlr 22). In our xprimnts, F fiinyinu oxitiv strss in pnut plnts ws vint to th inrs MDA ontnt n th O 2 gnrtion rt (Tl 5). In norml physiologil onitions, ROS kps ynmi ln twn onstntly prou n lr. Howvr, th ln ws stroy n th proution of toxi oxygn rivtivs ws inrs s rsult of F fiiny strss. F fiiny inrs SOD tivity to onvrt th O 2 ril to th H 2 O 2. Howvr, it rs POD n CAT tivitis. POD n CAT r ll hm-ontining nzyms n thir tivitis r likly to fft y F fiiny. Thrfor, in th stuy, SA n/or SNP inrs tiv F ontnt (Tl 4) n lso inrs th tivitis of POD n CAT. SA n/or SNP trtmnt inrs th tivitis of ntioxint nzyms n ru th vrs fft of ROS on myls tivity unr F fiiny strss. Our finings init tht SA n SNP t s plnt growth rgultors tht n llvit oxitiv mg inu y F fiiny. Ths rsults r in grmnt with rnt rsrhs (Simi t l. 211). Folir pplition of xognous SA or SNP, it lso oul llvit th F fiiny inu hlorosis. Howvr, th ffts of SA+SNP wr ttr thn SA or SNP lon, or 1/2(SA+SNP). This my us SA+SNP m th onntrtion of SA n NO in th plnt oy hiv th st lvl, so s to onsirly llvit hlorosis inu y F fiiny. Conlusions Th prsnt work monstrts tht SA n SNP n llvit F fiiny-inu hlorosis sprtly or togthr. Aitionlly, th omintion of SA n SNP in llviting hlorosis is ttr thn SA or SNP lon, ut n pproprit onntrtion of SA n SNP ws n. Th mhnism of SA n/or SNP llviting F-fiiny inu hlorosis minly ontins: (1) promot F uptk, trnslotion n tivtion, (2) moult th ln of minrl lmnts, (3) prott F fiiny inu oxitiv strss. Our rsults my srv s n intgrt n optimiz mngmnt strtgy to llvit F fiiny in pnuts proution, ut furthr stuy is n. Arvitions C: Clium; Cr: Crotnois; CAT: Ctls; Chl: Chlorophyll; Cu: Coppr; FCR: F (III) -Chlt Ruts; F: Iron; Fo: Th miniml fluorsn; Fv/Fm: Mximl quntum yil of PS II; MDA: Mlonilhy; Mg: Mgnsium; Mn: Mngns; O 2 : Suproxi nion; Pn: Nt photosynthti; POD: Proxiss; ΦPSII: Th fftiv quntum yil of PS II; SNP: Soium nitroprussi; SA: Sliyli i; SOD: Suproxi ismuts; Tr: Trnspirtion rts; Zn: Zin. Compting intrsts Th uthors lr tht thy hv no ompting intrsts. Authors ontriutions KJ, XLL, LS n BXY r rsponsil for growth of th plnts, strss pplitions, smpling, physiologil n iohmil nlysis n t nlysis. DYJ KJ suppli ll lortory n hmil sustns us in this stuy oniv of th stuy. KJ sign th xprimnt n lso rft th mnusript. All uthors r n pprov th finl mnusript. Aknowlgmnts Th uthors thnk English Lturr Mr Sturt Crig MA (Engln, Tishn Univrsity of hin) n English lturr Xiujun Wng (Collg of Forign Lngugs, Shnong Agriulturl Univrsity) for thir ritil ring n rvision of th mnusript. W lso thnk Pingping Yng, Collg of Animl Sin n Thnology, Shnong Agriulturl Univrsity, Chin, for hr supplying instrumnts n ptint guin. Spil knowlgmnts r givn to th itors n rviwrs. This rsrh ws fun y Shnong Provinil Nturl Sin Fountion of Chin (ZR213CM3). Riv: 22 Sptmr 213 Apt: 7 Novmr 213 Pulish: 2 Jnury 214 Rfrns Brfor MM (1976) A rpi n snsitiv mtho for th quntifition of mirogrm quntitis of protin utilizing th prinipl of protin-y ining. Annu Rv Biohm 72: Briskin DP, Lonr RT, Hogs TK (1987) Isoltion of th plsm mmrn: mrkrs n gnrl prinipls. Mtho Enzymol 148: , oi:1.116/ (87) Buhnn BB, Gruissm W, Jons RL (2) Biohmistry n Molulr Biology of Plnts. Amrin Soity of Plnt Physiologists, Rokvill, MD. ISBN Bush DS (1993) Rgultion of ytosoli lium in plnts. 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Plnt Cll 14: , oi:1.115/tp.1388 Yilirim E, Turn M, Guvn I (28) Efft of folir sliyli i pplitions on growth, hlorophyll n minrl ontnt of uumr (Cuumis stivus L.) grown unr slt strss. J Plnt Nutr 31: Zhng XW, Zhng M, Wng QH, Qiu XK, Hu GQ, Dong YJ (211) Efft of xognous nitri oxi on physiologil hrtristi of pnut unr ironfiint strss. J Plnt Nutr n Frt 17: , org/cn/strt/strt275.shtml Zhng XW, Dong YJ, Qiu XK, Hu GQ, Wng YH, Wng QH (212) Exognous nitri oxi llvits iron-fiiny hlorosis in pnut growing on lrous soil. Plnt Soil Environ 58: Zottini M, Cost A, Mihl RD, Ruzzn M, Crimi F, Shivo FL (27) Sliyli i tivts nitri oxi synthsis in Ariopsis. J Exp Bot 58: , oi:1.193/jx/rm1 Zuo YM, Zhng FS, Li XL, Co YP (2) Stuis on th improvmnt in iron nutrition of pnut y intrropping with miz on lrous soil. Plnt Soil 22:13 25, oi:1.123/a: oi:1.1186/ Cit this rtil s: Kong t l.: Effts of folir pplition of sliyli i n nitri oxi in llviting iron fiiny inu hlorosis of Arhis hypog L.. Botnil Stuis :9.
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