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First published online October 15, 2004; 10.1104/pp.104.046672 Plant Physiology 136:3824-3837 (2004) © 2004 American Society of Plant Biologists Cesium Toxicity in Arabidopsis1Warwick HRI, Warwick CV35 9EF, United Kingdom (C.R.H., H.C.B., J.P.H., A.M., K.A.P., P.J.W.); School of Biological Sciences, The University of Birmingham, Birmingham B15 2TT, United Kingdom (C.R.H., J.P.); and Plant Sciences Division, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, United Kingdom (M.R.B., J.P.H., K.A.P.)
Cesium (Cs) is chemically similar to potassium (K). However, although K is an essential element, Cs is toxic to plants. Two contrasting hypotheses to explain Cs toxicity have been proposed: (1) extracellular Cs+ prevents K+ uptake and, thereby, induces K starvation; and (2) intracellular Cs+ interacts with vital K+-binding sites in proteins, either competitively or noncompetitively, impairing their activities. We tested these hypotheses with Arabidopsis (Arabidopsis thaliana). Increasing the Cs concentration in the agar ([Cs]agar) on which Arabidopsis were grown reduced shoot growth. Increasing the K concentration in the agar ([K]agar) increased the [Cs]agar at which Cs toxicity was observed. However, although increasing [Cs]agar reduced shoot K concentration ([K]shoot), the decrease in shoot growth appeared unrelated to [K]shoot per se. Furthermore, the changes in gene expression in Cs-intoxicated plants differed from those of K-starved plants, suggesting that Cs intoxication was not perceived genetically solely as K starvation. In addition to reducing [K]shoot, increasing [Cs]agar also increased shoot Cs concentration ([Cs]shoot), but shoot growth appeared unrelated to [Cs]shoot per se. The relationship between shoot growth and [Cs]shoot/[K]shoot suggested that, at a nontoxic [Cs]shoot, growth was determined by [K]shoot but that the growth of Cs-intoxicated plants was related to the [Cs]shoot/[K]shoot quotient. This is consistent with Cs intoxication resulting from competition between K+ and Cs+ for K+-binding sites on essential proteins.
Potassium (K) is an essential macronutrient. It is required (as K+) at concentrations of 100 to 150 mM in the cytoplasm of plant cells to activate enzymes and stabilize protein and nucleotide structure (Leigh and Wyn Jones, 1984  ; Marschner, 1995). The cation Cs+ shares similar chemical properties to K+ and competes with K+ for cation binding sites in proteins (Avery, 1995). Unfortunately, Cs+ does not behave identically to K+ and inhibits the activity of many K+-activated enzymes (Avery, 1995). Consequently, Cs+ is potentially toxic to plants. In addition, Cs+ inhibits the inward-rectifying K channels in the plasma membranes of plant cells (White, 1997; White and Broadley, 2000), including the major inward-rectifying K channels involved in plant K nutrition (e.g. AtAKT1 in Arabidopsis [Arabidopsis thaliana]). Excessive Cs+ in the rhizosphere could, therefore, induce K starvation in plants. The growth of a number of plant species, including bean, tomato, Arabidopsis, and rice, is inhibited by Cs+ concentrations in the rhizosphere exceeding 200 µM (Cline and Hungate, 1960; Kordan, 1987; Sheahan et al., 1993; Hasegawa, 1996; White and Broadley, 2000). The symptoms of Cs intoxication can be reversed, however, by supplying more K. This is consistent with the hypothesis that Cs is toxic because it interferes with K uptake and/or K biochemistry.
Natural soil Cs concentrations are generally low and nontoxic to plants. The stable isotope 133Cs occurs naturally in the aluminosilicate mineral pollucite and may reach concentrations of 25 µg g–1 dry soil (White and Broadley, 2000 Here we investigate the mechanism(s) of Cs toxicity in Arabidopsis. We consider three hypotheses: (1) Cs inhibits plant growth because it reduces K+ uptake and causes K starvation; (2) intracellular Cs is toxic per se, perhaps due to irreversible binding to essential K-dependent proteins; and (3) Cs+ competes with K+ for essential biochemical functions and, therefore, Cs toxicity is related to the [Cs]shoot/[K]shoot quotient. We conclude that Cs toxicity is determined by the [Cs]shoot/[K]shoot quotient. However, we did observe that the expression of many (but not all) genes was altered similarly in response to both K starvation and Cs intoxication. Thus, although Cs intoxication was not perceived genetically solely as K starvation, some Cs-induced K deficiency may be evident. We also note a significant increase in the expression of the gene encoding the H+/Cs+ symporter AtHAK5 in K-starved plants. This resulted in an increased Cs+ influx to K-starved plants and characteristic changes in its pharmacology.
K Dependence of Shoot Growth
The Arabidopsis accession Wassilewskija (Ws2) was grown for 21 d on agar containing a complete mineral supplement with K concentrations ([K]agar) between 0.5 and 20,000 µM (Fig. 1). The relationships between (A) shoot fresh weight (FW) and (B) mean shoot K concentration ([K]shoot) and [K]agar fitted the equation of a rectangular hyperbola (Table I). Shoot FW increased with increasing [K]agar up to a maximum value (Fig. 1A). At the highest [K]agar assayed (20 mM), shoot FW was 20.0 ± 4.5 mg (n = 6 experiments). The critical [K]agar, at which shoot FW was 90% of its value at 20 mM [K]agar, was 9.9 mM. The [K]shoot also increased with increasing [K]agar up to a maximum value (Fig. 1B). This approximated 220 µmol g–1 FW (Table I). The [K]agar at which the [K]shoot was half-maximal was 0.93 mM. This value is similar to the Km of the low affinity mechanism for K+ uptake into plants (Epstein, 1972
K Alleviates the Inhibition of Shoot Growth by Cs
To determine the effects of Cs concentration in the agar ([Cs]agar) on growth, plants were grown for 21 d on agar containing a complete mineral supplement plus 134Cs-labeled [Cs]agar between 0 and 10 mM. Since the toxicity of Cs in the rhizosphere has been shown to depend on the rhizosphere K concentration (Kordan, 1987 Arabidopsis grown at low [Cs]agar at a [K]agar of 20 mM had greater shoot FWs than those of plants grown in the absence of Cs (Fig. 2). The reason for this is unknown. There was a gradual decline in shoot FW as [Cs]agar was increased above 0.3 mM, in the presence of 2 mM [K]agar, or above 1 mM, in the presence of 20 mM [K]agar. The relationship between shoot FW and [Cs]agar fitted the equation of a logistic sigmoidal curve. The minimal shoot FW in the presence of high [Cs]agar was close to zero. The maximal shoot FW of plants grown in the presence of 20 mM K was generally greater than that of plants grown in the presence of 2 mM K (Parameter C in Table I). The [Cs]agar at which shoot FW was half-maximal (Ka50), which is a measure of the tolerance of a plant to Cs in the rhizosphere, was significantly lower for plants grown with 2 mM [K]agar than for plants grown with 20 mM [K]agar (P < 0.001). The rate of change of shoot FW as the [Cs]agar was increased (Parameter B in Table I) did not differ significantly (P > 0.05) when plants were grown in the presence of 2 mM or 20 mM [K]agar.
The shoot Cs concentration ([Cs]shoot) increased linearly with increasing [Cs]agar up to an apparent maximum [Cs]shoot (Fig. 3). At the maximal [Cs]shoot, shoot FW was minimal. When assayed at a specific [Cs]agar, the [Cs]shoot was higher with 2 mM [K]agar than with 20 mM [K]agar, and the rate of increase in [Cs]shoot with [Cs]agar (Parameter K in Table I) differed significantly (P < 0.001) between plants grown with 2 mM and 20 mM [K]agar. Thus increasing rhizosphere K concentration reduces the accumulation of Cs in the shoot.
Increasing the [Cs]agar reduced [K]shoot (Fig. 4A). In general, [K]shoot was smaller in plants grown in the presence of 2 mM [K]agar than those grown in the presence of 20 mM [K]agar at the same [Cs]agar. Intriguingly, the [K]shoot of plants grown at low [Cs]agar (<0.01 mM [Cs]agar at 2 mM [K]agar, <2 mM [Cs]agar at 20 mM [K]agar) were greater than those grown in the absence of Cs. When [Cs]agar was increased beyond these concentrations, [K]shoot declined.
Since [Cs]shoot increased (Fig. 3) and [K]shoot decreased (Fig. 4A) with increasing [Cs]agar, it follows that the [Cs]shoot/[K]shoot quotient increased as [Cs]agar increased (Fig. 4B). As expected, [Cs]shoot/[K]shoot was greater in plants grown in the presence of 2 mM [K]agar than those grown in the presence of 20 mM [K]agar at the same [Cs]agar. The [Cs]shoot approximated one-fortieth that of [K]shoot when grown in the presence of 0.2 mM [Cs]agar and 2 mM [K]agar and one-twentieth that of [K]shoot when grown in the presence of 2 mM [Cs]agar and 20 mM [K]agar. The rate of increase in [Cs]shoot/[K]shoot with increasing [Cs]agar was greater in plants grown with 2 mM [K]agar than those grown with 20 mM [K]agar (Fig. 4B). The relationship between [Cs]shoot/[K]shoot versus [Cs]agar in the presence of 2 mM [K]agar also appeared to be biphasic, the rate of increase in [Cs]shoot/[K]shoot with increasing [Cs]agar increasing abruptly at [Cs]agar greater than 0.5 mM. This might indicate a change in the complement of transporters contributing to the uptake of monovalent cations as [Cs]agar was increased, but other interpretations are possible.
From the data presented above, three hypotheses might be considered to explain Cs toxicity in Arabidopsis. The first is that [Cs]agar reduces shoot FW because it causes K starvation by lowering [K]shoot (Fig. 4A). The second is that [Cs]shoot is toxic per se (Avery, 1995
Cs Toxicity Is Not Caused Solely by K Starvation
The Relationship between Shoot Cs Concentration and Shoot FW Depends on Shoot K Concentration Shoot FW decreased as [Cs]shoot increased in the presence of either 2 mM or 20 mM K (Fig. 6A). The exact relationship between shoot FW and [Cs]shoot is derived from the logistic sigmoidal relationships between shoot FW versus [Cs]agar (Fig. 2) and the linear relationships between [Cs]shoot versus [Cs]agar (Fig. 3). It resembles a logistic sigmoidal curve. The shoot FWs of seedlings grown in the presence of 20 mM K were greater than those grown in the presence of 2 mM K at the same [Cs]shoot when plants were alive. This implies that the absolute shoot FW does not depend solely on [Cs]shoot. The [Cs]shoot at which shoot FW was half-maximal (Ks50), which is a measure of the tissue Cs tolerance of a plant, was lower for plants grown with 2 mM [K]agar than for plants grown with 20 mM [K]agar. When grown in the presence of 2 mM [K]agar, the Ks50 was 9,570 ± 285 µmol g–1 FW, and when grown in the presence of 20 mM [K]agar, the Ks50 was 11,440 ± 352 µmol g–1 FW. The observation that plants grown at 20 mM [K]agar had a greater shoot FW at the same [Cs]shoot than those grown at 2 mM [K]agar may be related to a protective effect of increased [K]shoot (Figs. 1 and 4). Indeed, when shoot FW was expressed as a percentage of the value obtained in the absence of [Cs]agar, the effect of [Cs]shoot on (maximal) shoot FW was similar irrespective of the [K]agar (Fig. 6B). This suggests that an interaction between Cs and K might determine shoot FW.
To investigate the effects of interactions between Cs and K on shoot FW, the relationship between shoot FW and the [Cs]shoot/[K]shoot quotient was determined (Fig. 7). At a low [Cs]shoot/[K]shoot, the shoot FWs of plants grown in the presence of 20 mM K were greater than those grown in the presence of 2 mM K. This implies that when [Cs]shoot does not affect growth, shoot FW is determined primarily by [K]shoot. However, the shoot FW of plants grown at 2 mM K or 20 mM K decreased with increasing [Cs]shoot/[K]shoot with the same relationship when [Cs]shoot becomes toxic. This suggests that the [Cs]shoot/[K]shoot quotient determines the reduction in shoot FW, probably because Cs+ cannot replace K+ in its biochemical functions and competes for its binding sites. Thus, Cs toxicity might be perceived by a plant cell as K deficiency.
Transcriptional Profiles of K-Replete, K-Starved, and Cs-Intoxicated Plants To test the hypothesis that Cs toxicity might be perceived by a plant cell as K deficiency, the transcriptional profiles of K-replete, K-starved, and Cs-intoxicated plants were compared. It was assumed that if Cs intoxication were perceived as K deficiency, then the transcriptional profiles of these two treatments would be identical. However, it is obvious that the transcriptional profiles of Arabidopsis plants subjected to K starvation or Cs toxicity will change with the magnitude and/or duration of stress. Therefore, plants were harvested 7 d after the imposition of these stresses when tissue K concentration had declined (compare with Table I; Hammond et al., 2003 ) or tissue Cs concentration had become toxic (C.R. Hampton, unpublished data).
When compared with K-replete plants, the expression of 1,349 genes differed significantly (P < 0.05) in roots and the expression of 3,972 genes differed significantly (P < 0.05) in shoots of K-starved plants. The 50 statistically most significant changes in gene expression (based on P values) in K-starved roots and shoots are shown in Table II. It is noteworthy that many genes involved in defense responses, and also numerous transcription factors, are among these genes. In addition, the expression of the K-transporter gene AtHAK5/AtPOT5 was increased 9-fold in Arabidopsis roots by K starvation (Table II). This transporter is likely to catalyze the uptake of both K+ and Cs+ (White et al., 2004
Several, but not all, of the genes whose expression responded to K starvation showed similar changes in expression upon Cs intoxication. When compared with K-replete plants, the expression of 964 genes differed significantly (P < 0.05) in roots and the expression of 2,551 genes differed significantly in shoots (P < 0.05) of Cs-intoxicated plants. The expression of 22% (211) of the genes whose expression was altered (P < 0.05) in roots by Cs intoxication was also altered by K starvation. Assuming that the expression of 24,000 genes was being assayed on the ATH1 array, if the genetic responses to Cs intoxication and K starvation in roots were independent, only 54 differentially expressed genes would be expected to be common to both stresses [(964/24,000) x (1,349/24,000) x 24,000 = 54]. Thus, the transcriptional responses in Arabidopsis roots to both Cs intoxication and K starvation do not appear to be independent phenomena (  21df = 501). The expression of 43% (1,098) of the genes whose expression was altered (P < 0.05) in shoots by Cs intoxication was also altered by K starvation. Again, if the genetic responses to Cs intoxication and K starvation in shoots were independent, only 422 differentially expressed genes would be expected to be common to both [(2,551/24,000) x (3,972/24,000) x 24,000 = 422]. Thus, the transcriptional responses in Arabidopsis shoots to both Cs intoxication and K starvation do not appear to be independent phenomena (21df = 1,451). These observations are consistent with Cs intoxication being perceived, in part, as K deficiency. Interestingly, four (At2g021020, At1g19610, At2g46600, and At2g46750) of the 50 statistically most significant changes in gene expression in Cs-intoxicated roots and two (At5g26340 and At1g65690) of the 50 statistically most significant changes in gene expression in Cs-intoxicated shoots were also in the 50 statistically most significant changes in gene expression upon K starvation (compare Tables II and III). The expression of several genes encoding transporters that might contribute to Cs+ fluxes was increased significantly (P < 0.05) in Cs-intoxicated plants. The expression of genes encoding AtGLR1.2 and AtGLR1.3 was increased in roots of Cs-intoxicated plants. In shoots of Cs-intoxicated plants, the expression of AtKUP6, AtCNCG1, AtCNGC11, AtCNGC12, AtCNGC13, AtCNGC20, and AtGLR1.3 was increased significantly (P < 0.05).
The Pharmacology of Cs Influx Changes with Plant K Status The transcriptional profiling of Arabidopsis roots suggests that the complement of transport proteins able to catalyze Cs+ influx to plants changes with plant K-status. In K-replete plants, Cs influx is likely to be dominated by VICCs, such as those encoded by CNGCs and GLRs (White and Broadley, 2000 ). However, in K-deficient plants, KUPs may contribute significantly to Cs+ influx (Table II; White et al., 2004). To test this hypothesis, advantage can be taken of the different pharmacologies of VICCs and KUPs. VICCs are inhibited by Ca2+ and lanthanides (White, 1997; White and Broadley, 2000), whereas high-affinity K+ transporters, such as KUPs, appear to be inhibited by ammonium (Spalding et al., 1999). As observed previously (Broadley et al., 2001), Cs influx to K-replete Arabidopsis was inhibited by Ca2+ and Gd3+ but not by tetraethylammonium (TEA+) or ammonium (Table IV). By contrast, Cs influx to K-starved Arabidopsis was inhibited by ammonium and Gd3+ but not by Ca2+ or TEA+. These changes in the pharmacology of Cs+ influx, as well as the larger Cs influx to K-deficient plants than into K-replete plants (Table IV, legend), are consistent with the increased expression of AtKUPs encoding H+/Cs+ symporters in plants starved of K (Table IV).
Cs is toxic to Arabidopsis. The shoot FW of plants grown on agar decreased when [Cs]agar was increased above 0.3 mM in the presence of 2 mM [K]agar and when [Cs]agar was increased above 1 mM in the presence of 20 mM [K]agar. However, since the K concentration in the soil solution is commonly in the millimolar range (Marschner, 1995 ) and the Cs concentration in the soil solution is generally in the low micromolar range (White and Broadley, 2000), Cs is unlikely to cause environmental toxicity in most natural environments.
The relationship between shoot FW and [Cs]agar fitted the equation of a logistic sigmoidal curve. The [Cs]agar at which shoot FW was one-half its maximal value (Ka50) was greater when plants were grown at higher [K]agar (Table I). This might be explained if increasing [K]agar reduced the entry of Cs to plants and/or increased K within the plant, which protected it against cellular Cs toxicity. It was observed that increasing [K]agar lowered [Cs]shoot (Fig. 3). Thus, one mechanism whereby increasing rhizosphere K protects plants from Cs in the environment is by reducing their Cs uptake. This observation is consistent with previous studies showing that increasing rhizosphere K reduces Cs uptake (Sutcliffe, 1957
We considered three hypotheses to explain cellular Cs toxicity in Arabidopsis. These were: (1) increasing [Cs]agar reduced shoot FW because it inhibited K+ uptake and caused K starvation; (2) [Cs]shoot was toxic per se; and (3) Cs+ competed with K+ for essential biochemical functions and, therefore, Cs toxicity was related to the [Cs]shoot/[K]shoot quotient. Increasing [Cs]agar reduced [K]shoot (Fig. 4A). This is consistent with previous studies showing that increasing rhizosphere Cs reduces K uptake and accumulation in plants (Sutcliffe, 1957
The transcriptional profiles of K-replete, K-starved, and Cs-intoxicated plants differed. In particular, the expression of several genes encoding proteins that might catalyze Cs+ transport across cell membranes was altered. In K-replete plants, Cs+ appears to be taken up largely by VICCs (White and Broadley, 2000
Since the Chernobyl accident of 1986, a variety of agricultural countermeasures have been implemented to reduce the entry of radiocesium into the food chain, and this has been the most effective means of reducing the total radiation dose to the population (Alexakhin, 1993
Plant Material
Seeds of Arabidopsis (Arabidopsis thaliana) L. Heynh. accession Wassilewskija (Ws2; N1601) were obtained from the Nottingham Arabidopsis Stock Centre (NASC, Nottingham, UK). Seeds were washed in 70% (v/v) ethanol/water, rinsed in distilled water, and surface sterilized using NaOCl (1% active chlorine). Seeds were rinsed again and imbibed for 3 to 6 d in sterile distilled water at 4°C to break dormancy. Following imbibation, seeds were sown into 10 cm (length) x 10 cm (width) x 9.5 cm (depth), unvented, polycarbonate culture boxes (Sigma-Aldrich, Gillingham, UK). For the analysis of plant growth and cation content, six seeds were sown directly on 75 mL of 0.8% (w/v) sterile agar medium (Murashige and Skoog [MS] agar) containing 1% (w/v) Suc and a basal salt mix at 10% of the full-strength MS formulation (Murashige and Skoog, 1962
The effect of K concentration in the agar ([K]agar) on shoot FW and shoot K concentration ([K]shoot) was determined in the absence and presence of Cs. In the first experiment, plants were grown on agar containing 0.5, 1, 3, 10, 30, 100, 300, 1,000, 2,000, 10,000, and 20,000 µM K. The [K]agar in 10% MS agar was 2 mM. To raise [K]agar above 2 mM, KCl was added. To reduce [K]agar below 2 mM, KNO3 and KH2PO4 were replaced with Ca(NO3)2 and Ca(H2PO4)2. In the second experiment, the effect of Cs concentration in the agar ([Cs]agar) on shoot FW, shoot Cs concentration ([Cs]shoot), and [K]shoot was determined in the presence of 2 mM and 20 mM K. The [Cs]agar was raised to 0.3, 1, 10, 100, 178, 300, 562, 794, 1,000, 1,778, 3,162, and 10,000 µM using CsCl, and the [K]agar was raised from 2 mM to 20 mM using KCl. The shoot FW of individual plants was determined and six shoots were bulked to determine [K]shoot by inductively coupled plasma optical emission spectrometry (J Y Horiba Ultima 2 ICP-OES, Jobin Yvon, Middlesex, UK). Different plants were used to determine [K]shoot and [Cs]shoot. The radioisotope 134Cs (Radioisotope Centre Polatom,
Transcriptional profiling was performed on shoot and root tissues. Plants were transferred from 10% MS agar to hydroponics 14 d after germination. In the hydroponics system, plants were fed one of three nutrient solutions (pH 5.6): (1) a basal salt mix at 10% of the full-strength MS formulation (MS solution containing 2 mM K+) to produce K-replete plants; (2) an MS solution containing only 0.5 µM K+, in which K salts were replaced by Ca salts, to produce K-starved plants; or (3) an MS solution plus 2 mM CsCl2 to produce Cs-intoxicated plants. Plants were grown in these solutions for 7 d before plants were harvested. At each harvest, shoot and root material from 20 to 30 plants from each treatment were bulked into 1.5-mL colorless, sterile, screw-cap polypropylene tubes and snap-frozen in liquid nitrogen. Tissue samples were stored at –70°C prior to the extraction of total RNA.
Total RNA was extracted following the addition of 1 mL TRIzol reagent to tissue samples placed in liquid nitrogen according to the manufacturer's instructions (Invitrogen Life Technologies, Paisley, UK) but with the following modifications (Hammond et al., 2003
Signal and detection call values were generated by Affymetrix Microarray Analysis Suite 5.0 software (Affymetrix). Raw data were normalized and analyzed using GeneSpring version 6.1 (Silicon Genetics, Redwood City, CA). Signal values below 20 were set to 20 to limit the number of false positive results (Hammond et al., 2003
Plants used for radiocesium influx experiments were transferred from 10% MS agar to hydroponics 7 d after germination. In the hydroponics system, plants were initially fed MS solution for 7 d. Plants were then transferred for a further 7 d to one of three solutions: (1) MS solution (2 mM K), to produce K-replete plants; (2) an MS solution containing only 100 µM K+; or (3) an MS solution containing only 0.5 µM K+, to produce K-starved plants. In solutions (2) and (3), K salts were replaced by Ca salts. Shoots and roots of representative plants grown in each solution were harvested and weighed and their K content determined using ICP-OES. Cs influx experiments were then performed as described by Broadley et al. (2001)
Each experiment described was repeated at least three times. Data were fitted to a variety of equations using GenStat for Windows (sixth edition, release 6.1.0.200, VSN International, Oxford). The significance of differences in parameters for contrasting experimental treatments was tested using parallel regression analysis. The significance of commonalities in transcriptional profiles was assessed using chi-squared analysis of the two-way contingency table.
We thank Simon Elliott, Mark Powell, and Joan Yurkwich (HRI) for mineral analyses and staff at the Nottingham Arabidopsis Stock Centre for their support. Received May 19, 2004; returned for revision May 30, 2004; accepted May 30, 2004.
1 This work was supported by the Biotechnology and Biological Sciences Research Council (UK). C.R.H. was supported by an HRI/Birmingham University Studentship, J.P.H. was supported by an HRI Browning Studentship, and K.A.P. was supported by a BBSRC Committee Studentship.  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.046672. * Corresponding author; e-mail philip-j.white{at}warwick.ac.uk; fax 44–(0)24–76574500.
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and 
radiation, relatively long half-lives, and rapid incorporation into biological systems (White and Broadley, 2000
) or 20 mM (
). All data represent means ± SE from at least eight replicate experiments. A logistic sigmoidal curve was fitted to the relationships between shoot FW versus [Cs]agar. The parameters for these equations are given in 
), or containing between 0.0003 and 10 mM Cs and 2 mM (
wierk, Poland) was used to quantify [Cs]shoot. Plants on which [Cs]shoot was estimated were grown on agar spiked with 134Cs at an activity of 9.165 kBq L–1 (4 pM 134Cs). Six shoots were bulked, and their 134Cs content was determined using a Wallac 1480, Wizard gamma counter (Perkin-Elmer Life Sciences, Turku, Finland). 
