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Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 DOI: 10.1515/agri-2016-0008 Original paper EFFECT OF CADMIUM ON GROWTH, PHOTOSYNTHETIC PIGMENTS, IRON AND CADMIUM ACCUMULATION OF FABA BEAN (VICIA FABA CV. AŠTAR) 1* 1 2 3 BEÁTA PIRŠELOVÁ , ROMAN KUNA , PETER LUKÁČ , MICHAELA HAVRLENTOVÁ Constantine the Philosopher University in Nitra, Slovak Republic West Slovakia water company, a.s. Nitra, Slovak Republic National Agricultural and Food Centre – Research Institute of Plant Production, Piešťany, Slovak Republic PIRŠELOVÁ, B. ‒ KUNA, R. ‒ LUKÁČ, P. ‒ HAVRLENTOVÁ, M.: Effect of cadmium on growth, photosynthetis pig- ments, iron and cadmium accumulation of faba bean (Vicia faba cv. Aštar). Agriculture (Poľnohospodárstvo), vol. 62, 2016, no. 2, p. 72–79. The influence of different concentrations of cadmium (Cd) ions (50 and 100 mg/kg soil) on growth, photosynthetic pigment content, Cd, and iron accumulation in faba bean (Vicia faba L. cv. Aštar) was studied under laboratory con - ditions. No significant changes were observed in the growth parameters of shoots (length, fresh, and dry weight). Both tested Cd doses resulted in decrease in root fresh weight by 31.7% and 28.68% and in dry weight by 32.2% and 33.33%, respectively. Increased accumulation of Cd was observed in roots (125- and 173- fold higher than in control) and shoots (125- and 150- fold higher than in control) as a result of applied doses of Cd. Increased accumulation of iron was detected in roots (1.45- and 1.69-fold higher than in control). Decrease in the content of chlorophyll a (by 25.52 and 24.83%, respectively) and chlorophyll b (by 6.90%) after application of Cd 100 as well as decrease in carotenoids (by 40.39 and 38.36%, respectively) was detected. Weak translocation of Cd from roots to shoots pointed to low phy - toremediation potential of the tested bean variety in contaminated soil. However, the high tolerance of this cultivar, its relative fast growth, as well as priority of Cd accumulation in roots presume this plant species for phytostabilisation and revegetation of the Cd-contaminated soils. Key words: faba bean, cadmium, tolerance, photosynthesis, oxidative stress, remediatory potential Contamination of soils with Cadmium (Cd) is lated to its ability to generate reactive oxygen spe - a major threat to ecosystems. Cd is rapidly taken cies (ROS) resulting in unbalanced cellular redox up by plant roots and can be loaded into the xylem homeostasis (Schützendübel et al. 2001). The ROS for its transport to leaves. Many species accumu- generation is indirect because Cd does not partic- late toxic metals mainly in the roots (Benavides et ipate in Fenton-type reactions; therefore, it is a al. 2005); according to Wu (1990), about 70–85% non-redox metal (Romero-Puertas et al. 2004). In of the absorbed Cd remains in the roots in various plants, exposure to Cd causes inhibition of growth, plants. The differences in Cd accumulation capacity activation or inhibition of enzymes, reduction of and localisation appear to be the major factors in transpiration rate and water content (Benavides et al. determining plant tolerance to Cd exposure (Obata 2005). Stomatal closure due to entry of Cd into the & Umebayashi 1993). The toxic effect of Cd is re - guard cells in competition to Ca (Perfus-Barbeoch RNDr. Beáta Piršelová, PhD. ( Corresponding author), doc. RNDr. Roman Kuna, PhD., Department of Botany and Genetics, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Nábrežie mládeže 91, 949 74 Nitra, Slovak Republic. E-mail: email@example.com; firstname.lastname@example.org RNDr. Peter Lukáč, West Slovakia water company, a.s., Nábrežie za hydrocentrálou 4, 949 01, Nitra, Slovak Republic. E-mail: email@example.com RNDr. Michaela Havrlentová, PhD., National Agricultural and Food Centre – Research Institute of Plant Production, Bratislavská cesta 122, 921 68 Piešťany, Slovak Republic. E-mail: firstname.lastname@example.org 72 Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 et al. 2002) and reduction in stomata count per unit MATERIAL AND METHODS area are also characteristic symptoms of Cd stress resulting in lesser conductance to CO (Pietrini et Plant material and growth conditions al. 2010), which consequently lead to the overall Seeds of beans (Vicia faba cv. Aštar) were inhibition of photosynthesis. In addition, Cd may surface-sterilized with 5% sodium hypochloride disturb plant mineral metabolism. For example, Cd for 15 min and planted in pots containing mix of almost completely inhibits iron (Fe) translocation soil (BORA, pH 6‒7, 1.0% N; 0.3% P O ; 0.4% 2 5 from roots to shoots, leading to increased root Fe K O) and perlite (4:1). The plants were cultivat - concentrations in plants (Muradoglu et al. 2015). ed in a growth chamber at 20°C, 12 h light/12 h Many studies have attempted to clarify the dark period (illumination of 400 lux), and rela - mechanism of Cd toxicity in plants (Békésiová et al. tive humidity 60‒70%. Pots were watered daily to 2008; Tamás et al. 2012; Balestri et al. 2014); how- 60% water-holding capacity of the soil. When the ever, relationships between growth inhibition and first assimilating leaves were developed, plants physiological processes under Cd condition are still were supplied with distilled water (control) or discussed. Mainly because of the fact that its toxic two doses of Cd: 50 (Cd 50) and 100 (Cd 100) effects are expressed in relation to plant species or mg/kg of soil, respectively. Cd was added as varieties. The toxicity of Cd is also greatly influ - Cd(NO ) .4H O. 3 2 2 2+ enced by the concentration of Cd ions, their form The test concentrations of cadmium were used and availability in the soil, duration of their appli- due to predicted toxicity of this element to bean cation, as well as by other different factors of the plants (Piršelová et al. 2015). environment (pH of the soil, soil humidity, and oth- Growth parameters ers). There are also no univocal reports on the rela - On day 10 after application of metal solutions tionships between Cd stress and some physiological (BBCH 31-2 visibly extended internodes), roots processes (e.g., water relations) since Cd can inter - were separated from the above-ground part of the fere in several ways on the parameters that affect plants, washed with tap water, and growth param- these physiological processes in leaves (Barceló & eters (length and fresh weights) were determined. Poschenrieder 1990). Knowledge of mechanisms of After washing, the plant samples were oven-dried plants’ tolerance to heavy metals ions provides an at 70°C for 24 h to constant dry weight, and this pa - opportunity of breeding varieties suitable for phy- rameter was also determined. Three replicates were toremediation. Besides, metal hyper-accumulating used per treatment and eight plants from each pot plants, non-accumulating Cd, and high biomass were analysed (altogether 24 plants). crops are also considered for phytoextraction pur - poses, but it has been suggested that the success Photosynthetic pigments determination of this approach might be limited by Cd-induced For photosynthetic pigments (chlorophyll a and phytotoxicity problems (McGrath et al. 2001). Al- b, carotenoids) analysis, fully developed trifoliate though plants belonging to family Fabaceae are leaves were extracted with 80% acetone. Pigments sensitive to high concentrations of heavy metals contents were determined spectrophotometrical- (Kuboi et al. 1987), several studies indicated that ly (UV-VIS spectrophotometer, Shimadzu) at the plant such as Lupinus albus or Vicia faba are used following wavelengths: 663, 646 and 470 nm and in re-vegetation and phytostabilization of cadmium calculated according to Lichtenthaler and Wellburn contaminated soils (Vazquez et al. 2006; Pichtel & (1983). The experiment was performed in four rep - Bradway 2008). licates. In the presented article, the influence of different Determination of tolerance index concentrations of Cd ions (50 and 100 mg/kg soil) on Tolerance index (TI) was calculated as a ratio of growth, photosynthetic pigment content, Cd and Fe the mean dry weight of plants grown in the presence accumulation in faba bean (cv. Aštar) is presented. In of Cd and the mean dry weight of control plants ex - addition, the potential of broad bean for the phytore- pressed as percentage. mediation of Cd in a contaminated soil was presented. 73 Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 In vivo detection of H O in leaves the Student’s t-test, P < 0.05 was considered as sta- 2 2 Diaminobenzidine (DAB) was used for the de - tistically significant. tection of H O staining in leaf tissues (Thord- 2 2 al-Christensen et al. 1997). On day 10 after applica - tion of metal solutions, fully developed leaves (the RESULTS AND DISCUSSION first bifoliate – developmental stage 1 and second trifoliate – developmental stage 2) excised from Plant growth 2+ Cd-treated plants (50 and 100 mg Cd /kg soil) or Growing in a contaminated soil, the bean plants did from untreated plants were placed in Petri dishes not show any apparent visual symptoms of intoxica - containing DAB solution (1 mg/ml). Plates were left tion by the metal. Similar conclusion was also reached in a climate chamber at 24°C in darkness, and DAB by Dobroviczká et al. (2013) at cultivation of soy - staining was assessed visually 12 h later. Leaves bean (Glycine max cv. Bólyi 44, cv. Cordoba) in soil were bleached by immersing in boiling ethanol to contaminated with Cd in concentration of 50 mg/kg visualize the brown spots characteristic of the reac - soil and by Pinto et al. (2004), who exposed sor- tion of DAB with H O . ghum (Sorghum sp.) to various doses of Cd. 2 2 Measurements of metal content in leaves and roots Dried plant material (0.5 g roots and shoots) was digested in the mixture of 5 ml water, 5 ml of concentrated HNO p.a. (Merck, Darmstadt, Ger - many), and 1.5 ml of H O p.a. (Slavus, Bratisla- 2 2 va) by using the microwave oven Mars Xpress (CEM Corporation, Matthews, USA). Decompo- sition temperature was 140°C, ramp time 15 min, and hold time 13 min. After digestion, the solu- tion was diluted to 25 ml with deionised water and filtered through an acid-resistant cellulose filter (Whatman No. 42). Blank samples were prepared in a similar way. The elements (Cd and Fe) were determined by electrothermal atomic absorption spectroscopy (AAS Perkin Elmer 1100B, Nor- walk, Connecticut, USA). The biological accumulation coefficient for cadmium - BAC, biological transfer coefficient - BTC and biological concentration factor - BCF were determined (Tukura et al. 2012). BAC = (metal content in the above-ground part of plant/metal content in soil) × 100 BTC = (metal content in the above-ground part of plant/metal content in root) × 100 BCF = (metal content in root/metal content in soil) × 100 Statistical analysis Data were analysed by one-way ANOVA or Kru- Figure 1. Effect of cadmium on length – a, fresh weight skal-Wallis tests using XLSTAT software. The sig - (FW) – b, and dry weight (DW) – c of roots and shoots of bean plants. Data are presented as means ± SD, n = 24. nificance of differences between the concentrations Different letters indicate significant differences at of heavy metals in plant tissues was shown by using p < 0.05. 74 Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 Plant length, fresh and dry weight of shoots were in the roots, which suggests a strong Cd retention not significantly affected by Cd (Figure 1); however, during its long distance transport from roots to each of the tested doses of Cd resulted in decrease shoots, which might be a plant mechanism to toler- of root fresh weight by 31.70 and 28.68% and dry ate the metal stress (Zornoza et al. 2002). Increased weight by 32.2% (TI = 67.80) and 33.33% (TI = Fe accumulation was detected only in roots (1.5 and 66.67), respectively (Figure 1). Decrease in root 1.69-more compared to control). In shoots, just the biomass after exposure to Cd was also observed by same content of Fe was detected in control as well others (Kochlar et al. 2004; Rodriguez-Serrano et al. as in stressed samples (Table 1). Our results corre - 2009). By contrast, low doses of Cd often cause spond to the results of Luo et al. (2012), who ob- increase in the amount of fresh biomass of shoots served increased accumulation of given metal and (Pinto et al. 2004; Shah et al. 2008). In our experi - Fe mainly in roots influenced by Cd concentration. ment, due to doses Cd 50 and Cd 100, the length of The intake of Fe from the soil by roots in non-gram- shoots was also increased by 1.35% and 5.08% (Fig - inaceous monocots and dicots is primarily regulated ure 1a), and fresh biomass of shoots was increased by the Fe transporter IRT1 (Curie & Briat 2003). by 0.82 and 4.41%, respectively (Figure 1b). De - Several studies also provide strong evidence that the tected TI calculated on the dry mass of roots and Fe transporter IRT1 is also primarily responsible for 2+ shoots (66.67‒91.99) suggests high tolerance of the Cd influx into root cells (Vert et al. 2002). given variety to Cd. Plants with TI higher than 60 Although no leaves chlorosis and no changed are considered as tolerant (Lux et al. 2004). Fe content in shoots were observed in our experi - ments, strong differences in the Fe content in roots Accumulation of Cd and Fe in plant tissue and shoots indicate inhibition of Fe translocation With increased concentration of the applied met- from roots to shoots. Although the mechanism un- al, also the increased accumulation of Cd in roots derlying Cd-induced Fe deficiency in plants has not (125 and 173-more compared to the control) and in been identified, there are several possible expla - shoots (125 and 150-more compared to the control) nations. The root Fe-deficiency-inducible enzyme of faba bean was observed (Table 1). Our results Fe(III)-chelate reductase is inhibited by Cd (Parmar indicate that the majority of Cd was accumulated T a b l e 1 Cadmium (Cd) and iron (Fe) content in roots and shoots [ μg/g dry weight] Root Shoot Variant of experiment Cd Fe Cd Fe Control 0.50 ± 0.01 1,035 ± 103.00 0.11 ± 0.03 117 ± 1.53 + + + Cd 50 62.26 ± 9.60 1,503 ± 175.00 13.73 ± 3.27 108 ± 0.71 + + + Cd 100 86.40 ± 0.99 1,754 ± 104.00 16.53 ± 4.37 119 ± 11.72 Data are presented as means ± SD; n = 3; indicate the level of significance at p < 0.05 T a b l e 2 Effect of soil pollution with cadmium on the biological accumulation coefficient (BAC), biological transfer coefficient (BTC), and biological concentration factor (BCF) Variant of experiment BAC BTC BCF Cd 50 0.275 0.221 1.245 Cd 100 0.165 0.191 0.864 75 Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 et al. 2013), suggesting that Cd may directly im - pair Fe acquisition. Also, Cd usually accumulating in roots, almost completely inhibits Fe transloca- tion from roots to shoots, leading to increased root Fe concentrations in strawberry (Muradoglu et al. 2015) and mung bean (Liu et al. 2000). As a result of the Cd accumulation in roots, the BAC and BTC values were very low and less than 1 (Table 2). Despite the relative high value of BCF at lower concentration of Cd (BCF > 1) was deter - Figure 2. Chlorophyll a (Chl a), chlorophyll b (Chl b), mined, bean are not suitable for phytoremediation and carotenoids (Car) contents in leaves affected by Cd of soils contaminated with Cd because of low BAC (50 or 100mg/kg soil). Data are presented as means ± and BTC values. Plants exhibiting BTC (particular - SD, n = 4. FW – fresh weight. Different letters indicate significant differences at p < 0.05. ly BCF) value less than one are unsuitable for phy - toextraction (Fitz & Wenzel 2002). However, higher BCF values (Table 2) presume this plant species for phytostabilisation and revegetation of the Cd-con- caused by metal stress are the result of the inhibition taminated soils. By the influence of higher doses of of the enzymatic activity converting Chl a to Chl b Cd, low decrease in values of BAC, BCF, and BTC and to what extent they derive from different rate were observed (Table 2), probably as an effect of of degradation of both chlorophyll species (Myśli - Cd toxicity. Cd-dependent increase of BTC at lower wa-Kurdziel & Strzałka 2002). Carotenoid content concentration and decrease at higher concentration in plants exposed to Cd also does not exhibit a set of Cd were also observed by de Maria et al. (2013) pattern, and may either increase or decrease. The in- in sunflower. crease was observed in Cucumis sativus (Burzynski Pigment content and H O accumulation in leaves 2 2 & Zurek 2007) and Nicotiana tabacum (Procház- Upon the exposure to both doses of Cd, decreases ková et al. 2014). Oppositely, decrease was also ob - in content of chlorophyll a (by 25.52% and 24.83%, served, for example, in Pisum sativum (Hattab et al. respectively), chlorophyll b (by 6.90% upon appli- 2009). cation of Cd 100 only) as well as carotenoids (by Inhibitory effect of Cd on photosynthetic ap- 40.39% and 38.36%, respectively) were detected paratus has previously been reported by many (Figure 2). These decreases were statistically sig - other authors (Kummerová et al. 2010; Wang et nificant. Reduction of the pigment contents in our al. 2013), although the opposite reaction has also study is comparable with the results of Kumar et al. been observed (Bindhu & Bera 2001). Reduction (2000), who observed reduction of chlorophyll a by of chlorophyll content could result in enzymat - 38.37%, chlorophyll b by 26.27% and carotenoids ic degradation of these pigments or inhibition of by 31.27% in broad bean leaves treated with Cd their biosynthesis, which could be connected with (120 mg/kg soil). Cd-induced deficiency of Fe and zinc, decrease of The results of the effect of Cd on the ratio of magnesium content or Cd bond to essential thiol chlorophyll a and b diverge. The results of many groups in various enzymes (Parmar et al. 2013). authors suggest that Cd ions cause degradation of Cd does not participate in Fenton-type reactions; chlorophyll a more rapidly than chlorophyll b, re- therefore, it can only indirectly lead to oxidative sulting in decreased Chl a/b ratio (Myśliwa-Kurdziel stress (Romero-Puertas et al. 2004). Thus, it is & Strzałka 2002; Kummerová et al. 2010). On the much more likely that Cd-related oxidative stress contrary, increased Chl a/b ratio was observed by is a consequence of inhibition of photosynthesis, some authors (Azevedo et al. 2005). From the data especially in leaves. This fact is supported by the available in the literature, it is difficult to conclude results of histochemical staining of bean leaves to what extent the changes in the Chl a/b ratio with DAB for detection of H O (Figure 3). 2 2 76 Agriculture (Poľnohospodárstvo), 62, 2016 (2): 72−79 Despite the fact that on leaves no symptoms of fast growth, high biomass as well as priority of Cd toxicity have been observed, Cd induced a signifi - accumulation in roots presume this plant species for cant accumulation of H O especially in older bean phytostabilisation and revegetation of the Cd-con- 2 2 leaves treated with higher dose of Cd (Figure 3). taminated soils. More in-depth biochemical and mo- While the content of Cd was not examined in dif - lecular biological analyses can contribute to reveal- ferent developmental stages of leaves, higher ac- ing some further potential mechanisms of resistance cumulation of H O was observed in older leaves, of this faba bean variety to Cd. 2 2 which may indicate increased accumulation of Cd in older leaves compared with younger. The high Cd Acknowledgements. This work was support- concentration, found mainly in roots and old leaves, ed by the European Community under Project no. suggests that plants tend to avoid toxicity in the 26220220180: Building Research Centre “AgroBio - physiologically most active portions of the plants Tech” and by grant No. APPV-VV-0758-11. by reducing Cd translocation to the epigeous por- tion, and by promoting the re-translocation of toxic metals from shoots to roots (de Maria et al. 2013). REFERENCES AZEVEDO, H.G. − PINTO, G. – SANTOS, C. 2005. 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