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SN Applied Sciences

, 1:1665 | Cite as

Distribution of cesium and cationic mineral elements in napiergrass

  • Dong-Jin KangEmail author
  • Young-Jin Seo
  • Yasuyuki Ishii
Research Article
  • 74 Downloads
Part of the following topical collections:
  1. 2. Earth and Environmental Sciences (general)

Abstract

Napiergrass is fast-growing perennial known for its high potential for accumulation of cesium (Cs). Cs is highly mobile within a plant and can be distributed to various plant organs. Here, we investigated the distribution of cesium-133 (133Cs) and competitively translocated cationic minerals, such as potassium (K), calcium (Ca), and magnesium (Mg), in different organs of napiergrass. Treatments comprised four concentrations of 133Cs applied to soil: 0 (as control); 300; 500; and 1000 μM. Leaf blades contained significantly higher concentrations of 133Cs than stems under 300 and 500 μM 133Cs treatments (P < 0.01). Specifically, significantly greater 133Cs content was measured in younger parts of stems and leaf blades compared with mature or older plant parts. The 133Cs content in younger parts was 5302, 13,059, and 51,678 mg kg−1 in stems and 6961, 16,363, and 52,781 mg kg−1 in leaf blades under 300, 500, and 1000 μM 133Cs treatments, respectively. Distribution ratios of K were higher in stems than in leaf blades in all 133Cs-treated conditions (P < 0.05). A significantly negative correlation was found between K and Ca or Mg in leaf blades, suggesting that 133Cs and K are similarly competitive with Ca or Mg within napiergrass. We conclude that 133Cs is distributed to younger plant parts, especially leaf blades, and that translocation of Ca and Mg is strongly inhibited by the presence of 133Cs or K within organs. This suggests that 133Cs or K can inhibit Mg translocation and could lead to Mg deficiency in younger plant parts.

Keywords

Competition 133Cs Macronutrients Pennisetum purpureum Schum Plant organ Translocation 

1 Introduction

Many areas surrounding the Fukushima Daiichi Nuclear Power Plant in Fukushima Prefecture, Japan, remain highly contaminated with long-lived radiocesium (Cs) since the 2011 tsunami, in particular 137Cs, which has a half-life of 30 years [12]. 137Cs is one of the most dangerous radionuclides; it is highly water soluble and has a marked tendency to accumulate in sediment and aquatic organisms [2, 27].

Cs and potassium (K) are both Group I alkali metals [9], but the higher atomic weight and ionic radius and lower hydration energy of Cs result in slightly different behaviors [2]. It has been suggested that competitive and inhibitory interactions between 137Cs and K play an important role in the uptake and translocation of alkaline and alkaline-earth metals by plant roots [19]. One possible reason for this inhibition could be that small amounts of 137Cs block K+-channels [27]. Low concentrations of 134Cs were shown to be easily taken up by plant roots and translocated to aboveground plant parts [17]. 134Cs translocation and accumulation vary by plant species and plant organs [20]. Because Cs is mobile and can be easily distributed, its distribution within plants or within organs also varies among different plant species [2]. Examples include uptake via the vascular system of stems and leaves in Arabidopsis thaliana [9], seeds in Vicia faba [15], growing parts such as fruits, leaves, twigs, and bark in woody trees [1, 18], new leaves in cedar plants [16], leaves in Indian mustard [22], and leaves in Chengiopanax sciadophylloides [24].

The uptake of nutrient elements by roots is also influenced by the presence of Cs. Cs is transported from the soil solution to the plant by various cation transporters located in the plasma membrane of root cells [25, 27]. The concentration of K in soil can influence Cs uptake, with greater uptake occurring as K concentrations increase, suggesting that K channels are blocked, potentially affecting mineral nutrition [21]. Therefore, it is important to consider the nutrient status of the soil [2], because interactions with the analogs K and calcium (Ca) affect 137Cs transfer [6]. Additionally, it is well established that high concentrations of K in soil competitively inhibit magnesium (Mg) uptake, and that even within plants, excess K competes with Mg to reduce protein synthesis function [8].

Napiergrass (Pennisetum purpureum Schum) produces the greatest shoot-mass of all herbaceous plants [5], and it has a relatively high 137Cs removal ratio (CR) among species studied for phytoremediation [10, 11]. In a previous field study, a maximum CR of 0.57% was achieved in napiergrass planted at high density on soils contaminated with high levels of 137Cs (3404 kBq m−2) [12]. We also previously confirmed that 133Cs and 137Cs became more localized in leaf blades of napiergrass compared with stems [10, 11]. However, the distribution of 133Cs within napiergrass stems or leaf blades after translocation has not been fully elucidated. We anticipated that 133Cs distribution would vary between leaf blades and stems and may in fact also be quite different depending on organ maturity. Therefore, in the present study, we hypothesized that 133Cs content would be highest in the leaf blades of napiergrass following translocation, and that 133Cs would be primarily distributed in the younger parts of stems and leaf blade organs. We further hypothesized that alkaline cationic minerals, such as K, Ca, and Mg, would be competitively distributed in the presence of 133Cs within plant organs.

2 Materials and methods

We used a common variety of napiergrass (var. Merkeron), which showed high 137Cs accumulation compared with other napiergrass varieties [11]. The experiment was conducted in a rainout greenhouse in Goshogawara, Aomori Prefecture (40.5494 N, 140.2743 E), northern Japan, between May 25 and August 21, 2017 (88 days). In this study, five pots (replicates) per each 133Cs treatment concentration were used. Four-week-old nursery plants were transplanted into 1/2000a Wagner pots filled with 7 kg dried commercial soil on May 25, 2017. A compound fertilizer, N–P–K (15–15–15), was applied as a basal dressing at 4.0 g pot−1, and the same amount was applied as a top dressing once per month (total two times) until harvest. The maximum and minimum temperatures in the greenhouse were measured using a data logger (Temperature and Humidity USB Datalogger DL171, AS ONE Co. Ltd., Osaka, Japan) throughout the experiment (Fig. 1).
Fig. 1

Daytime air temperature during the plant growth period. DAT = days after transplanting

Cs (atomic weight 133Cs) at concentrations of 0 (control), 300, 500, and 1000 µM, as cesium chloride (CsCl) in 2 L water, was applied to the soil in each pot prior to transplanting. Pots were watered by applying 1050 mL of tap water when soil tension reached approximately − 20 to − 30 kPa. The total water applied equaled 15% of the total soil volume during the growth period. Soil tension in the pots was continuously assessed at a depth of 20 cm using a tension meter (DIK-8333, Daikirika Co. Ltd.) until harvest.

Before being harvested, five individual plants were measured for plant height, tiller number, and SPAD value (SPAD-502; Minolta Co., Ltd., Osaka, Japan); the SPAD value indicates chlorophyll content or color of a leaf. These plants were harvested, on the same day, from each 133Cs-treatment group to determine the 133Cs content in each part of the leaf blade and stem (including the leaf sheath). The harvested leaf blades and stems were further separated into young, mature, and old sections (Fig. 2), and then the plant materials were dried in an oven at 80 °C for 72 h. To determine 133Cs concentration within each plant, 0.2 g each of dried leaf blades and stems were digested in 10 mL HNO3 (nitric acid) using a Milestone microwave digestion system (ETHOS; Milestone Inc., Sorisole, Italy). After cooling, the samples were centrifuged and supernatants were passed through a 0.45-µm filter. 133Cs concentrations were measured using an inductively coupled plasma-mass spectrophotometer (ICP-MS; PerkinElmer Elan, Co., Ltd., Fremont, CA, USA) according to a protocol by Kang et al. [10].
Fig. 2

Schematic diagram showing the parts of organ material collected from napiergrass and used in the present study (a) and their descriptions (b)

2.1 Statistical analysis

Five plant replicates in the four 133Cs treatment groups were measured for plant height, tiller number, SPAD value, and 133Cs content within both leaf blades and stems. The data obtained in the experiments were analyzed using Tukey’s multiple-range test to determine the significance of any differences between the mean values, using KaleidaGraph (ver. 4.1, Synergy Software) software. Significant differences in 133Cs content between mean values in leaf blades and stems were determined using Fisher’s least significant difference test.

3 Results and discussion

We investigated where 133Cs is specifically distributed in the aboveground parts of napiergrass and also examined cationic mineral distribution within plant organs in the presence of 133Cs under a range of soil treatment concentrations. To assess the toxic effect of Cs on napiergrass, we measured various morphological and physiological stress parameters, including plant height, SPAD values, and tiller number. In our study, no significant differences were observed in plant height, SPAD values, or tiller number of napiergrass with increasing 133Cs concentration in soil (Table 1). For the other plants investigated, chlorophyll content and several chlorophyll fluorescence parameters in Plantago major (2–20 mM 133Cs) [4], Arabidopsis halleri (0.2–20 mM 133Cs) [3], and Brassica juncea (25–100 mg L−1 133Cs) [26] significantly decreased under Cs exposure during hydroponic growth; the dry weight of leaves, however, did not differ significantly compared with control plants [3, 4, 26]. Previously, we observed that napiergrass exhibited reduced plant height and SPAD value and increased tiller number at relatively high 133Cs concentrations (1000–3000 µM) in hydroponic culture solution [10]. However, the results with regard to plant height, SPAD value, and tiller number at a concentration of 1000 µM 133Cs differed in the present study compared with the previous study [10]. We considered that this difference might have arisen due to the different cultivation conditions between soil and hydroponic media, therefore further work is necessary to explore these growth differences.
Table 1

Effect of different levels of cesium-133 (133Cs) treatment on plant height, SPAD value (SPAD), and tiller number

Treatment

Plant height (cm)

SPAD

Tiller number (plant−1)

0 μM 133Cs

119.2 ± 2.4ns

31.4 ± 0.8ns

19.4 ± 2.0ns

300 μM 133Cs

115.9 ± 2.7ns

32.9 ± 0.7ns

15.6 ± 0.7ns

500 μM 133Cs

111.0 ± 0.8ns

31.4 ± 0.4ns

19.6 ± 1.1ns

1000 μM 133Cs

111.7 ± 2.5ns

30.9 ± 0.3ns

19.2 ± 1.5ns

ns indicates no significant difference at the 5% level by Tukey’s multiple-range test

Values indicate the mean ± standard error (n = 5 individual plants)

The content of 133Cs in the aboveground parts of napiergrass significantly increased with increasing 133Cs concentrations in soil (Table 2). The mean 133Cs content within leaf blades was significantly higher than in stems following treatment with 300 and 500 μM 133Cs. As with our study, a trend of 133Cs accumulation (leaf > stem) in a hydroponic experiment was also observed for leaves of Brassica juncea and Vicia faba under conditions of 25 and 50 mg kg−1 Cs [7], Plantago major under 0.002 to 20 mM Cs [4], and Calla palustris under 0.5 and 1 mM Cs [14]. Similar Cs accumulation in leaf blades was also observed in napiergrass grown on 137Cs-contaminated soil, where 137Cs accumulation was approximately two to three times greater in leaf blades of napiergrass than in the stems [11]. On the other hand, in the present study, significant differences in 133Cs content between leaf blades and stems disappeared at relatively high concentrations of 133Cs treatment (1000 μM). Similar results were observed in a hydroponic experiment, with differences between the 133Cs content of leaf blades and sheaths (including stems) of napiergrass diminishing at 7 weeks after transplanting under 1000 and 3000 μM 133Cs-treated hydroponic solution [10]. Here, we found a significantly greater distribution of 133Cs within the younger parts of stems and leaf blades (ST1 and LB1) of napiergrass than within the older parts (ST3 and LB3) (P < 0.05). This trend of higher 133Cs distribution in younger plant parts was observed across all 133Cs treatments and represents a new finding in napiergrass. Concerning 133Cs, however, small differences in the distribution of 133Cs were observed between the stems (ST1) and leaf blades (LB1) of younger parts at 1000 μM 133Cs compared with 500 μM 133Cs treatment (Table 2). In particular, the 133Cs content of leaf blades (LB2) in mature organs under 1000 μM 133Cs was lower than in stems (ST2). Lai et al. [15] observed various growth stages of Vicia faba under soil conditions with high concentrations of 133Cs (25, 50, and 100 mg kg−1) and determined that the pattern of 133Cs accumulation and redistribution in plants depends on the plant growth time and the 133Cs concentration. Therefore, we considered that napiergrass, although it has a large capacity for Cs accumulation, may have exhibited limited translocation from stem to leaf blades under excess 133Cs exposure in this study.
Table 2

Cesium-133 (133Cs) content in the stems (ST) and leaf blades (LB) at different levels of 133Cs-treated soil conditions

Label

300 µM 133Cs

500 µM 133Cs

1000 µM 133Cs

ST1

5301.7 ± 357.4a

13,059.1 ± 584.7a

51,677.6 ± 2214.2a

ST2

4951.5 ± 333.8ab

12,387.5 ± 980.1a

45,003.2 ± 2994.4a

ST3

3868.5 ± 220.6b

8997.0 ± 486.9b

28,513.5 ± 1686.9b

Mean (stem)

4707.2 ± 232.4

11,481.2 ± 610.2

41,731.5 ± 2891.7ns

LB1

6960.7 ± 623.0a

16,363.3 ± 1189.0a

52,780.6 ± 689.4a

LB2

5333.1 ± 172.0b

13,746.6 ± 716.4ab

38,844.7 ± 1193.3b

LB3

5048.4 ± 164.6b

12,562.7 ± 597.3b

33,780.4 ± 718.4c

Mean (leaf blade)

5780.7 ± 305.1**

14,224.2 ± 630.6**

41,801.9 ± 2200.0ns

ST1, ST2, ST3 and LB1, LB2, LB3 indicate young, mature, and old organs in stems and leaf blades, respectively

Values indicate the mean ± standard error (n = 5 individual plants)

The same letters indicate no significant difference within the stem or leaf blade at the 5% level according to Tukey’s multiple-range test

ns indicates no significant difference at the 5% level

**indicates significant correlations between the means of stems and leaf blades at the 1% level by Fisher’s least significant difference test

Table 3 shows the distribution ratio of cationic mineral elements within napiergrass in the presence of 133Cs under different concentrations of 133Cs treatment. The distribution ratio of cationic minerals was affected by plant organ as well as maturity. Potassium (K), which behaves similar to 133Cs, was easily translocated and accumulated within plants when the 133Cs treatment concentration was relatively low, at 300 and 500 μM. However, K translocation was heavily suppressed at 133Cs concentrations of 1000 μM. It is well established that the transport of Cs from the soil solution into a plant usually happens via K and Ca transporters [25, 27]. Komínková et al. [14] reported a study in which Calla palustris plants were exposed to 133Cs-treated hydroponic solutions (0.5 and 1 mM 133Cs) and several concentrations of K (0.5, 1, 2, 5, and 10 mM K); they found that 133Cs uptake and translocation were affected not only by the external concentration of K but also by the external concentration of 133Cs. Similarly, Burger and Lichtscheidl [2] stated that a low concentration of K in plants increased their uptake of Cs and that higher concentrations led to reduced Cs uptake. On the other hand, K uptake is also influenced by 133Cs content in the soil. In the present study, the K distribution ratio was consistently higher in stems than in leaf blades in all 133Cs treatment groups. This is contrary to the 133Cs distribution measured within plant organs (Table 2) and suggests that 133Cs and K, which have chemically similar behavior, inhibit each other within napiergrass. It is well established that Cs (133Cs and 137Cs) ions are chemically similar to K ions under several growth conditions [1, 9]. In the present study, Ca content in plant organs was greatly suppressed by the presence of 133Cs at all treatment levels (Table 3). Ca distribution ratios (Ca/133Cs) decreased with increasing 133Cs concentrations, because the Cs uptake competitively into plants using Ca and K transporters in the plasma membrane [2, 25]. The distribution ratio of Ca in leaf blades was significantly higher in older leaf blades compared with younger ones (Table 3, Ca/133Cs). A similar trend in distribution was also observed in the stems, because there is almost no redistribution of Ca within the plant following root uptake [13], resulting in lower Ca distribution ratios in newly emerged stems and leaf blades (younger plant parts). In contrast, Ca accumulation in the leaves of Plantago major significantly increased in the 2 mM 133Cs-treated hydroponic condition [4]. Concerning the accumulation of Ca in the presence of 133Cs in hydroponic culture medium, Burger et al. [4] concluded that the presence of 133Cs in the medium did not decrease Ca uptake; decreased biomass may therefore possibly be related to a K deficiency. As with Ca, the distribution of Mg in the presence of 133Cs was also greatly suppressed, but, in contrast, Mg was found to be significantly more likely to be distributed among stems rather than leaf blades (Table 3, Mg/133Cs). Within the stems, Mg was localized primarily in the more mature or older parts than in younger parts. Similar to 133Cs, Mg uptake is competitively inhibited by large amounts of K, and excess K competes with Mg resulting in reduced protein synthesis [8]. Considering that Cs uptake occurs via K and Ca channels [25], we suggest 133Cs has similar behavior to K within plants, which also affects the translocation or distribution of cationic minerals.
Table 3

Distribution ratio of cationic minerals compared with cesium-133 (133Cs) in each part of the stems (ST) and leaf blades (LB) grown in different 133Cs treatment concentrations

Treatment

Label

K/133Cs

Ca/133Cs

Mg/133Cs

300 μM 133Cs

ST1

6.74 ± 0.30b

0.20 ± 0.01c

0.36 ± 0.02bc

 

ST2

9.42 ± 0.32a

0.26 ± 0.02bc

0.85 ± 0.06a

 

ST3

8.39 ± 0.20ab

0.22 ± 0.01bc

0.89 ± 0.06a

 

LB1

3.48 ± 0.21c

0.17 ± 0.02c

0.15 ± 0.01c

 

LB2

3.74 ± 0.09c

0.43 ± 0.02b

0.25 ± 0.02bc

 

LB3

3.33 ± 0.09c

0.90 ± 0.06a

0.50 ± 0.04b

500 μM 133Cs

ST1

2.80 ± 0.08b

0.08 ± 0.00c

0.14 ± 0.00bc

 

ST2

3.51 ± 0.10a

0.11 ± 0.01bc

0.34 ± 0.02a

 

ST3

3.12 ± 0.14ab

0.10 ± 0.00bc

0.34 ± 0.01a

 

LB1

1.55 ± 0.06c

0.06 ± 0.00c

0.06 ± 0.00d

 

LB2

1.48 ± 0.05c

0.15 ± 0.00b

0.08 ± 0.00cd

 

LB3

1.44 ± 0.06c

0.31 ± 0.02a

0.16 ± 0.01b

1000 μM 133Cs

ST1

0.73 ± 0.01b

0.02 ± 0.00c

0.04 ± 0.00d

 

ST2

1.01 ± 0.02a

0.04 ± 0.00b

0.10 ± 0.00b

 

ST3

0.85 ± 0.03b

0.04 ± 0.00b

0.13 ± 0.00a

 

LB1

0.48 ± 0.00c

0.02 ± 0.00c

0.02 ± 0.00e

 

LB2

0.57 ± 0.01c

0.05 ± 0.00b

0.02 ± 0.00de

 

LB3

0.56 ± 0.01c

0.13 ± 0.00a

0.06 ± 0.00c

ST1, ST2, ST3 and LB1, LB2, LB3 indicate young, mature, and old organs in stems and leaf blades, respectively

Values indicate the mean ± standard error (n = 5 individual plants)

The same letters indicate no significant difference within the stems or leaf blades at the 5% level according to Tukey’s multiple-range test

Distribution ratio calculated as cationic mineral content divided by 133Cs content in each part

K potassium; Ca calcium; Mg magnesium

Different levels of 133Cs concentration in soil led to significant correlations between cationic minerals (Table 4). A significantly negative correlation between K and Ca (P < 0.001) and K and Mg (P < 0.01) was observed in the leaf blades compared with the stems. This could be explained by the chemical similarity between 133Cs and K, and competition between K and Mg or Ca translocation within plant organs. From this, in the present study, we considered that 133Cs or K, which are effectively redistributed within plants, have similar competitive behaviors toward Ca or Mg in napiergrass. Conversely, no competition was observed between Ca and Mg within napiergrass (Table 4, Ca vs. Mg). Karley and White [13] suggested that this lack of competition was due to phylogenetic constraints or the control of Ca and Mg concentrations in tissues. Similarly, Smolders et al. [23] observed the uptake of 137Cs in spinach under 15 different nutrient solutions containing 137Cs and showed 137Cs levels were significantly reduced, approximately threefold, by increasing Ca and Mg concentrations. These divalent cations compete with Cs uptake through competition in the apoplast of the root cortex [23]. With regard to the competition between cationic minerals within napiergrass, we suggest that high levels of 133Cs or K translocation will inhibit not only Ca but also Mg translocation and lead to Mg deficiency.
Table 4

Effect of different concentrations of cesium-133 (133Cs) treatment on the correlation coefficient between cations in stems (ST) and leaf blades (LB)

Treatment

K versus Ca

K versus Mg

Ca versus Mg

ST

LB

ST

LB

ST

LB

300 µM 133Cs

0.7701***

− 0.8185***

0.5290*

− 0.7176**

0.4785

0.9786***

500 µM 133Cs

0.9211***

− 0.7998***

0.3762

− 0.7267**

0.5369*

0.9768***

1000 µM 133Cs

0.8193***

− 0.8134***

0.1960

− 0.6883**

0.6898**

0.9548***

K potassium; Ca calcium; Mg magnesium

*, **, and *** indicate significant correlations at the 5%, 1%, and 0.1% levels

4 Conclusion

We investigated the distribution of cesium-133 (133Cs) and competitively translocated cation minerals, such as potassium (K), calcium (Ca), and magnesium (Mg), in different organs of napiergrass under 133Cs-treated conditions. The results of our experiment showed that: (1) 133Cs content was significantly higher in leaf blades than in stems, (2) 133Cs was principally distributed throughout the younger parts of the stems or leaf blades, and (3) translocation of Ca and Mg, particularly Mg, was strongly inhibited by the presence of 133Cs or K within plant organs.

Our results suggest that large amounts of 133Cs or K translocation could lead to nutrient imbalance, especially Mg deficiency, in younger plant organs of napiergrass. Further studies are necessary to verify the competition between 133Cs and cationic minerals, particularly Mg, under relatively low 133Cs concentrations, such as 300 or 500 µM, applied with different levels of K fertilizer.

Notes

Funding

This study was funded by Grant-in-Aid for Scientific Research (Grant Number 17K08163).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Anjos RM, Mosquera B, Sanches N, Cambui CA, Mercier H (2009) Caesium, potassium and ammonium distributions in different organs of tropical plants. Environ Exp Bot 65:111–118CrossRefGoogle Scholar
  2. 2.
    Burger A, Lichtscheidl I (2018) Stable and radioactive cesium: a review about distribution in the environment, uptake and translocation in plants, plant reactions and plants’ potential for bioremediation. Sci Total Environ 618:1459–1485CrossRefGoogle Scholar
  3. 3.
    Burger A, Weiginger M, Adlassnig W, Puschenreiter M, Lichtscheidl I (2019) Response of Arabidopsis halleri to cesium and strontium in hydroponics: extraction potential and effects on morphology and physiology. Ecotoxicol Environ Saf 184:109625CrossRefGoogle Scholar
  4. 4.
    Burger A, Weiginger M, Adlassnig W, Puschenreiter M, Lichtscheidl I (2019) Response of Plantago major to cesium and strontium in hydroponics: absorption and effects on morphology, physiology and photosynthesis. Environ Pollut 254:113084CrossRefGoogle Scholar
  5. 5.
    Cooper JP (1975) Control of photosynthetic production in terrestrial system. In: Cooper JP (ed) Photosynthesis and productivity in different environments. Cambridge Univ Press, Cambridge, pp 593–621Google Scholar
  6. 6.
    Crout N, Beresford N, Sanchez A (2003) Predicting transfer of radionuclides: soil-plant-animal. In: Scott EM (ed) Modelling radioactivity in the environment. Elsevier Science Ltd, Amsterdam, pp 261–286CrossRefGoogle Scholar
  7. 7.
    Fu QF, Tao ZY, Han N, Wu G (2016) Characterizations of bio-accumulations, subcellular distribution and chemical forms of cesium in Brassica juncea, and Vicia faba. J Environ Radioact 154:52–59CrossRefGoogle Scholar
  8. 8.
    Guo W, Nazim H, Liang Z, Yang D (2016) Magnesium deficiency in plants: an urgent problem. Crop J 4:83–91CrossRefGoogle Scholar
  9. 9.
    Isaure MP, Fraysse A, Deves G, Lay PL, Fayard B, Susini J, Bourguignon J, Ortega R (2006) Micro-chemical imaging of cesium distribution in Arabidopsis thaliana plant and its interaction with potassium and essential trace elements. Biochimie 88:1583–1590CrossRefGoogle Scholar
  10. 10.
    Kang DJ, Seo YJ, Saito T, Suzuki H, Ishii Y (2012) Uptake and translocation of cesium-133 in napiergrass (Pennisetum purpureum Schum.) under hydroponic conditions. Ecotoxicol Environ Saf 82:122–126CrossRefGoogle Scholar
  11. 11.
    Kang DJ, Tazoe H, Yamada M, Ishii Y (2014) Differences in remediation effect of 137Cs in napiergrass (Pennisetum purpureum Schum.) under different land-use soil and cutting frequency conditions. Water Air Soil Pollut 225:2022CrossRefGoogle Scholar
  12. 12.
    Kang DJ, Ishii Y, Tazoe H, Isobe K, Higo M, Hosoda M, Yamada M, Tokonami S (2017) Remediation of radiocesium-137 affected soil using napiergrass under different planting density and cutting frequency regimes. Water Air Soil Pollut 228:268CrossRefGoogle Scholar
  13. 13.
    Karley AJ, White PJ (2009) Moving cationic minerals to edible tissues: potassium, magnesium, calcium. Curr Opin Plant Biol 12:291–298CrossRefGoogle Scholar
  14. 14.
    Komínková D, Berchová-Bimová K, Součková L (2018) Influence of potassium concentration gradient on stable caesium uptake by Calla palustris. Ecotoxicol Environ Saf 165:582–588CrossRefGoogle Scholar
  15. 15.
    Lai JL, Fu A, Tao ZY, Lu H, Luo XG (2016) Analysis of the accumulation and redistribution patterns of cesium in Vicia faba grown on contaminated soils. J Environ Radioact 164:202–208CrossRefGoogle Scholar
  16. 16.
    Nishikiori T, Watanabe M, Koshikawa MK, Takamatsu T, Ishii Y, Ito S, Takenaka A, Watanabe K, Hayashi S (2015) Uptake and translocation of radiocesium in cedar leaves following the Fukushima nuclear accident. Sci Total Environ 502:611–616CrossRefGoogle Scholar
  17. 17.
    Sahr T, Voigt G, Schimmack W, Paretzke HG, Ernst D (2005) Low-level radiocaesium exposure alters gene expression in roots of Arabidopsis. New Phytol 168:141–148CrossRefGoogle Scholar
  18. 18.
    Sanches N, Anjos RM, Mosquera B (2008) 40K/137Cs discrimination ratios to the aboveground organs of tropical plants. J Environ Radioact 99:1127–1135CrossRefGoogle Scholar
  19. 19.
    Singh S, Eapen S, Thorat V, Kaushik CP, Raj K, D’Souza SF (2008) Phytoremediation of 137cesium and 90strontium from solutions and low-level nuclear waste by Vetiveria zizanoides. Ecotoxicol Environ Saf 69:306–311CrossRefGoogle Scholar
  20. 20.
    Skarlou V, Papanicolaou EP, Nobeli C (1996) Soil to plant transfer of radioactive cesium and its relation to soil and plant properties. Geoderma 72:53–63CrossRefGoogle Scholar
  21. 21.
    Soudek P, Tykva R, Vanek T (2004) Laboratory analyses of 137Cs uptake by sunflower, reed and poplar. Chemosphere 55:1081–1087CrossRefGoogle Scholar
  22. 22.
    Su Y, Maruthi Sridhar BB, Han FX, Diehl SV, Monts DL (2007) Effects of bioaccumulation of Cs and Sr natural isotopes on foliar structure and plant spectral reflectance of Indian mustard (Brassica juncea). Water Air Soil Pollut 180:65–74CrossRefGoogle Scholar
  23. 23.
    Smolders E, Sweeck L, Merckx R, Cremers A (1997) Cationic interaction in radiocaesium uptake from solution by spinach. J Environ Radioact 34:161–170CrossRefGoogle Scholar
  24. 24.
    Sugiura Y, Kanasashi T, Ogata Y, Ozawa H, Takenaka C (2016) Radiocesium accumulation properties of Chengiopanax sciadophylloides. J Environ Radioact 151:250–257CrossRefGoogle Scholar
  25. 25.
    White PJ, Broadley MR (2000) Mechanisms of caesium uptake by plants. New Physiol 147:241–256CrossRefGoogle Scholar
  26. 26.
    Zhang Y, Liu GJ (2018) Effects of cesium accumulation on chlorophyll content and fluorescence of Brassica juncea L. J Environ Radioact 195:26–32CrossRefGoogle Scholar
  27. 27.
    Zhu YG, Smolders E (2000) Plant uptake of radiocaesium: a review of mechanisms, regulation and application. J Exp Bot 51:1635–1645CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Faculty of Agriculture and Life Science, Teaching and Research Center for Bio-coexistenceHirosaki UniversityGoshogawaraJapan
  2. 2.Kyungpook Agricultural Technology StationDaeguKorea
  3. 3.Department of Biological Production and Environment Sciences, Faculty of AgricultureMiyazaki UniversityMiyazakiJapan

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