Accumulation of metal ions in selected plants from Brassicaceae and Lamiaceae families
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1 Reserch rticle Biotechnology nd Food Sciences Accumultion of metl ions in selected plnts from Brssiccee nd Lmicee fmilies Agnieszk Szczodrowsk,* Kmil Kult, Bet Smolińsk, Jonn Leszczyńsk Institute of Generl Food Chemistry, Lodz University of Technology Wolcznsk 171/173, Lodz, Polnd Astrct: This pper exmines the ccumultion of metl ions from soil in selected edile plnts elonging to the Brssiccee nd Lmicee fmilies. The effect of metl ions on fctors, such s growth nd morphology re lso investigted. The results indicte tht the ddition of selected metl ions to the soil significntly increses the concentrtion of metl ions in the plnts. The ppliction of zinc ions significntly enhnces Zn uptke in Ocimum silicum nd Menth piperit (Lmicee fmily). Nickel ions significntly increse Ni ccumultion in Lepidium stivum (Brssicee fmily). The reserch shows tht nickel, zinc nd copper ccumulte in leves t different concentrtions depending on the plnt species. Keywords: metl ions, toxicity, ioconcentrtion fctor, Brssiccee fmily, Lmicee fmily. Introduction Hevy metls re currently mtter of serious environmentl concern. They re hrmful to humns nd nimls, nd tend to ioccumulte in the food chin. The thret tht hevy metls pose to humns is ggrvted y their long term persistence in the environment [1]. Metls re sored y the humn ody through the skin or respirtory system, or with food of niml or plnt origin. The min source of metl ions in plnts is their ssimiltion from soil. Soil hs generlly een the most common depository for wstes contining hevy metls. Soil cts like sponge s it ccumultes hevy metl ions [2]. Plnts ccumulte metls from soil to vrying degrees. The presence of toxic metl ions in soil cn ffect plnt growth. Higher concentrtions of metl ions in plnts cuse severl physiologicl nd iochemicl disorders, including reduced growth nd yield, less efficient nutrient uptke, chnges in chloroplst ultrstructure nd initition of oxidtive stress. In recent decdes, governments nd regultory uthorities hve mde it priority to prevent further hevy metls contmintion nd resultnt soil deteriortion, nd to implement possile methods of remedition [3]. Biotechnol Food Sci 2016, 80 (1), 29-42
2 30 Szczodrowsk et l. Zinc plys crucil role in plnt metolism. Both zinc deficiency nd excess zinc limit plnt growth nd development. Zinc deficiency is ssocited with zinc concentrtions elow 20 mg kg -1 of soil wheres zinc sorption is considered excessive ove concentrtions of mg kg -1. Zinc deficiency destilizes the metolism of proteins, phosphtes, crohydrtes nd RNA/DNA synthesis, stunting plnt growth nd genertive orgn formtion [4]. Similrly to zinc deficiency, excessive Zn content in the soil nd incresed sorption vi roots results in reduced plnt development. The symptoms of excessive Zn sorption re chlorotic nd necrotic chnges on lef surfces nd s consequence decresed rtes of photosynthesis. Most often, zinc is sored y plnts in proportion to its content in the soil. However, oth the properties of the soil nd the species of the plnts hve n impct on zinc ccumultion [4]. Li et l. (2013) oserved significnt reduction in the mount of totl chlorophyll in whet seedlings exposed to zinc t concentrtion of 3 mm for 6 dys. They noticed tht excess zinc concentrtion in the soil cused n increse in the concentrtion of hydrogen peroxide (H 2 O 2 ) in the leves nd incresed peroxidse (POD), ctlse (CAT), glutthione reductse (GR) nd scorte peroxidse (APX) ctivities. They lso oserved significnt increse in proline in leves nd roots of plnts under Zn stress in comprison to untreted seedlings. The concentrtion of proline ws higher in the roots thn in the leves. Totl protein content in whet seedlings under Zn stress ws higher in the roots [5]. Zinc cts s structurl nd ctlytic component of proteins nd enzymes, s well s cting s co-fctor in the norml development of pigment iosynthesis. Zn tretment ffects tissue phosphorus significntly, which decreses s the Zn concentrtion increses [6]. Zn nd P hve een oserved to interct nd ech my interfere with the vilility nd utiliztion of the other. High Zn uptke efficiency my depress root phosphorous uptke nd lso involves high rte of Zn trnsport from roots to shoots vi the xylem [7]. It hs lso een oserved tht, s with P, Zn ppliction hs n dverse effect on Fe content nd Fe uptke in Mungen plnts. The decrese in Fe my e due to competitive interctions with Zn, which proly occur t the sorption sites of plnt roots [8, 9]. Zn strongly influences the metolic function of iron in plnts. If one is present in excessive mounts, the uptke of the other my e depressed. Another element tht cn e tken up y higher plnts from soil is Cu. Reserch conducted y Zengin nd Kirg (2007) showed tht copper stress cuses significnt increse in proline concentrtion in sunflower seedlings (Helinthus nnuus L.) [10]. They lso oserved decreses in chlorophyll nd chlorophyll, s well s shrp decrese in totl protein concentrtion. The contents of chlorophyll ( + ) nd totl protein decresed with the concentrtion of copper in the soil. Similr results were oserved in en seedlings treted with Zn nd Co y Zengin (2006). The presence of Zn nd Co decresed the contents
3 Accumultion of metl ions in selected plnts 31 of chlorophyll nd totl protein nd lso enhnced ccumultion of proline in the leves [11]. Hevy metl ions such s Cu 2+, Zn 2+, Fe 2+ re essentil micronutrients for plnt metolism ut when present in excess they cn ecome extremely toxic [12]. Ni is lso essentil for plnts, ut in the mjority of plnt species the required concentrtion is very low ( mg kg -1 dry weight) [13]. Indeed, s levels of Ni pollution increse, over-ccumultions of Ni rther thn Ni deficiencies re more commonly found in plnts [14]. The toxic effects of high concentrtions of Ni in plnts re well known for exmple, inhiition of miotic ctivity in pigeonpe (Cjnus cjn L., Millspugh) [15], reduced plnt growth in cge (Brssic olerce) [16] nd lower fruit yield nd qulity in whet (Triticum estivum L.) [17]. Extremely high soil Ni concentrtions hve left some frmlnd unsuitle for growing crops, fruits nd vegetles in Lison, Portugl [18]. The present study investigtes the ioconcentrtion nd poisoning of Cu, Zn nd Ni on Ocimum silicum L., Menth piperit L. nd Lepidium stivum L. It ws our hypothesis tht the different metl ions would e ccumulted y the plnts, negtively ffecting plnt growth. Experimentl Mterils The investigtions focused on the grden cress Lepidium stivum L. from the Brssiccee fmily (500 seeds per pot), mint Menth piperit L. nd sil Ocimum silicum L. from the Lmicee fmily (25-30 seeds per pot). The plnts were cultivted on universl soil with ph 6.45±1, KCl 1.0 g dm -3, CCl mg dm -3, P 2 O mg dm -3 in photoperiodic system dy/night 16/8 hours. The temperture ws 23/18±2 o C. Irrigtion ws provided in sufficient quntities for plnt growth. The reltive humidity of the soil ws round 60-70%. The soil ws mixed with perlite in rtio of 3:1. Perlite, which is neutrl medium, does not provide ny nutrients to the plnt roots. It is product of minerl origin, which sors nd stores wter, improves soil ertion nd ccumultes het, ccelerting plnt growth. Use of Perlite provides excellent conditions for the development of the root system. A suitle weight of soil mixed with perlite ws emptied onto lrge, deep dish, nd ws then comined with solution of hevy metl slts to otin the pproprite concentrtions. To contminte the soil cettes of the metls nickel, copper nd zinc were used in rnge from 50 mg kg -1 to 3000 mg kg -1. The concentrtions of hevy metls pplied to the soil re shown in Tle 1.
4 32 Szczodrowsk et l. Tle 1. Concentrtions of hevy metls pplied to the soil Lmicee fmily [mg kg -1 ] Nickel Zinc Copper Brssiccee fmily [mg kg -1 ] Nickel Zinc Copper Methods At the end of the cultivtion phse (for Lepidium stivum L. this ws fter 10 dys, for Menth piperit L. fter 56 dys nd for Ocimum silicum L. 33 dys), ll the leves of the plnts (excluding cotyledons) were collected, lyophilized nd then minerlized in microwve minerliser (0.3 g of dried plnt tissue in 5 ml of 65% nitric cid). The concentrtions of metls in the resultnt minerliztes were exmined using Inductively Coupled Plsm Mss Spectrometry (ICP-MS), (Eln DRC-e, PerkinElmer, SCIEX, USA). Quntittive nlysis ws performed with reference to the rhodium stndrd curve ( 103 Rh). The Zn, Ni nd Cu concentrtions in the plnt tissues were expressed in μg g -1 of dry weight. The degree of concentrtion of hevy metls is expressed s the ioconcentrtion fctor (BCF) nd the percentge of control, where the control is considered to e 100%. The BCF is considered to e fctor of efficiency for metl ion uptke. It ws clculted s the rtio of the concentrtion of metl ions in the orgnism to the chemicl concentrtion in the soil in the initil culture period. The BCF ws clculted using the following formul [19]: BCF = Metl ion concentrtion in shoots / Metl ion concentrtion in the soil. All redings documented in this reserch re the verge of three replictes from three independent cultivtions. Sttisticl nlyses were using STATISTICA, Version 10: New Fetures nd Enhncements. The significnce of differences were nlyzed for ech plnt nd metl individully using ANOVA nlyses of vrince followed y the Duncn multiple rnge post hoc test. Sttisticl proilities of P < 0.05 were considered significnt nd mrked using different letters. Results nd Discussion Metl ccumultion in plnts ws clerly relted to the concentrtion of metl ions in the growing medium. Bsil (Ocimum silicum L.) plnts used s reference were chrcterized y the following concentrtions of metl ions in their leves: nickel 18.6 mg kg -1 d.w., copper 29.2 mg kg -1 d.w., zinc 34.2 mg kg -1 d.w. [20], wheres grden cress (Lepidium stivum L.) reference plnts were chrcterized y the following concentrtions of metl ions in their leves: zinc mg L -1, nickel elow the detection limit [21].
5 Accumultion of metl ions in selected plnts 33 The results otined for metl ion ccumultion re presented s BCF coefficients in Tles 2 nd 3, s metl concentrtion in μg g -1 of dry weight (DW) on Figures 1-6 nd s metls concentrtion in μg g -1 of fresh weight (FW) on Figures 7-9. The dt re mens ± stndrd devition (SD) of three replictes. Brs with different letters re significntly different t P < Tle 2. Effect of exogenous nickel, zinc nd copper concentrtion in soil on metl ion uptke of Ocimum silicium L. nd Menth piperit L. seedlings Tretment Ocimum silicum L. Menth piperit L. BCF±SD Ni 100 mg kg ± ± Ni 210 mg kg ± ± Ni 500 mg kg ± ± Cu 200 mg kg ± ± Cu 500 mg kg ± ± Cu 1000 mg kg ± ± Zn 720 mg kg ± ± Zn 1500 mg kg Zn 3000 mg kg Tle 3. Effect of exogenous nickel, zinc nd copper concentrtion in soil on metl ion uptke of Lepidium stivum L. seedlings Tretment BCF±SD Ni 50 mg kg ± Ni 100 mg kg ± Ni 300 mg kg ± Cu 100 mg kg ± Cu 300 mg kg ± Cu 600 mg kg ± Zn 250 mg kg ± Zn 500 mg kg ± Zn 1000 mg kg ± 0.001
6 34 Szczodrowsk et l. c d Figure 1. The concentrtions of nickel ions in mint tissue (Menth piperit L.) c Figure 2. The concentrtions of copper ions in mint tissue (Menth piperit L.)
7 Accumultion of metl ions in selected plnts 35 Figure 3. The concentrtion of zinc ions in mint tissue (Menth piperit L.) c d Figure 4. The concentrtions of nickel ions in sil tissue (Ocimum silicum L.)
8 36 Szczodrowsk et l. d c Figure 5. The concentrtions of copper ions in sil tissue (Ocimum silicum L.) Figure 6. The concentrtion of zinc ions in sil tissue (Ocimum silicum L.)
9 Accumultion of metl ions in selected plnts 37 c d Figure 7. The concentrtions of nickel ions in grden cress tissue (Lepidium stivum L.) c c Figure 8. The concentrtions of copper ions in grden cress tissue (Lepidium stivum L.)
10 38 Szczodrowsk et l. Figure 9. The concentrtions of zinc ions in grden cress tissue (Lepidium stivum L.) Menth piperit L. The germintion process ws much more efficient in the control compred to the plnts grown on soil contminted with hevy metls, in terms oth of the numer of germinted plnts nd the growth rtes of the plnts. This difference my e indictive of iotic stress nd simultneous sorption of hevy metls from the soil. Plnts grown on soil contminted with nickel showed norml growth, slightly lower compred to the control. The plnts grown on soil contminted with nickel to concentrtion of 210 mg kg -1 were slightly smller in comprison to those grown on soil contminted with 100 mg kg -1 nd 500 mg kg -1. Mint plnts grown on soil contminted with copper were lso chrcterized y norml growth, slightly lower or equl to tht of the control plnts. Plnts showed the est growth with the highest numer of lrge, well-developed plnts in the presence of Cu t concentrtion of 200 mg kg -1. Plnts which hd een growing on soil contminted with zinc showed the gretest morphologicl chnges compred with the control. There ws mrked inhiition of growth nd development. None of the plnts could grow with Zn t concentrtion of 3000 mg kg -1. The smple with 1500 mg kg -1 of Zn grew three smll plnts. 720 mg kg -1 of zinc contmintion did not result in visile chnges to the morphologicl fetures of peppermint. The germintion process seemed to e more efficient for control smples when compred to those cultivted on soils contminted with hevy metl ions.
11 Accumultion of metl ions in selected plnts 39 Efficiency ws considered oth in terms of the numer of germinted plnts nd their growth rte. This difference possily rose due to the iotic stress on plnts nd difficulties ssocited with growth nd simultneous sorption of hevy metl ions into plnt cells. The mount of nickel ions in smples contminted t concentrtions of 100 mg kg -1, 210 mg kg -1 nd 500 mg kg -1 were 5.03 μg g -1, 6.09 μg g -1 nd 7.84 μg g -1, respectively. In comprison, the control smple contined only 1.22 μg g -1 ions. The growth rte correlted with soil contmintion (Fig. 1). The influence of copper contminted soil ws rther typicl. In plnts grown on soil contminted with 200 mg kg -1 copper, the content of Cu in the leves ws mesured t μg g -1. The control smple contined only 20 μg g -1 copper. However, with copper concentrtions of 500 mg kg -1 nd 1000 mg kg -1, respectively, the copper content in the leves remined t lmost the sme level: μg g -1 nd μg g -1 (Fig. 2). Becuse of the insufficient numer of smples produced with ll zinc concentrtions, the nlysis of zinc content ws conducted for zinc 720 mg kg -1 smples only. The level of Zn ws extremely high, t μg g -1, compred to the control smples with μg g -1 zinc (Fig. 3). Ocimum silicum L. In the erly stges of plnt growth, no differences were oserved in the morphology of sil. Chnges were the most visile during the finl phses of the experiment, fter 33 dys of plnt growth. There were no negtive morphologicl chnges in sil grown on soil contminted with different concentrtions of copper. The plnts were lrge nd their leves did not show ny signs of disese or discolortion. Smples grown on soil contminted with smller mounts of nickel (Ni 100 mg kg -1, Ni 210 mg kg -1 ) hd similr fetures to ech other. With the highest nickel concentrtion (Ni 500 mg kg -1 ) lef yellowing ws oserved nd in one cse lef withering. The concentrtions of nickel ions in plnt tissues grown on soil smples contminted with 100 mg kg -1, 210 mg kg -1 nd 500 mg kg -1 of the metl were 3.39 μg g -1, 5.22 μg g -1 nd μg g -1, respectively, wheres the control smples contined on verge round 0.75 μg g -1 (Fig. 4). The presence of copper ions in the soil did not ffect the growth nd development of sil. The concentrtion of copper ions in plnt tissues grown on smples contminted with 200 mg kg -1, 500 mg kg -1 nd 1000 mg kg -1 concentrtions were μg g -1, μg g -1 nd μg g -1, respectively. The control smples contined μg g -1 (Fig. 5). Bsil grown on soil contminted with zinc showed negtive morphologicl chnges when compred to the control plnts. The lowest zinc concentrtion (Zn 720 mg kg -1 ) resulted in slight lef yellowing. Higher concentrtion (Zn 1500 mg kg -1 ) inhiited plnt development nd cused lef yellowing nd withering. The highest concentrtion (Zn 3000 mg kg -1 ) ppered to e toxic
12 40 Szczodrowsk et l. enough to cuse lef deth fter 33 dys of growth with the only green prts eing cotyledons. As with the mint plnts, ecuse of the insufficient mount of plnt mteril for ll zinc concentrtions, the nlysis ws performed for zinc 720 mg kg -1 only. The concentrtion of zinc in the sil tissues ws μg g -1 nd much higher thn the control, with concentrtion of μg g -1 (Fig. 6). Lepidium stivum L. The content of prticulr metl ions ws determined over 10-dy cultivtion of Lepidium stivum L. At no time during the cultivtion did ny of the tested vrints of plnt differ morphologiclly. The plnts possessed fully developed leves without ny signs of disese. The gretest increse in metl ions ws noted for nickel its content grdully incresed with the concentrtion of nickel in the soil. The ion contents were μg g -1 (50 mg kg -1 ), μg g -1 (100 mg kg -1 ) nd μg g -1 (300 mg kg -1 ) in comprison to the control where the concentrtion ws 0.65 μg g -1 (Fig. 7). A slight increse in copper ion content compred to the control smple with 4.67 μg g -1 ws oserved for vrints with copper concentrtions of 5.00 μg g -1 (100 mg kg -1 ), μg g -1 (300 mg kg -1 ) nd μg g -1 (600 mg kg -1 ) (Fig. 8). Similr results were otined for vrints with zinc. The content of zinc ions in the control smple reched μg g -1 nd in vrints with the ddition of zinc: μg g -1 (250 mg kg -1 ), μg g -1 (500 mg kg -1 ) nd μg g -1 (1000 mg kg -1 ) (Fig. 9). The results of this study indicte tht nickel, zinc nd copper contmintion in soil significntly decreses growth, development nd iomss of plnts from Lmicee fmily wheres nickel nd copper contmintion does not ffect plnt growth nd development. In plnts from Brssicee fmily there were no negtive morphologicl chnges. The highest BCF vlues were noted for the effect of exogenous zinc in plnts from the Lmicee fmily, nd for the effect of exogenous nickel in plnts from the Brssicee fmily. In generl, most studies hve reported higher concentrtions of metls in roots thn in shoots. Normlly, Zn or Ni concentrtions re 10 or more times higher in roots thn in shoots [22]. In reserch y Soltn nd Rshed (2003), wter hycinth ws treted with severl hevy metls (Cd, Co, Cr, Cu, Mn, Ni, P nd Zn). The uthors concluded tht wter hycinth ccumultes higher concentrtions of hevy metls in the roots thn tht in the eril prts [23]. The present study hs demonstrted tht nickel, zinc nd copper ccumulte in leves t different concentrtions depending on the plnt species [24]. Conclusions Fitoextrction of specific hevy metls in plnt tissues vries depending on the otnicl fmily. The highest concentrtion of zinc ws oserved in plnts from the Lmicee fmily. Plnts from the Brssiccee fmily were found to e hyperccumultors of nickel. Our reserch lso suggests tht Ocimum
13 Accumultion of metl ions in selected plnts 41 silicum L., Menth piperit L. nd Lepidium stivum L. could e used to extrct considerle mounts of pollutnts such s hevy metls from soil. References 1. Nzir A, Mlik RN, Aji M, Khn N, Siddiqui MF. Hyperccumultors of hevy metls of industril res of Islmd nd Rwlpindi. Pk J Bot 2011, 43: Jdi CD, Fulekr MH. Phytoremedition: the ppliction of vermicompost to remove zinc, cdmium, copper, nickel nd led y sunflower plnt. Environ Eng Mng J 2008, 7: Ahmd K, Ejz A, Azm M, Khn ZI, Ashrt M, Al-Quriny F, Frdous A, Gondel S, Byt AR, Vleem EE. Led, cdmium nd chromium contents of cnol irrigted with sewge wter. Pk J Bot 2011, 43: Kt-Pendis A, Mukherjee AB. Trce elements from soil to humn. Berlin- Heidelerg: Springer-Verlg; Li X, Yng Y, Ji L, Chen H, Wei X. Zinc-induced oxidtive dmge, ntioxidnt enzyme response nd proline metolism in roots nd leves of whet plnts. Ecotoxicol Environ Sf 2013, 89: Blshouri, P. Effect of zinc on germintion, growth nd pigment content nd phytomss of Vign rdit nd Sorghum icolor. J Ecoiol 1995, 7: Smreen T, Humir, Ullh Shh H, Ullh S, Jvid M. Zinc effect on growth rte, chlorophyll, protein nd minerl contents of hydroponiclly grown mungens plnt (Vign rdit). Ar J Chem 2013, doi: /j.r jc Lonergn JF, We MJ. Interction etween zinc nd other nutrients ffecting the growth of plnts. In: Roson, A.D. (ed.), Zinc in Soils nd Plnts. Kluwer Acdemic Pulishers, Dordrecht 1993, pp Rjie M, Ejrie AK, Owliie HR, Tvkoli AR. Effect of zinc nd oron interction on growth nd minerl composition of lemon seedlings in clcreous soil. Int J Plnt Prod 2009, 2: Zengin FK, Kirg S. Effects of copper on chlorophyll, proline, protein nd scisic cid level of sunflower (Helinthus nnuus L.) seedlings. J Environ Biol 2007, 28: Zengin FK. The effects of Co2+ nd Zn2+ on the contents of protein, scisic cid, proline nd chlorophyll in en (Phseolus vulgris cv. Strike) seedlings. J Environ Biol 2006, 27: Willims LE, Pittmn JK, Hll JL. Emerging mechnisms for hevy metl trnsport in plnts. Biochim Biophys Act 2000, 1465: Nieminen TM, Ukonmnho L, Rusch N, Shotyk W. Biogeochemistry of nickel nd its relese into the environment. Met Ions Life Sci 2007, 2: Slt DE, Krmer U. Mechnisms of metl hyperccumultion in plnts. In: Rskin I, Ensley BD (eds.) Phytoremedition of Toxic Metls Using Plnts to Clen up the Environment, Wiley, New York, 1993, pp Mdhv Ro KV, Sresty TV. Antioxidtive prmeters in the seedlings of pigeonpe (Cjnus cjn L. Millspugh) in response to Zn nd Ni stresses. Plnt Sci 2000, 157: Mols J. Chnges of chloroplst ultrstructure nd totl chlorophyll concentrtion in cge leves cused y excess of orgnic Ni (II) complexes. Environ Exp Bot 2002, 47:
14 42 Szczodrowsk et l. 17. Gjewsk E, Sklodowsk M, Sl M, Mzur J. Effect of nickel on ntioxidtive enzyme ctivities, proline nd chlorophyll contents in whet shoots. Plnt Biol 2006, 50: Durte B, Delgdo M, Cdor I. The role of citric cid in cdmium nd nickel uptke nd trnsloction, in Hlomine portulcoides. Chemosphere 2007, 69: Arnot JA, Gos F. A review of ioconcentrtion fctor (BCF) nd ioccumultion fctor (BAF) ssessments for orgnic chemicls in qutic orgnisms. Environ Rev 2006, 14: Jen V, Gupt S. Study of hevy metl distriution in medicinl plnt sil. J Environ Anl Toxicol 2012, 2: Mojiri A, Aziz HA, Aziz SQ, Gholmi A, Aoutor M. Impct of urn wstewter on soil properties nd Lepidium stivum in n Arid Region. IJSRES 2013, 1: Chney RL, Mlik M, Li YM, Brown SL, Angle JS, Bker AJM. Phytoremedition of soil metls. Curr Opin Biotechnol 1997, 8: Soltn ME, Rshed MN. Lortory study on the survivl of wter hycinth under severl conditions of hevy metl concentrtions. Adv Environ Res 2003, 7: Swin G, Adhikri S, Mohnty P. Phytoremedition of copper nd cdmium from wter using wter hycinth, Eichhorni crssipes. IJAST 2014, 2:1-7.
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