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The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.)
CHNAES-00535; No of Pages 6 Acta Ecologica Sinica xxx (2017) xxx–xxx
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The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.) Zhongjun Hu a, Shulan Jin a, Yizong Huang b,⁎, Ying Hu c, Wei Cheng a, Haichao Lin a a b c
College of History, Geography and Tourism, Shangrao Normal University, Shangrao 334000, China Agro-Environmental Protection Institute, Ministry of Agriculture, Tianjin 300191, China Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
a r t i c l e
i n f o
Article history: Received 7 September 2017 Received in revised form 30 October 2017 Accepted 13 November 2017 Available online xxxx Keywords: Iron plaque Lanthanum Neodymium Rice Transfer Enrichment coefficient
a b s t r a c t The effect of root surface iron plaque formation on the uptake, transfer and accumulation of La and Nd in the rice root system was evaluated by using solution cultures. The results showed that La and Nd pollution stress inhibit formation of rice root surface iron plaques. The amount of La and Nd absorbed by the rice root surface iron plaque rose with the increase of La and Nd solution concentrations. Iron plaque formation on the rice root surface significantly decreases the La and Nd concentrations in rice roots and shoots. At growth solution La concentrations of 0.1, 0.5, and 1.0 mmol.L−1, concentrations of La in rice roots with induced iron plaques decreased by 17.1%, 37.4%, and 31.2%, respectively, and concentrations of La in rice shoots decreased by 43.9%, 60.6%, and 27.0%, respectively, when compared to plants with non-induced iron plaques. Also, with Nd solution concentrations of 0.1, 0.5, and 1.0 mmol.L−1, the Nd concentrations in rice roots and shoots of plants with induced iron plaques decreased by 21.0–31.7% and 22.7–47.5%, respectively when compared to plants with non-induced iron plaques. Iron plaque formation on the rice root surface affects the accumulation and transfer of La and Nd in rice roots. Accumulation of La and Nd was greater in rice roots than in rice shoots regardless of whether the plants had induced or noninduced iron plaques. Transfer coefficients of iron plague on rice root surface and root system under La treatments were both higher than those under Nd treatment. For rice roots and iron plaques on the root surface, the enrichment coefficient in the La treatment group was less than that in the Nd treatment group, while for rice shoots, the enrichment coefficient in the La treatment group was greater than that in the Nd treatment group. Clearly, the mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated. © 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
1. Introduction The rare earth elements (REEs) consist of seventeen chemical elements including the fifteen lanthanides (No. 57 to No. 71 in the periodic table) as well as scandium and yttrium [1]. Scandium and yttrium are considered rare earth elements because they exhibit chemical properties similar to the lanthanides. The abundance of REE in the earth's crust is 0.01534% by mass, and the most abundant REE, with a crustal content of 0.0046% by mass, followed by yttrium, neodymium and lanthanum. The atomic and ionic radii of lanthanides, as well as their capacity, decrease with the increase of atomic number. In other words, La is the most reactive element in the lanthanide series. Because of their unique characteristics, REEs are widely used in petroleum, chemical engineering, metallurgy, textiles, ceramics, glass, permanent magnets, etc. Mining, refining and the use of REEs can cause serious environmental problems [2–4]. Serkan and Michael showed that the use of rare earth catalysts in industrial production increased the ⁎ Corresponding author at: Agro-Environmental Protection Institute, Ministry of Agriculture, Tianjin 300191, China. E-mail address: [email protected] (Y. Huang).
concentration of REEs in industrial sewage discharged into the Rhine to 52 mg·kg−1, resulting in the addition of 1.5 tons of La into the Arctic Ocean from the Rhine every year [5]. REEs were also accumulated in tobacco due to the use of rare earth fertilizer. Böhlandt et al. [6] found that the average concentrations of La in the air in smoking and non-smoking residences were 5.9 ng·m−3 and 0.2 ng·m−3, respectively, while concentrations of Ce were 9.6 ng·m−3 and 0.4 ng·m−3, respectively; for La and Ce, smoking residences contain 29.5 and 24 times the concentrations found in non-smoking residences, respectively. China is a major producer, consumer, and exporter of rare earth elements. Domestic rare earth resources are mainly distributed in Baotou and southern Jiangxi. Due to poor supervision during rare earth resource exploitation, mining plots surroundings were severely contaminated by sewage and industrial waste [7–8]. Li et al. [9] suggested that the rare earth content in the soil 10 km downwind from Baotou Steel Rare-Earth Hi-Tech Co. Ltd. of the Inner Mongolia Autonomous Region is 118 times that in the control group. The average soil REE content in mining areas in Jiangxi Province is 976.94 mg·kg−1, 4.53 times the background value in Jiangxi Province and 5.09 times the domestic background value [10]. The average REE content of the well water is 0.033 mg·kg−1, 10.55 times the concentration in control group well water. The average REE content in
https://doi.org/10.1016/j.chnaes.2017.11.002 1872-2032/© 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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rivers is 55.72 mg·kg−1, 8974.7 times the content in control group rivers. The daily average REE intake of local residents from crops and well water is 295.33 g·kg−1·d−1, much higher than the critical threshold for subclinical damage to humans [11]. Because of the high REE content of water and soil in the mining area, the average REE content of crops such as green vegetables and sweet potato is 10 to 20 times above the national hygienic standard [12]. Research has indicated that La accumulated in the rice root system can cause accumulation in the rice cytomembrane and affect the integrity of the plasma membrane. As a consequence, the physiological functions of the rice root may degrade [13]. Also, after prolonged, highdosage exposure to La, the percentage of live sperm and the integrity of the perforatorium in mice decreased, and the frequency of sperm deformity increased [14]. In rats, LaCl3 may cause severe degradation of learning, memory, and the ultrastructure of hippocampal neurons and synapses; the degree of damage increases with increasing La dosage [15]. One form of rare earth, partial Nd2O3, can move into rat lung tissue through non-tracheal exposure, causing acute lung injury for rat. Early symptoms include inflammation, which may lead to the formation of fiber cell nodules [16]. In rice, mitochondrion enzyme activity is passivized and restrained when the concentration of the rare earth compound neodymium trichloride reaches 40 to 60 mg·L−1 [17–18]. Researchers have used REE treatments, including La and Nd, on soybean, cucumber, maize, and mung bean crops, finding that high REE concentrations can significantly inhibit the germination of crop seeds and the growth of seedling roots [19]. Under the condition of severe contamination, growth of crop root system ceases completely. Other researchers studied the impact of REEs, such as La and Nd, on soil animal community structure in a plum garden. Their results showed that the number of animal classes and the number of soil animal communities decreased as the concentration of rare earth elements increased [20]. La3+ and Nd3+ can damage the ultrastructure of splenocyte and cause oxidative stress to splenic tissue. The degree of and mechanisms governing damage to mice may be related to the number of electrons in the REE 4f orbital [21]. Rare earth in the natural environment may enter the human body through the food chain, which affected human's health. Research has shown that when the daily intake of rare earth reached 6 to 6.7 mg, residents from mining areas in Southern Jiangxi Province experienced negative health effects [22]. The problem of rare earth entering the human body through the food chain becomes important in mining areas. At present, cleaning and recovery of heavy metal pollution from edaphophyte is the most studied approach. Many studies have shown that iron plaque on the plant root surface can inhibit the absorption and translocation of heavy metal elements [23]. Iron plaque on the rice root surface can lead to Cd, Pb, and Sb enrichment [24–25] and inhibit these elements from translocating towards the rice seedlings [26–27]. Because copper is passivated by iron on the root cortex, and aluminum precipitates with phosphate on the plant root surface, iron plaque on the root surface can reduce the toxicity of copper and aluminum [28–30]. However, some studies suggest that a small amount of iron plaque can accelerate plant absorption of heavy metal elements. Liu et al. [31] argued that iron plaque on the rice root system can promote the translocation of Pb into the root to a certain degree. In academic circles, researchers have mainly focused on the mechanisms by which iron plaque inhibits or promotes plant absorption of heavy metal and other hazardous substances. However, there has been little study of the impact of iron plaque on edaphophyte absorption and translocation of REEs. Although REE characteristics are similar to heavy metals, the mechanisms of passivation and restoration of iron plaque on the root surface are very complex and are affected by the physical and chemical properties of the iron plaque, the growth medium, and the condition of the plant. Because of these complexities, the impact of iron plaque on the absorption and translocation of REE is worth studying. The seventeen REEs have similar atomic structure and ionic radius, which is logical since they are paragenetic. Due to their comparatively high crustal contents, La and Nd exert
great influence on the ecological environment in mining areas. In order to mitigate the impacts of REEs on environmental and human health, this paper presents hydroponic experiments on the impact of iron plaque on the absorption and translocation of La and Nd; the results herein provide a theoretical foundation for rare earth pollution control and prevention measures. 2. Materials and methods 2.1. Experimental rice The experimental rice seed, named Jiahua-1, is a local type of midmaturation japonica rice grown in Jinhua, Zhejiang Province. Whole grains of consistent size were selected and 30% hydrogen peroxide (H2O2) was used to sterilize them for 15 min. The grains were washed three times using deionized water, and were sowed in soaked perlite, and allowed to grow for twenty days. When the rice seedlings developed four leaf pieces, healthy seedlings with consistent growth were selected and transplanted to PVC pots with a diameter of 7.5 cm and a height of 14 cm for further study. Each pot grown one rice seedling; the nutrient solution was changed twice a week. The compositions of the nutrient solutions are shown in Table 1; solution pH was adjusted to 5.5 using 0.1 mol·L−1 KOH or HCl, as needed. In plants showing crystalline salt formation on the rice surface, a nutrient solution of 1/3 concentration was used during pot cultivation. 2.2. Experimental design A total of 56 pots of rice were cultivated in phytotron. The growth conditions were as follows: sunlight duration = 14 h·d−1, illumination intensity = 260 to 350 μmol·(m2·s)−1, relative humidity = ~5%, and temperature = ~ 25 °C. When the length of the rice root reached about 15 cm, the nutrient solution was poured away in 28 pots of rice, soaked them with distilled water for 12 h, treated them with 40 ppm ferrous sulfate (Fe2SO4) solution for 36 h, and finally discarded the sulfate solution and treated the plants using a 1/3-concentration nutrient solution for 48 h. These 28 pots of rice comprise the iron-plaque-induced group (hereafter referred to as the induced group), and the other 28 pots are non iron-plaque-induced group (hereafter referred to as the control group). Half of these 56 pots of rice were treated with lanthanum nitrate (La(NO3)3) solutions and another half with neodymium nitrate (Nd(NO3)3) solutions. Both treatments consisted of four concentrations of 0.0 (CK), 0.1, 0.5 and 1.0 mmol·L−1, and each concentration was replicated for four times. After ten days of lanthanum nitrate and neodymium nitrate treatments, all rice plants were harvested and divided into two parts: aboveground and underground. 2.3. Sample treatment and analysis After harvesting, the iron plaque on the root system was extracted by using the DCB (dithionite-citrate-bicarbonate) method. Specific procedures were as follows: the rice roots were washed using distilled water, dried using absorbent paper, and separated from the rest of the plant. The roots were soaked in a 100-ml beaker containing 30 ml of a mixed 0.03 mol·L−1 trisodium citrate (Na3C6H5O7·2H2O) and Table 1 Nutrient solution composition for rice. Nutriment
Concentrations/mg·L−1 Nutriment
Concentrations/mg·L−1
CaCl2 NH4NO3 MgSO4·7H2O K2SO4 KH2PO4 Fe EDTA NaCl
444 402 368 348 180 21 5.85
0.85 0.62 0.29 0.25 0.12 0.053
MnSO4·1H2O H3BO3 ZnSO4·7H2O CuSO4·5H2O Na2MoO4·2H2O CoSO4·7H2O
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
Z. Hu et al. / Acta Ecologica Sinica xxx (2017) xxx–xxx
0.125 mol·L−1 sodium bicarbonate (NaHCO3) solution for 10 min. Then, 1 g sodium hydrosulfite (Na2S2O4) was added into the beaker and soaked the roots at room temperature (20–25 °C) until they turned completely white. Then, the extract liquid was transferred into a 50ml volumetric flask. The rice roots were washed in deionized water for three times and then transferred this cleaning fluid into the 50-ml volumetric flask. After filtering the extract liquid through a 0.45-μm filter membrane, plasma power spectral (ICP-OES) methods such as inductive coupling to measure the concentrations of Fe and REEs of La and Nd were used. The extracted rice roots and shoots were washed using deionized water and then were dried. Then, the plants were placed into a 50 °C drying oven, dried them to constant weight, and ground them using a stainless steel grinder. A 0.2000 ± 0.0001 g sample of shoot and a 0.1000 ± 0.0001 g sample of root were placed into a 50ml centrifuge tube. Each sample was replicated four times. A total of 5 ml pure HNO3, was added and the samples were soaked overnight, and allowed to dissolve in a microwave-accelerated reaction system. After dissolution, the solution in the centrifuge tube was transferred into a 50-ml volumetric flask, diluted the sample with ultrapure water to 50 ml, and shook thoroughly. Then the solution was filtered with a 0.45-μm filter membrane and collected the supernatant. ICP-OES was used to measure the concentrations of La and Nd, using a national standard sample (Tea GBW10016) for quality control.
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Table 3 The correlation coefficients among La concentrations in solution, iron plaque contents on root surface and La concentrations in root surface iron plaque.
Solution-La RSIP RSIP-La
Solution-La
RSIP
RSIP-La
1 −0.963 0.874
1 −0.710
1
Note: Solution-La: La concentrations in solution, RSIP: root surface iron plaque, RSIP-La: La concentrations in root surface iron plaque.
on the root surface under both La and Nd treatment is inferior to that formed in the CK group. As the concentrations of La and Nd increase, the amount of iron plaque on rice is decreased. These results show that La and Nd pollution stress may inhibit the formation of the rice root surface to a certain degree. The accumulation of La and Nd in iron plaque on the root surface increased as the concentration of La and Nd in the nutrient solution increased and the amount of iron plaque decreased. The coefficients are shown in Tables 3 and 4. 3.2. La and Nd content in rice shoots and root systems It can be seen in Figs. 1 and 2 that, under 0.1, 0.5 and 1.0 mmol·L−1 La and Nd treatments, the REE content of the shoots and root systems in the induced group was significantly lower than that in the non-induced group. Fig. 1 shows that when La solution concentrations were 0.1, 0.5, and 1.0 mmol·L− 1, La content in the rice root system in the induced group was reduced by 17.1%, 37.4% and 31.2%, respectively, and La content in shoots was reduced by 43.9%, 60.6% and 27.0%, respectively, as compared to the non-induced group. When Nd solution concentrations were 0.1, 0.5 and 1.0 mmol·L−1, Nd content in the rice root system in the induced group was reduced by 21.0%, 31.6% and 31.7%, respectively, and Nd content in shoots was reduced by 47.5%, 22.7% and 28.3%, respectively, when compared to the non-induced group. These results suggest that iron plaque on the root surface inhibits absorption and translocation of La and Nd efficiently. These effects are influenced by several factors, including the type and concentration of REEs in the nutrient solution, the amount of iron plaque, and the amount of REEs absorbed by the iron plaque. The mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated. Under La and Nd treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the La and Nd content in the root system was significantly higher than that in the shoot for both the induced and non-induced groups. The REE content of the root system was positively correlated with the concentration of rare earth in the nutrient solution. In other words, the La and Nd content of the root system rose with the increase of nutrient solution concentrations. The REE content in shoots was positively correlated with nutrient solution and root system concentrations.
2.4. Data analysis The transfer coefficient (TF) indicates the ability of the iron plaque and the root system to transfer La to shoots and is calculated via: TFx ¼ Cshoot‐REE =Cx−REE In this formula, x stands for DCB, root. REE stands for La or Nd. TFx is the transfer coefficient for La or Nd in the DCB or root. Cshoot-REE stands for the concentration of La or Nd in the shoot. Cx-REE stands for the concentration of La or Nd in the DCB or root, respectively. The enrichment coefficient (BAF) indicates the ability of rice to concentrate La and Nd and is calculated via: BAFy ¼ Cy‐REE =Csolution−REE In this formula, y stands for DCB, root, or shoot. BAFy is the enrichment coefficient for La or Nd in the DCB, root, or shoot, as indicated by other subscripts. Cy-REE stands for the concentration of La or Nd in the DCB, root, or shoot. Csolution-REE stands for the concentration of La or Nd in the nutrient solution. SPSS 19.0 and Excel 2007 were used to analyze the experimental data. 3. Results and analysis
3.3. Translocation of La and Nd from the iron plaque and the root system to the shoots
3.1. Iron plaque formation on the root surface, and iron plaque La and Nd content
It can be seen in Table 5 that, under La and Nd treatment, the translocation coefficients of rice root systems in both the induced and noninduced groups increased with increasing REE concentration in the treatment solution. Under La treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the translocation coefficient between root
DCB-Fe indicates the amounts of iron plaque on the root surface. The amount and rare earth content of iron plaques under four different La and Nd solution concentrations (0, 0.1, 0.5 and 1.0 mM) are shown in Table 2. It can be seen in Table 1 that the amount of iron plaque formed Table 2 Amount of iron plaque on the root surface and La and Nd contents in the iron plaque of rice. CK
Fe/g·kg−1 REE/mg·kg−1
15.00 ± 1.41d ND
La treatment
Nd treatment
0.1
0.5
1
0.1
0.5
1
14.36 ± 1.02c 148.03 ± 33.73a
14.00 ± 0.70 b 255.93 ± 40.01b
12.52 ± 0.49a 266.42 ± 7.55b
14.27 ± 0.28a 473.56 ± 51.25c
13.58 ± 0.65b 505.87 ± 48.16b
13.08 ± 0.23a 617.32 ± 39.901a
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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Table 4 The correlation coefficients among Nd concentrations in solution, iron plaque contents on root surface and Nd concentrations in root surface iron plaque.
Solution-Nd RSIP RSIP-Nd
Solution-Nd
RSIP
RSIP-Nd
1 −0.988 0.971
1 −0.921
1
Note: Solution-Nd: La concentrations in solution, RSIP: root surface iron plaque, RSIP-Nd: La concentrations in root surface iron plaque.
system and shoots in the non-induced group increased from 0.014 to 0.15 (becoming 10.71 times higher); the coefficient in the induced group increased from 0.008 to 0.159 (becoming 19.88 times higher). Under Nd treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the translocation coefficient between root system and shoots in the non-induced group increased from 0.008 to 0.117 (becoming 14.63 times higher); the coefficient in the induced group increased from 0.005 to 0.122 (becoming 24.4 times higher). The translocation coefficients between the iron plaque and shoots were higher than those between the iron plaque and root system, irrespective of the treatment (La or Nd). The type of REE affected the translocation of REEs by the rice root system. Under La treatment, the translocation coefficients of both the iron plaque and the root system were higher than those under Nd treatments of the same concentration. This suggests that the translocation of La from underground plant parts to above-ground parts is easier than translocation of Nd. This may be due to the fact that La is the most reactive metal in the lanthanide series. Fig. 2. The impact of iron plague on the contents of Nd in rice's roots and shoots (n = 4, a, b and A, B stand for significant difference of different treatment in induced group and noninduced group respectively, p b 0.05).
3.4. Enrichment of La and Nd in different parts of the rice plant It can be seen in Table 6 that, for the non-induced group, the enrichment coefficients for the rice root system were higher than those for the shoots under both La and Nd treatments. For the induced group, enrichment coefficients are ranked in the following order: root system N iron plaque N shoots. Under La and Nd treatments, the enrichment coefficients of the root system decreased as the treatment REE concentration increased in both the induced and non-induced groups. The enrichment coefficients of the shoots increased as the treatment REE concentration increased in both induced and non-induced groups. The enrichment coefficients of the iron plaque decreased as the treatment REE concentration increased in the induced group. Under La and Nd treatments of three different concentrations, the enrichment coefficients of the rice root system and shoots were higher in the non-induced group than in the induced group at the same treatment concentration. The iron plaque and root system enrichment coefficients were higher under Nd treatment than under La treatment, while the shoot enrichment coefficients were lower under Nd treatment than under La treatment. This suggests that REE enrichment in rice is affected by the type and concentration of REEs, the amount of iron plaque, and the part of the rice plant in question. 4. Discussion
Fig. 1. The impact of iron plague on the contents of La in rice's roots and shoots (n = 4, a, b and A, B stand for significant difference of different treatment in induced group and noninduced group respectively, p b 0.05).
The cleaning and treatment of sewage by wetland ecosystems is a topic of current research. Waterlogged environments induce aerenchyma in plants, which transfers oxygen from leaves to the root system. Thus, many kinds of wetland plants can release oxygen from their root systems [32–33]. When the growth medium is rich in Fe2 +, the Fe2+ can participate in a chemical reaction with the oxygen released from the root system, forming iron plaque [34–35]: 4Fe2+ + O2 + 10H2O
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
Z. Hu et al. / Acta Ecologica Sinica xxx (2017) xxx–xxx
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Table 5 Transfer coefficients of iron plague and root system transferring La and Nd to shoots. Iron plague
La Nd
Non-induced group Induced group Non-induced group Induced group
Roots
0.1
0.5
1
0.1
0.5
1
ND 0.126 ± 0.033a ND 0.027 ± 0.007a
ND 0.376 ± 0.078b ND 0.168 ± 0.068b
ND 2.239 ± 0.247c ND 0.830 ± 0.122c
0.014 ± 0.003a 0.008 ± 0.001a 0.008 ± 0.001a 0.005 ± 0.002a
0.054 ± 0.019a 0.034 ± 0.011a 0.021 ± 0.001a 0.024 ± 0.008a
0.150 ± 0.098a 0.159 ± 0.03a 0.117 ± 0.037b 0.122 ± 0.049b
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
= 4Fe(OH)3 + 8H+. The concentration of Fe2+ in the growth medium is one of the factors affecting the formation of iron plaque. If we were to add Fe2 + into the soil or nutrient solution, the redox potential would increase and the reaction shown above would go forward as the root system released oxygen. Thus, the amount of iron plaque on the root surface of wetland plants would increase. This study suggests that iron plaque can be formed when 40 ppm Fe2SO4 is added to the nutrient solution, whereby the roots form an iron film. The formation of iron plaque is also related with the oxidative potential of the root system, the type of rice, the growing period, and the growth environment [36]. Pan et al. [32] found that sediments including rare-earth phosphates, rare-earth sulfates, and rare-earth hydroxides in the medium can attach to the rice root surface and inhibit iron plaque formation to a certain degree. This result is consistent with the conclusions of this study. The iron plaque found on the rice root surface has characteristics similar to iron oxide in the natural environment. It is a kind of ampholytoid, with relatively high specific surface area and –OH functional group content. It can initiate adsorption-desorption, oxidationreduction, and organic-inorganic complexation reactions with metals and other anions and cations [37]. Many researchers have shown that iron plaque increases absorption of nutrient elements including iron, phosphorus, zinc, magnesium, manganese, etc. and heavy metal including Cd, Pb, Sb and As near the root area [23]. As an ampholytoid, iron oxide and its hydrous oxide can adsorb anions in soils and nutrient so2− lutions such as PO3− 4 and CO3 . Anions adsorbed by the oxide can combine with metal cations in the medium. Hansel et al. [38] found that metal carbonates formed by manganese and zinc were attached to root surfaces. Cai et al. found that aluminum formed a phosphate rather than bind with iron oxide, and that this phosphate could be deposited on a root surface with iron plaque [28]. When the growth medium has a high PO3− 4 content, iron oxide and phosphate can form a mononuclear complex which is easily desorbed; when the medium has a relatively low PO3− content, a binuclear complex is formed that is difficult to de4 sorb. Nutrient solutions of 1/3 concentration were used when cultivating rice in pots; the concentration of PO34 − and CO2– 3 was relatively low in these solutions. Nonetheless, phosphate and carbonate compounds were formed with the La and Nd that attached tightly to the iron plaque. The ability of iron plaque to adsorb and deposit La and Nd can affect REE bioavailability, thus affecting the uptake and
translocation of REEs by rice. In this study, the La and Nd content of rice root systems and shoots were significantly lower in the induced group than in the non-induced group. The translocation and enrichment coefficients of the root system were higher for the non-induced group than for the induced group. Iron plaque forms a barrier against REE uptake by plants. The mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated and vary with the type and concentration of REEs in the medium. Because La is the most reactive metal in the lanthanide series, and because La and Nd have different numbers of electrons in their 4f orbitals, the iron plaque formed on the root surface and its impact on the uptake and translocation of REEs by rice were different under La and Nd treatments. In both the induced and non-induced groups, the iron plaque and root system translocation coefficients and the shoot enrichment coefficients were higher under La treatment than under a Nd treatment of the same concentration. The iron plaque and root system enrichment coefficients were lower under La treatment than under Nd treatment.
5. Conclusions La and Nd pollution stress can inhibit root surface iron plaque formation in rice to a certain degree. The accumulation of La and Nd in iron plaque on the root surface increased with increasing nutrient solution La and Nd concentrations and decreasing amounts of iron plaque. Iron plaque on the rice root surface inhibited the uptake and translocation of La and Nd. Under La solution concentrations of 0.1, 0.5 and 1.0 mmol·L−1, La content in the rice root system was reduced by 17.1%, 37.4% and 31.2%, respectively, in plants with an induced iron plaque; the La content in shoots was reduced by 43.9%, 60.6% and 27.0%, respectively. Under Nd solution concentrations of 0.1, 0.5 and 1.0 mmol·L− 1, Nd content in the rice root system was reduced by 21.0%, 31.6% and 31.7% respectively, in plants with an induced iron plaque, and the Nd content in shoots was reduced by 47.5%, 22.7% and 28.3%, respectively. Because La is the most reactive metal in the lanthanide series, and because La and Nd have different numbers of electrons in their 4f orbitals, the iron plaque formed on the root surface and its impact on the uptake and translocation of REEs by rice were different under La and Nd treatments.
Table 6 Enrichment coefficients of La and Nd in different parts of rice. Iron plague 0.1 La
Roots 0.5
1
Non-induced group Induced 11.78 ± 2.431ab 4.105 ± 0.581a 2.108 ± 0.050a group Nd Non-induced group Induced 32.84 ± 7.684b 7.01 ± 1.194a 4.27 ± 0.347a group
Shoots
0.1
0.5
1
0.1
194.8 ± 22.143f
65.83 ± 9.951d
39.16 ± 4.622c
2.778 ± 0.839a 3.562 ± 1.220a 5.866 ± 2.736a
0.5
1
161.4 ± 40.586d
41.2 ± 13.512c
29.6 ± 3.801bc
1.347 ± 0.362a 1.402 ± 0.421a 4.284 ± 0.463a
203.782 ± 113.351a 161.567 ± 57.493b
72.695 ± 42.175 ± 9.620c 1.664 ± 0.223a 1.526 ± 0.455a 4.953 ± 1.262b 26.879b 49.69 ± 14.612a 29.98 ± 3.164a 0.874 ± 0.263b 1.18 ± 0.397a 3.55 ± 0.865a
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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Acknowledgments The authors would like to thank Natural Science Foundation of China (No. 41561096), Science and Technology Project of Jiangxi Provincial Education Department of China (No. GJJ161048) and Jiangxi Provincial Science and Technology Planning Project of China (No. 20142BAB203026) for financial support, the authors would also like to thank Agro-Environmental Protection Institute, Ministry of Agriculture in Tianjin and Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences in Beijing of China for their experimental supports. References [1] J.M. Klinger, A historical geography of rare earth elements: from discovery to the atomic age, Extractive Ind. Soc. 2 (2015) 572. [2] M. Patrycja, K. Borowiak, P. Niedzielski, Phytoextraction of rare earth elements in herbaceous plant species growing close to roads, Environ. Sci. Pollut. Res. 24 (2017) 14091. [3] O. Wiche, N.A. Kummer, H. Heilmeier, Interspecific root interactions between white lupin and barley enhance the uptake of rare earth elements (REEs) and nutrients in shoots of barley, Plant Soil 402 (2016) 235. [4] S. Suja, L. Lina, V. Fernandes, R. Purnachandra, Distribution and fractionation of rare earth elements and Yttrium in suspended and bottom sediments of the Kali estuary, western India, Environ. Earth Sci. 76 (2017) 174. [5] K. Serkan, B. Michael, Rare earth elements in the Rhine River, Germany: first case of anthropogenic lanthanum as a dissolved micro contaminant in the hydrosphere, Environ. Int. 37 (2011) 973. [6] A. Böhlandt, R. Schierl, J. Diemer, C. Koch, G. Bolte, M. Kiranoglu, H. Fromme, D. Nowak, High concentrations of cadmium, cerium and lanthanum in indoor air due to environmental tobacco smoke, Sci. Total Environ. 414 (2012) 738. [7] M.Q. Zhuang, J.S. Zhao, S.Y. Li, D.R. Liu, K.B. Wang, P.R. Xiao, L.L. Yu, Y. Jiang, J. Song, J.Y. Zhou, L.S. Wang, Z.H. Chu, Concentrations and health risk assessment of rare earth elements in vegetables from mining area in Shandong, China, Chemosphere 168 (2017) 578. [8] H. Song, W.J. Shin, J.S. Ryu, H.S. Shin, H. Chung, K.S. Lee, Anthropogenic rare earth elements and their spatial distributions in the Han River, South Korea, Chemosphere 172 (2017) 155. [9] J.X. Li, M. Hong, X.Q. Yin, J.L. Liu, Effects of the accumulation of the rare earth elements on soil macrofauna community, J. Rare Earths 28 (2010) 967. [10] S.L. Jin, Y.Z. Huang, Y. Hu, et al., Rare earth elements content and health risk assessment of soil and crops in typical rare earth mine area in Jiangxi Province, Acta Sci. Circumst. 34 (12) (2014) 3084–3093. [11] J.H. Zhu, Z.K. Yuan, X.Y. Wang, S.M. Yan, Investigation on the contents of rare earth elements in environment of rare earth ore area in Jiangxi, Environ. Health 19 (2002) 443. [12] T. Liang, K.X. Li, L.Q. Wang, State of rare earth elements in different environmental components in mining areas of China, Environ. Monit. Assess. 186 (2014) 1499. [13] Q.M. Xu, H. Chen, Antioxidant responses of rice seedling to Ce4+ under hydroponic cultures, Ecotoxicol. Environ. Saf. 74 (2011) 1693. [14] J. Chen, H.J. Xiao, T. Qi, D.L. Chen, H.M. Long, S.H. Liu, Rare earths exposure and male infertility: the injury mechanism study of rare earths on male mice and human sperm, Environ. Sci. Pollut. Res. 22 (3) (2015) 2076. [15] H.Q. Zhao, Z. Cheng, R.P. Hu, J. Chen, M.M. Hong, M. Zhou, X.L. Gong, L. Wang, F.S. Hong, Oxidative injury in the brain of mice caused by lanthanid, Biol. Trace Elem. Res. 2 (2011) 174. [16] J. Yang, Q. Liu, L. Zhang, S.W. Wu, M. Qi, S. Lu, Q. Xi, Y. Cai, Lanthanum chloride impairs memory, decreases pCaMK IV, pMAPK and pCREB expression of hippocampus in rats, Toxicol. Lett. 190 (2009) 208.
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Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.) Zhongjun Hu a, Shulan Jin a, Yizong Huang b,⁎, Ying Hu c, Wei Cheng a, Haichao Lin a a b c
College of History, Geography and Tourism, Shangrao Normal University, Shangrao 334000, China Agro-Environmental Protection Institute, Ministry of Agriculture, Tianjin 300191, China Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
a r t i c l e
i n f o
Article history: Received 7 September 2017 Received in revised form 30 October 2017 Accepted 13 November 2017 Available online xxxx Keywords: Iron plaque Lanthanum Neodymium Rice Transfer Enrichment coefficient
a b s t r a c t The effect of root surface iron plaque formation on the uptake, transfer and accumulation of La and Nd in the rice root system was evaluated by using solution cultures. The results showed that La and Nd pollution stress inhibit formation of rice root surface iron plaques. The amount of La and Nd absorbed by the rice root surface iron plaque rose with the increase of La and Nd solution concentrations. Iron plaque formation on the rice root surface significantly decreases the La and Nd concentrations in rice roots and shoots. At growth solution La concentrations of 0.1, 0.5, and 1.0 mmol.L−1, concentrations of La in rice roots with induced iron plaques decreased by 17.1%, 37.4%, and 31.2%, respectively, and concentrations of La in rice shoots decreased by 43.9%, 60.6%, and 27.0%, respectively, when compared to plants with non-induced iron plaques. Also, with Nd solution concentrations of 0.1, 0.5, and 1.0 mmol.L−1, the Nd concentrations in rice roots and shoots of plants with induced iron plaques decreased by 21.0–31.7% and 22.7–47.5%, respectively when compared to plants with non-induced iron plaques. Iron plaque formation on the rice root surface affects the accumulation and transfer of La and Nd in rice roots. Accumulation of La and Nd was greater in rice roots than in rice shoots regardless of whether the plants had induced or noninduced iron plaques. Transfer coefficients of iron plague on rice root surface and root system under La treatments were both higher than those under Nd treatment. For rice roots and iron plaques on the root surface, the enrichment coefficient in the La treatment group was less than that in the Nd treatment group, while for rice shoots, the enrichment coefficient in the La treatment group was greater than that in the Nd treatment group. Clearly, the mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated. © 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
1. Introduction The rare earth elements (REEs) consist of seventeen chemical elements including the fifteen lanthanides (No. 57 to No. 71 in the periodic table) as well as scandium and yttrium [1]. Scandium and yttrium are considered rare earth elements because they exhibit chemical properties similar to the lanthanides. The abundance of REE in the earth's crust is 0.01534% by mass, and the most abundant REE, with a crustal content of 0.0046% by mass, followed by yttrium, neodymium and lanthanum. The atomic and ionic radii of lanthanides, as well as their capacity, decrease with the increase of atomic number. In other words, La is the most reactive element in the lanthanide series. Because of their unique characteristics, REEs are widely used in petroleum, chemical engineering, metallurgy, textiles, ceramics, glass, permanent magnets, etc. Mining, refining and the use of REEs can cause serious environmental problems [2–4]. Serkan and Michael showed that the use of rare earth catalysts in industrial production increased the ⁎ Corresponding author at: Agro-Environmental Protection Institute, Ministry of Agriculture, Tianjin 300191, China. E-mail address: [email protected] (Y. Huang).
concentration of REEs in industrial sewage discharged into the Rhine to 52 mg·kg−1, resulting in the addition of 1.5 tons of La into the Arctic Ocean from the Rhine every year [5]. REEs were also accumulated in tobacco due to the use of rare earth fertilizer. Böhlandt et al. [6] found that the average concentrations of La in the air in smoking and non-smoking residences were 5.9 ng·m−3 and 0.2 ng·m−3, respectively, while concentrations of Ce were 9.6 ng·m−3 and 0.4 ng·m−3, respectively; for La and Ce, smoking residences contain 29.5 and 24 times the concentrations found in non-smoking residences, respectively. China is a major producer, consumer, and exporter of rare earth elements. Domestic rare earth resources are mainly distributed in Baotou and southern Jiangxi. Due to poor supervision during rare earth resource exploitation, mining plots surroundings were severely contaminated by sewage and industrial waste [7–8]. Li et al. [9] suggested that the rare earth content in the soil 10 km downwind from Baotou Steel Rare-Earth Hi-Tech Co. Ltd. of the Inner Mongolia Autonomous Region is 118 times that in the control group. The average soil REE content in mining areas in Jiangxi Province is 976.94 mg·kg−1, 4.53 times the background value in Jiangxi Province and 5.09 times the domestic background value [10]. The average REE content of the well water is 0.033 mg·kg−1, 10.55 times the concentration in control group well water. The average REE content in
https://doi.org/10.1016/j.chnaes.2017.11.002 1872-2032/© 2017 Published by Elsevier B.V. on behalf of Ecological Society of China.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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rivers is 55.72 mg·kg−1, 8974.7 times the content in control group rivers. The daily average REE intake of local residents from crops and well water is 295.33 g·kg−1·d−1, much higher than the critical threshold for subclinical damage to humans [11]. Because of the high REE content of water and soil in the mining area, the average REE content of crops such as green vegetables and sweet potato is 10 to 20 times above the national hygienic standard [12]. Research has indicated that La accumulated in the rice root system can cause accumulation in the rice cytomembrane and affect the integrity of the plasma membrane. As a consequence, the physiological functions of the rice root may degrade [13]. Also, after prolonged, highdosage exposure to La, the percentage of live sperm and the integrity of the perforatorium in mice decreased, and the frequency of sperm deformity increased [14]. In rats, LaCl3 may cause severe degradation of learning, memory, and the ultrastructure of hippocampal neurons and synapses; the degree of damage increases with increasing La dosage [15]. One form of rare earth, partial Nd2O3, can move into rat lung tissue through non-tracheal exposure, causing acute lung injury for rat. Early symptoms include inflammation, which may lead to the formation of fiber cell nodules [16]. In rice, mitochondrion enzyme activity is passivized and restrained when the concentration of the rare earth compound neodymium trichloride reaches 40 to 60 mg·L−1 [17–18]. Researchers have used REE treatments, including La and Nd, on soybean, cucumber, maize, and mung bean crops, finding that high REE concentrations can significantly inhibit the germination of crop seeds and the growth of seedling roots [19]. Under the condition of severe contamination, growth of crop root system ceases completely. Other researchers studied the impact of REEs, such as La and Nd, on soil animal community structure in a plum garden. Their results showed that the number of animal classes and the number of soil animal communities decreased as the concentration of rare earth elements increased [20]. La3+ and Nd3+ can damage the ultrastructure of splenocyte and cause oxidative stress to splenic tissue. The degree of and mechanisms governing damage to mice may be related to the number of electrons in the REE 4f orbital [21]. Rare earth in the natural environment may enter the human body through the food chain, which affected human's health. Research has shown that when the daily intake of rare earth reached 6 to 6.7 mg, residents from mining areas in Southern Jiangxi Province experienced negative health effects [22]. The problem of rare earth entering the human body through the food chain becomes important in mining areas. At present, cleaning and recovery of heavy metal pollution from edaphophyte is the most studied approach. Many studies have shown that iron plaque on the plant root surface can inhibit the absorption and translocation of heavy metal elements [23]. Iron plaque on the rice root surface can lead to Cd, Pb, and Sb enrichment [24–25] and inhibit these elements from translocating towards the rice seedlings [26–27]. Because copper is passivated by iron on the root cortex, and aluminum precipitates with phosphate on the plant root surface, iron plaque on the root surface can reduce the toxicity of copper and aluminum [28–30]. However, some studies suggest that a small amount of iron plaque can accelerate plant absorption of heavy metal elements. Liu et al. [31] argued that iron plaque on the rice root system can promote the translocation of Pb into the root to a certain degree. In academic circles, researchers have mainly focused on the mechanisms by which iron plaque inhibits or promotes plant absorption of heavy metal and other hazardous substances. However, there has been little study of the impact of iron plaque on edaphophyte absorption and translocation of REEs. Although REE characteristics are similar to heavy metals, the mechanisms of passivation and restoration of iron plaque on the root surface are very complex and are affected by the physical and chemical properties of the iron plaque, the growth medium, and the condition of the plant. Because of these complexities, the impact of iron plaque on the absorption and translocation of REE is worth studying. The seventeen REEs have similar atomic structure and ionic radius, which is logical since they are paragenetic. Due to their comparatively high crustal contents, La and Nd exert
great influence on the ecological environment in mining areas. In order to mitigate the impacts of REEs on environmental and human health, this paper presents hydroponic experiments on the impact of iron plaque on the absorption and translocation of La and Nd; the results herein provide a theoretical foundation for rare earth pollution control and prevention measures. 2. Materials and methods 2.1. Experimental rice The experimental rice seed, named Jiahua-1, is a local type of midmaturation japonica rice grown in Jinhua, Zhejiang Province. Whole grains of consistent size were selected and 30% hydrogen peroxide (H2O2) was used to sterilize them for 15 min. The grains were washed three times using deionized water, and were sowed in soaked perlite, and allowed to grow for twenty days. When the rice seedlings developed four leaf pieces, healthy seedlings with consistent growth were selected and transplanted to PVC pots with a diameter of 7.5 cm and a height of 14 cm for further study. Each pot grown one rice seedling; the nutrient solution was changed twice a week. The compositions of the nutrient solutions are shown in Table 1; solution pH was adjusted to 5.5 using 0.1 mol·L−1 KOH or HCl, as needed. In plants showing crystalline salt formation on the rice surface, a nutrient solution of 1/3 concentration was used during pot cultivation. 2.2. Experimental design A total of 56 pots of rice were cultivated in phytotron. The growth conditions were as follows: sunlight duration = 14 h·d−1, illumination intensity = 260 to 350 μmol·(m2·s)−1, relative humidity = ~5%, and temperature = ~ 25 °C. When the length of the rice root reached about 15 cm, the nutrient solution was poured away in 28 pots of rice, soaked them with distilled water for 12 h, treated them with 40 ppm ferrous sulfate (Fe2SO4) solution for 36 h, and finally discarded the sulfate solution and treated the plants using a 1/3-concentration nutrient solution for 48 h. These 28 pots of rice comprise the iron-plaque-induced group (hereafter referred to as the induced group), and the other 28 pots are non iron-plaque-induced group (hereafter referred to as the control group). Half of these 56 pots of rice were treated with lanthanum nitrate (La(NO3)3) solutions and another half with neodymium nitrate (Nd(NO3)3) solutions. Both treatments consisted of four concentrations of 0.0 (CK), 0.1, 0.5 and 1.0 mmol·L−1, and each concentration was replicated for four times. After ten days of lanthanum nitrate and neodymium nitrate treatments, all rice plants were harvested and divided into two parts: aboveground and underground. 2.3. Sample treatment and analysis After harvesting, the iron plaque on the root system was extracted by using the DCB (dithionite-citrate-bicarbonate) method. Specific procedures were as follows: the rice roots were washed using distilled water, dried using absorbent paper, and separated from the rest of the plant. The roots were soaked in a 100-ml beaker containing 30 ml of a mixed 0.03 mol·L−1 trisodium citrate (Na3C6H5O7·2H2O) and Table 1 Nutrient solution composition for rice. Nutriment
Concentrations/mg·L−1 Nutriment
Concentrations/mg·L−1
CaCl2 NH4NO3 MgSO4·7H2O K2SO4 KH2PO4 Fe EDTA NaCl
444 402 368 348 180 21 5.85
0.85 0.62 0.29 0.25 0.12 0.053
MnSO4·1H2O H3BO3 ZnSO4·7H2O CuSO4·5H2O Na2MoO4·2H2O CoSO4·7H2O
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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0.125 mol·L−1 sodium bicarbonate (NaHCO3) solution for 10 min. Then, 1 g sodium hydrosulfite (Na2S2O4) was added into the beaker and soaked the roots at room temperature (20–25 °C) until they turned completely white. Then, the extract liquid was transferred into a 50ml volumetric flask. The rice roots were washed in deionized water for three times and then transferred this cleaning fluid into the 50-ml volumetric flask. After filtering the extract liquid through a 0.45-μm filter membrane, plasma power spectral (ICP-OES) methods such as inductive coupling to measure the concentrations of Fe and REEs of La and Nd were used. The extracted rice roots and shoots were washed using deionized water and then were dried. Then, the plants were placed into a 50 °C drying oven, dried them to constant weight, and ground them using a stainless steel grinder. A 0.2000 ± 0.0001 g sample of shoot and a 0.1000 ± 0.0001 g sample of root were placed into a 50ml centrifuge tube. Each sample was replicated four times. A total of 5 ml pure HNO3, was added and the samples were soaked overnight, and allowed to dissolve in a microwave-accelerated reaction system. After dissolution, the solution in the centrifuge tube was transferred into a 50-ml volumetric flask, diluted the sample with ultrapure water to 50 ml, and shook thoroughly. Then the solution was filtered with a 0.45-μm filter membrane and collected the supernatant. ICP-OES was used to measure the concentrations of La and Nd, using a national standard sample (Tea GBW10016) for quality control.
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Table 3 The correlation coefficients among La concentrations in solution, iron plaque contents on root surface and La concentrations in root surface iron plaque.
Solution-La RSIP RSIP-La
Solution-La
RSIP
RSIP-La
1 −0.963 0.874
1 −0.710
1
Note: Solution-La: La concentrations in solution, RSIP: root surface iron plaque, RSIP-La: La concentrations in root surface iron plaque.
on the root surface under both La and Nd treatment is inferior to that formed in the CK group. As the concentrations of La and Nd increase, the amount of iron plaque on rice is decreased. These results show that La and Nd pollution stress may inhibit the formation of the rice root surface to a certain degree. The accumulation of La and Nd in iron plaque on the root surface increased as the concentration of La and Nd in the nutrient solution increased and the amount of iron plaque decreased. The coefficients are shown in Tables 3 and 4. 3.2. La and Nd content in rice shoots and root systems It can be seen in Figs. 1 and 2 that, under 0.1, 0.5 and 1.0 mmol·L−1 La and Nd treatments, the REE content of the shoots and root systems in the induced group was significantly lower than that in the non-induced group. Fig. 1 shows that when La solution concentrations were 0.1, 0.5, and 1.0 mmol·L− 1, La content in the rice root system in the induced group was reduced by 17.1%, 37.4% and 31.2%, respectively, and La content in shoots was reduced by 43.9%, 60.6% and 27.0%, respectively, as compared to the non-induced group. When Nd solution concentrations were 0.1, 0.5 and 1.0 mmol·L−1, Nd content in the rice root system in the induced group was reduced by 21.0%, 31.6% and 31.7%, respectively, and Nd content in shoots was reduced by 47.5%, 22.7% and 28.3%, respectively, when compared to the non-induced group. These results suggest that iron plaque on the root surface inhibits absorption and translocation of La and Nd efficiently. These effects are influenced by several factors, including the type and concentration of REEs in the nutrient solution, the amount of iron plaque, and the amount of REEs absorbed by the iron plaque. The mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated. Under La and Nd treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the La and Nd content in the root system was significantly higher than that in the shoot for both the induced and non-induced groups. The REE content of the root system was positively correlated with the concentration of rare earth in the nutrient solution. In other words, the La and Nd content of the root system rose with the increase of nutrient solution concentrations. The REE content in shoots was positively correlated with nutrient solution and root system concentrations.
2.4. Data analysis The transfer coefficient (TF) indicates the ability of the iron plaque and the root system to transfer La to shoots and is calculated via: TFx ¼ Cshoot‐REE =Cx−REE In this formula, x stands for DCB, root. REE stands for La or Nd. TFx is the transfer coefficient for La or Nd in the DCB or root. Cshoot-REE stands for the concentration of La or Nd in the shoot. Cx-REE stands for the concentration of La or Nd in the DCB or root, respectively. The enrichment coefficient (BAF) indicates the ability of rice to concentrate La and Nd and is calculated via: BAFy ¼ Cy‐REE =Csolution−REE In this formula, y stands for DCB, root, or shoot. BAFy is the enrichment coefficient for La or Nd in the DCB, root, or shoot, as indicated by other subscripts. Cy-REE stands for the concentration of La or Nd in the DCB, root, or shoot. Csolution-REE stands for the concentration of La or Nd in the nutrient solution. SPSS 19.0 and Excel 2007 were used to analyze the experimental data. 3. Results and analysis
3.3. Translocation of La and Nd from the iron plaque and the root system to the shoots
3.1. Iron plaque formation on the root surface, and iron plaque La and Nd content
It can be seen in Table 5 that, under La and Nd treatment, the translocation coefficients of rice root systems in both the induced and noninduced groups increased with increasing REE concentration in the treatment solution. Under La treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the translocation coefficient between root
DCB-Fe indicates the amounts of iron plaque on the root surface. The amount and rare earth content of iron plaques under four different La and Nd solution concentrations (0, 0.1, 0.5 and 1.0 mM) are shown in Table 2. It can be seen in Table 1 that the amount of iron plaque formed Table 2 Amount of iron plaque on the root surface and La and Nd contents in the iron plaque of rice. CK
Fe/g·kg−1 REE/mg·kg−1
15.00 ± 1.41d ND
La treatment
Nd treatment
0.1
0.5
1
0.1
0.5
1
14.36 ± 1.02c 148.03 ± 33.73a
14.00 ± 0.70 b 255.93 ± 40.01b
12.52 ± 0.49a 266.42 ± 7.55b
14.27 ± 0.28a 473.56 ± 51.25c
13.58 ± 0.65b 505.87 ± 48.16b
13.08 ± 0.23a 617.32 ± 39.901a
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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Table 4 The correlation coefficients among Nd concentrations in solution, iron plaque contents on root surface and Nd concentrations in root surface iron plaque.
Solution-Nd RSIP RSIP-Nd
Solution-Nd
RSIP
RSIP-Nd
1 −0.988 0.971
1 −0.921
1
Note: Solution-Nd: La concentrations in solution, RSIP: root surface iron plaque, RSIP-Nd: La concentrations in root surface iron plaque.
system and shoots in the non-induced group increased from 0.014 to 0.15 (becoming 10.71 times higher); the coefficient in the induced group increased from 0.008 to 0.159 (becoming 19.88 times higher). Under Nd treatments with concentrations ranging from 0.1 to 1.0 mmol·L−1, the translocation coefficient between root system and shoots in the non-induced group increased from 0.008 to 0.117 (becoming 14.63 times higher); the coefficient in the induced group increased from 0.005 to 0.122 (becoming 24.4 times higher). The translocation coefficients between the iron plaque and shoots were higher than those between the iron plaque and root system, irrespective of the treatment (La or Nd). The type of REE affected the translocation of REEs by the rice root system. Under La treatment, the translocation coefficients of both the iron plaque and the root system were higher than those under Nd treatments of the same concentration. This suggests that the translocation of La from underground plant parts to above-ground parts is easier than translocation of Nd. This may be due to the fact that La is the most reactive metal in the lanthanide series. Fig. 2. The impact of iron plague on the contents of Nd in rice's roots and shoots (n = 4, a, b and A, B stand for significant difference of different treatment in induced group and noninduced group respectively, p b 0.05).
3.4. Enrichment of La and Nd in different parts of the rice plant It can be seen in Table 6 that, for the non-induced group, the enrichment coefficients for the rice root system were higher than those for the shoots under both La and Nd treatments. For the induced group, enrichment coefficients are ranked in the following order: root system N iron plaque N shoots. Under La and Nd treatments, the enrichment coefficients of the root system decreased as the treatment REE concentration increased in both the induced and non-induced groups. The enrichment coefficients of the shoots increased as the treatment REE concentration increased in both induced and non-induced groups. The enrichment coefficients of the iron plaque decreased as the treatment REE concentration increased in the induced group. Under La and Nd treatments of three different concentrations, the enrichment coefficients of the rice root system and shoots were higher in the non-induced group than in the induced group at the same treatment concentration. The iron plaque and root system enrichment coefficients were higher under Nd treatment than under La treatment, while the shoot enrichment coefficients were lower under Nd treatment than under La treatment. This suggests that REE enrichment in rice is affected by the type and concentration of REEs, the amount of iron plaque, and the part of the rice plant in question. 4. Discussion
Fig. 1. The impact of iron plague on the contents of La in rice's roots and shoots (n = 4, a, b and A, B stand for significant difference of different treatment in induced group and noninduced group respectively, p b 0.05).
The cleaning and treatment of sewage by wetland ecosystems is a topic of current research. Waterlogged environments induce aerenchyma in plants, which transfers oxygen from leaves to the root system. Thus, many kinds of wetland plants can release oxygen from their root systems [32–33]. When the growth medium is rich in Fe2 +, the Fe2+ can participate in a chemical reaction with the oxygen released from the root system, forming iron plaque [34–35]: 4Fe2+ + O2 + 10H2O
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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Table 5 Transfer coefficients of iron plague and root system transferring La and Nd to shoots. Iron plague
La Nd
Non-induced group Induced group Non-induced group Induced group
Roots
0.1
0.5
1
0.1
0.5
1
ND 0.126 ± 0.033a ND 0.027 ± 0.007a
ND 0.376 ± 0.078b ND 0.168 ± 0.068b
ND 2.239 ± 0.247c ND 0.830 ± 0.122c
0.014 ± 0.003a 0.008 ± 0.001a 0.008 ± 0.001a 0.005 ± 0.002a
0.054 ± 0.019a 0.034 ± 0.011a 0.021 ± 0.001a 0.024 ± 0.008a
0.150 ± 0.098a 0.159 ± 0.03a 0.117 ± 0.037b 0.122 ± 0.049b
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
= 4Fe(OH)3 + 8H+. The concentration of Fe2+ in the growth medium is one of the factors affecting the formation of iron plaque. If we were to add Fe2 + into the soil or nutrient solution, the redox potential would increase and the reaction shown above would go forward as the root system released oxygen. Thus, the amount of iron plaque on the root surface of wetland plants would increase. This study suggests that iron plaque can be formed when 40 ppm Fe2SO4 is added to the nutrient solution, whereby the roots form an iron film. The formation of iron plaque is also related with the oxidative potential of the root system, the type of rice, the growing period, and the growth environment [36]. Pan et al. [32] found that sediments including rare-earth phosphates, rare-earth sulfates, and rare-earth hydroxides in the medium can attach to the rice root surface and inhibit iron plaque formation to a certain degree. This result is consistent with the conclusions of this study. The iron plaque found on the rice root surface has characteristics similar to iron oxide in the natural environment. It is a kind of ampholytoid, with relatively high specific surface area and –OH functional group content. It can initiate adsorption-desorption, oxidationreduction, and organic-inorganic complexation reactions with metals and other anions and cations [37]. Many researchers have shown that iron plaque increases absorption of nutrient elements including iron, phosphorus, zinc, magnesium, manganese, etc. and heavy metal including Cd, Pb, Sb and As near the root area [23]. As an ampholytoid, iron oxide and its hydrous oxide can adsorb anions in soils and nutrient so2− lutions such as PO3− 4 and CO3 . Anions adsorbed by the oxide can combine with metal cations in the medium. Hansel et al. [38] found that metal carbonates formed by manganese and zinc were attached to root surfaces. Cai et al. found that aluminum formed a phosphate rather than bind with iron oxide, and that this phosphate could be deposited on a root surface with iron plaque [28]. When the growth medium has a high PO3− 4 content, iron oxide and phosphate can form a mononuclear complex which is easily desorbed; when the medium has a relatively low PO3− content, a binuclear complex is formed that is difficult to de4 sorb. Nutrient solutions of 1/3 concentration were used when cultivating rice in pots; the concentration of PO34 − and CO2– 3 was relatively low in these solutions. Nonetheless, phosphate and carbonate compounds were formed with the La and Nd that attached tightly to the iron plaque. The ability of iron plaque to adsorb and deposit La and Nd can affect REE bioavailability, thus affecting the uptake and
translocation of REEs by rice. In this study, the La and Nd content of rice root systems and shoots were significantly lower in the induced group than in the non-induced group. The translocation and enrichment coefficients of the root system were higher for the non-induced group than for the induced group. Iron plaque forms a barrier against REE uptake by plants. The mechanisms governing the effect of iron plaque on La and Nd uptake and transfer in the rice root system are rather complicated and vary with the type and concentration of REEs in the medium. Because La is the most reactive metal in the lanthanide series, and because La and Nd have different numbers of electrons in their 4f orbitals, the iron plaque formed on the root surface and its impact on the uptake and translocation of REEs by rice were different under La and Nd treatments. In both the induced and non-induced groups, the iron plaque and root system translocation coefficients and the shoot enrichment coefficients were higher under La treatment than under a Nd treatment of the same concentration. The iron plaque and root system enrichment coefficients were lower under La treatment than under Nd treatment.
5. Conclusions La and Nd pollution stress can inhibit root surface iron plaque formation in rice to a certain degree. The accumulation of La and Nd in iron plaque on the root surface increased with increasing nutrient solution La and Nd concentrations and decreasing amounts of iron plaque. Iron plaque on the rice root surface inhibited the uptake and translocation of La and Nd. Under La solution concentrations of 0.1, 0.5 and 1.0 mmol·L−1, La content in the rice root system was reduced by 17.1%, 37.4% and 31.2%, respectively, in plants with an induced iron plaque; the La content in shoots was reduced by 43.9%, 60.6% and 27.0%, respectively. Under Nd solution concentrations of 0.1, 0.5 and 1.0 mmol·L− 1, Nd content in the rice root system was reduced by 21.0%, 31.6% and 31.7% respectively, in plants with an induced iron plaque, and the Nd content in shoots was reduced by 47.5%, 22.7% and 28.3%, respectively. Because La is the most reactive metal in the lanthanide series, and because La and Nd have different numbers of electrons in their 4f orbitals, the iron plaque formed on the root surface and its impact on the uptake and translocation of REEs by rice were different under La and Nd treatments.
Table 6 Enrichment coefficients of La and Nd in different parts of rice. Iron plague 0.1 La
Roots 0.5
1
Non-induced group Induced 11.78 ± 2.431ab 4.105 ± 0.581a 2.108 ± 0.050a group Nd Non-induced group Induced 32.84 ± 7.684b 7.01 ± 1.194a 4.27 ± 0.347a group
Shoots
0.1
0.5
1
0.1
194.8 ± 22.143f
65.83 ± 9.951d
39.16 ± 4.622c
2.778 ± 0.839a 3.562 ± 1.220a 5.866 ± 2.736a
0.5
1
161.4 ± 40.586d
41.2 ± 13.512c
29.6 ± 3.801bc
1.347 ± 0.362a 1.402 ± 0.421a 4.284 ± 0.463a
203.782 ± 113.351a 161.567 ± 57.493b
72.695 ± 42.175 ± 9.620c 1.664 ± 0.223a 1.526 ± 0.455a 4.953 ± 1.262b 26.879b 49.69 ± 14.612a 29.98 ± 3.164a 0.874 ± 0.263b 1.18 ± 0.397a 3.55 ± 0.865a
Note: The data in the table is mean value (n = 4). Different letters stand for significant difference (p b 0.05). ND stands for ‘not detected’.
Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002
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Z. Hu et al. / Acta Ecologica Sinica xxx (2017) xxx–xxx
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Please cite this article as: Z. Hu, et al., The impact of iron plaque on La and Nd uptake and translocation in rice (Oryza sativa L.), Acta Ecologica Sinica (2017), https://doi.org/10.1016/j.chnaes.2017.11.002