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Phosphorus Enhances Cr(VI) Uptake and Accumulation in Leersia hexandra Swartz

  • Chan-Cui Wu
  • Jie Liu
  • Xue-Hong Zhang
  • Shi-Guang Wei
Article

Abstract

The effects of P supplementation on chromium(VI) uptake by Leersia hexandra Swartz were studied using pot-culture experiment. P-deficiency and zero-P addition controls were included. The Cr(VI) uptake followed Michaelis–Menten kinetics. Compare with the control, the P-supply decreased the Michaelis constant (Km) by 16.9% and the P-deficiency decreased the maximum uptake velocity (Vmax) by 18%, which indicated no inhibition and competition between P and Cr(VI) uptake by L. hexandra. Moreover, there were a synergistic action between P and Cr(VI) suggests that Cr(VI) uptake by the roots of L. hexandra may be an active process. The bioconcentration factor (BCF) and the transport factor (TF′) increased with the increase in P supply. The highest BCF was 3.6-folds higher than the control, indicating that the additional P contribute to a higher ability of L. hexandra transporting Cr from root to the aboveground parts.

Keywords

Leersia hexandra Swartz Chromium (Cr) Phosphate (P) Cr hyperaccumulators Phytoremediation 

Environmental contamination with chromium (Cr) is a serious concern in recent years, because global discharge of Cr exceeds than those of lead (Pb), mercury (Hg), and cadmium (Cd), which adversely affects the mineral uptake and metabolic processes in plants when present in excess (UdDin et al. 2015). Naturally, Cr exists in two oxidation states, the trivalent form [Cr(III)] and hexavalent form [Cr(VI)] that differs in terms of mobility, bioavailability and toxicity (Panda and Choudhury 2005). Cr(III) is a micronutrient in human and animal physiology with relatively low toxicity (Economou-Eliopoulos et al. 2011; Mills et al. 2011). However, Cr(VI) is highly carcinogenic and mutagenic to living organisms (Chrysochoou et al. 2016). It usually occurs in association with oxygen as chromate (CrO42−) or dichromate (Cr2O72−) oxyanions (Saha et al. 2011). The U.S. Environmental Protection Agency (EPA) has classified Cr(VI) as a Group ‘A’ human carcinogen and is one of the main pollutants. The maximum allowable levels of total Cr in agricultural soils of Canada, Austria, Poland, and China is 64, 100, 150, and 250 mg kg−1, respectively (Shahid et al. 2017). Therefore, removing Cr(VI) from soil is important for environmental and health protection (Liu et al. 2015).

Phytoremediation is an effective method to remove Cr(VI) from soil because of its success to select plant species for not only tolerating high levels of the metals but also accumulating high metal concentrations in shoots (Redondo-Gómez et al. 2011). In previous work, we reported that Leersia hexandra Swartz is a Cr hyperaccumulator and has great potential to remediate Cr-contaminated soil (Zhang et al. 2007). To increase the phytoremediation efficiency of Cr contamination, an insight into the mechanism of Cr uptake and accumulation in L. hexandra should be gained. Although the mechanism of Cr(III) uptake in L. hexandra was studied, Cr(VI) uptake mechanism still remained unclear (Liu et al. 2011).

The chromate and dichromate compounds conform with the oxygen tetrahedral structures, similar to structures that form with some mineral nutrients such as phosphate and sulfate (Shupack 1991), and it has been shown that phosphate competing with Cr(VI) for uptake (Cervantes et al. 2001). López-Bucio et al. (2014) reported that Cr(VI) uptake is decreased by P in A. thaliana plants. Previous research has shown that by supplementation of inorganic nutrients in combination (ammonium, phosphate and potassium), the uptake and translocation of some metals (As and Pb) can be improved but not for other metals (Cu, Zn and Cd) in sorghum and sunflower plants (Marchiol et al. 2007). Oliveira et al. (2015) working with P. vittata in presence of P showed that P inhibited Cr(VI) uptake but helped its translocation. However, little is known about the effects of P on Cr(VI) uptake and translocation in a Cr-hyperaccumulator. It is essential to investigate the relationship between the uptake of P and Cr in L. hexandra.

The overall objective of this study was to evaluate the impacts of P on uptake and translocation of Cr(VI) in L. hexandra, which were exposed to Cr(VI) and P at different concentrations in hydroponic solutions. Our objectives were to: (1) study the effects of P on Cr(VI) uptake of L. hexandra by Michaelis–Menten kinetics, (2) investigate the effects of P on Cr(VI) translocation in L. hexandra, and (3) analyze the effects of Cr with additional P on the growth of the plant. Information obtained from this study should provide insight for improving the efficiency of remediate Cr-contaminated soil.

Materials and Methods

Seedlings of L. hexandra were collected from the wetland of Yanshan District in Guilin where Cr concentration in soil is 8–14 mg kg−1. Cr concentrations in seedling of L. hexandra grown in this site were not detectable. The seedlings were washed thoroughly (at least three times) with redistilled water and placed in the round plastic pots filled with 1.5 L 25% Hoagland’s nutrient solution. The nutrient solution renewed every 3 days with the volume being restored to its original level. Plants were grown in the pots for 20 days in a controlled environment growth cabinet (14 h photoperiod, 25 °C day/18 °C night, relative humidity 70%–75%, and a light intensity of 300 µmol (m2s)−1).

Two steps of study were performed to investigate the effect of P on the uptake of Cr(VI) by L. hexandra. In the first step, the plants were divided into three groups: (1) control (cultured with normal nutrient solution); (2) P deficiency (cultured without P supply); (3) P supply (cultured with the nutrient solution adding 5 mmol L−1 H2PO4). After 48 h of culture according to the first step, the K2Cr2O7 was added into the all groups in six levels: 0, 10, 20, 30, 40, and 50 µmol L−1. Four hours after treatment, the plants were harvested. The second step was performed by culturing the plant with the nutrient solution adding H2PO4 in eight levels: 0, 5, 10, 20, 40, 60, 80, and 100 mmol L−1. After 48 h, 100 µmol L−1 K2Cr2O7 was added into the every plant. Fifteen days after treatment, the plants were harvested. Each treatment was replicated three times.

Before harvesting, the plants were washed thoroughly with running tap water and rinsed in ultrasonic cleaner with 10 mmol L−1 EDTA solution three times (10 min each time), then cleaned with ultra pure water three times to remove any ions attached to surfaces of the plant. At harvest, root, stem and leaves were cut and put in paper bags respectively. After oven-dried at 65 °C for 72 h, the dried samples were weighed immediately upon removal from a desiccator. Oven-dried plant samples were digested in a microwave digester (ETHOS A, Milestone, Italy) using USEPA Method 3050B (de Oliveira et al. 2014). The microwave program was listed in Table 1. The digested samples were washed into 10 ml comparison tubes which were made up to volume (10 mL) using Ultra pure water.

Table 1

The microwave program of digesting plant samples

Step

Time (min)

Temperature (°C)

Microwave power

1

4

85

Up to 1500 W

2

9

145

Up to 1500 W

3

4

200

Up to 1500 W

4

14

200

Up to 1500 W

Cr concentrations in the digested samples were determined using atomic absorption spectrophotometer (AA-6300, Shimadzu, Japan). Working standard solutions for analysis of the elements were prepared with serial dilutions of stock standard solutions Cr (GBW(E)080257). P concentrations in the digested samples were determined using a modified molybdenum blue method (Carvalho et al. 1998) with a spectrophotometer (UV-2550, Shimadzu, Japan). For quality control, certified reference spinach (GBW10015) was also analyzed in triplicate using the same method in each batch of analyses. The analyses results were only accepted when the measured standard concentrations were within 95%–105% of the certified value.

The bioconcentration factor indicates the efficiency of a plant in accumulating the metal from the surrounding environment, usually the soil, into its tissues (Ladislas et al. 2012). In this case, the surrounding environment was a nutrient solution, and the factor was calculated as follows:
$${\text{Bioconcentration}}\,{\text{factor}}\,\left( {BCF} \right)\,=\,\frac{{{C_{plant}}}}{{{C_{nutrient\,solution}}}}$$
(1)
where Cplant is the concentration of the Cr in the dried plant tissue and Cnutrient solution is the concentration of the same metal in the water solution.
To determine the efficiency of the plant in the transport of Cr from the roots to the aboveground parts, the transport factor was calculated as follows (Wu et al. 2010):
$$Transport{\text{ }}factor{\text{ }}\left( {TF^{\prime}} \right)=\frac{{Mthe{\text{ }}aboveground{\text{ }}parts}}{{Mroot}}$$
(2)
where Mthe aboveground parts is the Cr accumulation in the aboveground parts and Mroot is the Cr accumulation in roots.

The data presented in this paper are the average of three independent replicates ± standard error of means (SD). Each experiment was repeated at least three times. Analysis of variance (ANOVA) was performed on all data sets, and least significant difference (LSD) was used to compare treatments. Graphical work was performed using Origin Pro 8.

Results and Discussion

The effect of P on the uptake of Cr(VI) by L. hexandra was investigated in the presence and absence of H2PO4. Cr uptake rate were increase as increasing of the Cr(VI) concentration. The Cr uptake rate in the P-supplied plants was higher than control, whereas, it in the P-deficient plants was lower than control (Fig. 1). At 100 µmol L−1 Cr(VI) treatment, Cr uptake increased by 23.9% in the P-supplied plants, whereas, it decreased by 14.4% in the P-deficient plants. The uptake of Cr(VI) in the plants treated with or without P could be fitted satisfactorily with the Michaelis–Menten kinetic equation (Table 2). It is known that the Michaelis–Menten constant (Km) reflects affinity between substrate and carrier (Yu et al. 2018). In this work, the Km values were 76.27, 91.76 and 93.04 µmol L−1 for P-supplied, control and P-deficient plants, indicating the affinity of uptake sites on root cell membrane with substrates was increased in P-supplied plants. Compared with the control plants, P deficiency decreased the maximum initial velocity (Vmax), while P-supply increased Vmax slightly. It suggested that P-supply cause the higher rates of Cr(VI) uptake by L. hexandra. Considering the above, we believe that it is no antagonism between P and Cr in L. hexandra, instead of a synergistic effect. Therefore, different H2PO4 concentrations added in nutrient solution were tested to further confirmed that P enhanced Cr(VI) uptake in L. hexandra.

Fig. 1

Concentration-dependent kinetics (a) and Lineweaver–Burk plot of Cr(VI) uptake (b) by L. hexandra in the presence and absence of H2PO4. Where V is the rate of Cr(VI) uptake, and S is the Cr concentration supplied

Table 2

Parameters of Michaelis–Menten kinetic equation fitted to the data on Cr(VI) uptake of L. hexandra

Treatment

Vmax (µmol g−1 DW h−1)

Km (µmol L−1)

R2

P Supply

0.969

76.27

0.99

Control

0.903

91.76

0.99

P deficiency

0.740

93.04

0.99

When P supplementation increased from 0 to 80 mmol L−1, the Cr concentration both in aboveground part (leaves and stems) and belowground part (root) were also increased (Fig. 2). The highest Cr concentration was observed in P supplementation of 80 mmol L−1, and Cr concentration increased by 6.16- and 3.62-fold compared to control in the aboveground part and root, respectively. It is obvious that Cr concentration was influenced to a greater extent in aboveground part than in belowground part with P supplementation. These results indicate that P additions increase Cr(VI) uptake, especially in aboveground part. This is opposite to the report that the presence of P inhibited Cr uptake by Raphanus sativus L (Sayantan and Shardendu 2013). Some researchers speculated that Cr(VI) is probably taken up by plants via P transporters (Castro et al. 2007; Oliveira et al. 2015) while others hold negative attitude towards it. Lee and Wang (2001) reported that Cr accumulation in Ulva fasciata increased significantly with increasing P concentration. There was a strong positive correlation of Cr uptake by plants T. angustata L. with phosphorus concentration (Bose et al. 2008). Sinha et al. (2007) working with the plants of fenugreek grown in soil with tannery sludge indicated that Cr showed significant positive correlation with available phosphorus. The above views are in agreement with the result of this study. The different result implied that the influences of P on Cr accumulation were highly plant-specific.

Fig. 2

Cr concentration of L. hexandra in H2PO4 supplementation

With the supplementation of H2PO4 increased, the concentrations of P both in the aboveground part and the root of L. hexandra also increase (Fig. 3). Moreover, there was a significant positive correlation between the Cr and P uptake in aboveground and belowground of L. hexandra, with all levels of P supplementation (Fig. 4). The simulation equations were y = 0.8455x − 780.87 (R2 = 0.9621) and y = 2.5496x – 816.81 (R2 = 0.8966), respectively. The result indicated once more that it is no competitive relationship between P and Cr uptake in L. hexandra, and demonstrated that H2PO4 enhance Cr(VI) uptake in L. hexandra.

Fig. 3

P concentration of L. hexandra in H2PO4 supplementation

Fig. 4

A correlation analysis of P uptake and Cr uptake in aboveground and belowground of L. hexandra

Bioconcentration factor (BCF) index is used to evaluate metal accumulation efficiency in plants. There were significantly differences among the BCF with the different supplementations of H2PO4 (Table 3). An increased tendency was observed in BCF with increasing of H2PO4 concentration from 5 to 80 mmol L−1. The BCF at 80 mmol L−1 H2PO4 reached as high as 248.118, which is 3.6 fold than the control. The BCF of Cr in this study is considerably higher than that reported for the Cr-hyperaccumulator S. argentinensis with a 6.7 BCF (Redondo-Gómez et al. 2011) and maize plants with the supplement of P was about 11 (Martinez-Trujillo and Carreon-Abud 2015). The result indicates that phosphate provides a great help for L. hexandra to take up Cr(VI) from nutrient solution.

Table 3

Bioconcentration factor (BCF) and transport factor (TF′) of L. hexandra (means ± SD) in respond to Cr(VI) in H2PO4 supplementation

P supplementation (mmol L−1)

BCF

TF′

0

68.498 ± 7.148e

0.6742 ± 0.2972

5

108.72 ± 22.74d

1.0908 ± 0.5583

10

121.64 ± 17.28cd

1.2384 ± 0.8117

20

142.97 ± 22.00c

1.1072 ± 0.3249

40

204.86 ± 12.27b

1.1122 ± 0.1975

60

208.16 ± 22.16b

1.3133 ± 0.2854

80

248.12 ± 18.55a

1.1432 ± 0.2421

100

226.17 ± 11.01ab

1.1148 ± 0.3690

Different letters behind the figures indicated significant difference at P < 0.05

Another factor to determine the efficiency of the plant in the translocation of Cr from the roots to the stems is transport factor (TF′). At the P concentrations tested, the value of TF′ are all higher than the control, although there were no significant differences among them (Table 3). With H2PO4 supplement, the TF′ values of L. hexandra were higher than the critical value (1.0), which indicates that L. hexandra displays a higher ability to transfer Cr from roots to stems and leaves with supplementation of H2PO4. The results of BCF and TF′ show that the supplementation of H2PO4 is beneficial both to take up Cr(VI) from nutrient solution and to transport Cr from root to stem.

Biomass is one of important factors to determine the growth and development in plants. After 15 days experiment, it was no significant difference on biomass with 100 µmol L− 1 K2Cr2O7 and increasing of H2PO4 supplementation (Table 4). It indicates that at the P concentrations tested, PO43−-supply have no negative effects on growth of L. hexandra. Cr accumulation, defined as the total quantity of Cr in plant tissues, increased rapidly in aboveground of L. hexandra as the P addition increased from 5 to 80 mmol L−1, treated with Cr(VI) (Fig. 5). At P addition of 80 mmol L−1, the Cr contents both in aboveground and belowground reached maximum value. The value in aboveground was 8.37-fold higher than those in the control. In the control plants, the Cr content in the belowground part was higher than those in the aboveground parts. However, when P supplementation > 5 mmol L−1, the Cr content in the belowground part was lower than those in the aboveground parts. Based on such information,it was found that the additional P enhanced Cr(VI) accumulation as well as helped L. hexandra to alleviate Cr toxicity.

Table 4

Plant biomass of L. hexandra (means ± SD) in H2PO4supplementation

P supplementation (mmol L−1)

Stems (g pot−1)

Leaves (g pot−1)

Roots (g pot−1)

0

5.4860 ± 0.4856

1.1620 ± 0.5504

2.1473 ± 0.5554

5

5.8243 ± 0.5138

1.4530 ± 0.1702

2.2387 ± 0.9719

10

5.9543 ± 1.7773

3.6773 ± 1.5376

2.5747 ± 1.0004

20

5.5947 ± 0.6962

3.5757 ± 1.0269

2.3563 ± 0.6726

40

5.7007 ± 0.8274

3.1593 ± 0.8744

2.2503 ± 0.3811

60

6.1287 ± 0.9585

1.3723 ± 0.3105

2.1727 ± 0.9521

80

6.9560 ± 1.1266

3.0647 ± 0.5242

3.0213 ± 1.1577

100

6.0943 ± 0.7282

2.6350 ± 0.6241

2.8403 ± 1.0478

Fig. 5

The effect of H2PO4 supplementation on total content of Cr(VI) taking up by L. hexandra

Phosphorus is important in metabolic energy transfer (for example, ATP) (Touchette and Burkholder 2000). The energy required for biosynthesis and ion active uptake is mainly supplied by ATP. That is to say, increasing phosphorus supply is equivalent to increasing metabolic energy. Uptake of Cr(VI) by roots of L. hexandra was significantly increased by high phosphorus levels, which demonstrated that uptake of Cr(VI) by roots of L. hexandra depended on metabolic energy. On the other hand, an active uptake of Cr(VI) has been reported by previous research (Zayed and Terry 2003). In this study, we also demonstrated that an active uptake of Cr(VI) occur in L. hexandra. The metabolic energy is required in an active process, which could explain why phosphate supplementation can increase the uptake and translocation of Cr(VI) in L. hexandra.

The hyperaccumulators generally tend to take up and translocate heavy metals into their aboveground parts. The stronger ability to uptake and transport heavy metals, the higher phytoremediation efficiency the hyperaccumulators perform. In other words, the application of P fertilizers can contribute to improve the efficiency of Cr removal from Cr-contaminated soil by L. hexandra.

The results from this study showed that P additions increase uptake and translocation of Cr(VI) by hyperaccumulator plant L. hexandra. It suggests that uptake of Cr(VI) by roots of L. hexandra is an active process, which depends on metabolic energy increasing with H2PO4 supplementation. The results also showed that it is no antagonism between P and Cr in L. hexandra, instead of a synergistic effect. Moreover, the greatly high of BCF and acceptable TF′ in this study indicated that supplementation of H2PO4 can improve the abilities of L. hexandra to accumulate and transfer Cr. According to the results, the application of P fertilizers can contribute to improve the efficiency of Cr removal from Cr-contaminated soil by L. hexandra.

Notes

Acknowledgements

The authors thank the financial supports from the National Natural Science Foundation of China (41471270, 31460155) and Guangxi Science and Technology Major Project (Gui Ke AA17204047).

References

  1. Bose S, Vedamati J, Rai V, Ramanathan AL, Bose S, Vedamati J, Rai V (2008) Metal uptake and transport by Tyaha angustata L. grown on metal contaminated waste amended soil: an implication of phytoremediation. Geoderma 145:136–142CrossRefGoogle Scholar
  2. Carvalho LHM, De Koe T, Tavares PB (1998) An improved molybdenum blue method for simultaneous determination of inorganic phosphate and arsenate. Ecotoxicol Environ Restor 1:13–19Google Scholar
  3. Castro RO, Trujillo MM, Bucio JL, Dubrovsky CC,J (2007) Effects of dichromate on growth and root system architecture of Arabidopsis thaliana seedlings. Plant Sci 172:684–691CrossRefGoogle Scholar
  4. Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347CrossRefGoogle Scholar
  5. Chrysochoou M, Theologou E, Bompoti N, Dermatas D, Panagiotakis I (2016) Occurrence, Origin and Transformation Processes of Geogenic Chromium in Soils and Sediments. Curr Pollution Rep 2:224–235CrossRefGoogle Scholar
  6. de Oliveira LM, Lessl JT, Gress J, Tisarum R, Guilherme LRG, Ma LQ (2015) Chromate and phosphate inhibited each other’s uptake and translocation in arsenic hyperaccumulator Pteris vittata L. Environ Pollut 197:240–246CrossRefGoogle Scholar
  7. de Oliveira LM, Ma LQ, Santos JAG, Guilherme LRG, Lessl JT (2014) Effects of arsenate, chromate, and sulfate on arsenic and chromium uptake and translocation by arsenic hyperaccumulator Pteris vittata L. Environ Pollut 184:187–192CrossRefGoogle Scholar
  8. Economou-Eliopoulos M, Megremi I, Vasilatos C (2011) Factors controlling the heterogeneous distribution of Cr(VI) in soil, plants and groundwater: Evidence from the Assopos basin. Greece Chemie der Erde 71:39–52CrossRefGoogle Scholar
  9. Ladislas S, El-Mufleh A, Gérente C, Chazarenc F, Andrès Y, Béchet B (2012) Potential of aquatic macrophytes as bioindicators of heavy metal pollution in urban stormwater runoff. Water Air Soil Pollut 223:877–888CrossRefGoogle Scholar
  10. Lee W-Y, Wang W-X (2001) Metal accumulation in the green macroalga Ulva fasciata: effects of nitrate, ammonium and phosphate. Sci Total Environ 278:11–22CrossRefGoogle Scholar
  11. Liu J, Duan C-Q, Zhang X-H, Zhu Y-N, Hu C (2011) Characteristics of chromium(III) uptake in hyperaccumulator Leersia hexandra Swartz. Environ Exp Bot 74:122–126CrossRefGoogle Scholar
  12. Liu J, Zhang X-H, You S-H, Wu Q-X, Zhou K-N (2015) Function of Leersia hexandra Swartz in constructed wetlands for Cr(VI) decontamination: A comparative study of planted and unplanted mesocosms. Ecol Eng 81:70–75CrossRefGoogle Scholar
  13. López-Bucio JS, Dubrovsky JG, Raya-González J, Ugartechea-Chirino Y, López-Bucio J, de Luna-Valdez LA, Ramos-Vega M, León P, Guevara-García AA, A.A (2014) Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J Exp Bot 65:169–183CrossRefGoogle Scholar
  14. Marchiol L, Fellet G, Perosa D, Zerbi G (2007) Removal of trace metals by Sorghum bicolor and Helianthus annus in a site polluted by industrial wastes: a field experience. Plant Physiol Biochem 45:379–387CrossRefGoogle Scholar
  15. Martínez-Trujillo M, Carreón-Abud Y (2015) Effect of mineral nutrients on the uptake of Cr(VI) by maize plants. New Biotechnol 32:396–402CrossRefGoogle Scholar
  16. Mills CT, Morrison JM, Goldhaber MB, Ellefsen KJ (2011) Chromium(VI) generation in vadose zone soils and alluvial sediments of the southwestern Sacramento Valley, California: A potential source of geogenic Cr(VI) to groundwater. Appl Geochem 26:1488–1501CrossRefGoogle Scholar
  17. Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol 17:95–102CrossRefGoogle Scholar
  18. Redondo-Gómez S, Mateos-Naranjo E, Vecino-Bueno I, Feldman SR (2011) Accumulation and tolerance characteristics of chromium in a cordgrass Cr-hyperaccumulator, Spartina argentinensis. J Hazard Mater 185:862–869CrossRefGoogle Scholar
  19. Saha R, Nandi R, Saha B (2011) Sources and toxicity of hexavalent chromium. J Coord Chem 64:1782–1806CrossRefGoogle Scholar
  20. Sayantan D, Shardendu (2013) Amendment in phosphorus levels moderate the chromium toxicity in Raphanus sativus L. as assayed by antioxidant enzymes activities. Ecotoxicol Environ Saf 95:161–170CrossRefGoogle Scholar
  21. Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533CrossRefGoogle Scholar
  22. Shupack SI (1991) The chemistry of chromium and some resulting analytical problems. Environ Health Perspect 92:7–11CrossRefGoogle Scholar
  23. Sinha S, Gupta AK, Bhatt K (2007) Uptake and translocation of metals in fenugreek grown on soil amended with tannery sludge: Involvement of antioxidants. Ecotoxicol Environ Saf 67:267–277CrossRefGoogle Scholar
  24. Touchette BW, Burkholder JAM (2000) Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Mar Biol Ecol 250:133–167CrossRefGoogle Scholar
  25. UdDin I, Bano A, Masood S (2015) Chromium toxicity tolerance of Solanum nigrum L. and Parthenium hysterophorus L. plants with reference to ion pattern, antioxidation activity and root exudation. Ecotoxicol Environ Saf 113:271–278CrossRefGoogle Scholar
  26. Wu F, Yang W, Zhang J, Zhou L (2010) Cadmium accumulation and growth responses of a poplar (Populus deltoids × Populus nigra) in cadmium contaminated purple soil and alluvial soil. J Hazard Mater 177:268–273CrossRefGoogle Scholar
  27. Yu X-Z, Feng Y-X, Liang Y-P (2018) Kinetics of phyto-accumulation of hexavalent and trivalent chromium in rice seedlings. Int Biodeterior Biodegrad 128:72–77CrossRefGoogle Scholar
  28. Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156CrossRefGoogle Scholar
  29. Zhang X-H, Liu J, Huang H-T, Chen J, Zhu Y-N, Wang D-Q (2007) Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere 67:1138–1143CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Chan-Cui Wu
    • 1
    • 2
  • Jie Liu
    • 3
  • Xue-Hong Zhang
    • 1
  • Shi-Guang Wei
    • 1
  1. 1.School of Life and Environmental SciencesGuilin University of Electronic TechnologyGuilinPeople’s Republic of China
  2. 2.Light industry and Food Engineering CollegeGuangxi UniversityNanningPeople’s Republic of China
  3. 3.College of Environmental Science and EngineeringGuilin University of TechnologyGuilinPeople’s Republic of China

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