Growth, gas exchange and function of antioxidant defense system in two contrasting rice genotypes under Zn and Fe deficiency and hypoxia
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- Rodney Hines
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1 Volume 52(2): , 28 At Biologi Szegedieis Artile Growth, gs exhnge nd funtion of ntioxidnt defee system in two ontrsting rie genotypes under Zn nd Fe defiieny nd hypoxi Roghieh Hjiolnd, Niere Beirmzdeh Plnt Siene Deprtment, University of Triz, Triz, Irn ABSTRACT For study of underlying physiologil mehnisms for genotypi differenes in tolerne to Zn nd Fe defiieny nd hypoxi, two ontrsting rie genotypes (Oryz stiv L. v. nd Dshti) were studied in nutrient solution with or without ertion. Growth of the lowlnd genotype () ws signifintly improved in nutrient solution without ertion, the opposite ws oserved for uplnd genotype (Dshti). Tolerne of to low Zn ws higher thn Dshti, in ontrst the former genotype ws more suseptile to Fe defiieny. Photohemistry of leves ws ffeted strongly y Fe ut not Zn defiieny. Low supply of Zn nd Fe impired photosyntheti pity of plnts minly vi stomtl limittion nd the mount of redution in net ssimiltion rte orrelted well with differentil growth redution under Zn nd Fe defiieny stress. Under hypoxi, plnts hd lower stomtl ondutne nd trpirtion rte leding to improved photosyntheti wter use effiieny. Ativity of sorte peroxidse (APX) nd guiol peroxidse (POD) indued y low Zn supply, ut low Fe used redution of APX, CAT nd POD. Ativity of SOD deresed in low Zn plnts, ut inresed in plnts suffered from Fe defiieny. Inresed APX tivity in respoe to hypoxi onditio in ws ssoited with higher tolerne in this genotype, in ontrst POD tivity only monitored stress onditio without ny proteting role. A lose orreltion ws oserved etween umultion of nd differentil seitivity of genotypes to hypoxi. At Biol Szeged 52(2): (28) Key Words hlorophyll fluoresene lowlnd rie photosynthesis retive oxygen speies (ROS) uplnd rie Rie ulture is divided into two rod groups, uplnd nd lowlnd ulture. Uplnd rie refers to rie grown on oth flt nd sloping fields tht re prepred nd seeded under drylnd onditio nd relies entirely on rinfll or irrigtion depending on the mount of preipittion. Flooded rie, known lso s lowlnd or wterlogged rie, is grown on fltlnd in flooded soils (Fgeri et l. 1997). In sumerged or flooded soils, limited oxygen vilility nd ltered hemil retio tht involve in the nutrients vilility e.g. Zn nd Fe for plnts, retes onditio mrkedly different from those of drined soils. Beuse of wter otrints, rie prodution is now in trition from the trditionl high wter ouming lowlnd rie ultivtion on flooded fields to new ultivtion system of eroi rie (Go et l. 25). Aeroi rie is grown s dry field rop in irrigted ut non-flooded soils (Boumn et l. 25). Zin defiieny ws reported for oth uplnd (Fgeri et l. 1997; Fgeri nd Bligr 25) nd lowlnd rie (Yng et l. 1994; Hjiolnd et l. 23), however, Fe defiieny is ommon disorder of rie growing on well drined (eroi) soils (Nerkr et l. 1984), whether these re neutrl, lreous or lkline. Aepted Nov 17, 28 Corresponding uthor. E-mil: ehsn@trizu..ir Hypoxi nd noxi onditio mintin trition metl io in more or less redued stte nd indue formtion of retive oxygen speies (ROS). The sme onditio n rise within sumerged plnts (Hendry nd Broklenk 1985). Therefore, hypoxi survivl my depend on the pity of plnt tissues to ounterttk retive oxygen speies nd limit dmges. One of the primry effets of these moleulr speies in ells is the peroxidtion of memrnes forming toxi produts suh s mlondildehyde (MDA; Kppus 1985). Plnts hve evolved vrious protetive mehnisms to eliminte or redue ROS. Enzymti ntioxidnt system, whih is one of the protetive mehnisms inluding superoxide dismutse (SOD) re loted in vrious ell omprtments nd tlyse the disproportion of two rdils to H 2 nd (Slin 1987). H 2 is eliminted y vrious ntioxidnt enzymes suh s tlse (CAT) nd peroxidses (POD) onverting H 2 to wter (Slin 1987). Asorte peroxidse (APX) elimintes peroxides y onverting sori id to dehydrosorte (Asd 1992). Asorte peroxidse nd glutthione redutse (GR) re importnt omponents of the sorte-glutthione yle respoile for the removl of H 2 in different ellulr omprtments (Jiménez et l. 1997). 283
2 Hjiolnd, Beirmzdeh Ativity of enzymes ontining Zn or Fe s tlyti or struturl omponent is expeted to e hnged sustntilly in plnts supplied with indequte mounts of these nutrients. Among enzymes of ntioxidnt defee system, SOD onti Zn (Cu/Zn SOD isozyme) or iron (Fe-SOD isozyme in hloroplsts); iron ontriutes lso s heme group in the struture of H 2 svenging enzymes inluding APX, POD nd CAT (Mrshner 1995). Therefore, plnt growth under indequte nutrients supply my e influened per se y redution in the pity of ntioxidnt defee system. Chnges in hlorophyll fluoresene emissio re inditio of hnges in photosyntheti tivity nd the stte of Photosystem II (Mxwell nd Johon 2). The flow of eletro through PSII is inditive of the overll rte of photosynthesis nd is n estimtion of photosyntheti performne. It is plusile tht not only low supply of Fe euse of its involvement in eletron trport nd hlorophyll synthesis ut lso of Zn onerning its role for mintenne of integrity of memrnes nd protetion of lipids nd protei git oxidtive dmge (Mrshner 1995), my ffet the photohemistry of leves nd inhiit iophysil proesses of photosynthesis. Due to predominne of polyuturted ftty ids in thylkoid lipids (Gounries et l. 1986), photosyntheti memrnes in hloroplsts ould e oidered the most suseptile strutures in plnts grown under onditio of oxidtive stresses. Wter vilility differs gretly under flooded ompred with non-flooded onditio. Therefore, plnt strtegies for wter eonomy my e hnged in trition from flooded to eroi onditio, nd every hnge vi modifition of stomtl ondutne ffets in turn photosyntheti C fixtion. Reent studies showed tht the wter produtivity (rop yield/wter oumptively used in evpotrpirtion) of rie under eroi onditio is 32-88% higher thn tht under flooded onditio (Boumn et l. 25). In Irn, rie is the seond importnt food rop fter whet nd is ultivted minly under flooded onditio in the north of the ountry. In south nd entrl Irn, however, inresing wter srity prolem uses reltively long term non-sumerged onditio during irrigtion intervls in the field. Genotypes seleted for higher tolerne to lternte sumerged nd non-sumerged onditio, re now eing used for uplnd ultivtion. It is expeted tht, genotypes dpted nd red for one of these ultivtion systems, hve different tolerne to Zn nd Fe defiieny nd prtiulrly hypoxi. Currently, eroi rie vrieties re developed y rossing lowlnd with uplnd vrieties (Boumn et l. 25). Physiologil sis of differenes etween trditionl lowlnd genotypes with new genotypes with lower suseptiility to non-flooded onditio nd its oequenes for nutrients defiieny tolerne is not known. Understnding the physiologil mehnisms my filitte future reeding progrms. One ojetive of the present work ws to evlute the funtionl signifine of ntioxidnt defee pity of plnts in dpttion to Zn nd Fe defiieny in omintion with flooded onditio. Two ontrsting rie genotypes used in this work, differed in tolerne to Zn nd Fe defiieny nd hypoxi. An ttempt ws lso mde to determine tht up to wht extent photosynthesis nd relted hrteristis re ssoited with the tolerne to Zn nd Fe defiieny nd hypoxi. Mterils nd Methods Two genotypes of rie (Oryz stiv L.) were used in this work, one genotype () ws hosen from north of Irn nd nother (Gsrol-Dshti) from south of the ountry euse of their dpttion to their own lol ulture onditio. Seeds were provided y Rie Reserh Center (Rsht, Guiln Provine, Irn) nd Agriulturl Reserh Center (Shirz, Frs Provine, Irn) for nd Dshti genotypes respetively. Plnts ulture nd tretments The experiments were onduted in growth hmer with temperture regime of 25 /18 C dy/night, 14/1 h light/ drk period nd reltive humidity of 7/8% under photon flux deity of 35-4 µmol m -2 s -1. Germintion of seeds nd plnts pre-ulture were performed s desried previously (Hjiolnd nd Slehi 26). Zin experiments Conventionl nutrient solution (Yoshid et l. 1972) ws used for pre-ulture of plnts with Zn onentrtion of.5 µm (dequte Zn, ontrol) nd <.8 µm (low). In the following growth period, it ws neessry to use heltor-uffered nutrient solution tehnique (Yng et l. 1994) for elimintion of Zn ontmintio nd prodution of Zn defiient plnts. Thus, sixteen-dy-old plnts were trferred to heltoruffered nutrient solution oisted of two levels of dded ZnSO 4 t 2. µm whih equls 12 pm free Zn 2+ tivity ( Zn) or 2 µm equls 13 pm free Zn 2+ tivity (+Zn). Fe experiments Plnts were grown in the onventionl rie nutrient solution either in pre-ulture or min experiment. Fe onentrtion in the pre-ulture medium ws 1 µm (dequte Fe) or 1 µm (low) nd in the min experiment ws 1 µm (dequte Fe, +Fe) or zero ( Fe). Plnts were grown for 21 dys nd nutrient solutio were ompletely hnged every 7 dys nd ph ws djusted every dy. Hypoxi tretments For omprison of growth of plnts under hypoxi nd eroi onditio, plnts were ultivted simultneous in erted 284
3 Zn nd Fe defiieny nd hypoxi in rie nd non-erted nutrient solutio during pre-ulture s well s tretment. Nutrient solutio were ompletely hnged every 7 dys nd ph ws djusted every dy. Hrvest After wshing using doule-distilled wter, plnts were divided into shoots nd roots, weighed nd lotted dry on filter pper nd dried t 7 C for 2 dys to determine plnt dry weight. Another group of plnts ws used for determintion of root length (Tennnt 1975) nd hlorophyll (Morn 1982). The third group of plnts ws used for mesurement of gs exhnge prmeters, hlorophyll fluoresene nd determintion of enzymes tivity nd onentrtion of metolites. Determintion of gs exhnge prmeters C ssimiltion nd trpirtion rtes of tthed leves were mesured with lirted portle gs exhnge system (LCA-4, ADC Biosientifi Ltd., UK) lwys etween 9: A.M. nd 13: P.M. with the exeption of PPFD (4-42 µmol m -2 s -1 ), no miroenvironmentl vrile iide the hmer ws ontrolled. The net photosynthesis rte y unit of lef re (A), trpirtion rte (E), stomtl ondutne to wter vpor (g s ), tmospheri C molr frtion (Ci/C) nd photosyntheti wter use effiieny (WUE=A/E) were determined Determintion of hlorophyll fluoresene Chlorophyll fluoresene prmeters were reorded in prllel for gs exhnge mesurements in the sme lef, using portle fluorometer (FIM, ADC Biosientifi Ltd., UK). Leves were limted to drk for 3 min efore mesurements were tken. Initil (F ), mximum (F m ), vrile (F v =F m -F ) s well s F v :F m nd F v :F rtios were reorded. Gs exhnge nd hlorophyll fluoresene mesurements were rried out using four independent replitio s seprte pots, in eh pot four mture, fully expnded nd tthed leves used for mesurements. Averge of dt from eh pot ws otined nd the men of four pots per tretment were sujeted to sttistil nlysis. Determintion of enzyme tivities nd onentrtion of oxidnts, totl mino ids nd protein Fresh lef smples were ground in the presene of liquid nitrogen using mortr nd pestle. Eh enzyme ssy ws tested for linerity etween the volume of rude extrt nd the mesured tivity. All mesurements were undertken using spetrophotometer (Speord 2, Anlytil Jen, Germny) ording to optimized protools desried elsewhere (Hjiolnd nd Hsni 27). The tivity of sorte peroxidse (APX, EC ) ws mesured y determining sori id oxidtion, one unit of APX oxidizes sori id t rte of 1 µmol min -1 t 25 C. Ctlse (CAT, EC ) tivity ws ssyed y monitoring the derese in sorne of H 2 t 24 nm, unit tivity ws tken s the mount of enzyme, whih deomposes 1 µmol of H 2 in one min. Peroxidse (POD, EC ) tivity ws ssyed using the guiol test, the enzyme unit ws lulted s enzyme protein required for the formtion of 1 µmol tetrguiol for 1 min. Totl superoxide dismutse (SOD, EC ) tivity ws determined using monoformzn formtion test. One unit of SOD ws defined s the mount of enzyme required to indue 5% inhiition of NBT redution s mesured t 56 nm, ompred with ontrol smples without enzyme liquot. The tivity of glutthione redutse (GR, EC ) ws ssyed y following the oxidtion of NADPH t 34 nm, one unit of enzyme tivity ws lulted s enzyme protein required for oxidtion of one µmol NADPH in 1 min. Solule protei were determined using ommeril Brdford regent (Sigm) nd BSA (Merk) s stndrd. Content of totl free α-mino ids ws ssyed using ninhydrin olorimetri method t 57 nm, glyine ws used for prodution of stndrd urve. The onentrtion of H 2 ws determined using potssium titnium-oxlte t 58 nm. Lipid peroxidtion ws estimted from the mount of mlondildehyde (MDA) formed in retion mixture ontining thiorituri id (Sigm) t 532 nm. MDA levels were lulted from 1,1,3,3-tetrethoxypropne (Sigm) stndrd urve. The ssy of NADPH-dependent genertion ws rried out y mesuring the rte of SOD-inhiitle NBT redution t 25 C. Experiments were undertken in omplete rndomized lok design with 4 replitio. Sttistil nlyses inluding one-wy ANOVA (Tukey test) nd Person Correltion Test were rried out using Sigm Stt (3.2) t p<.5. Results Zin defiieny used signifint redution of shoot nd root growth, however, genotypes differed mrkedly in tolerne to low Zn supply. Shoot growth of ws redued y out 38%, while tht of Dshti ws inhiited up to 67%. Similr differentil respoe of genotypes to low Zn stress ws oserved in root dry weight nd length (Fig. 1). In ontrst to high tolerne to low Zn supply, ws muh more suseptile to Fe defiieny thn Dshti. Growth redution of due to Fe defiieny ws 69% nd 67% for shoot of erted nd non-erted plnts respetively. The orresponding vlues for Dshti were only 52% nd 55% under erted nd non-erted onditio (Fig. 2). Hypoxi onditio influened plnts growth depending on tested genotypes. In Zn nd Fe suffiient plnts, growth of ws stimulted up to 26% nd 53% when grown 285
4 Hjiolnd, Beirmzdeh 2 A erted U nerted A erted U nerted 1 5 A mo l D s hti Root lenght Root DW Shoot DW 1 Shoot DW Root DW Root Length 1 d d d d + Zn Zn T re tm e nts + Zn Zn T re tme nts Figure 1. Effet of Zn defiieny on shoot nd root dry weight (mg plnt -1 ) nd root length (m plnt -1 ) of two ontrsting rie (Oryz stiv L. vs. nd Dshti) genotypes grown under erted or non-erted onditio. Eh vlue is the men of 4 repetitio ± SD. in non-erted nutrient solution ompred with ertion tretment in Zn nd Fe experiment respetively. In ontrst, Dshti showed higher root nd shoot growth in erted tretment, shoot iomss redution due to growth in non-erted nutrient solution ws 21% nd 33% in Zn nd Fe experiment respetively. The sme tendeny ws oserved for Zn nd Fe defiient plnts (Figs. 1, 2). Zin defiieny did not ffet the sum of hlorophyll nd ontent (hlorophyll +) in, ut deresed it in Dshti prtiulrly in non-erted plnts. Hypoxi onditio used slight inrese of hlorophyll + mounts in oth genotypes. F v nd F v /F rtios were not ffeted either y Zn defiieny or ertion tretments (Tle 1). Zin defiient plnts showed signifintly lower net photosynthesis rte (A). Redution of A ws higher in Dshti (65-74%) thn in (47-54%). Hypoxi onditio did not ffet A in oth tested genotypes. Redution of A ws ssoited y gret redution of stomtl ondutne (g s ). In ddition of net photosynthesis rte, trpirtion (E) ws lso ffeted negtively y low Zn supply, redution of E y 286
5 Zn nd Fe defiieny nd hypoxi in rie Root lenght Root DW Shoot DW Shoot 5 DW 3 2 Root 1DW Root 2 Length A erted U nerted A m o l A erted U nerted D s hti d 1 + F e F e T re tme nts + F e F e T re tm e nts Figure 2. Effet of Fe defiieny on shoot nd root dry weight (mg plnt -1 ) nd root length (m plnt -1 ) of two ontrsting rie (Oryz stiv L. vs. nd Dshti) genotypes grown under erted or non-erted onditio. Eh vlue is the men of 4 repetitio ± SD. low Zn ws higher in Dshti (67-69%) thn (43-52%). As the oequene of lower stomtl ondutne, the Ci/ C rtio inresed in Zn defiient plnts. Wter use effiieny (WUE) ws diminished y oth low Zn supply nd ertion of nutrient solution (Tle 1). As expeted, the mount of hlorophyll + in leves deresed drmtilly in Fe defiient plnts nd in ontrst to the effet of Zn defiieny, F v rtio ws signifintly redued y low supply of Fe. Redution of optiml quntum effiieny of PSII in drk-dpted hloroplsts (F v rtio) due to Fe defiieny ws greter in (34-17%) thn Dshti (24-8%). Moreover, in Fe defiient plnts, the F v rtio ws signifintly ffeted y hypoxi onditio e.g. deresed up to 21% nd 18% in nd Dshti respetively. The rtio of F v /F deresed with low Fe supply in oth tested genotypes. The redution ws more pronouned in erted (62-61% in nd Dshti respetively) thn non-erted (46-3% in nd Dshti respetively) plnts (Tle 2). Similr with Zn defiieny, Fe defiieny onditio ffeted lso negtively net photosynthesis rte, redution ws greter in (74-81%) thn Dshti (65-7%). Trpirtion rte ws lso redued y Fe defiieny, more in (53%) thn Dshti (26-33%). In ordne with the dt of net photosynthesis nd trpirtion rte, stomtl on- 287
6 Hjiolnd, Beirmzdeh Tle 1. Chlorophyll (+) onentrtion (mg g -1 FW), hlorophyll fluoresene nd gs exhnge prmeters inluding net photosyntheti rte (A), trpirtion (E), the rtio of interellulr ir spe nd tmospheri C molr frtio (Ci/C), stomtl ondutne to wter vpor (gs) nd itntneous wter use effiieny (WUE) in two ontrsting rie genotypes (Oryz stiv L. vs. nd Dshti) treted either with dequte or low levels of Zn under erted or non-erted onditio. The me refer to 4 repetitio ± SD. Dt within eh genotype followed y the sme letter re not signifintly different (P<.5). Dshti Aerted Non-erted Aerted Non-erted Chlorophyll (+) +Zn 2.96± ± ± ±.59 Zn 1.81± ± ± ±.23 Fv/Fm +Zn.788±.2.794±.5.8±.4.82±.4 Zn.792±.6.797±.1.86±.1.87±.4 Fv/F +Zn 3.73± ± ± ±.24 Zn 4.84± ± ± ±.11 A (µmol m -2 s -1 ) E (mmol m -2 s -1 ) g s (mol m -2 s -1 ) +Zn 1.12± ± ± ±.1 Zn.59±.1.6±.6.56±.9.39±.9 +Zn.64±.18.48±.6.83±.6.73±.12 Zn.36±.13.23±.2.26±.4.24±.7 +Zn 12.67± ± ± ±4.16 Zn 2.± ±.1 4.2±.1 2.±.2 Ci/C +Zn.548± ± ± ±.31 Zn.75± ± ± ±.39 WUE (µmol mol -1 ) +Zn 1.81± ± ± ±.23 Zn 1.63± ± ± ±.6 Tle 2. Chlorophyll (+) onentrtion (mg g -1 FW), hlorophyll fluoresene nd gs exhnge prmeters inluding net photosyntheti rte (A), trpirtion (E), the rtio of interellulr ir spe nd tmospheri C molr frtio (Ci/C), stomtl ondutne to wter vpor (gs) nd itntneous wter use effiieny (WUE) in two ontrsting rie genotypes (Oryz stiv L. vs. nd Dshti) treted either with dequte or low levels of Fe under erted or non-erted onditio. The me refer to 4 repetitio ± SD. Dt within eh genotype followed y the sme letter re not signifintly different (P<.5). Dshti Aerted Non-erted Aerted Non-erted Chlorophyll (+) +Fe 1.84±.1 3.3± ± ±.53 Fe.7±. d.25±.7.15±.5.39±.17 Fv/Fm +Fe.785±.4.791±.1.81±.6.85±.3 Fe.518±.1.653±.11.68± ±.4 Fv/F +Fe 3.64±.6 3.8± ± ±.7 Fe 1.38±.7 d 2.4± ± ±.18 A (µmol m -2 s -1 ) E (mmol m -2 s -1 ) g s (mol m -2 s -1 ) +Fe.93±.2.94± ±.26.89±.24 Fe.18±.3.24±.8.34±.13.31±.5 +Fe.51±.9.4±.6.61±.1.63±.14 Fe.24±.11.19±.1.45±.13.42±.19 +Fe 6.67± ±.55 1.± ±2.43 Fe 1.±.1 1.8±. 5.33± ±.76 Ci/C +Fe.557± ± ±.13.54±.14 Fe 1.89± ± ± ±.23 WUE (µmol mol -1 ) +Fe 1.82± ± ± ±.64 Fe.89± ±.44.62±.1.73±.12 dutne ws strongly inhiited y Fe defiieny, nd more redution ws oserved in (85-97%) ompred with Dshti (48-65%). Wter use effiieny (WUE) deresed in Fe defiient plnts with no ovious genotypi differene, moreover, slight redution of WUE ws oserved in erted plnts (Tle 2). A signifint inrese in the speifi tivity of APX ws oserved in roots of non-erted plnts y low Zn supply tht rehed up to 46% nd 65% in nd Dshti respetively. This inrese in shoot ws in tendeny nd oserved only in. On the other hnd, APX tivity inresed in Zn defiient plnts y hypoxi tretment, whih ws signifint 288
7 Zn nd Fe defiieny nd hypoxi in rie Tle 3. Effet of Zn defiieny on the speifi tivity of sorte peroxidse (APX), tlse (CAT), peroxidse (POD), superoxide dismutse (SOD) nd glutthione redutse (GR) in two genotypes of rie (Oryz stive L. vs. nd Dshti) grown in erted or non-erted nutrient solution. Dt in eh olumn within eh genotype followed y the sme letter re not signifintly different (P<.5). APX CAT POD SOD GR Genotypes Tretments nmol H 2 µmol H 2 µmol Guiol Unit mg -1 protein nmol NADPH Shoot Dshti Dshti Aer. +Zn 42.6± ±.62.13± ± ±.6 Zn 51.5± ±.52.18± ± ±2.6 Uner. +Zn 45.3± ±.72.13± ± ±.8 Zn 67.8± ±.64.19± ± ±1.7 Aer. +Zn 52.1± ±.37.14± ± ±1.8 Zn 47.2± ±.78.18± ±1. 7.9±1.5 Uner. +Zn 49.2± ±.4.15± ± ±.8 Zn 4.1± ±.52.39± ± ±.7 Root Aer. +Zn 46.3± ± ± ± ±3.9 Zn 58.2± ± ± ± ±3.9 Uner. +Zn 53.3± ± ± ± ±.7 Zn 88.2± ± ± ± ±1.4 Aer. +Zn 26.± ±.6.6± ± ±.5 Zn 34.9± ±.6.54± ± ±1.4 Uner. +Zn 27.9± ±.17.64± ± ±1.4 Zn 4.7± ± ± ± ±1.6 in roots (52%) ut in tendeny in shoot. Ativity of CAT did not respond either to low Zn stress or ertion tretment. In ontrst, tivity of POD responded to oth Zn nd ertion tretments in shoot nd root. Zn defiieny indued tivity of POD (with the exeption of erted Dshti) up to 46% nd 16% for shoot nd 75% nd 81% for roots of non-erted nd Dshti, respetively. As expeted, Zn defiieny used redution of SOD tivity in oth shoot nd root irrespetive to ertion tretment. The most ovious respoe ws deteted in Dshti with up to 53% nd 6% redution of SOD tivity under erted nd non-erted onditio, respetively. Ativity of GR did not respond to low Zn supply nd hypoxi, with the exeption of Dshti, in whih ertion used signifint redution of GR tivity up to 48% in shoot (Tle 3). A oistent, though non signifint redution of APX tivity ws oserved due to Fe strvtion in oth genotypes. As expeted, tivity of CAT deresed strongly y low Fe supply; oidering reltive mounts of redution (% over ontrol), inhiition of CAT tivity ws minly higher in thn Dshti nd in erted thn non-erted plnts. Similr with CAT, POD tivity ws lso inhiited y low Fe supply. In ontrst, tivity of SOD inresed in shoot nd roots of Fe defiient plnts ompred with ontrol, this effet ws more prominent in thn Dshti. Ativity of GR inresed in Fe defiient plnts, whih ws minly in tendeny nd non signifint (Tle 4). Conentrtion of H 2 responded to Zn defiieny in shoot nd root. In shoot, Zn defiieny used redution in onentrtion of H 2, ut in roots n inrese of H 2 onentrtion ws oserved. Aertion used higher umultion of H 2, signifintly or in tendeny. Superoxide rdils ( ) umulted in Zn defiient plnts in oth genotypes, however, ertion tretments hd different effet on onentrtion depending on genotype. In, ertion used n inrese of onentrtion in oth Fe suffiient nd defiient plnts, in ontrst, in Dshti n umultion of ws oserved in plnts grown under hypoxi onditio. Conentrtion of MDA inresed in respoe to Zn defiieny. Similr with, ertion showed differentil effet on MDA onentrtion, e.g. redution in nd inrese in Dshti under hypoxi (Tle 5). Conentrtion of H 2 inresed y low Fe supply in root, however, the opposite ws oserved for shoot, its onentrtion ws lower in Fe defiient ompred with ontrol plnts. Conentrtion of inresed y low Fe supply, moreover, MDA onentrtion inresed signifintly or in tendeny in Fe defiient plnts (Tle 6). Zin defiieny used redution of protein onentrtion in oth shoot nd root nd in oth genotypes. In this respet, two tested genotypes did not differ in their respoe to Zn defiieny. In ordne with the results of protein onentrtion, free mino ids umulted signifintly or in tendeny in oth shoot nd root of low Zn plnts (Tle 5). 289
8 Hjiolnd, Beirmzdeh Tle 4. Effet of Fe defiieny on the speifi tivity of sorte peroxidse (APX), tlse (CAT), peroxidse (POD), superoxide dismutse (SOD) nd glutthione redutse (GR) in two genotypes of rie (Oryz stive L. vs. nd Dshti) grown in erted or non-erted nutrient solution. Dt in eh olumn within eh genotype followed y the sme letter re not signifintly different (P<.5). APX CAT POD SOD GR Genotypes Tretments nmol H 2 µmol H 2 µmol Guiol Unit mg -1 protein nmol NADPH Shoot Dshti Dshti Aer. +Fe 46.5± ±.14.11± ± ±2.9 Fe 4.9± ±.6.8± ± ±.6 Uner. +Fe 48.1± ±.43.14± ± ±.7 Fe 23.6± ±.18.9± ± ±.9 Aer. +Fe 46.4± ±.67.17± ± ±.9 Fe 3.5± ±.2.12± ± ±1.5 Uner. +Fe 39.2± ±.48.19± ± ±.4 Fe 21.6± ±.5.15± ± ±.6 Root Aer. +Fe 46.9± ± ± ± ±.7 Fe 45.3±5.7.36±.5.72± ± ±.9 Uner. +Fe 6.2±7.4.82±.9 1.7± ± ±1.1 Fe 52.7±3.8.38±.5.81± ± ±2.2 Aer. +Fe 3.9± ±.5.44± ± ±.8 Fe 25.4±7.1.22±.2 d.31± ± ±3.5 Uner. +Fe 42.3± ±.11.47± ± ±1.6 Fe 35.3±3.9.68±.9.35± ± ±.1 Similr with Zn, Fe defiieny used redution of protein onentrtion nd inrese in totl mino ids onentrtion, the ltter hnge ws minly in tendeny (Tle 6). Disussion A distint genotypi differene ws oserved in plnts respoe to hypoxi onditio. Dry mtter prodution of the lowlnd genotype () ws signifintly improved in nutrient solution without ertion, the opposite ws oserved for flooding seitive genotype (Dshti). Root length ws lso ffeted y ertion tretments differently. Differentil respoe of root length to hypoxi my hve importnt oequenes for nutrients quisition of plnts grown in soils with different oxygen vilility. Zin defiieny tolerne of ws greter thn Dshti. hs een hrterized s n extremely Zneffiient genotype in our previous work (Hjiolnd nd Slehi 26). Our experiment demotrted lso tht, there is no diret reltiohip etween tolerne to flooding nd Zn defiieny in Irnin rie genotypes (Hjiolnd nd Slehi 26). In ontrst, suseptiility to Fe defiieny ws oviously relted to flooding respoe in tested genotypes in this work s judged y iomss nd hlorophyll ontent. Co-ourrene of flooding nd high ville Fe in soils is likely the use of this reltiohip. Flooding uses the soil to eome neroi with low redox potentil leding to high nd proly ner toxi Fe 2+ vilility. Therefore, lowlnd rie genotypes hve developed in n edphi environment, in whih there is no need for soring Fe with high effiieny tht in turn hs een led to higher suseptiility to Fe defiieny. In ontrst, drined soils prtiulrly lreous ones re defiient in ville Fe. Aordingly, Fe defiieny tolerne hs een developed during seletion nd improvement of uplnd genotype. Zin defiieny did not ffet strongly photohemistry of leves, suggesting tht though prodution of more tive oxygen speies in Zn defiient plnts in this work, thylkoid otituents hs not een dmged seriously. It ws suggested tht, for nutrients without diret involvement in the eletron trport or hlorophyll synthesis suh s Zn, lose linkge etween nutritionl sttus of leves nd spetrl hrteristis seems unlikely (Adms et l. 2). However, there re reports on signifint redution of mximum quntum effiieny of PSII (Wng nd Jin 25) nd severe dmge to the ultrstruture of hloroplsts (Chen et l. 27) in plnts sujeted to indequte Zn supply. It is likely tht, the severity nd/or durtion of Zn defiieny stress in our experiment were not enough for indution of serious dmge to photosyntheti memrnes nd disturne in the photohemistry of leves. In ontrst, Fe defiieny depressed strongly mximl quntum effiieny of PSII (F v ). Redution in F v ws due to oth derese in the eletron trport hin (redution of F m ) nd prtiulrly due to struturl modifitio of PSII minly t the pigment level (inrese in F ). The negtive effet of Fe defiieny for oth rie genotypes foused minly 29
9 Zn nd Fe defiieny nd hypoxi in rie Tle 5. Effet of Zn defiieny on the onentrtion of protein (mg g -1 FW), totl free -mino ids (TAA), hydrogen peroxide (H 2 ), superoxide rdils ( ) nd mlondildehyde (MDA) in two genotypes of rie (Oryz stive L. vs. nd Dshti) grown in erted or non-erted nutrient solution. Dt in eh olumn within eh genotype followed y the sme letter re not signifintly different (P<.5). H 2 MDA Protein TAA Genotypes Tretments nmol g -1 FW nmol g -1 FW µmol g -1 FW mg g -1 FW mmol g -1 FW Dshti Dshti Shoot Aer. +Zn 135±176 nd 1.49± ± ±33 Zn 934±211 nd 2.74± ± ±23 Uner. +Zn 1289±56 nd 1.5± ±2.3 28±2 d Zn 1167±11 nd 1.32± ± ±11 Aer. +Zn 1748±166 nd 3.24± ± ±82 Zn 669±36 nd 5.1± ± ±31 Uner. +Zn 177±38 nd 4.34± ± ±3 Zn 843±116 nd 6.1± ± ±29 Root Aer. +Zn 2.8± ±23.98± ± ±2.4 Zn 4.5± ±3 1.4± ± ±1.9 Uner. +Zn 6.5±1.7 18±19 d.52± ± ±2.2 Zn 18.5± ±8.83± ± ±2.7 Aer. +Zn 18.8± ± ± ± ±4.3 Zn 3.± ± ± ± ±1.3 Uner. +Zn 17.6± ± ± ± ±3.1 Zn 42.2± ± ± ± ±2.5 Tle 6. Effet of Fe defiieny on the onentrtion of protein (mg g -1 FW), totl free -mino ids (TAA), hydrogen peroxide (H 2 ), superoxide rdils ( ) nd mlondildehyde (MDA) in two genotypes of rie (Oryz stive L. vs. nd Dshti) grown in erted or non-erted nutrient solution. Dt in eh olumn within eh genotype followed y the sme letter re not signifintly different (P<.5). H 2 MDA Protein TAA Genotypes Tretments nmol g -1 FW nmol g -1 FW µmol g -1 FW mg g -1 FW mmol g -1 FW Dshti Dshti Shoot Aer. +Fe 1853±429 nd 1.22± ± ±17 Fe 424±19 nd 1.35± ±1.2 35±46 Uner. +Fe 1347±74 nd 1.6±.2 6.1± ±7 Fe 344±32 nd 1.34± ±.9 284±42 Aer. +Fe 1367±236 nd 4.41± ± ±23 Fe 367±38 nd 5.58± ± ±75 Uner. +Fe 1254±159 nd 5.62± ± ±3 Fe 215±69 nd 1.23± ± ±15 Root Aer. +Fe 45.9± ±2 2.13± ± ±1.5 Fe 59.5± ± ±. 13.2± ±2.6 Uner. +Fe 9.2± ± ± ± ±2.6 Fe 36.8±2. 464± ± ± ±3.3 Aer. +Fe 21.9±3.8 21±17 2.8± ± ±2.8 Fe 4.3± ± ± ± ±3.9 Uner. +Fe 19.5±.5 222± ± ± ±1.8 Fe 32.2± ± ± ± ±1.1 on the deresed proportion of tive hlorophyll ssoited with the retion enter of PSII (deresed F v /F ). Inrese in F ould e originted from inreses in the drk redution of the plstoquinone pool (Belkhodj et l. 1998) or from the intivtion of the ferredoxin, n eletron trmitter, due to hnges in its hemil struture. Aordingly, in Fe defiient plnts lose orreltion ws found etween the rte of net photosynthesis nd photohemil properties of leves (Tle 7), suggesting tht inhiited light retio in Fe defiient leves ontriutes signifintly in redution of C ssimil- 291
10 Hjiolnd, Beirmzdeh Tle 7. Correltion oeffiient etween plnts dry weight nd net photosynthesis rte, photohemil properties of leves, tivity of ntioxidnt enzymes nd onentrtion of oxidnts in two genotypes of rie (Oryz stive L. vs. nd Dshti) grown under different nutritionl sttus of Zn nd Fe. Shoot nd root dry weight dt nd the vlues for tivity of enzymes in these prts were sujeted to nlysis of their orreltion. For nlysis of orreltion etween photosyntheti prmeters nd plnts DW, dry weight of shoot (ut not root) ws regrded. Dt of two studied genotypes were omined. Coeffiients ove the dshed line refer to the Zn experiment nd those elow it to the Fe experiment. : non signifint, signifint t.5, signifint t.1. Plnt DW A.85 F v -.71 F v /F.73 APX.15 CAT.94 POD -.56 SOD.26 GR -.36 H MDA -.37 Plnt DW A F v F v /F APX CAT POD SOD GR H 2 MDA nd nd nd nd -.31 Ns nd.86 nd Ns tion. However, even in Fe defiient plnts the ontriution of stomtl losure in redution of net ssimiltion rte (85%) ws more pronouned thn tht of redution in quntum effiieny of PSII (34%). In ontrst, lower ssimiltion rte in low Zn plnts ws solely ttriutle to the stomtl limittion. Redution of stomtl ondutne due to low supply of Zn ws reported for other plnts suh s hikpe (Rengel et l. 24) nd mize (Wng nd Jin 25). Stomtl limittion ws lso oserved for Fe defiient plnts (Choulirs et l. 24; Molssiotis et l. 26). Aertion of nutrient solution redued stomtl ondutne in tendeny or signifintly nd in oth tested genotypes. Therefore, plnts grown under eroi onditio lost more wter vi trpirtion, leding to lower WUE. Chnge of wter mngement nd shift from flooded to eroi onditio in rie fields ws reommended euse of inresing wter srity in the world (Boumn et l. 25). Our results, however, showed tht rie plnts would hve use soil wter resoures more ineffiiently when grown in drined soils ompred with flooded fields. Derese in stomtl ondutne under flooded onditio hs een demotrted in mny woody speies of temperte nd tropil forest eosystems (Mielke et l. 23) nd ws ttriuted to derese in root hydruli ondutivity under soil neroi onditio leding to internl wter stress nd reduing lef turgor (Pezeshki 21) or prodution of sisi id (Zhng nd Zhng 1994). Very limited informtion is ville on the effet of flooding on stomtl ehvior in leves of soil grown rie plnts (Ishihr nd Sito 1987). However, field study showed tht the wter produtivity of rie under eroi onditio ws 32-88% higher thn under flooded onditio (Boumn et l. 25). In the lultion of wter produtivity the mount of evpotrpirtion is oidered (Kssm nd Smith 21), therefore, lower vlues for wter produtivity ould e the result of higher wter tle evportion in the flooded soils rther higher trpirtion y plnts. Nevertheless, our dt for nutrient solution grown plnts, in whih flooded onditio ws simulted y only one of severl ftors funtioning in sumerged soils, should e oidered only with gret utio. Ativity of two H 2 svenging enzymes, APX nd POD ws indued y low Zn supply. Indution of APX nd prtiulrly POD under the effet of defiieny of mro (Tewri et l. 27) or mironutrients (Cndn nd Trhn 23) ws frequently reported. In ontrst to the effet of Zn, Fe used redution of APX, CAT nd POD. Iron is one omponent of prostheti group of peroxidses, therefore redution of tivity of peroxidses in Fe defiient plnts is 292
11 Zn nd Fe defiieny nd hypoxi in rie expeted (Mrshner 1995). Ativity of CAT responded more strongly to Fe defiieny thn APX nd POD. In ddition, lose orreltion oserved etween tivity of CAT, net C ssimiltion nd mximum quntum effiieny of PSII in Fe defiient leves (Tle 7) further onfirms the relevne of using its tivity s n inditor of Fe nutritionl sttus of plnts (Mrshner 1995). Ativity of GR did not seem to e respoive to Fe or Zn defiieny nd GR seems to e not involved in ntioxidnt defee system of Zn nd Fe strved plnts. Glutthione redutse effet on protetion of plnts git stresses evoked y sulfur (Hjiolnd nd Amjd 27), nitrogen nd K (Tewri et l. 27) defiieny ws reported, likely euse of its effet on keeping redued GSH t given level. Greter APX tivity in under hypoxi onditio, whih ws ssoited with higher tolerne (rther growth improvement) suggests possile role for this enzyme in protetion of plnts git hypoxi. Chnge in the tivity of APX ws refleted in H 2 onentrtion in plnts, i.e. higher APX tivity in non-erted ws ssoited with lower umultion of H 2 in plnts; roots were more respoive thn shoot. Indution of APX tivity ws suggested to provide plnt roots with inresed tolerne to wterlogged stress (Lin et l. 24). Ativity of POD inresed in Dshti treted with hypoxi, this tretment used stress for plnts s judged y lower growth. In ddition, higher POD tivity in non-erted Dshti did not result in lower H 2 onentrtion. As it is ovious from orreltion oeffiient presented in Tle 7, there is rther negtive reltiohip etween POD tivity nd plnts growth, e.g. lower growth ws ompnied y higher tivity of POD. It implies tht, POD tivity only monitored stress onditio without ny proteting role. The upeifi POD tivity ssyed with guiol s universl sustrte n exhiit tivity of APX (ntioxidnt enzyme), oniferyl lohol peroxidse (lignifying enzyme), NADH oxidse nd IAA oxidse (growth limiting peroxidses). The individul tivity of these enzymes with the exeption of APX, were not distinguished from the solule pool in our extrtion proedure. On the other hnd, the funtionl signifine of peroxidses mesured y guiol test in the protetion of plnts git oxidtive stresses hs een questioned y mny uthors (Vn Asshe nd Clijsters 199; Choui et l. 1997; Cuypers et l. 2). Ativity of SOD deresed in low Zn plnts, whih ws ssoited with higher umultion of (r=-.6) nd MDA (r=-.51) s inditor of memrne dmge. Ativity of SOD ws suggested to e n inditor of Zn nutritionl sttus of plnts (Ckmk et l. 1997) nd is the first enzyme tivity known to e redued under low Zn stress. In ontrst, SOD tivity inresed in plnts suffered from Fe defiieny. Indution of SOD tivity y low Fe supply ws reported y other uthors (Molssiotis et l. 26) nd is ttriutle to prodution of more retive oxygen speies in Fe defiient plnts. Inrese in the umultion in Fe defiient plnts ws oserved though tivity of SOD did not redued or rther inresed (r=.78). In me tht, prodution of in Fe defiient plnts ws muh higher thn the pity of svenging enzymes. In ontrst, hnge in the tivity of SOD in Zn defiient plnts ws refleted well in the onentrtion of (r=-.6). In this work, respoes of plnts to low Zn nd Fe s well s hypoxi stress re minly ttriutle to the umultion of thn tht of H 2 or memrne dmge. Detrimentl effet of in omprison with H 2 ws well demotrted in negtive orreltion etween onentrtion of nd plnts dry weight (r=-.79). Suh orreltion for H 2 ws rther positive (r=.88-.9). It me tht like POD tivity, H 2 onentrtion hs no determinnt role in plnts growth respoe. Superoxide rdil is one of the most deleterious retive oxygen speies ttks memrnes nd indues peroxidtion of lipids (Kppus 1985). It ould e ssumed tht, tolerne to low Zn nd Fe s well s hypoxi is highly relted to the tivity of superoxide rdil svenging system nd prtiulrly to the onentrtion of rther to the H 2 or its svenging enzymes. The ility to mintin lne etween the formtion nd detoxifition of superoxide rdils ppered to inrese the plnts tolerne to low supply of tested nutrients s well s hypoxi. The importne of the superoxide svenging system for mintining the struturl stility of suellulr plnt orgnelles, integrity of ell memrnes nd protetion of protei, DNA nd hlorophyll nd deleterious effets of superoxide nion in ellulr metolism (Fridovih 1995) provide good reson for this onlusion. Referenes Adms ML, Norvell WA, Philpot WD, Peverly JH (2) Spetrl detetion of mironutrient defiieny in Brgg soyen. Agron J 92: Asd K (1992) Asorte peroxidse- hydrogen peroxide-svenging enzyme in plnts. Physiol Plnt 85: Belkhodj R, Morles F, Quilez R, Lopez-Milln AF, Adi A, Adi J (1998) Iron defiieny uses hnges in hlorophyll fluoresene due to the redution in the drk of the Photosystem II eptor side. Photosynth Res 56: Boumn BAM, Peng S, Cstñed AR, Vispers RM (25) Yield nd wter use of tropil eroi rie systems in the Philippines. 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12 Hjiolnd, Beirmzdeh tosyntheti pity, 77K hlorophyll fluoresene nd hloroplst ultrstruture etween Zn-effiient nd Zn-ineffiient rie genotypes (Oryz stiv L.) under low Zn stress. Physiol Plnt 132: Choulirs V, Therios I, Molssitis A, Ptks A, Dimntidis G (24) Effet of iron defiieny on gs exhnge nd tlse nd peroxidse tivity in itrus. J Plnt Nutr 27: Cuypers A, Vngroveld J, Clijsters H (2) Biphsi effet of opper on the sorte-glutthione pthwy in primry leves of Phseolus vulgris L. seedlings during the erly stges of metl ssimiltion. Physiol Plnt 11: Fgeri NK, Bligr VC, Jones CA (1997) Growth nd Minerl Nutrition of Field Crops. 2 nd ed. Mrel Dekker, New York, USA. Fgeri NK, Bligr VC (25) Growth omponents nd zin reovery effiieny of uplnd rie genotypes. Pesq Agrope Brs 4: Fridovih I (1995) Superoxide rdil nd superoxide dismutses. Ann Rev Biohem 64: Go X, Zou C, Zhng F, Vn der Zee EATM, Hofflnd E (25) Tolerne to zin defiieny in rie orreltes with zin uptke nd trlotion. 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New Phytol. 11: Ishihr K, Sito K (1987) Diurnl ourses of photosynthesis trpirtion nd diffusive ondutne in the single-lef of the rie plnts grown in the pddy field under sumerged ondition. Jpn. J. Crop Si. 56:8 17. Jiménez A, Hernández JA, del Río LA, Sevill F (1997) Evidene for the presene of the sorte-glutthione yle in mitohondri nd peroxisomes of pe leves. Plnt Physiol. 114: Kppus H (1985) Lipid peroxidtion: mehnisms, nlysis, enzymology nd iologil relevne. In Sies H, ed., Oxidtive Stress. Ademi Press, London, Kssm A, Smith M (21) FAO methodologies on rop wter use nd rop wter produtivity. In Proeedings of Expert Meeting on Crop Wter Produtivity. Rome, Itli, Lin K-HR, Weng C-C, Lo H-F, Chen J-T (24) Study of the root ntioxidtive system of tomtoes nd eggplnts under wterlogged onditio. Plnt Si. 167: Mrshner H (1995) Minerl Nutrition of Higher Plnts. 2 nd ed. Ademi Press, UK. Mxwell K, Johon GN (2) Chlorophyll Fluoresene- A Prtil Guide. 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