Environmental Science and Pollution Research

Uptake of different forms of antimony by wheat and rye seedlings Irina Shtangeeva, Eiliv Steinnes & Syverin Lierhagen Environmental Science and Pollution Research ISSN 0944-1344 Environ Sci Pollut Res DOI 10.1007/s11356-011-0589-y 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23  Author's personal copy Environ Sci Pollut Res DOI 10.1007/s11356-011-0589-y RESEARCH ARTICLE Uptake of different forms of antimony by wheat and rye seedlings Irina Shtangeeva & Eiliv Steinnes & Syverin Lierhagen Received: 28 April 2011 / Accepted: 1 August 2011 # Springer-Verlag 2011 Abstract The bioaccumulation of Sb led to significant variations Purpose The objectives of the research were to study how in concentrations of various elements in different plant antimony (Sb) chemical form present in the growth medium parts. can affect Sb uptake by plants and estimate effects of Sb on Conclusions Wheat and rye seedlings were capable of wheat and rye seedlings, in particular, assess variations in identifying different Sb forms and demonstrated certain concentrations of nutrients resulting from bioaccumulation differences in the ability to uptake Sb and survive under of Sb. high external Sb concentrations. An increase of Sb in the Methods Seedlings were (1) germinated in media spiked plants caused important variations in the concentrations of with Sb(III) or Sb(V) and then transferred to clean water, many essential nutrients. and (2) germinated in Sb-free medium and then grown in water enriched with Sb. Variations of Sb concentrations in Keywords Wheat . Rye . Antimony bioaccumulation . Leaf the seedlings were studied, and effects of Sb bioaccumula- necrosis . Macro-nutrients . Trace elements tion on plant development and concentrations of macro- and trace elements in the plants were assessed. Results Rye was capable of accumulating more Sb than 1 Introduction wheat. This resulted in necrosis of the rye leaves. During germination in Sb-rich medium rye and wheat The knowledge of environmental chemistry and biogeo- accumulated Sb differently. When the seedlings germi- chemistry of toxic metals is quite extensive. However, most nated in Sb-amended medium were then grown in of this information is limited to a few elements, so-called clean water, Sb concentration in all plant parts heavy metals, such as As, Cd, Cr, Cu, Hg, Ni, Pb, Se and U decreased. Plant concentrations of Sb increased signif- (although both metals and metalloids are present in the list). icantly when seedlings germinated in Sb-free medium Until recently, information about biogeochemical behaviour were transferred to Sb-spiked water. However, with of other trace elements is scarce. This has resulted in a time saturation with Sb in the plants was observed. commonly accepted opinion that many trace elements presented in plants at rather low concentrations are non- necessary impurities that do not play an essential role in the Responsible editor: Zhihong Xu Notes biochemical processes in the plants. I. Shtangeeva (*) Antimony (Sb) is a metalloid found in more than 100 St. Petersburg University, minerals (Draggan 2008). Various industrial applications of Universitetskaya nab., 7/9, St. Petersburg 199034, Russia Sb have led to an increasing release of Sb into the e-mail: [email protected] environment by human activities (Filella et al. 2002a; Burford et al. 2010). As a consequence, Sb contamination E. Steinnes : S. Lierhagen has become a growing concern over the last 10 years, and Department of Chemistry, Norwegian University of Science and Technology, the biogeochemistry of Sb has also attracted more interest NO-7491 Trondheim, Norway of researchers (Baroni et al. 2000; Shotyk et al. 2005;  Author's personal copy Environ Sci Pollut Res Nakamaru et al. 2006; He 2007; Filella et al. 2009; Wilson of essential plant nutrients resulting from bioaccumulation et al. 2010). of Sb. However, in spite of these efforts, the impact of Sb on the environment is still poorly understood, and many basic questions on the biological behaviour of Sb remain unclear. 2 Materials and methods Little is known about the mechanisms of Sb uptake by different plant species as well as its toxicity to the plants. 2.1 Experimental design Since Sb is a global contaminant, there is an urgent need to improve our knowledge on Sb biogeochemistry and risks Seeds of wheat Triticum astevium L. and rye Secale cereale associated with its presence in the environment. L. were germinated during 4 days on a moist filter paper. The toxicity and environmental cycling of elements are The seeds were divided into three groups. The first group strongly dependent upon their oxidation states. The Sb(III) served as a control. Seeds from the second and third groups and Sb(V) are the most common valence states of Sb under were germinated in media where either Sb(III) as SbCl3 or ordinary environmental conditions. The +3 form occurs Sb(V) as SbCl5 had been added. Concentration of Sb in the under moderately oxidizing conditions, whereas the +5 media was 75 mg L−1. After the end of germination, the form predominates in highly oxidizing environments first portion of plant samples from all groups was collected (Krachler et al. 2001; Tschan et al. 2008). It was reported and saved for elemental analysis. The rest of the seedlings that in soils, Sb(III) is oxidized within hours to Sb(V) was transferred to vessels (volume of 1.5 L) filled with (Krachler et al. 2001). However, as was shown (Belzile et al. water. At this stage, the following treatments were applied: 2001), even under oxidizing conditions substantial fractions seedlings germinated under control conditions (in Sb-free of Sb may be present as Sb(III). Leuz and co-authors (2006) medium) were transferred to vessels where either Sb(III) or reported that half-lives for oxidation of Sb(III) to Sb(V) were Sb(V) were added (concentration of Sb in the growth media of 8.9, 6.7 and 1.6 days at pH 3, 5.9 and 9.7, respectively. was 75 mg L−1). No other treatments were applied to the Moreover, in natural waters, presence of organic matter can growth media. Seedlings germinated in the medium play a stabilizing role preventing transfer of Sb(III) to Sb(V) enriched with Sb(III) or Sb(V), as well as seedlings (Filella et al. 2002b). One may assume that root organic germinated under ordinary conditions (in Sb-free medium), exudates released to the growth medium could partly play were transferred to vessels filled with clean water. The such a role. temperature in the naturally illuminated greenhouse was Antimony may be taken by plants from the growth typically 25°C during the day and 20°C at night, pH of the medium in different forms; in this case, toxicity of Sb will growth media was maintained at the level of 6.0±0.1 in the depend on its chemical form. Experiments with mammal course of the tests. The experiments were performed in cells showed that Sb(III) form is ten times more toxic than triplicate. Plant samples were collected within 1, 3 and Sb(V) (Krachler et al. 2001). However, at present, there is 5 days after transplanting, carefully washed just after not enough information on Sb phytotoxicity to make sampling, and air-dried at room temperature to constant general conclusions. One may only assume that different weight. Then, the plants were divided into roots, leaves and Sb forms may have different availability to plant uptake. seeds, weighed and prepared for elemental analysis by Available experimental data partially confirm this assump- digesting with 10 mL of 50% ultra-pure HNO3 in an tion (He and Yang 1999; Tschan et al. 2010). Ultraclave microwave oven for 12 min at 240°C. Because of similar chemical parameters of As and Sb, it is commonly accepted that the biogeochemistry of these 2.2 Elemental analysis elements is also similar (Krachler et al. 2001; Filella et al. 2002a). However, despite similarities in the chemistry of HR-ICP-MS analysis was performed using a Termo the two metalloids, there are many differences in their Finnigan model Element 2 instrument (Bremen, Germany). environmental behaviour, particularly, in their uptake by Plant samples were introduced by a CETAC ASX 500 plants (Tschan et al. 2008; Shtangeeva et al. unpublished). autosampler with a peristaltic pump (1 mL min−1). The Thus, it is hardly possible to interpret the behaviour of Sb instrument was equipped with a concentric PFA-ST in plants based solely on the available information on the nebulizer connected to a Scott PFA spray chamber, biogeochemistry of As. platinum sample and skimmer cones and a demountable The objectives of the present work were (1) to study how torch of quartz with guard electrode. The instrument was the chemical form of Sb present in the growth medium can calibrated using 0.6 M HNO3 solutions of multi-element affect uptake of the element by plants, and (2) to estimate standards (including Sb). An aqueous certified reference effects of different Sb forms on two crop plants, wheat and material (SPS-SW-2, Spectrapure Standards, Norway) was rye, and in particular, assess variations in the concentrations analysed at the beginning and at the end of each analytical  Author's personal copy Environ Sci Pollut Res sequence to check the calibration of the instrument. were certain differences between uptake of Sb by wheat and Additionally, certified reference material NIST 1573a rye as well as in plant uptake of different Sb forms. (Tomato leaves) from the National Institute of Standards Compared to the control, the most significant increase of Sb and Technology (NIST, Gaithersburg, MD, USA) was concentration was observed for seeds, and the least for analysed together with plant samples (determined/certified leaves. In most cases, rye was capable of accumulating value for Sb was 92%). larger amounts of Sb than wheat. Although wheat and rye are botanically similar, concen- 2.3 Data processing trations of many organic compounds in the plants may differ (Pomeranz 1988). Concentrations of trace and macro- Data analysis was performed using STATISTICA for elements in wheat and rye may be rather different too Windows 6.0 Software package. The statistical treatment (Sager and Hoesch 2005; Shtangeeva et al. 2011). As is included calculation of mean concentrations of elements seen from Table 1, rye and wheat also differed in the ability and analysis of variances to estimate statistically significant to uptake Sb(III) and Sb(V). Concentrations of Sb in roots, differences between groups of the samples. The logarithmic leaves and seeds of rye were higher when the seedlings model was used to create all curves. This model was found were germinated in the medium spiked with Sb(V) than the the most suitable for presentation of the datasets. Addition- corresponding values in rye seedlings germinated in the ally, correlation analysis and cluster analysis were applied medium spiked with Sb(III). In wheat, the opposite to the experimental data to assess the contribution of situation was observed. Concentrations of Sb were higher specific factors that may have an impact on the accumula- in roots, seeds and leaves of wheat seedlings germinated in tion of Sb in plants and to estimate the effects of Sb on the medium spiked with Sb(III) compared to those in all uptake and distribution of macro- and trace elements in parts of the wheat seedlings geminated in the medium different parts of the plants. enriched with Sb(V), although statistically significant differences were registered only for roots, but the same tendency was also observed for seeds and leaves of wheat 3 Results and discussion seedlings. Possible explanations of this observation are the following: (1) Sb(III) did not oxidize completely to Sb(V) 3.1 Antimony uptake by rye and wheat seedlings in the germination medium, and (2) different plant species are capable of identifying Sb(III) and Sb(V) and are able to Concentrations of Sb in leaves, roots and seeds of 4-day-old take up the preferred form selectively. rye and wheat seedlings germinated in control (Sb-free) Parsons and co-authors (2008) studied uptake of As by medium and in the media spiked with Sb(III) or Sb(V) are corn seedlings grown hydroponically in media spiked either shown in Table 1. Concentration of Sb in seeds of the with As(V) or with As(III). It was found that after the As control seedlings was at least ten times lower than in roots (V) and As(III) treatments, concentrations of As in the plant and leaves of the seedlings germinated under control roots were 95 and 112 mg kg−1, respectively. However, in conditions. When seedlings were germinated in the media the shoots, As concentrations were 18 mg kg−1 after the As spiked with Sb, the concentration of this trace element (V) treatments and 12 mg kg−1 after treatments with As(III). increased significantly in all plant parts. However, there On the first glance, these results seem contrary to our Table 1 Mean concentrations±SD of Sb (milligrammes per kilogramme) in wheat and rye seedlings germinated under control (Sb-free) conditions and in the media spiked with Sb(III) and Sb(V) Treatments Control Sb(III) Sb(V) Wheat Rye Wheat Rye Wheat Rye Roots 1.05±0.21a 2.57±0.76a 68.8±11.5c 42.5±10.0bd 32.6±9.7 64±9b Seeds 0.07±0.03a 0.08±0.04a 13.9±3.9 21.4±5.2 10.1±2.3 34.0±10.9b Leaves 0.98±0.14a 1.56±0.32a 3.06±1.00 8.33±4.02bd 2.16±0.66 33.2±11.2b a Differences between Sb concentrations in the seedlings germinated in Sb-free medium and in media spiked with Sb are statistically significant (P< 0.05) b Differences between Sb concentrations in wheat and rye seedlings treated by the same form of Sb are statistically significant (P<0.05) c Differences between Sb concentrations in wheat seedlings treated by Sb(III) and Sb(V) are statistically significant (P<0.05) d Differences between Sb concentrations in rye seedlings treated by Sb(III) and Sb(V) are statistically significant (P<0.05)  Author's personal copy Environ Sci Pollut Res experimental data. However, as was recently shown, despite The dynamics of the leaf biomass of wheat seedlings is chemical similarities between As and Sb, the biogeochem- shown in Fig. 1. With time, the biomass of control seedlings ical behaviour of these trace elements may be different increased. When control seedlings were transferred to water (Casiot et al. 2007; Kilgour et al. 2008; Tschan et al. 2009; spiked with Sb, the plant development was suppressed Shtangeeva et al. unpublished). Therefore, experimental (Fig. 1a). Development of leaf biomass of wheat seedlings data on As plant uptake should be used with caution to grown in water enriched with Sb(V) was in fact stopped, simulate the behaviour of Sb in plants. while biomass of plants grown in Sb(III) enriched water Recently, Tschan and co-authors (2010) reported results increased with time, although the level of the increase was of pot experiments with sunflower and maize grown in soil less than was observed for the control plants. When seedlings spiked with Sb(III) and Sb(V). They found that accumula- germinated in Sb-spiked solution were then transferred to Sb- tion of Sb tended to be slightly higher after the Sb(V) free media and grown in the clean water for 5 days, the treatment in sunflower, while no difference in Sb uptake biomass of the seedlings constantly increased with time. between the two Sb treatments was found in maize. As one Interestingly, in this case, leaf biomass of wheat seedlings can see, these authors also observed different Sb accumu- germinated in Sb(V) spiked medium increased even more lation in two different plant species. It should be remem- significantly compared to biomass of control seedlings. bered however that uptake of elements by plants grown in Figure 2 illustrates results of cluster analysis of 4-day- so different media as soil and aqueous solution may be old rye and wheat seedlings germinated under control difficult to compare. 3.2 Effects of Sb accumulation on wheat and rye seedlings The accumulation of Sb in rye and wheat seedlings resulted in statistically significant (P<0.05) variations in concentrations of many macro- and trace elements in different plant parts. In roots of wheat and rye seedlings, concentrations of Mg, Ti and K decreased compared to concentrations of the same elements in roots of the control plants. Besides, in roots of wheat, concentration of Co, and in roots of rye, concentration of Rb were lower than in roots of the control plants. In seeds of wheat, an increase of Sb resulted in decrease of K and increase of Mn. In seeds of rye, a statistically significant increase of seed Sb concentration was accompanied by increase of Li and Al and decrease of Mo concentrations compared to concen- trations of the elements in seeds of the control plants. No appreciable influence from Sb to the levels of other elements was found in leaves of any of the two plant species. This is probably because concentration of Sb increased less significantly in leaves as compared to seeds and roots. Such an unbalance in concentrations of macro- and trace elements in the seedlings resulting from the bioaccumula- tion of Sb could provide certain variations in the physio- logical state of the plants. It was found that enhanced uptake of Sb by rye seedlings caused necrosis of the plant leaves. As a consequence, a large part of the rye seedlings died before the end of the experiment. On the other hand, no visible symptoms of phytotoxicity, such as chlorosis or Fig. 1 Dynamics of leaf biomass of wheat seedlings. a Seedlings necrosis, were observed for wheat seedlings. Thus, we may germinated during 4 days under control conditions (in Sb-free assume that rye was more sensitive to the treatments than medium) transferred to vessels filled with clean water (1), water spiked with trivalent Sb (2) and water spiked with pentavalent Sb (3); wheat. This different sensitivity of rye and wheat seedlings b Seedlings germinated under control conditions (1) and in solutions to Sb impact might be a result of physiological differences enriched with trivalent Sb (2) and pentavalent Sb (3) transferred to between the two plant species in the Sb tolerance. vessels filled with clean water  Author's personal copy Environ Sci Pollut Res tration of Sb both in roots and in leaves decreased with time (Fig. 3). From this fact, it may be concluded that Sb was easily taken up by the plant and in a similar fashion easily removed from it when the plant was brought into a growth medium with no Sb. Living organisms have an ability to decrease uptake of toxic elements in order to survive in the presence of unwanted substances (Nagajyoti et al. 2010). Besides, one may assume that after such a fast uptake of Sb by the plants, it was not bound tightly to organic molecules of the plant cells. Plants have evolved several mechanisms preventing undesirable effects from toxic metals, including reduction of metal uptake by changes in the kinetic properties of transporters and exudation of complexing agents (Kochian et al. 2002). Metal influxes and effluxes are controlled by plants considering the needs of the whole plant to maintain metal-ion homeostasis. At the moment, we have only limited information on efflux from plants As and P, elements chemically similar to Sb. As was reported, Fig. 2 Cluster analysis (Ward's method) of leaves (a), seeds (b) and roots (c) of 4-day-old rye and wheat seedlings germinated under control conditions and in the media spiked with Sb(III) or Sb(V) conditions and in the media spiked with Sb(III) and Sb(V). The analysis was performed on the basis of concentrations of all determined in the plants elements. For each plant part (leaves, seeds and roots), a good separation of the samples into two groups—wheat and rye—was observed. Seeds of both plant species germinated in Sb-free medium were separated from seeds of the seedlings germinated in Sb- spiked media. However, for roots and leaves, we did not observe such a good separation. 3.3 Dynamics of Sb plant concentrations. Dependence of Sb uptake on the Sb form in the growth medium and plant species Fig. 3 Variations in Sb concentrations in roots (a) and leaves (b) of When 4-day-old seedlings germinated in Sb-spiked media wheat seedlings transferred to vessels filled with clean water after were transferred to vessels filled with clean water, concen- germination during 4 days in media enriched with Sb(III) and Sb(V)  Author's personal copy Environ Sci Pollut Res following uptake of arsenate by roots, some of the arsenate may be lost from the cells via efflux to the external medium (Xu et al. 2007); this is similar to the situation for phosphate, which can also be lost via efflux especially under high P concentrations (Mimura 1999). The mecha- nism of arsenate efflux is not known, but may be similar to that of phosphate efflux which is thought to be via anion channels (Mimura 1999). Zhao and co-authors (2009) reported that within 24 h of exposure to As, a significant As efflux was observed, suggesting rapid cycling of As between plant roots and the medium. It appears that the As efflux by roots is very rapid immediately following As uptake. According to several authors, trivalent Sb compounds are more toxic than pentavalent forms of Sb (Winship 1987; Gurnani et al. 1992; Filella et al. 2002a; Wilson et al. 2010). He and Yang (1999), however, expressed the opposite view based on the experimental evidence. It may be suggested that toxic effects of different Sb forms may be different for different plant species. We found that treatment with Sb(V) was probably more toxic for rye seedlings since they all died before end of the experiment after treatment with pentavalent Sb. More significant impact on wheat leaf biomass was also observed after treatment with Sb(V) compared to treatment with Sb(III) (Fig. 1a). The dynamics of Sb in roots and leaves of rye and wheat seedlings germinated in the medium spiked with Sb(III) and then grown in vessels filled with clean water is shown in Fig. 4. The variations in root Sb concentrations and the Fig. 4 Comparison of dynamics of Sb concentrations in roots (a) and level of Sb concentrations in the roots of wheat and rye leaves (b) of wheat and rye seedlings transferred to vessels filled with seedlings were similar for both plant species. Concentration clean water after germination during 4 days in media enriched with Sb of Sb in rye leaves was much higher than in leaves of (III) wheat. Probably, this was one of the main reasons of necrosis of the rye leaves. Figure 5 demonstrates the dynamics of Sb in roots and 3.4 Correlation between Sb and As leaves of wheat seedlings germinated in control medium and subsequently grown in water spiked with Sb(III) or Sb Although As and Sb are chemical analogues and thus a (V). With time, roots of the seedlings grown in the medium similar behaviour of the elements in plants might be enriched with Sb(III) accumulated more Sb, and the expected, no correlation between As and Sb in leaves increase of the root Sb concentration was almost linear. and seeds was found. Therefore, it may be assumed that However, the increase of Sb in leaves was followed by a their transfer within a plant may have a different nature. subsequent decrease of its concentration. It may be Only in roots of the plants grown in Sb-spiked medium, suggested that in due course, a similar trend might be the correlation between As and Sb was statistically observed in roots too. At least a tendency of saturation of significant and positive. Positive correlation between roots with Sb is seen for the seedlings grown in the medium these elements in roots may be explained by similar amended with Sb(V) (Fig. 5a). To a certain degree, this was mechanism of their uptake by plants. Besides, a also observed for leaves of the seedlings grown in the statistically significant correlation between As and Sb medium spiked with pentavalent Sb (Fig. 5b). Interestingly, in roots was observed only in the case when Sb older wheat seedlings (age from 4 to 9 days) accumulated concentration in the growth medium was high enough. more Sb when grown in water spiked with Sb(V) compared No correlation between Sb and As was found when with the seedlings of the same age grown in water spiked concentration of Sb in roots was low. As was recently with Sb(III). For younger (4-day-old) seedlings, the shown (Xia 2011), statistically significant positive corre- opposite trend was observed (Table 1). lation between As and Sb in plants is not always evident.  Author's personal copy Environ Sci Pollut Res Acknowledgements Irina Shtangeeva thanks the Ellen Gleditsch Stipendiefond for a fellowship providing her possibility to perform analyses at the Norwegian University of Science and Technology. References Baroni F, Boscagli A, Protano G, Riccobono F (2000) Antimony accumulation in Achillea ageratum, Plantago lanceolata and Silene vulgaris growing in an old Sb mining area. Environ Pollut 109:347–352 Belzile N, Chen YW, Wang ZJ (2001) Oxidation of antimony (III) by amorphous iron and manganese oxyhydroxides. Chem Geol 174:379–387 Burford N, Carpenter Y-Y, Conrad E, Saunders CDL (2010) The chemistry of arsenic, antimony and bismuth. In: Sun H (ed) Biological chemistry of arsenic, antimony and bismuth. 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