Transfer of radiocesium from hydroponic medium to potherb mustard and tomato plants

Abstract

Potherb mustard (Brassica rapa var. nipposinica) and tomato plants (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum) were cultured in hydroponic medium containing cesium-137 (¹³⁷Cs) at three different concentrations (0.03, 0.13 and 1.03 Bq L⁻¹), and uptake of ¹³⁷C into the plants was determined. When the ¹³⁷Cs radioactivity concentration in the medium was 1.03 Bq L⁻¹, the ¹³⁷Cs radioactivity concentrations in the edible portions of the plants were 4.80 Bq kg⁻¹ fresh weight for the potherb mustard plants and 3.60 Bq kg⁻¹ fresh weight for the tomato plants. In both species, the ¹³⁷Cs radioactivity concentration in the edible portions decreased with decreasing ¹³⁷Cs radioactivity concentration in the culture medium. When the ¹³⁷Cs radioactivity concentration in the medium was 0.03 Bq L⁻¹, a concentration observed in many streams and in tap water in Fukushima Prefecture after the accident at the Fukushima Daiichi Nuclear Power Plant, the ¹³⁷Cs radioactivity concentrations in the edible portions of the plants were 0.50 and 0.15 Bq kg⁻¹ fresh weight for potherb mustard and tomato plants, respectively. These values are less than the Japanese allowable limit for radiocesium in food. For both species, the transfer factors for ¹³⁷Cs uptake from the culture media to the edible portions and the average transfer rates over the cultivation period were calculated.

Key words:

• Fukushima
• hydroponic culture
• potherb mustard
• radiocesium
• tomato

1. INTRODUCTION

The March 2011 accident at the Fukushima Daiichi Nuclear Power Plant (FDNPP) released a large quantity of radiocesium [approximately 1.3 × 10¹⁶ Bq cesium-137 (¹³⁷Cs)] into the atmosphere (Chino et al. 2011). Of the total radiocesium emitted, 10–20% is estimated to have been deposited over land in northeastern Japan (Morino et al. 2011). The deposited radiocesium poses a substantial radioactive risk because of its long physical half-life [2.06 years for cesium-134 (¹³⁴Cs) and 30.2 years for ¹³⁷Cs] and the large amount that was deposited. A major pathway for ingestion of radiocesium is consumption of contaminated agricultural products. Therefore, monitoring radiocesium concentrations in agricultural products and evaluating the transfer of radioactive elements from contaminated soil to plants are very important tasks.

Radiocesium adsorption by plants can occur by the following pathways: (1) uptake of radiocesium deposited from the atmosphere onto the aboveground portions of plants, (2) root uptake of radiocesium deposited in the soil and (3) direct root uptake of radiocesium dissolved in water, such as the water used to irrigate paddy fields and the nutrient solutions used for hydroponic culture.

Because the radiocesium concentration in the atmosphere in Fukushima Prefecture decreased dramatically with time after the FDNPP accident, from 30.3 Bq m⁻³ on March 25, 2011 (Ministry of Education Culture Sports Science and Technology in Japan 2011) to less than 0.003 Bq m⁻³ on December 25, 2011 (Ministry of Education Culture Sports Science and Technology in Japan 2012), the risk of radiocesium adsorption via the first pathway also decreased with time. For example, in Fukushima Prefecture, the average concentration of radiocesium in spinach (Spinacia oleracea L, cv. Subito) reached 6000 Bq kg⁻¹ in March 2011 but was less than the detection limit of ~30 Bq kg⁻¹ by July 2011 (Ministry of Health, Labor and Welfare 2012b).

There have been many studies of the second radiocesium adsorption pathway, uptake from the soil via the roots (Brambilla et al. 2002, Sabbarese et al. 2002). The amount of radiocesium transferred from soil to the edible portions of plants is generally expressed in terms of a soil-to-plant transfer factor (TF; (IAEA 2009). Because radiocesium is strongly adsorbed by clay minerals in soils (Nakao et al. 2008; Takeda et al. 2008), radiocesium in soil is not easily transferred to plants. Recent investigations confirmed that concentrations of ¹³⁷Cs in vegetable plants in Fukushima Prefecture were low after July 2011 (Ministry of Health, Labor and Welfare 2012b) and that the TF for ¹³⁷Cs uptake from soil to vegetable plants in cultivated soil in the prefecture after the accident was low.

There have been only a few studies of radiocesium uptake by the third pathway, root uptake of radiocesium dissolved in culture media (Myttenaere et al. 1974; Uchida et al. 1987; Smolders et al. 1997; Šuňovská et al. 2013). Myttenaere et al. (1974) investigated the absorption of radiocesium chlorides and stable cesium chloride by tomato plants (Lycopersicum Esculentum) grown in nutrient solutions containing various concentrations of the chlorides. Smolders et al. (1997) examined interionic effects on radiocesium uptake by spinach cultured in solution. Uchida et al. (1987) conducted hydroponic experiments to estimate the amount of radiocesium transferred from the culture solution to the edible portions of seven types of plants. Šuňovská et al. (2013) studied the dependence of ¹³⁷Cs uptake and translocation on the presence of potassium and ammonium ions in the culture medium. In these studies, the radiocesium concentrations in the culture media ranged from 10 to 370,000 Bq L⁻¹. However, the concentrations of dissolved radiocesium in river water in Fukushima Prefecture in 2012 ranged from 0.004 to 0.13 Bq L⁻¹ (Yasutaka et al. 2012; Nagao et al. 2013), a range that is much lower than the concentrations used in these studies.

Therefore, in the present study, we prepared hydroponic culture medium containing low concentrations of radiocesium (0.03–1.03 Bq L⁻¹), similar to those observed after the FDNPP accident, and we investigated ¹³⁷Cs transfer from the culture medium to potherb mustard (Brassica rapa var. nipposinica) (a leafy vegetable plant) and tomato (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum) (a fruiting vegetable plant) grown in the medium. We evaluated the transfer of radiocesium from the medium to the edible portions of the plants in terms of the ratio of the concentration of radiocesium in the medium to that in the edible portions (TF_CM) and in terms of the average transfer rate (TR) over the cultivation period. The mechanism by which radiocesium dissolved in hydroponic media is transferred to plants is quite different from the mechanism by which radiocesium is transferred from soil, and evaluation of the direct uptake of dissolved radiocesium by roots is important for the reconstruction of nutriculture systems and plant factories in Fukushima Prefecture.

2. MATERIALS AND METHODS

2.1. Plant materials

For this study, we selected Japanese potherb mustard plants and tomato plants, which were grown in a greenhouse at the Fukushima Agricultural Technology Centre.

2.2. Analytical equipment

Radiocesium concentrations in plant samples were measured with a gamma-ray spectrometer equipped with a germanium semiconductor detector (SEG-EMS GEM20-70; Seiko EG&G Co., Tokyo, Japan). The detector was calibrated with a standard that was appropriate for the volume of the sample container (MX033U8PP for the U-8 container and MX033MR for the 2-L Marinelli container; Japan Radioisotope Association). The radioactivity concentrations of ¹³⁴Cs and ¹³⁷Cs were measured, but ¹³⁷Cs was the only species monitored because it is minimally affected by radionuclide decay.

2.3. Preparation of radiocesium stock solutions

Radiocesium-contaminated coniferous leaves collected in Fukushima Prefecture after the FDNPP accident were transferred to the Fukushima Agricultural Technology Centre. The leaves were soaked in tap water for 2 weeks, the supernatant was passed through a 0.45-μm membrane filter, and the filtrate was collected and used as the radiocesium stock solution. The radioactivity concentrations of ¹³⁷Cs and ¹³⁴Cs in the solution, measured with a germanium semiconductor detector, were 1014 and 647 Bq kg⁻¹, respectively.

2.4. Culture medium for potherb mustard plants

The potherb mustard plants were seeded and grown in Otsuka-A nutrient solution (260 ppm total N (Nitrogen), 120 ppm P₂O₅ (Phosphorus pentoxide), 405 ppm K₂O (Potassium oxide), 30 ppm CaO (Calcium oxide), and 60 ppm MgO (Magnesium oxide)). The culture medium for the tomato plants is described in Section 2.6. The radiocesium stock solution was added to the culture medium to produce final ¹³⁷Cs radioactivity concentrations of 0.03, 0.13 and 1.03 Bq L⁻¹.

2.5. Hydroponic culture of potherb mustard plants

On August 9, 2012, seeds of potherb mustard were sown on a urethane mat, which was immersed in seedling culture medium containing ¹³⁷Cs at each of the three tested concentrations. After 12 d, the seedlings were transplanted into 120-L plastic containers with 100 L of growth culture medium containing ¹³⁷Cs at the three concentrations. Three panels of 41 plants each were established for each concentration. At the beginning of the cultivation period, the total volume of culture medium in each container was 100 L. Because the volume of the culture medium was over 60 L at the end of the cultivation period and sufficient, the medium was not supplemented before harvest.

On September 18, 2012 (at which point the 3-week-old plants were at least 35 cm tall), the leaves and roots of the plants in each panel were harvested. The leaf and root samples were weighed, washed with deionized water, dried at 80°C for 48 h, weighed again and placed in a U-8 container for radioactivity analysis.

2.6. Hydroponic culture of tomato plants

In October 2012, purchased tomato seedlings were planted in soil; they were then watered with radiocesium-free water until November 13, 2012, when they were transplanted into 120-L plastic containers containing 100 L of growth culture medium containing ¹³⁷Cs at the three tested concentrations. Three panels of five tomato plants each were established for each concentration. Each tomato plant was pruned at below the second fruit truss, and fruit was harvested from the first truss.

During the first growth stage, the plants were cultured in 100 L of Otsuka-A nutrient solution diluted 0.5-fold and containing ¹³⁷Cs at the three concentrations. On January 9, 2013 and again on January 22, 2013, 30 L of 0.8-fold-diluted Otsuka-A solution containing ¹³⁷Cs at the three concentrations was added to each container. On February 6, 2013, 30 L of 1.6-fold-concentrated Otsuka-A solution containing ¹³⁷Cs at the three concentrations was added. Finally, 30 L of water without nutrient solution was added on February 28 and again on March 11, 2013. During the cultivation period (128 d), the total amount of ¹³⁷Cs-containing culture medium was 250 L.

Starting on March 3, 2013, and continuing until March 21, 2013, plants in each panel were harvested when the fruits began to redden. After the fruits were washed with tap water, they were cut to pieces, weighed and frozen at –25°C until needed. The roots, leaves and stems were separated and dried at 80°C for 48 h and placed in a U-8 container for radioactivity analysis. Frozen fruits were thawed and placed in a 2-L Marinelli container for radioactivity analysis.

2.7. TRs and TF_CMs for ¹³⁷Cs uptake from culture medium to plants

For plants grown in hydroponic cultures, various measures have been used to assess the relationship between radiocesium concentration in the culture medium and that in the edible portions of the plants. For example, Smolders et al. (1997) calculated TF_CMs, and Uchida et al. (1987) reported TRs, that is, ratios of radiocesium concentrations in the culture medium to concentrations in the edible portions of plants divided by the duration of the cultivation period; TR values account for the effect of experiment duration on the amount of radiocesium adsorbed by the plants.

To evaluate radiocesium uptake from the culture medium to the edible portions of the two plant species, we calculated both TF_CMs and average TRs over the cultivation period.

3. RESULTS AND DISCUSSION

3.1. Effect of radiocesium on plant growth

We determined the uptake of dissolved ¹³⁷Cs by the edible portions of potherb mustard leaves and tomato fruits obtained from plants grown in hydroponic culture medium containing ¹³⁷Cs at a concentration of 0.03, 0.13 or 1.03 Bq L⁻¹. These concentrations were chosen on the basis of previous findings showing that the concentration of dissolved radiocesium in the water of the Abukuma River (one of the largest streams in Fukushima Prefecture) was 0.004–0.13 Bq L⁻¹ in September 2012 (Yasutaka et al. 2012).

At harvest, the fresh weights of the edible portions of the potherb mustard and tomato plants did not differ substantially at the three ¹³⁷Cs radioactivity concentrations (Table 1), indicating that the ¹³⁷Cs in the culture medium had no toxic effect on the growth of either species at any of the tested concentrations.

Table 1 Harvested weight of the edible portions of potherb mustard (Brassica rapa var. nipposinica) and tomato plants (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum) grown in nutrient solution containing different cesium-137 (¹³⁷Cs) radioactivity concentrations

^137Cs in culture medium (Bq L^−1)	Weight of edible part
	Potherb mustard (leaf) (g per panel)	Tomato (fruit) † (g per plant)
0.03	2420 ± 366*	785.0 ± 0.2*
0.13	2135 ± 158*	894.4 ± 7.2*
1.03	2197 ± 242*	861.2 ± 8.0*

Values reported as mean ± SD (n = 3 individual panels). †Weight of tomato is the first fruit cluster. *No significant difference by Tukey test for each ¹³⁷Cs radioactivity concentration (P < 0.05).

3.2. ¹³⁷Cs uptake by edible portions of plants

Analysis of the ¹³⁷Cs concentrations in the edible portions of potherb mustard and tomato plants grown in ¹³⁷C-containing culture medium revealed that uptake of ¹³⁷Cs by the two species increased linearly with increasing ¹³⁷Cs radioactivity concentration in the medium (Fig. 1). At a ¹³⁷Cs radioactivity concentration of 1.03 Bq L⁻¹ (the highest concentration used in this study), the mean concentrations of ¹³⁷Cs in the potherb mustard leaves and tomato fruits were 4.80 and 3.60 Bq kg⁻¹ fresh weight, respectively. Under the same culture conditions, the sums of ¹³⁷Cs and ¹³⁴Cs concentrations in the edible portions of the potherb mustard and tomato plants were 7.7 and 5.4 Bq kg⁻¹ fresh weight, respectively; both of these concentrations are less than 10% of the Japanese standard limit for radiocesium in food (100 Bq kg⁻¹ for the sum of ¹³⁷Cs and ¹³⁴Cs; Ministry of Health, Labor and Welfare 2012a).

Figure 1 Uptake of cesium-137 (¹³⁷Cs) by the edible portions of potherb mustard (Brassica rapa var. nipposinica) and tomato plants (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum) from nutrient solution containing different ¹³⁷Cs radioactivity concentrations.

When the potherb mustard and tomato plants were grown at a ¹³⁷Cs radioactivity concentration of 0.03 Bq L⁻¹ in the culture medium (the lowest concentration used in this study), the concentration detected in streams and tap water in Fukushima Prefecture in September 2013, the ¹³⁷Cs radioactivity concentrations in the potherb mustard leaves and tomato fruits were 0.50 and 0.15 Bq kg⁻¹ fresh weight, respectively.

3.3. ¹³⁷Cs distributions in plants

The distribution of ¹³⁷Cs in the plants differed between the two species (Fig. 2). In the potherb mustard plants, ¹³⁷Cs tended to concentrate more in the roots than in the leaves at all three ¹³⁷Cs radioactivity concentrations (Fig. 2A). These results agree with the results of a study of hydroponic culture of lettuce (Lactuca sativa L.) (Šuňovská et al. 2013), a leafy crop plant, although a different culture medium was used. In contrast, a study of spinach cultured in 15 different nutrient solutions revealed that radiocesium uptake by spinach shoots was greater than that by spinach roots, although the differences in radiocesium concentration between the shoots and roots did not exceed 1.35-fold for any of the nutrient solutions (Smolders et al. 1997). Taken together, these results demonstrate the complexity of ¹³⁷Cs mobility in leafy crop plants.

Figure 2 (A) Cesium-137 (¹³⁷Cs) radioactivity concentration accumulated in plant edible portions and (B) the ratio of ¹³⁷Cs radioactivity concentration in organs to that in the edible portions of potherb mustard (Brassica rapa var. nipposinica) and tomato plants (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum).

The concentrations of ¹³⁷Cs in the organs of tomato plants decreased in the order leaf > root ≈ stem > fruit. This result suggests that ¹³⁷Cs moves easily from the roots to the aboveground portions of the plants. In addition, the fact that the ¹³⁷Cs radioactivity concentration in the leaves was at least four times that in the fruits at all three ¹³⁷Cs radioactivity concentrations (Fig. 2B) suggests that ¹³⁷Cs may be trapped in the leaves and unable to move easily to other organs (e.g., fruits) in fruiting vegetable plants such as tomatoes. In contrast, extrapolation of the data from an early study of radiocesium retention in tomato plants grown in nutrient solutions (Myttenaere et al. 1974) revealed that tomato roots accumulate more ¹³⁷Cs than leaves. This difference in distribution patterns may be due to the addition of stable cesium to the nutrient solution and concentration of nutrient solution used for the 1974 study.

3.4. TF_CMs and TRs for ¹³⁷Cs uptake from culture medium to plants

As shown in Table 2, the TF_CM values for the edible portions of the potherb mustard plants (4.7–16.6 L kg⁻¹) were greater than those for the tomato plants (3.5–4.8 L kg⁻¹). All these TF_CM values are lower than those for spinach plants (41–117 L kg⁻¹) grown in a high-concentration radiocesium solution (10,000 Bq L⁻¹) (Smolders et al. 1997). These differences of TF_CM value between our research and Smolders et al. (1997) lead us to assume that the TF_CM values for low-concentration radiocesium solutions tested in the current study may be less than the TF_CM values for high-concentration solutions, but further studies are needed to confirm this tendency.

Table 2 Concentration of cesium-137 (¹³⁷Cs) in potherb mustard (Brassica rapa var. nipposinica) and tomato plants (scion, ‘CF Momotaro haruka’; rootstock, ‘Dokutar K’; Solanum lycopersicum) grown in nutrient solution containing different ¹³⁷Cs radioactivity concentrations

	[^137Cs] (Bq L ^−1)	Potherb mustard		Tomato
	in culture medium	Leaf	Root	Fruit	Leaf	Stem	Root
TFCM(L kg^−1)	0.03	16.6	46.5	4.8	23.5	12.1	14.7
	0.13	6.5	25.9	3.9	23.5	12.4	14.2
	1.03	4.7	12.0	3.5	21.2	11.0	10.6
TR(L kg^−1 day^−1)	0.03	0.41	1.16	0.03	2.2	0.9	1.9
	0.13	0.16	0.65	0.03	1.2	0.9	1.8
	1.03	0.12	0.30	0.02	1.1	0.8	1.3

Values reported as mean ± standard error (SE; n = 3 individual panels).

The TR values also indicate that transfer from the culture medium to the edible portions of the potherb mustard plants (0.12–0.41 L kg⁻¹ day⁻¹) was greater than transfer to the edible portions of the tomato plants (0.02–0.03 L kg⁻¹ day⁻¹). This result agrees with the findings of Uchida et al. (1987), who reported that the TR values for the edible portions of leafy crop plants (komatsuna (Brassica rapa var. perviridis) and spinach) are greater than those for fruiting crop plants (cucumber (Cucumis sativus L.) and eggplant (Solanum melongena)).

In the present study, the patterns of the TF_CM and TR values were similar to each other. Therefore, uptake of ¹³⁷Cs from the culture medium to the organs of potherb mustard and tomato plants can be evaluated from either the TF_CM or the TR values.

4. CONCLUSIONS

We examined the effect of low-concentration radiocesium on potherb mustard and tomato plants cultured in hydroponic media containing ¹³⁷Cs at three different concentrations (0.03, 0.13 and 1.03 Bq L⁻¹) to evaluate the effect of radiocesium on nutriculture. The TF_CM values for the edible portions of potherb mustard plants were 4.7–16.6 L kg⁻¹, and those for tomato plants were 3.5–4.8 L kg⁻¹. The TF_CM and TR values for the edible portions of both plant species were less than the values for the other parts of the plants. The ¹³⁷Cs radioactivity concentrations in the edible portions of the potherb mustard and tomato plants were 4.80 and 3.60 Bq kg⁻¹ fresh weight, respectively, when the plants were grown in medium with the maximum tested ¹³⁷Cs radioactivity concentration (1.03 Bq L⁻¹). Both of these values were less than the Japanese limit for radiocesium in food.

ACKNOWLEDGMENTS

The authors thank the Japan Environment Science Co. for conducting the radioactivity analysis.