Europium and Cerium Accumulation in Wheat and RyeSeedlings

Irina Shtangeeva

Received: 8 December 2013 /Accepted: 7 April 2014# Springer International Publishing Switzerland 2014

Abstract The purposes of this research were (1) tocompare level of uptake and accumulation of Eu andCe by wheat and rye seedlings grown in soil spiked withthese metals, (2) to estimate short-term variations of Euand Ce in soil and in plants and (3) to study effects of Euand Ce accumulation on concentrations of other macro-and trace elements in the plants. The experiments wereperformed in a naturally illuminated greenhouse.Instrumental neutron activation analysis was used todetermine concentrations of rare earth elements andessential nutrients and trace elements in the plants andsoil. The experimental results indicate that addition ofEu and Ce to soil can lead to enhanced uptake of thetrace elements by plants. Plants more easily accumulat-ed Eu than Ce. Moreover, for rye, differences betweenamounts of Ce in the seedlings grown in Ce-spiked soiland in Ce-free soil were statistically insignificant.During the first hours after transfer of seedlings to soilspiked with Eu, concentration of Eu in the roots of bothplant species increased significantly. An increase of leafEu concentration was also observed, however, thesevariations were not as marked as those in roots. Duringthe following 10-day growth in the Eu-spiked soil,concentration of Eu in plants constantly increased. Thebioaccumulation of Eu resulted in certain decrease of Euin the rhizosphere soil. However, no variations in soil Ceconcentrations were found. The accumulation of Eu andCe in rye and wheat seedlings did not significantly affect

concentrations of essential plant nutrients and otherREEs.

Keywords Rare earth elements . Plant uptake .

Short-term variations . Neutron activation analysis

1 Introduction

The rare earth elements (REEs) are chemically similarmetallic elements (15 lanthanides plus scandium andyttrium). The REEs have close related electronic con-figurations leading to very similar chemical and physi-cal properties of the elements. Except for Ce, whichoccurs in the environment both as trivalent (+3) andtetravalent (+4) ions and Eu (it was found in +2 and +3 valence state), all REEs appear in trivalent valencestate under ordinary environmental conditions.

Rare earth elements are widely distributed in theenvironment (Chen 2011). Despite the name, they arenot quite rare in the nature. The abundance of Ce in soilis almost equal to that of Cu and Zn. The abundance ofthe rarest REEs, Lu and Tm, in the majority of soils iscomparable to that of Cd and Se. While REEs areabundant in soil, their concentrations in plants are usu-ally low (Tyler 2004; Brioschi et al. 2013). The biogeo-chemical behaviour of REEs is not fully understood.Until recently, REEs were not characterised either asessential plant nutrients or as environmentally hazard-ous metals. However, the last experimental studies dem-onstrated toxic effects of REEs for bacteria (Ozaki et al.2006; Haferburg and Kothe 2007), plants (Babula et al.

Water Air Soil Pollut (2014) 225:1964DOI 10.1007/s11270-014-1964-3

I. Shtangeeva (*)Chemical Department, St. Petersburg University,Universitetskaya nab., 7/9, St. Petersburg 199034, Russiae-mail: shtangeeva@gmail.com

2008; Liu et al. 2012a), and animals (Che et al. 2011). Itis likely that both toxic and beneficial effects of REEsare similar to those of other trace metals.

Rare earth elements are critical to hundreds of hightechnical applications, many of which define ourmodern way of life. The rapidly growing demand forREEs has led to an exponential increase of globalREE mining production from about 50 kt per year in1990 to 130 kt per year in 2010 (Haxel et al. 2002;Chen 2011). This growing use resulted in environ-mental contamination, and REEs are therefore con-sidered now as emerging pollutants (Kulaksiz andBau 2011; Yang et al. 2012).

China controls approximately 97 % of the world’sREE market (Humphries 2010). Besides, in China,REEs have been used in agriculture since the 1970s ofthe last century; in particular, REE-based fertilisers werewidely used to increase the yield and quality of crops(Liu et al. 2012b). Pot and field experiments have beenperformed to demonstrate the beneficial influence ofREEs on plant growth and soil properties. Till now,the effects of REEs on plants and soils have been re-ported mainly by Chinese researchers. Notice, however,that reported data may be contradictory. For example,Maheswaran et al. (2001) studied the effects of La andCe on seed germination using various rates ranging from0 to 0.16%. They found that both shoot and root lengthswere not improving with application of the REEs.Moreover, it was shown that application of La or Ceto the shoots or roots generally reduced corn andmungbean growth rate (Diatloff et al. 1999). Theauthors concluded that in view of toxicity of REEsto these crops, it seemed unlikely that reported bene-ficial effects could result from direct influence of theelements on the growth processes of a particular plant.Such a beneficial action may result from variousindirect effects that influence agronomic performanceof crop plants. Besides, it seems that positive responseis possible when the soils contain low quantities (lessthan 10 mg kg−1) of available REEs (Maheswaranet al. 2001; Diatloff et al. 2008). Thus, the contradic-tory observations may also be explained by differentlevels of applied REEs. At present, Chinese scientistsstate themselves that REEs have promoting effects atlow concentrations and negative effects at compara-tively high concentrations (Liu et al. 2013; Zhanget al. 2013a, b).

A considerable number of publications are dedicatedto the distribution of REEs in different cereal crops

(Ding et al. 2006; Fang et al. 2007; Shtangeeva andAyrault 2007; Challaraj Emmanuel et al. 2010; Jianget al. 2012; Šmuc et al. 2012; Liu et al. 2013).Concentrations of La and Ce in plants were found tobe 10–100 times higher than concentrations of otherREEs. Probably, this is a reason why many publicationsare devoted to these elements in comparison to otherREEs.

In this report, the results of experiments with Eu andCe will be discussed. Compared to other REEs, both Euand Ce can change (depending on the environmentalconditions) their valence state and thus, can serve asindicators of biogeochemical processes.

The Eu3+ ion has similar atomic radius as the Ca2+

ion and therefore may replace Ca2+ in the calcium/calmidulindependent phytochrome signal transduc-tion system and, as a consequence, play an importantrole in the plant development by promoting Ca trans-portation across plasma membrane (Zeng et al. 2003).Till now, there have been not so many reports onbehaviour of Eu in different plants and beneficial ortoxic effects of this trace element on the plants (Tianet al. 2003; Zeng et al. 2003; Shtangeeva and Ayrault2007; d'Aquino et al. 2009; Bertoldi et al. 2009;Vijayaraghavan et al. 2010; Yang et al. 2012; Zhanget al. 2013a, b).

Cerium is the most abundant of the REEs.According to recent experimental studies, uptake ofK, Mg, Ca, Na, Fe, Mn, Zn, Cu and Mo in the rootsand shoots may be affected as a result of the exposureto Ce+3, thus indicating that Ce+3 is able to influencethe nutritional status of roots and shoots and furtheraffect the plant growth (Diatloff et al. 2008; Liu et al.2012a). But on the other hand, it was found thataddition of Ce to soil may promote N and C assimi-lations, increase PSII activities and improve the plantdevelopment (Zhao et al. 2012). It may be, however,suggested that these different conclusions on effectsof Ce on plants may be due to different approachesused for the experimental studies.

The purposes of this research were (1) to compare thelevel of uptake and accumulation of two REEs, Eu andCe, by wheat and rye seedlings grown in soil spikedwith these metals, (2) to estimate the short-term (fromfirst hours to first days after transfer of the seedlings tosoil) variations of Eu and Ce in soil and in different plantparts and (3) to study the effects of Eu and Ce accumu-lation on concentrations of other macro- and trace ele-ments in the plants.

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2 Materials and Methods

2.1 Experimental Design

Seeds of wheat Triticum aestivum L. and rye Secalecereale L. were germinated during 4 days on a moistfilter paper. After the end of germination, the first por-tion of plant samples was collected and saved for ele-mental analysis. The rest of the 4-day-old germinatedseedlings were transferred to ceramic pots filled withpodzolic soil (7 kg of soil in a pot). Before plants weretransferred to pots, soil in the pots was watered eitherwith 0.35 L of tap water (control), or with the sameamount of water spiked with nitrate of Eu (Eu(NO3)3×6H2O)-experiment 1, or nitrate of Ce (Ce(NO3)3×6H2O)-experiment 2. Based on published data, dosesfor each compound were chosen considering ecologi-cally relevant levels found in soils. Concentrations of Euand Ce in the water were 10 and 50mgL−1, respectively.The soil was mixed and allowed to equilibrate for 3 daysbefore seedling transplanting. Then, the bulk soil fromall pots was taken for analysis. The temperature in thenaturally illuminated greenhouse was typically 25 °Cduring the day and 20 °C at night. Soil pH was 6.3±0.2in the course of the tests. Plants, together with rhizo-sphere soil (i.e. soil from the surface of the plant roots)were collected seven times, namely within 0.5, 2.5 and5.5 h and 1, 2, 6 and 10 days after transfer of theseedlings to soil. The experiments were performed intriplicate. Plants were carefully washed just after sam-pling and air-dried at room temperature to constantweight. Then, the plants were divided into roots andleaves. Soil samples were also air-dried to constantweight before analysis. Samples were then placed inplastic bags and kept in a fridge till analysis.

2.2 Elemental Analysis

Low concentrations of REEs in plants require an appli-cation of analytical techniques which can provide asensitive and accurate determination of the trace ele-ments in the plant material. In this work, for this aiminstrumental neutron activation analysis was used ap-plying the k0-method (Lin and Henkelmann 2004). Plantand soil samples were weighed and placed in quartzampoules. In addition, Au–Al wire (10 mg, 0.5 mmdiameter) was used as a flux monitor. The samples wereirradiated at BER II reactor of Helmholtz-Zentrum,Berlin for 18 h (soils) and 24 h (plants) in a thermal

neutron flux of 1×1014 n cm−2 s−1. The neutron fluxparameters were determined and found to be as follow:epithermal flux shape factor α=0.296±0.026, thermal toepithermal flux ratio f=149±24. The irradiated sampleswere measured twice within 1 and 3 weeks after the endof irradiation using high pure germanium detectors. Thecertified reference materials (CRMs) NIST 1573 (toma-to leaves) from the National Institute of Standards andTechnology (NIST, Gaithersburg, MD, USA) andSOIL-7 (International Atomic Energy Agency) wereanalysed together with plant and soil samples. Theresults of the analysis of the CRMs showed a goodagreement with certified values. Certified values of Ceand Eu in CRM SOIL-7 are 61 and 1.0 mg kg−1, re-spectively, and measured values for Ce is 57 and1.1 mg kg−1 for Eu. Certified values of Ce and Eu inCRM tomato leaves are 1.6 and 0.04 mg kg−1, respec-tively, and measured values are 1.4 mg kg−1 (Ce) and0.05 mg kg−1 (Eu).

2.3 Data Processing

A statistical software package (Statistica for Windows6.0) was used for calculating mean concentrations ofelements and analysing the variances in order to esti-mate statistically significant differences between thegroups of samples. Additionally, correlation analysisand principal component analysis were applied to thedata sets.

3 Results and Discussion

3.1 Differences between Element Concentrationsin Wheat and Rye Seedlings Grown in Non-Spikedwith REEs Soil

Wheat and rye are botanically similar and differ only atthe level of the genus: wheat belongs to the genusTriticum and rye to the genus Secale. Meanwhile, con-centrations of several elements in wheat and rye grownunder the same conditions in the non-spiked with REEsoil were found to be rather different (Tables 1 and 2).Concentrations of Ca, As, Br, Sr and Eu were statisti-cally significantly higher in roots of rye than in roots ofwheat; root Cs concentration was higher (P<0.05) inwheat as compared to rye. Differences between leavesof wheat and rye were less marked than in roots.Concentration of Sc was statistically significantly

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higher, and concentration of Na was lower (P<0.05) inrye leaves as compared to those in leaves of wheat.

Concentrations of many elements in roots werehigher than in leaves. Roots served as a natural barrierpreventing the transfer of most chemical elements toupper plant parts. The exceptions were K and Br. Theirconcentrations in leaves were much higher than in roots.Concentration of Rb (chemical analogue of K) was alsoa bit higher in leaves than in roots.

3.2 Concentrations of Eu and Ce in Soil and in Plants

Once soil was spiked with Eu and Ce, concentration ofEu in the soil increased. This might be expected sinceconcentration of Eu in the water, which was added tosoil, was much higher in comparison with initial Euconcentration in the soil. However, Ce concentration inthe soil spiked with Ce did not change compared tocontrol (Table 3). Possible explanation might be that

Table 1 Mean concentrations (mg kg−1)±SD of elements in roots of wheat and rye seedlings grown in the REE-free soil (1) and in soilspiked either with Eu (2) or with Ce (3)

Roots

1 2 3

Wheat (21) Rye (21) Wheat (22) Rye (23) Wheat (24) Rye (20)

Na,% 0.53±0.09 0.50±0.17 0.59±0.09 0.52±0.10 0.60±0.14 0.45±0.10

K,% 1.6±0.4 2.1±0.5 1.8±0.3 1.7±0.5 1.6±0.5 2.4±0.6

Ca,% 0.46±0.11 0.93±0.30* 0.69±0.16 0.75±0.15 0.55±0.07 0.78±0.19

Sc 0.11±0.04 0.12±0.08 0.10±0.02 0.09±0.04 0.09±0.06 0.11±0.03

Cr 2.1±0.5 2.4±1.2 1.8±0.2 1.5±0.5 1.8±0.6 1.8±0.2

Fe 697±222 691±339 720±151 611±228 654±261 889±455

Co 0.61±0.23 0.61±0.20 0.51±0.11 0.69±0.30 0.59±0.32 0.79±0.36

Zn 193±58 161±65 182±44 190±61 189±63 152±65

As 0.58±0.11 0.78±0.12* 0.52±0.14 0.65±0.29 0.47±0.15 0.90±0.10

Br 10±3 16±3* 9.4±2.4 12±3 11±4 11±1

Rb 61±18 56±13 49±3 47±13 51±11 66±12

Sr 23±4 36±9* 25±7 33±10 28±4 39±12

Sb 0.08±0.03 0.09±0.04 0.08±0.01 0.11±0.06 0.08±0.04 0.09±0.03

Cs 0.77±0.29 0.39±0.07* 0.35±0.06+ 0.33±0.07 0.54±0.18 0.43±0.12

Ba 19±5 23±9 17±3 17±8 18±5 20±7

La 0.36±0.13 0.38±0.20 0.41±0.12 0.39±0.24 0.29±0.11 0.36±0.04

Ce 0.77±0.23 1.1±0.6 0.79±0.35 0.61±0.24 1.1±0.3+ 2.4±1.3

Sm 0.10±0.02 0.11±0.05 0.12±0.03 0.10±0.04 0.11±0.05 0.09±0.04

Eu 0.04±0.01 0.16±0.06* 4.7±3.7+ 10±6+ 0.05±0.05 0.16±0.06

Tb <0.004 <0.004 <0.02 <0.02 <0.008 <0.02

Yb <0.02 <0.02 <0.02 <0.02 <0.02 <0.02

Lu <0.08 <0.08 <0.08 <0.08 <0.08 <0.08

Hf 0.03±0.01 0.04±0.02 0.04±0.02 0.05±0.04 0.03±0.02 0.05±0.03

Ta <0.3 <0.3 <0.3 <0.3 <0.3 <0.3

Th 0.10±0.05 0.11±0.05 0.09±0.02 0.10±0.08 0.08±0.03 0.10±0.33

U 0.43±0.04 0.35±0.16 0.42±0.08 0.26±0.12 0.47±0.12 0.29±0.10

The number of samples analysed is shown in parentheses*Differences between concentration of the element in wheat and rye seedlings grown in REE-free soil (control) are statistically significant(P<0.05)+Differences between concentration of the element in the seedlings grown in REE-free soil and in soil spiked with REE are statisticallysignificant (P<0.05)

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Ce could leach to deeper soil layers. However, Ce and Euconcentrations in the soil taken from the bottom of the potswere the same both at the beginning and the end of theexperiment (data on concentrations of the elements in soiltaken from bottom of pots are not present). One importantpoint to remember is that the initial concentration of Ce insoil was already rather high (on the average, 50 mg kg−1).Moreover, we determined total soil Ce concentration (con-centration of Ce in aluminosilicates of the soil). Small

amount of water containing 50 mg L−1 Ce which wasadded to a large volume of soil did not lead to variationin total soil Ce concentration. Probably, Ce added to soilcould remain in the soil solution (the film of water whichcovers the particles in moist soil), and partly might betaken by the plant roots from the solution.

The addition of Eu and Ce to soil resulted in theuptake of the trace elements by plants (Tables 1 and2). It is notable that both rye and wheat accumulated

Table 2 Mean concentrations (mg kg−1) ± SD of elements in leaves of wheat and rye seedlings grown in the REE-free soil (1) and in soilspiked either with Eu (2) or with Ce (3)

Leaves

1 2 3

Wheat (23) Rye (22) Wheat (22) Rye (21) Wheat (24) Rye (20)

Na,% 0.09±0.02 0.03±0.01* 0.09±0.03 0.03±0.01 0.07±0.02 0.03±0.01

K,% 4.6±1.0 5.0±1.1 5.0±0.8 5.8±1.1 5.1±1.1 5.7±1.6

Ca,% 0.56±0.15 0.59±0.16 0.74±0.36 0.72±0.29 0.51±0.19 0.74±0.32

Sc 0.011±0.002 0.02±0.01* 0.013±0.004 0.016±0.005 0.010±0.003 0.010±0.002+

Cr 0.45±0.21 0.47±0.24 0.43±0.12 0.43±0.14 0.27±0.07 0.56±0.19

Fe 155±29 169±44 163±16 199±36 151±25 174±52

Co 0.03±0.01 0.05±0.01 0.03±0.01 0.04±0.02 0.04±0.03 0.05±0.02

Zn 55±10 57±13 52±7 71±14 54±14 60±13

As <0.09 <0.09 <0.09 <0.09 <0.09 <0.09

Br 20±5 22±9 14±2+ 14±4 15±5 19±4

Rb 88±22 89±39 71±10 83±24 85±20 84±20

Sr 15±5 20±8 17±6 19±9 16±7 20±9

Sb 0.04±0.02 0.06±0.02 0.03±0.01 0.05±0.02 0.04±0.01 0.05±0.02

Cs 0.26±0.06 0.25±0.13 0.13±0.02+ 0.17±0.03 0.19±0.03+ 0.20±0.05

Ba 15±7 16±9 14±6 13±7 14±6 15±8

La 0.07±0.02 0.08±0.03 0.07±0.03 0.09±0.05 0.05±0.01+ 0.07±0.01

Ce 0.15±0.01 0.31±0.23 0.20±0.09 0.23±0.14 0.38±0.22+ 0.38±0.25

Sm 0.008±0.003 0.008±0.005 0.010±0.005 0.007±0.003 0.008±0.005 0.007±0.003

Eu 0.03±0.01 0.04±0.01 0.41±0.28+ 0.45±0.30+ 0.04±0.02 0.05±0.02

Tb <0.002 <0.002 <0.002 <0.003 <0.003 <0.002

Yb <0.01 <0.01 <0.01 <0.01 <0.01 <0.01

Lu <0.08 <0.08 <0.08 <0.08 <0.08 <0.08

Hf <0.02 <0.02 <0.02 <0.02 <0.02 <0.02

Ta <0.2 <0.2 <0.2 <0.2 <0.2 <0.2

Th <0.007 <0.007 <0.01 <0.01 <0.01 <0.02

U <0.03 <0.03 <0.03 <0.02 <0.1 <0.1

The number of samples analysed is shown in parentheses*Differences between concentration of the element in wheat and rye seedlings grown in REE-free soil (control) are statistically significant(P<0.05)+Differences between concentration of the element in the seedlings grown in REE-free soil and in soil spiked with REE are statisticallysignificant (P<0.05)

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more Eu than Ce. Furthermore, level of translocationof Eu from roots to leaves was also higher as com-pared with transfer of Ce between these two plantparts. The similarities in the chemistry of Eu(III) andCe(III) have led to the assumption that there may beno fractionation during uptake by plants (Bulman1994). However, as was recently reported (Dinget al. 2006; Semhi et al. 2009), there is some frac-tionation of the REEs, but the mechanisms by whichthese occur are not quite clear. One of the possibleexplanations may be that Ce(III) has a solution

chemistry similar to its trivalent neighbours (otherREEs), however, its oxidation to Ce(IV), which couldtake place in the rhizosphere soil, might result in theformation of a less soluble form (Sholkovitz andSchneider 1991).

3.3 Effects of Eu and Ce Bioaccumulation on Uptakeof Other Elements by Rye and Wheat

Numerous studies demonstrated that different metalscan have an inhibitory effect on the fluxes of essential

Table 3 Mean concentrations (mg kg−1)±SD of elements in the rhizosphere soil of wheat and rye seedlings grown in the REE-free soil (1)and in soil spiked either with Eu (2) or with Ce (3)

Soil

1 2 3

Wheat (24) Rye (24) Wheat (23) Rye (24) Wheat (23) Rye (22)

Na,% 0.74±0.08 0.85±0.16 0.78±0.08 0.77±0.07 0.80±0.07 0.79±0.11

K,% 1.4±0.1 1.6±0.3 1.5±0.1 1.6±0.2 1.5±0.3 1.5±0.2

Ca,% 2.7±0.4 2.4±0.5 2.5±0.3 2.6±0.4 2.6±0.4 2.6±0.4

Sc 6.3±0.4 5.8±0.7 6.0±0.8 5.4±0.5 5.9±0.4 6.0±0.6

Cr 33±10 35±11 45±18 68±26 31±13 45±20

Fe,% 4.0±0.4 3.6±0.6 3.6±0.5 3.5±0.3 3.6±0.4 3.7±0.4

Co 7.9±0.6 7.2±1.2 7.6±1.0 7.0±0.6 7.1±0.5 7.6±0.7

Zn 59±9 58±11 66±14 55±13 54±9 55±11

As 6.9±0.5 5.5±0.9 6.0±0.6 6.0±0.7 6.0±0.7 6.5±0.9

Br 1.4±0.3 1.3±0.4 1.2±0.3 1.1±0.2 1.2±0.2 1.2±0.2

Rb 56±7 58±12 58±6 61±7 58±4 59±2

Sr 203±56 193±66 187±29 165±37 184±46 159±47

Sb 0.79±0.13 0.73±0.22 0.80±0.12 0.76±0.09 0.74±0.10 0.75±0.09

Cs 1.6±0.1 1.7±0.2 1.9±0.4 1.6±0.2 1.6±0.2 1.8±0.2

Ba 726±66 725±132 700±98 723±80 726±80 700±41

La 24±3 24±3 25±2 21±2 23±2 23±3

Ce 52±11 48±8 47±4 48±14 51±7 53±7

Sm 4.6±0.7 4.1±0.5 4.2±0.4 4.1±0.6 4.2±0.6 4.2±0.4

Eu 0.81±0.05 0.81±0.10 11±6* 12±8* 0.83±0.14 0.80±0.04

Tb 0.68±0.11 0.59±0.09 0.65±0.06 0.68±0.10 0.60±0.10 0.64±0.08

Yb 1.9±0.3 1.6±0.3 1.9±0.3 1.8±0.3 1.7±0.1 1.6±0.1

Lu 0.37±0.04 0.33±0.08 0.32±0.05 0.37±0.08 0.33±0.07 0.32±0.06

Hf 6.2±0.6 6.0±2.5 5.2±1.1 5.3±2.4 5.7±2.1 4.7±1.3

Ta 0.56±0.11 0.58±0.12 0.59±0.15 0.50±0.05 0.51±0.07 0.56±0.12

Th 6.9±1.7 5.7±1.1 6.0±0.5 5.8±0.7 5.9±1.1 6.3±1.2

U 3.1±0.7 2.6±0.4 2.8±0.6 2.7±0.5 2.9±0.4 2.7±0.3

The number of samples analysed is shown in parentheses*Differences between concentration of Eu in the rhizosphere soil of the seedlings grown in Eu-free soil (control) and in soil spiked with Euare statistically significant (P<0.05)

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nutrients in a plant (Adriano 2001; Ahsan et al. 2009;Solanki and Dhankhar 2011). We may also expectsimilar effects for REEs. As was reported, REEs canregulate the plant growth through changing the dis-tribution of enzymes (Ye et al. 2008) and significant-ly affect membrane stability (Hu et al. 2004; Xu et al.2012). Therefore, the REEs can influence the ionicinteractions with the cell. In particular, it was shownthat La can affect an uptake of K, Sc, Mn, Se and Rbeither increasing or decreasing the uptake rates(Wang et al. 2008). However, in our experiment,accumulation of Eu or Ce in rye and wheat seedlingshad little or no effect on the uptake of essential plant

nutrients as well as other REEs. In leaves, a statisti-cally significant decrease of La concentration wasobserved as a result of growth of wheat seedlings inCe-spiked soil, and concentration of Sc, the traceelement which is chemically similar to REEs, wasstatistically significantly lower in leaves of rye seed-lings grown in soil spiked with Ce. Besides, concen-tration of Cs in leaves and roots of the wheat seed-lings grown in Eu-spiked soil was statistically signif-icantly lower than Cs concentration in leaves androots of the control wheat seedlings (Tables 1 and2). It was found that correlation between Eu and Cs inroots and leaves of wheat seedlings was statistically

Fig. 1 Score plot of the secondand third principal components ofthe PCA of roots (a) and the firstand second principal componentsof the PCA of leaves (b) of wheatseedlings grown in Eu-free soil(1) and in soil spiked with Eu (2)

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significant and negative (−0.52 in leaves and −0.42 inroots). On the other hand, no correlation between Euand Cs in rye seedlings was observed. Although anincrease of Eu and Ce in roots was more significantthan in leaves, only statistically significant decreaseof root Cs concentrations associated with Eu bioac-cumulation was found. Moreover, these variations inCs concentrations were observed only for wheatseedlings. Besides, an addition of the REEs to soildid not affect the plant development.

Our previous experiments with germination ofwheat T. aestivum seeds in the water spiked with0.01 mg L−1 Eu(NO3)3 showed that the treatmentwas favourable for a following growth of the seed-lings in soil (Shtangeeva and Ayrault 2007). In thatexperiment, however, we also observed variations inconcentrations of different macro- and trace elementsin roots, leaves and seeds of the wheat seedlingswhich were germinated in the Eu-spiked medium.Probably, the effects may be more serious at the veryfirst stages of the plant development.

3.4 Principal Component Analysis of Plant Samples

Results of the principal component analysis (PCA)demonstrated that both roots and leaves of wheatseedlings grown in uncontaminated soil and in soilspiked with Eu were rather well separated into two

different groups (Fig. 1). The PC2 (24 % of the totalvariance) was responsible for the separation of rootsof wheat seedlings, and Eu was positively correlatedwith the second PC, while Cs and Rb were nega-tively correlated with the PC2. As was mentionedabove, an increase of Eu in the wheat seedlingsnegatively affected the uptake of Cs by the plants.Meanwhile, differences between Rb concentrationsin roots of control wheat seedlings and in roots ofthe seedlings grown in Eu-spiked soil were notstatistically significant. It is interesting to note thatafter excluding from calculation data on Eu we alsoobtained a good separation of the roots samples, andas before, main contribution was provided by Csand Rb.

Leaves of wheat seedlings were separated into differ-ent groups (control and grown in Eu-spiked soil) by thesecond PC (29 % of the total variance). Sodium and Cswere positively correlated and K was negatively corre-lated with the PC2 (Fig. 1b). Thus, just these elements,but not Eu, were mainly responsible for the separation ofthe wheat leaves into these two groups.

Leaves of rye seedlings grown in Eu-free soil andin soil spiked with Eu were also well separated intodifferent groups. The PC1 (20 % of the total variance)was responsible for the separation, and Zn, Eu, Cs, Feand Sc were highly correlated with the PC1 (Fig. 2).Among these elements, only Eu demonstrated

Fig. 2 Score plot of the first andsecond principal components ofthe PCA of leaves of rye seedlingsgrown in Eu-free soil (1) and insoil spiked with Eu (2)

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statistically significant difference between its concen-trations in leaves of the control rye seedlings andleaves of the rye seedlings grown in the Eu-spikedsoil (Table 2).

Although Eu concentration in roots of rye in-creased significantly compared to control, the PCAdid not demonstrate separation of roots of the ryeseedlings into different groups - control and roots ofthe plants grown in Eu-spiked soil. Besides, accu-mulation of Ce in the plants (its concentration in thewheat seedlings grown in Ce-spiked soil was statis-tically significantly higher than in control, while inrye seedlings, the variations of Ce concentrationswere not statistically significant) also “was not

seen” by the PCA. No separation between controlplants and plants grown in Ce-spiked soil wasfound both for roots and leaves of the rye andwheat seedlings.

3.5 Short-term Variations of Eu and Ce in Plants

Within the first 5.5 h after the transfer of seedlings to soilspiked with Eu, its concentration in roots increased sig-nificantly. An increase of leaf Eu concentration was alsoobserved, although these variations were not as markedas in roots. Figure 3 illustrates the short-term variations ofEu in roots and leaves of rye seedlings. Similar changesin the Eu concentrations were found for wheat seedlings.

Fig. 3 Short-term variations ofEu in roots (a) and leaves (b) ofrye seedlings grown in Eu-freesoil (1) and in soil spikedwith Eu (2)

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Then (during the following 10-day growth in the Eu-spiked soil), concentration of Eu in plants (especiallyin roots) constantly increased. The bioaccumulationof Eu resulted in decrease of Eu concentration in therhizosphere soil from ∼15 mg kg−1 in the beginning ofexperiment up to ∼5 mg kg−1 at the end of the exper-iment (Fig. 4). Thus, both these plant species may besuccessfully used for phytoextraction of Eu from con-taminated soils. Concentration of Ce in roots of theseedlings grown in Ce-spiked soil also increased withtime (Fig. 5). However, this increase (two times ascompared to control) was not as marked as an increaseof Eu. Besides, no statistically significant variations

in the Ce concentration in leaves and in the rhizo-sphere soil were found.

3.6 Relationships between REEs in Plants and in Soil

The behaviour of REEs in soil and in plants canalso be characterised by relationships between dif-ferent REEs and between REEs and trace elementsthat have chemically similar parameters with theREEs. One could expect that correlation betweenchemically similar elements is bound to be statisti-cally significant and positive. However, our calcu-lations showed that this suggestion is not

Fig. 4 Variations of Euconcentration in the rhizospheresoil (1), roots (2) and leaves (3) ofwheat (a) and rye (b) seedlingsgrown in Eu-spiked soil

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universally true. For example, correlation betweenLa and Sc was statistically significant (P<0.05) andpositive in both soil and different plant parts: cor-relation coefficients were 0.51 in soil, 0.77 in rootsand 0.33 in leaves. Correlation between La and Smwas statistically significant only in soil and in theplant roots (r=0.66 and 0.82, respectively); no cor-relation between these REEs was observed in theplant leaves. Moreover, statistically significant pos-itive correlation between Eu and Ce was registeredonly in soil (r=0.39, P<0.05), while no correlationbetween these two elements in roots and leaves wasfound. It may be assumed that behaviour of trace

elements, including REEs, in different media maybe distinct. In plants, REEs, probably, may bemainly included in organic molecules, while in soil,they may be mostly components of inorganiccompounds.

4 Conclusion

Wheat and rye seedlings grown in soil artificially con-taminated with Eu and Ce were capable of accumulatingthe REEs (especially Eu) without serious conse-quences for the plant development and concentrations

Fig. 5 Short-term variations ofCe in roots of wheat (a) and rye(b) seedlings grown in Ce-freesoil (1) and in soil spikedwith Ce (2)

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of essential plant nutrients in different plant parts. Theaccumulation of Eu in roots and leaves of seedlings affectedEu concentrations in the rhizosphere soil. The concentrationof Eu in the soil decreased. However, Ce soil concentrationdid not change significantly. The relationships betweenchemically similar REEs may be statistically significantand positive, however, for some pairs of similar REEs, inparticular, Eu and Ce, positive correlation may be observedin soil, but not found in plants.

Acknowledgements The author acknowledges financial sup-port of DFG Foundation for fellowship to perform the researchand grateful for kindly help and advices of Dr. Dorothea Alber andGregor Bukalis (Helmholtz-Zentrum Berlin).

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