- Email: [email protected]
Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz
Chemosphere 67 (2007) 1138–1143 www.elsevier.com/locate/chemosphere
Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz Xue-Hong Zhang a,1, Jie Liu a,b,*,1, Hai-Tao Huang a, Jun Chen a, Yi-Nian Zhu a, Dun-Qiu Wang a a
Department of Resources and Environmental Engineering, Guilin University of Technology, Jiangan Road 12#, Guilin, Guangxi 541004, PR China b School of Life Sciences, Yunnan University, Kunming 650091, PR China Received 13 July 2006; received in revised form 8 November 2006; accepted 10 November 2006 Available online 17 January 2007
Abstract Leersia hexandra Swartz (Gramineae), which occurs in Southern China, has been found to be a new chromium hyperaccumulator by means of field survey and pot-culture experiment. The field survey showed that this species had an extraordinary accumulation capacity for chromium. The maximum Cr concentration in the dry leaf matter was 2978 mg kg 1 on the side of a pond near an electroplating factory. The average concentration of chromium in the leaves was 18.86 times as that in the pond sediment, and 297.41 times as that in the pond water. Under conditions of the nutrient solution culture, it was found that L. hexandra had a high tolerance and accumulation capacity to Cr(III) and Cr(VI). Under 60 mg l 1 Cr(III) and 10 mg l 1 Cr(VI) treatment, there was no significant decrease of biomass in the leaves of L. hexandra (p > 0.05). The highest bioaccumulation coefficients of the leaves for Cr(III) and Cr(VI) were 486.8 and 72.1, respectively. However, L. hexandra had a higher accumulation capacity for Cr(III) than for Cr(VI). At the Cr(III) concentration of 10 mg l 1 in the culture solution, the concentration of chromium in leaves was 4868 mg kg 1, while at the same Cr(VI) concentration, the concentration of chromium in leaves was only 597 mg kg 1. These results confirmed that L. hexandra is a chromium hyperaccumulator which grows rapidly with a great tolerance to Cr and broad ecological amplitude. This species could provide a new plant resource that explores the mechanism of Cr hyperaccumulation, and has potential for usage in the phytoremediation of Cr-contaminated soil and water. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Hyperaccumulator; Leersia hexandra; Cr; Phytoremediation
1. Introduction Chromium is an essential trace element in metabolism of human beings and animals (Shrivastava et al., 2002). Low concentration of Cr can enhance growth of plants. However, excess Cr is highly toxic to animals and plants and may induce cancer and teratism (Shanker et al., 2005). Cr and its compounds originate from widespread use of this * Corresponding author. Address: Department of Resources and Environmental Engineering, Guilin University of Technology, Jiangan Road 12#, Guilin, Guangxi 541004, PR China. Tel.: +86 773 5897016; fax: +86 773 5897019. E-mail address: [email protected] (J. Liu). 1 These authors contributed equally to this work.
0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.11.014
metal in various industries such as metallurgical (steel, ferro- and nonferrous alloys), refractories (chrome and chrome–magnesite), and chemical (pigments, electroplating, tanning and other) (Zhang et al., 2004). These anthropogenic activities have led to the widespread contamination that Cr shows in the environment (Kotas and Stasicka, 2000). Although there are various other valence states which are unstable and shortlived in biological systems, the stable forms of Cr are the trivalent Cr(III) and the hexavalent Cr(VI) species. At present, Cr(VI) was considered as an important controlled contaminant by most countries of the world (Zayed and Terry, 2003). However, the effective but inexpensive means of remediating chromium pollution is still not found. Phytoremediation is a potential way to
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
solve the problem of chromium pollution using plants. It is attracting interest and attention from governments and enterprises as a potentially cost-effective, engineeringeconomical and environmentally-friendly green technique (Raskin et al., 1997; Pulford and Watson, 2003). The premise of this method is to find out the hyperaccumulator which has a great ability to accumulate the heavy metal. Some recent work in China has been devoted to hyperaccumulation of zinc (Yang et al., 2002), arsenic (Wei et al., 2002; Chen et al., 2003), manganese (Xue et al., 2004), cadmium (Liu et al., 2004; Wei et al., 2005). According to the criterion of concentrating >1000 mg kg 1 Cr in dry leaf tissue, suggested by Baker and Brooks (1989), only about two species could be qualified as chromium hyperaccumulators (Reeves and Baker, 2000), i.e., Dicoma niccolifera Wild Wild (1974) and Sutera fodina Wild (Baker and Brooks, 1989) in Zimbabwe, of which the maximum Cr concentrations in the dry leaves are 1500 mg kg 1 and 2400 mg kg 1, respectively. Leersia hexandra (Gramineae), a perennial herb, widely distributed in southern China, and mostly grown in swamps, paddyfields or riversides. This species was found on the side of a pond near an electroplating factory in Guangxi, China and possibly had a great accumulation capacity for chromium (Zhang et al., 2005). In the present work, field surveys have been further carried out in this Cr contaminated area. Plant, water, and sediment samples have been collected and analyzed for Cr. In order to confirm the ability of L. hexandra to concentrate chromium, more detailed experiments have been also made in non-contaminated area under controlled conditions.
1139
Fig. 1. Sketch map of the sampling locations. (a) Latitude and longitude of the electroplating factory.
The survey was conducted around a pond near an electroplating factory (E 110.38°, N 24.51°) located in Guilin (in North of Guangxi Province), China. The electroplating factory was put into production in 1996, and discharged wastewater that primarily contained Cr, Cu and Ni, etc (Huang et al., 2003). After a chemical treatment, the wastewater was drained into a pond (about 40 000 m2) near the factory, and then spilled into the Huangzhai River. As a result, Cr concentration in the sediment and water of the pond was considerably elevated. Abundant L. hexandra grew on the side of the pond. In October 2004, a detailed investigation on L. hexandra was conducted. Plant, water, and sediment samples were collected and analyzed for Cr concentration. Sampling locations are shown in Fig. 1. Each L. hexandra sample includes 15–25 individual plants. The sediment samples were composite mixtures of sediments from the rhizosphere of each plant.
in the tissue of L. hexandra grown in this site were not detectable. The seedlings were washed with redistilled water for three times and placed in 15 cm diameter round plastic pots filled with three liters half strength Hoagland’s nutrient solution in a greenhouse (14 h photoperiod; 25 °C day/ 18 °C night, relative humidity 70–75%). After 15 d, Cr treatment was conducted. Cr(III) (as CrCl3) solution was added to the pots in six levels: 0, 5, 10, 20, 40, 60 mg l 1. Cr(VI) (as K2Cr2O7) solution was added in six levels: 0, 5, 10, 15, 20, 30 mg l 1. Each treatment had three replicates, 25–30 plants per replicate. The solutions were renewed every three days to maintain the chromium concentration and species during the culture period. Several milliliters of the nutrient solution in each treatment were sampled everyday within the first three-day culture to inspect the possible transformation of the valence state of chromium. The concentrations of total Cr and Cr(VI) in the nutrient solution were determined by a flame atomic absorption spectrophotometer (AAS) (model PE-AA700) and a UV–Vis light spectrophotometer (Model UV-9100), respectively (Ball and Izbicki, 2004). The concentration of Cr(III) was calculated by subtracting Cr(VI) from total Cr. It was shown that chromium in the nutrient solution of CrCl3 treatment kept as Cr(III), and 84–96% of the chromium in the nutrient solution of K2Cr2O7 treatment kept as Cr(VI) during the three-day period, indicating that the transformation of chromium species was not significant.
2.2. Hydroponics culture
2.3. Biomass and Cr concentration measurement
Seedlings of L. hexandra were collected from the riverside of Taohua River in Guilin. Chromium concentrations
Forty five days after Cr treatment, the plants were harvested and washed with ultrapure water for three
2. Materials and methods 2.1. Field survey and sampling
1140
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
replicates. The washed plants were separated into roots, stems and leaves. They were first dried at 105 °C for 30 min, and then at 70 °C for 48 h to constant weight. The biomass (dry weight, DW) was determined. Furthermore, the dried plant tissues were ground with an agate mortar to pass a 40-mesh screen. The triturated plant tissues (about 0.5 g) were digested with a mixture of HNO3 and HClO4 (5:3, v/v) that was heated on an oven. After cooling, the extracts were diluted to 50 ml 0.2% HNO3. Chromium concentrations of the extract were determined by AAS. All the sediment samples were air-dried and sieved with a 2 mm sieve. The sieved sediment samples were mixed thoroughly. Then 2.5 g dry sediment was taken from each sample according to the quarter method (Liu, 1996) and digested with HCl + HNO3 + HClO4 (3:1:1, v/v). Chromium concentrations in the sediments were also determined by AAS. In each sediment sample, three parallels were determined. The water samples were diluted with ultrapure water and Cr concentrations were determined by AAS. 2.4. Statistical analyses One-way analysis of variance (ANOVA) was performed on all the data from culture experiment. The differences were statistically significant when P-value was less than 0.05. Multiple range test was done (with 95.0% confidence level) to find out which means were significantly different from others. This test is based on Fisher’s least significant difference (LSD) procedure. 3. Results 3.1. Cr accumulation by L. hexandra in the field L. hexandra, sediment and water were sampled from different locations around the pond (Fig. 1). Cr concentrations in L. hexandra, sediment and water are listed in
Table 1. The average Cr concentrations in water and sediment were 5.27 mg l 1and 103 mg kg 1, respectively, varying from 1.44 to 6.70 mg l 1 in water and from 34 to 186 mg kg 1 in sediment. The maximum Cr concentration in the dry leaf matter was 2978 mg kg 1 with a mean of 1626 mg kg 1. Except for the sample S10, Cr concentrations in leaves of all samples were higher than 1000 mg kg 1, the minimum Cr concentration for a Cr-hyperaccumulator. The Cr concentration in the stem dry matter changed from 135 to 514 mg kg 1 with an average of 237 mg kg 1. The ratio of Cr concentrations in leaves to those in sediment ranged from 5.82 (S1) to 56.83 (S5). The mean ratio of Cr concentration in stems to that in water was 297.41 with an maximum value of 517.86.
3.2. Growth responses of L. hexandra to different Cr supply levels L. hexandra grew normally in the nutrient solutions containing Cr(III) and did not show any obvious symptoms of Cr toxicity during the period of treatment. There was no significant difference among the leaf biomasses of all Cr(III) treatments (Fig. 2). When Cr concentration was below 20 mg l 1, the root biomasses were not significantly different (p > 0.05) to those of the control plants (0 mg l 1 Cr treatment). At the highest Cr(III) concentration (60 mg l 1), the root biomass was decreased by 58.5% compared to the control. The stem biomass decreased with the increasing of Cr(III) concentration in the nutrient solutions. However, at Cr(III) concentration below 10 mg l 1, the reduction of the stem biomass was not significant (p > 0.05). The effect of Cr(VI) on the biomass of L. hexandra was more pronounced than that of Cr(III) (Fig. 2). For example, a 20 mg l 1 Cr(VI) treatment could significantly decrease the leaf biomass (p < 0.01), but there was no significant decrease for 20 mg l 1 Cr(III) treatment (p > 0.05). When the external Cr(VI) concentration was 30 mg l 1, there were
Table 1 Cr concentrations in L. hexandra, sediment and water collected from the pond Cr concentration (mg kg 1, mg l 1)
Sample no.
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 a b c d
Ratio Ratio Ratio Ratio
of of of of
Cr Cr Cr Cr
Sediment
Water
Leaf
Stem
186 130 – – 52 114 104 – 99 34
6.70 5.55 – – 5.75 5.92 5.85 – 5.65 1.44
1084 1974 1372 2866 2978 2127 1105 1052 1454 347
135 170 270 514 332 514 160 154 386 213
concentration concentration concentration concentration
in in in in
leaf to that in sediment. leaf to that in water. stem to that in sediment. stem to that in water.
L/Sa
L/Wb
S/Sc
S/Wd
5.82 15.22 – – 56.83 18.59 10.62 – 14.70 10.24
161.82 355.69 – – 517.86 359.31 188.85 – 257.26 241.06
0.73 1.31 – – 6.33 4.50 1.54 – 3.90 6.29
20.18 30.70 – – 57.67 86.88 27.30 – 68.34 148.13
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
1141
control, the dry weights of leaf, stem, and root decreased to 54.7%, 50.4%, and 37.4%. 3.3. Cr accumulation by L. hexandra under the nutrient solution culture Under the nutrient solution culture condition, the Cr concentrations in roots, stems, and leaves of L. hexandra grown in different Cr(III) or Cr(VI) concentration are listed in Table 2. The Cr concentration in the leaves ranged from 1359 to 5608 mg kg 1 DW, and the bioaccumulation coefficient of leaves ranged from 83.4 to 486.8 when the plants were exposed to Cr(III). The maximum Cr concentration in leaves (5608 mg kg 1) was found in the plants that were exposed to 40 mg l 1 Cr(III). At 10 mg l 1Cr(III) treatment, the bioaccumulation coefficient of leaves reached a maximum (486.8) and significantly higher than those with other treatments (p < 0.05). In addition, the roots and stems of L. hexandra exposed to Cr(III) could also accumulate high Cr concentrations. The maximum Cr concentration in roots and stems were 18 656 mg kg 1 and 2976 mg kg 1, respectively. The Cr concentration in leaves of L. hexandra treated with Cr(VI) was positively correlated with Cr(VI) concentration in the nutrient solution (Table 2). The Cr concentration in leaves varied from 278 to 2164 mg kg 1. However, the bioaccumulation coefficients of leaves (averaged 58.2) were not significantly different among all Cr(VI) treatments (p > 0.05). The Cr concentration in roots also increased with Cr(VI) level in the nutrient solution, but much higher than that in leaves. The Cr concentration in stems ranged from 412 to 3475 mg kg 1 and the bioaccumulation coefficient of stems ranged from 62.2 to 115.8. Thus, it was obvious that the accumulation of Cr(III) in all plant tissues on a dry-weight basis was higher than the accumulation of Cr(VI).
Fig. 2. Effects of Cr treatment on the biomass of L. hexandra grown in nutrient solution. Different letters denote that differences are statistically significant (LSD, p < 0.05).
obvious symptoms of Cr toxicity for the 23-day treatment, e.g., some leaves began to wither. Compared with the Table 2 Chromium concentrations in tissue of L. hexandra grown in nutrient solution Treatment (mg l 1)
Cr concentration (mg kg Root b
1
Bioaccumulation coefficienta
DW)
Stem
Leaf
Root
Stem
Leaf
Cr(III)
0 5 10 20 40 60
ND 5130 ± 452a 6978 ± 1701a 8078 ± 3127a 18656 ± 962b 13054 ± 1749c
ND 628 ± 238a 1875 ± 634b 2661 ± 914bc 2756 ± 423bc 2976 ± 323c
ND 1359 ± 66a 4868 ± 310b 4317 ± 231b 5608 ± 3406b 5005 ± 1014b
– 1025.9 ± 90.5d 697.8 ± 170.1c 403.9 ± 156.3ab 466.4 ± 24.0b 217.6 ± 29.2a
– 125.6 ± 47.7bc 187.5 ± 63.4c 133.1 ± 45.7bc 68.9 ± 10.6ab 49.6 ± 5.4a
– 271.9 ± 13.3c 486.8 ± 31.0d 215.9 ± 11.5bc 140.2 ± 85.1ab 83.4 ± 16.9a
Cr(VI)
0 5 10 15 20 30
ND 813 ± 48a 1124 ± 222ab 1880 ± 612ab 2109 ± 752bc 3299 ± 1151c
ND 412 ± 101a 746 ± 53ab 932 ± 205ab 1401 ± 35b 3475 ± 980c
ND 278 ± 96a 597 ± 216ab 770 ± 212ab 1049 ± 407b 2164 ± 385c
– 162.6 ± 9.5a 112.4 ± 22.2a 125.3 ± 40.8a 105.5 ± 37.6a 110.0 ± 38.3a
– 82.3 ± 20.2a 74.6 ± 5.3a 62.2 ± 13.7a 70.1 ± 1.7a 115.8 ± 32.7b
– 55.5 ± 19.1a 59.7 ± 21.6a 51.3 ± 14.2a 52.4 ± 20.3a 72.1 ± 12.8a
Results are means ± SD, n = 3. Values followed by same letters are not significantly different at p < 0.05, according to LSD. a Ratio of Cr concentration in plant tissues to that in nutrient solution. b ND = not detectable.
1142
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
4. Discussions As for judging the standards of hyperaccumulators, the original and the foremost one was the critical concentration in stems or leaves of a plant suggested by Baker and Brooks (1989) with 10 000 mg kg 1 for Zn and Mn, 1000 mg kg 1 for Pb, Cu, Cr, Ni, Co and As, 1 mg kg 1 for Au and 100 mg kg 1 for Cd. More than 400 found hyperaccumulators were mostly validated by this standard. In the present, the Cr concentration in the leaves of L. hexandra growing in the pond near the electroplating factory averaged 1636 mg kg 1, which was greater than 1000 mg kg 1, the minimum Cr concentration for a Crhyperaccumulator. Under a nutrient solution culture, L. hexandra also showed a high accumulation capacity for Cr. The maximum Cr concentrations in the leaves of L. hexandragrowing in the nutrient solution with Cr(III) and Cr(VI) treatment were 5608 mg kg 1 and 2164 mg kg 1, respectively, and those in the stem were 2976 mg kg 1 and 3475 mg kg 1. The results confirmed that L. hexandra was a new hyperaccumulator for Cr. To date, the study on the Cr-hyperaccumulator is still scarce. Decoma niccolifera Wild Wild (1974) and Sutera fodina Wild (Baker and Brooks, 1989) were two wellknown chromium hyperaccumulators, of which the maximum Cr concentrations in the leaves dry matter are 1500 mg kg 1 and 2400 mg kg 1, respectively. Convolvulus arvensis L. could be considered as a potential Cr-hyperaccumulator plant species. Torresdey et al. (2004) reported that Cr concentration in leaves of C. arvensis was up to 2800 mg kg 1 when grown on an agar-based media containing 40 mg l 1 Cr(VI) for 15 days. In addition, Pearsonia metallifera Wild (Papilionoideae) was also reported to contain high concentrations of Cr (Wild, 1974). This species can accumulate up to 20 000 mg kg 1 Cr in the foliage ash when grown on serpentine soils. However, because the Cr concentration in dry leaf tissues is not known, it is difficult to identify whether this species meets the criterion of Cr-hyperaccumulator suggested by Baker and Brooks. Using a nutrient solution culture, Bennicelli et al., 2004 demonstrated that Azolla caroliniana has the capacity to accumulate Cr(III) and Cr(VI), and may be used as a bioaccumulator to remove the Cr from wastewater. But the maximum concentration of Cr(III) and Cr(VI) in the dry tissues of A. caroliniana was merely 964 and 356 mg kg 1, respectively. In the present study, L. hexandra displays an extraordinary accumulation capacity for chromium. Under nutrient solution culture, the Cr concentrations in leaves reached 5608 mg kg 1, which was higher than those in many Cr-hyperaccumulators reported previously. Furthermore, this species has high bioaccumulation coefficients of Cr (Table 2). Treated with Cr(III), the bioaccumulation coefficients of root, stem, and leaf averaged 562.3, 112.9, and 239.6, respectively. It was also found that L. hexandra has a strong ability to accumulate Cr even exposed to low concentrations of Cr. For instance, at the lowest concentration of Cr(III) treatment (5 mg l 1), the Cr
concentration in leaves of L. hexandra was as high as 1359 mg kg 1 DW. Cr is toxic to most high plants at 100 lmol kg 1 dry weight (Davies et al., 2002). Whereas, in this study, when the Cr concentration in the leaves reached 5608 mg kg 1 DW, L. hexandra did not show any obvious symptoms of Cr toxicity, which means that L. hexandra has a high tolerance to Cr. Moreover, it was also found that the effect of Cr(VI) on the growth of L. hexandra is more evident than that of Cr(III), which is in agreement with many previous observations (Skeffington et al., 1976; Zurayk et al., 2001; Becquer et al., 2003; Bennicelli et al., 2004; Torresdey et al., 2005). Cr(VI) is more soluble than Cr(III), and its compounds are also more easier to penetrate through physiological barriers. Therefore, Cr(VI) is more toxic for plants than Cr (III) (Shanker et al., 2005). Additionally, the Cr(III) accumulation in L. hexandra was higher than Cr(VI). It might be attributed to the different uptake mechanism of Cr(III) and Cr(VI) in plants. The use of metabolic inhibitors diminished Cr(VI) uptake in barely whereas it did not affect Cr(III) uptake, indicating that Cr(VI) uptake is an active mechanism depending on metabolic energy and Cr(III) does not (Skeffington et al., 1976). However, in this study, the Cr concentrations in the roots of L. hexandra exposed to Cr(III) were more than 100 times higher than that in culture solution. This phenomenon indicated that an active uptake of Cr(III) possibly occurred in L. hexandra. 5. Conclusions The results of field survey and pot-culture experiment show that L. hexandra is a new Cr hyperaccumulator with an extraordinary accumulation capacity for both Cr(III) and Cr(VI). It often grows rapidly and densely, and easily adapts to artificial cultivation. Moreover, this species can grow in both hygrophytic and terrestrial environments. Therefore, there is great potential for using L. hexandra in the remediation of Cr-contaminated water and soil. In addition, this species has a strong tolerance to Cr, growing normally on higher Cr concentration medium. It can also provide a new resource for exploring the biochemical mechanisms of chromium hyperaccumulation and detoxification. Acknowledgements The authors are grateful to Prof. Wang Dei-ai of Guangxi Institute of Botany Science, Chinese Academy of Science for identifying the plants. This work was cosponsored by the Ministry of Education of China (JiaoKeShi 2006-51), the Natural Science Foundation of China (No. 40663002, 20665003), the Provincial Personnel Department of Guangxi (No. 2004217) and Natural Science Foundation of Guangxi, China (No. 0542006, 0342001-4). The editor and an anonymous reviewer are thanked for a cogent revision of the manuscript.
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
References Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. Ball, J.W., Izbicki, J.A., 2004. Occurrence of hexavalent chromium in ground water in the western Mojave Desert, California. Appl. Geochem. 19, 1123–1135. Becquer, T., Quantin, C., Sicot, M., Boudot, J.P., 2003. Chromium availability in ultrafamic soils from New Caledonia. Sci. Total Environ. 301, 251–261. Bennicelli, R., Stezpniewska, Z., Banach, A., Szajnocha, K., Ostrowski, J., 2004. The ability of Azolla caroliniana to remove heavy metals (Hg(II), Cr(III), Cr(VI)) from municipal waste water. Chemosphere 55, 141–146. Chen, T.B., Huang, Z.C., Huang, Y.Y., Xie, H., Liao, X.Y., 2003. Cellular distribution of arsenic and other elements in hyperaccumulator Pteris nervosa and their relations to arsenic accumulation. Chin. Sci. Bull. 48, 1586–1591. Davies, F.T., Puryear, J.D., Newton, R.J., Egilla, J.N., Grossi, J.A.S., 2002. Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J. Plant Nutr. 25, 389–407. Huang, M., Wei, C.C., Lu, Y.Q., Zhang, X.H., Wang, D.Q., 2003. The chemical taxonomy treatment of wastewater of chrome plating. J. Guilin Univ. Technol. 23, 85–88 (in Chinese). Kotas, J., Stasicka, Z., 2000. Commentary: chromium occurrence in the environment and methods of its speciation. Environ. Pollut. 107, 263– 283. Liu, X.Y., 1996. Soil quality monitor. In: Xi, D.L., Guo, G.L., Liu, X.Y. (Eds.), Environmental Monitor. Higher Education Press, Beijing, pp. 266–284 (in Chinese). Liu, W., Shu, W.S., Lan, C.Y., 2004. Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin. Sci. Bull. 49, 29–32. Pulford, I.D., Watson, C., 2003. Phytoremediation of heavy metalcontaminated land by trees-a review. Environ. Int. 29, 529–540. Raskin, l., Smith, R.D., Salt, D.E., 1997. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr. Opin. Biotechnol. 8, 221–226. Reeves, R.D., Baker, A.J.M., 2000. Metal-accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment. John Wiley and Sons, New York, pp. 193–229.
1143
Shanker, A.K., Cervantes, C., Loza-Tavera, H., Avudainayagam, S., 2005. Chromium toxicity in plants. Environ. Int. 31, 739–753. Shrivastava, R., Upreti, R.K., Seth, P.K., Chaturvedi, U.C., 2002. Effects of chromium on the immune system. FEMS Immunol. Med. Microbiol. 34, 1–7. Skeffington, R.A., Shewry, P.R., Peterson, P.J., 1976. Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Planta 132, 209–214. Torresdey, J.L.G., Videa, J.R.P., Montes, M., Rosa, G., Diaz, C.B., 2004. Bioaccumulation of cadmium, chromium and copper by Convolvulus arvensis L.: Impact on plant growth and uptake of nutritional elements. Bioresour. Technol. 92, 229–235. Torresdey, J.L.G., Rosa, G., Videa, J.R.P., Montes, M., Jimenez, G.C., Aguilera, I.C., 2005. Differential uptake and transport of trivalent and hexavalent chromium by tumbleweed (Salsola kali). Arch. Environ. Contam. Toxicol. 48, 225–232. Wei, C.Y., Chen, T.B., Huang, Z.C., Zhang, X.Q., 2002. Cretan brake (Pteris cretica L.): an arsenic-accumulating plant. Acta Ecologica Sinica 22, 777–778 (in Chinese). Wei, S.H., Zhou, Q.X., Wang, X., Zhang, K.S., Guo, G.L., Ma, L.N., Qi, Y., 2005. A newly- discovered Cd-hyperaccumulator Solanum nigrum L. Chin. Sci. Bull. 50, 33–38. Wild, H., 1974. Indigenous plants and chromium in Rhodesia. Kiekia 9, 233–241. Xue, S.G., Chen, Y.X., Reeves, R.D., Baker, A.J.M., Lin, Q., Fernando, D.R., 2004. Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ. Pollut. 131, 393–399. Yang, X., Long, X.X., Ni, W.Z., Fu, C.X., 2002. Sedum alfredii H.: A new Zn hyperaccumulating plant first found in China. Chin. Sci. Bull. 47, 1634–1637. Zayed, A.M., Terry, N., 2003. Chromium in the environment: factors affecting biological remediation. Plant Soil 249, 139–156. Zhang, X.H., Wang, D.Q., Huang, M., 2004. Development of electroplating sludge technology. J. Guilin Univ. Technol. 24, 502–506 (in Chinese). Zhang, X.H., Luo, Y.P., Huang, H.T., Liu, J., Chen, J., 2005. Electroplating factory heavy metal pollution in soil and characteristics of plant accumulation. J. Guilin Univ. Technol. 25, 289–292 (in Chinese). Zurayk, R., Sukkariyah, B., Baalbaki, R., 2001. Common hydrophytes as bioindicators of nickel, chromium and cadmium pollution. Water Air Soil Poll. 127, 73–88.
Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz Xue-Hong Zhang a,1, Jie Liu a,b,*,1, Hai-Tao Huang a, Jun Chen a, Yi-Nian Zhu a, Dun-Qiu Wang a a
Department of Resources and Environmental Engineering, Guilin University of Technology, Jiangan Road 12#, Guilin, Guangxi 541004, PR China b School of Life Sciences, Yunnan University, Kunming 650091, PR China Received 13 July 2006; received in revised form 8 November 2006; accepted 10 November 2006 Available online 17 January 2007
Abstract Leersia hexandra Swartz (Gramineae), which occurs in Southern China, has been found to be a new chromium hyperaccumulator by means of field survey and pot-culture experiment. The field survey showed that this species had an extraordinary accumulation capacity for chromium. The maximum Cr concentration in the dry leaf matter was 2978 mg kg 1 on the side of a pond near an electroplating factory. The average concentration of chromium in the leaves was 18.86 times as that in the pond sediment, and 297.41 times as that in the pond water. Under conditions of the nutrient solution culture, it was found that L. hexandra had a high tolerance and accumulation capacity to Cr(III) and Cr(VI). Under 60 mg l 1 Cr(III) and 10 mg l 1 Cr(VI) treatment, there was no significant decrease of biomass in the leaves of L. hexandra (p > 0.05). The highest bioaccumulation coefficients of the leaves for Cr(III) and Cr(VI) were 486.8 and 72.1, respectively. However, L. hexandra had a higher accumulation capacity for Cr(III) than for Cr(VI). At the Cr(III) concentration of 10 mg l 1 in the culture solution, the concentration of chromium in leaves was 4868 mg kg 1, while at the same Cr(VI) concentration, the concentration of chromium in leaves was only 597 mg kg 1. These results confirmed that L. hexandra is a chromium hyperaccumulator which grows rapidly with a great tolerance to Cr and broad ecological amplitude. This species could provide a new plant resource that explores the mechanism of Cr hyperaccumulation, and has potential for usage in the phytoremediation of Cr-contaminated soil and water. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Hyperaccumulator; Leersia hexandra; Cr; Phytoremediation
1. Introduction Chromium is an essential trace element in metabolism of human beings and animals (Shrivastava et al., 2002). Low concentration of Cr can enhance growth of plants. However, excess Cr is highly toxic to animals and plants and may induce cancer and teratism (Shanker et al., 2005). Cr and its compounds originate from widespread use of this * Corresponding author. Address: Department of Resources and Environmental Engineering, Guilin University of Technology, Jiangan Road 12#, Guilin, Guangxi 541004, PR China. Tel.: +86 773 5897016; fax: +86 773 5897019. E-mail address: [email protected] (J. Liu). 1 These authors contributed equally to this work.
0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.11.014
metal in various industries such as metallurgical (steel, ferro- and nonferrous alloys), refractories (chrome and chrome–magnesite), and chemical (pigments, electroplating, tanning and other) (Zhang et al., 2004). These anthropogenic activities have led to the widespread contamination that Cr shows in the environment (Kotas and Stasicka, 2000). Although there are various other valence states which are unstable and shortlived in biological systems, the stable forms of Cr are the trivalent Cr(III) and the hexavalent Cr(VI) species. At present, Cr(VI) was considered as an important controlled contaminant by most countries of the world (Zayed and Terry, 2003). However, the effective but inexpensive means of remediating chromium pollution is still not found. Phytoremediation is a potential way to
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
solve the problem of chromium pollution using plants. It is attracting interest and attention from governments and enterprises as a potentially cost-effective, engineeringeconomical and environmentally-friendly green technique (Raskin et al., 1997; Pulford and Watson, 2003). The premise of this method is to find out the hyperaccumulator which has a great ability to accumulate the heavy metal. Some recent work in China has been devoted to hyperaccumulation of zinc (Yang et al., 2002), arsenic (Wei et al., 2002; Chen et al., 2003), manganese (Xue et al., 2004), cadmium (Liu et al., 2004; Wei et al., 2005). According to the criterion of concentrating >1000 mg kg 1 Cr in dry leaf tissue, suggested by Baker and Brooks (1989), only about two species could be qualified as chromium hyperaccumulators (Reeves and Baker, 2000), i.e., Dicoma niccolifera Wild Wild (1974) and Sutera fodina Wild (Baker and Brooks, 1989) in Zimbabwe, of which the maximum Cr concentrations in the dry leaves are 1500 mg kg 1 and 2400 mg kg 1, respectively. Leersia hexandra (Gramineae), a perennial herb, widely distributed in southern China, and mostly grown in swamps, paddyfields or riversides. This species was found on the side of a pond near an electroplating factory in Guangxi, China and possibly had a great accumulation capacity for chromium (Zhang et al., 2005). In the present work, field surveys have been further carried out in this Cr contaminated area. Plant, water, and sediment samples have been collected and analyzed for Cr. In order to confirm the ability of L. hexandra to concentrate chromium, more detailed experiments have been also made in non-contaminated area under controlled conditions.
1139
Fig. 1. Sketch map of the sampling locations. (a) Latitude and longitude of the electroplating factory.
The survey was conducted around a pond near an electroplating factory (E 110.38°, N 24.51°) located in Guilin (in North of Guangxi Province), China. The electroplating factory was put into production in 1996, and discharged wastewater that primarily contained Cr, Cu and Ni, etc (Huang et al., 2003). After a chemical treatment, the wastewater was drained into a pond (about 40 000 m2) near the factory, and then spilled into the Huangzhai River. As a result, Cr concentration in the sediment and water of the pond was considerably elevated. Abundant L. hexandra grew on the side of the pond. In October 2004, a detailed investigation on L. hexandra was conducted. Plant, water, and sediment samples were collected and analyzed for Cr concentration. Sampling locations are shown in Fig. 1. Each L. hexandra sample includes 15–25 individual plants. The sediment samples were composite mixtures of sediments from the rhizosphere of each plant.
in the tissue of L. hexandra grown in this site were not detectable. The seedlings were washed with redistilled water for three times and placed in 15 cm diameter round plastic pots filled with three liters half strength Hoagland’s nutrient solution in a greenhouse (14 h photoperiod; 25 °C day/ 18 °C night, relative humidity 70–75%). After 15 d, Cr treatment was conducted. Cr(III) (as CrCl3) solution was added to the pots in six levels: 0, 5, 10, 20, 40, 60 mg l 1. Cr(VI) (as K2Cr2O7) solution was added in six levels: 0, 5, 10, 15, 20, 30 mg l 1. Each treatment had three replicates, 25–30 plants per replicate. The solutions were renewed every three days to maintain the chromium concentration and species during the culture period. Several milliliters of the nutrient solution in each treatment were sampled everyday within the first three-day culture to inspect the possible transformation of the valence state of chromium. The concentrations of total Cr and Cr(VI) in the nutrient solution were determined by a flame atomic absorption spectrophotometer (AAS) (model PE-AA700) and a UV–Vis light spectrophotometer (Model UV-9100), respectively (Ball and Izbicki, 2004). The concentration of Cr(III) was calculated by subtracting Cr(VI) from total Cr. It was shown that chromium in the nutrient solution of CrCl3 treatment kept as Cr(III), and 84–96% of the chromium in the nutrient solution of K2Cr2O7 treatment kept as Cr(VI) during the three-day period, indicating that the transformation of chromium species was not significant.
2.2. Hydroponics culture
2.3. Biomass and Cr concentration measurement
Seedlings of L. hexandra were collected from the riverside of Taohua River in Guilin. Chromium concentrations
Forty five days after Cr treatment, the plants were harvested and washed with ultrapure water for three
2. Materials and methods 2.1. Field survey and sampling
1140
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
replicates. The washed plants were separated into roots, stems and leaves. They were first dried at 105 °C for 30 min, and then at 70 °C for 48 h to constant weight. The biomass (dry weight, DW) was determined. Furthermore, the dried plant tissues were ground with an agate mortar to pass a 40-mesh screen. The triturated plant tissues (about 0.5 g) were digested with a mixture of HNO3 and HClO4 (5:3, v/v) that was heated on an oven. After cooling, the extracts were diluted to 50 ml 0.2% HNO3. Chromium concentrations of the extract were determined by AAS. All the sediment samples were air-dried and sieved with a 2 mm sieve. The sieved sediment samples were mixed thoroughly. Then 2.5 g dry sediment was taken from each sample according to the quarter method (Liu, 1996) and digested with HCl + HNO3 + HClO4 (3:1:1, v/v). Chromium concentrations in the sediments were also determined by AAS. In each sediment sample, three parallels were determined. The water samples were diluted with ultrapure water and Cr concentrations were determined by AAS. 2.4. Statistical analyses One-way analysis of variance (ANOVA) was performed on all the data from culture experiment. The differences were statistically significant when P-value was less than 0.05. Multiple range test was done (with 95.0% confidence level) to find out which means were significantly different from others. This test is based on Fisher’s least significant difference (LSD) procedure. 3. Results 3.1. Cr accumulation by L. hexandra in the field L. hexandra, sediment and water were sampled from different locations around the pond (Fig. 1). Cr concentrations in L. hexandra, sediment and water are listed in
Table 1. The average Cr concentrations in water and sediment were 5.27 mg l 1and 103 mg kg 1, respectively, varying from 1.44 to 6.70 mg l 1 in water and from 34 to 186 mg kg 1 in sediment. The maximum Cr concentration in the dry leaf matter was 2978 mg kg 1 with a mean of 1626 mg kg 1. Except for the sample S10, Cr concentrations in leaves of all samples were higher than 1000 mg kg 1, the minimum Cr concentration for a Cr-hyperaccumulator. The Cr concentration in the stem dry matter changed from 135 to 514 mg kg 1 with an average of 237 mg kg 1. The ratio of Cr concentrations in leaves to those in sediment ranged from 5.82 (S1) to 56.83 (S5). The mean ratio of Cr concentration in stems to that in water was 297.41 with an maximum value of 517.86.
3.2. Growth responses of L. hexandra to different Cr supply levels L. hexandra grew normally in the nutrient solutions containing Cr(III) and did not show any obvious symptoms of Cr toxicity during the period of treatment. There was no significant difference among the leaf biomasses of all Cr(III) treatments (Fig. 2). When Cr concentration was below 20 mg l 1, the root biomasses were not significantly different (p > 0.05) to those of the control plants (0 mg l 1 Cr treatment). At the highest Cr(III) concentration (60 mg l 1), the root biomass was decreased by 58.5% compared to the control. The stem biomass decreased with the increasing of Cr(III) concentration in the nutrient solutions. However, at Cr(III) concentration below 10 mg l 1, the reduction of the stem biomass was not significant (p > 0.05). The effect of Cr(VI) on the biomass of L. hexandra was more pronounced than that of Cr(III) (Fig. 2). For example, a 20 mg l 1 Cr(VI) treatment could significantly decrease the leaf biomass (p < 0.01), but there was no significant decrease for 20 mg l 1 Cr(III) treatment (p > 0.05). When the external Cr(VI) concentration was 30 mg l 1, there were
Table 1 Cr concentrations in L. hexandra, sediment and water collected from the pond Cr concentration (mg kg 1, mg l 1)
Sample no.
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 a b c d
Ratio Ratio Ratio Ratio
of of of of
Cr Cr Cr Cr
Sediment
Water
Leaf
Stem
186 130 – – 52 114 104 – 99 34
6.70 5.55 – – 5.75 5.92 5.85 – 5.65 1.44
1084 1974 1372 2866 2978 2127 1105 1052 1454 347
135 170 270 514 332 514 160 154 386 213
concentration concentration concentration concentration
in in in in
leaf to that in sediment. leaf to that in water. stem to that in sediment. stem to that in water.
L/Sa
L/Wb
S/Sc
S/Wd
5.82 15.22 – – 56.83 18.59 10.62 – 14.70 10.24
161.82 355.69 – – 517.86 359.31 188.85 – 257.26 241.06
0.73 1.31 – – 6.33 4.50 1.54 – 3.90 6.29
20.18 30.70 – – 57.67 86.88 27.30 – 68.34 148.13
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
1141
control, the dry weights of leaf, stem, and root decreased to 54.7%, 50.4%, and 37.4%. 3.3. Cr accumulation by L. hexandra under the nutrient solution culture Under the nutrient solution culture condition, the Cr concentrations in roots, stems, and leaves of L. hexandra grown in different Cr(III) or Cr(VI) concentration are listed in Table 2. The Cr concentration in the leaves ranged from 1359 to 5608 mg kg 1 DW, and the bioaccumulation coefficient of leaves ranged from 83.4 to 486.8 when the plants were exposed to Cr(III). The maximum Cr concentration in leaves (5608 mg kg 1) was found in the plants that were exposed to 40 mg l 1 Cr(III). At 10 mg l 1Cr(III) treatment, the bioaccumulation coefficient of leaves reached a maximum (486.8) and significantly higher than those with other treatments (p < 0.05). In addition, the roots and stems of L. hexandra exposed to Cr(III) could also accumulate high Cr concentrations. The maximum Cr concentration in roots and stems were 18 656 mg kg 1 and 2976 mg kg 1, respectively. The Cr concentration in leaves of L. hexandra treated with Cr(VI) was positively correlated with Cr(VI) concentration in the nutrient solution (Table 2). The Cr concentration in leaves varied from 278 to 2164 mg kg 1. However, the bioaccumulation coefficients of leaves (averaged 58.2) were not significantly different among all Cr(VI) treatments (p > 0.05). The Cr concentration in roots also increased with Cr(VI) level in the nutrient solution, but much higher than that in leaves. The Cr concentration in stems ranged from 412 to 3475 mg kg 1 and the bioaccumulation coefficient of stems ranged from 62.2 to 115.8. Thus, it was obvious that the accumulation of Cr(III) in all plant tissues on a dry-weight basis was higher than the accumulation of Cr(VI).
Fig. 2. Effects of Cr treatment on the biomass of L. hexandra grown in nutrient solution. Different letters denote that differences are statistically significant (LSD, p < 0.05).
obvious symptoms of Cr toxicity for the 23-day treatment, e.g., some leaves began to wither. Compared with the Table 2 Chromium concentrations in tissue of L. hexandra grown in nutrient solution Treatment (mg l 1)
Cr concentration (mg kg Root b
1
Bioaccumulation coefficienta
DW)
Stem
Leaf
Root
Stem
Leaf
Cr(III)
0 5 10 20 40 60
ND 5130 ± 452a 6978 ± 1701a 8078 ± 3127a 18656 ± 962b 13054 ± 1749c
ND 628 ± 238a 1875 ± 634b 2661 ± 914bc 2756 ± 423bc 2976 ± 323c
ND 1359 ± 66a 4868 ± 310b 4317 ± 231b 5608 ± 3406b 5005 ± 1014b
– 1025.9 ± 90.5d 697.8 ± 170.1c 403.9 ± 156.3ab 466.4 ± 24.0b 217.6 ± 29.2a
– 125.6 ± 47.7bc 187.5 ± 63.4c 133.1 ± 45.7bc 68.9 ± 10.6ab 49.6 ± 5.4a
– 271.9 ± 13.3c 486.8 ± 31.0d 215.9 ± 11.5bc 140.2 ± 85.1ab 83.4 ± 16.9a
Cr(VI)
0 5 10 15 20 30
ND 813 ± 48a 1124 ± 222ab 1880 ± 612ab 2109 ± 752bc 3299 ± 1151c
ND 412 ± 101a 746 ± 53ab 932 ± 205ab 1401 ± 35b 3475 ± 980c
ND 278 ± 96a 597 ± 216ab 770 ± 212ab 1049 ± 407b 2164 ± 385c
– 162.6 ± 9.5a 112.4 ± 22.2a 125.3 ± 40.8a 105.5 ± 37.6a 110.0 ± 38.3a
– 82.3 ± 20.2a 74.6 ± 5.3a 62.2 ± 13.7a 70.1 ± 1.7a 115.8 ± 32.7b
– 55.5 ± 19.1a 59.7 ± 21.6a 51.3 ± 14.2a 52.4 ± 20.3a 72.1 ± 12.8a
Results are means ± SD, n = 3. Values followed by same letters are not significantly different at p < 0.05, according to LSD. a Ratio of Cr concentration in plant tissues to that in nutrient solution. b ND = not detectable.
1142
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
4. Discussions As for judging the standards of hyperaccumulators, the original and the foremost one was the critical concentration in stems or leaves of a plant suggested by Baker and Brooks (1989) with 10 000 mg kg 1 for Zn and Mn, 1000 mg kg 1 for Pb, Cu, Cr, Ni, Co and As, 1 mg kg 1 for Au and 100 mg kg 1 for Cd. More than 400 found hyperaccumulators were mostly validated by this standard. In the present, the Cr concentration in the leaves of L. hexandra growing in the pond near the electroplating factory averaged 1636 mg kg 1, which was greater than 1000 mg kg 1, the minimum Cr concentration for a Crhyperaccumulator. Under a nutrient solution culture, L. hexandra also showed a high accumulation capacity for Cr. The maximum Cr concentrations in the leaves of L. hexandragrowing in the nutrient solution with Cr(III) and Cr(VI) treatment were 5608 mg kg 1 and 2164 mg kg 1, respectively, and those in the stem were 2976 mg kg 1 and 3475 mg kg 1. The results confirmed that L. hexandra was a new hyperaccumulator for Cr. To date, the study on the Cr-hyperaccumulator is still scarce. Decoma niccolifera Wild Wild (1974) and Sutera fodina Wild (Baker and Brooks, 1989) were two wellknown chromium hyperaccumulators, of which the maximum Cr concentrations in the leaves dry matter are 1500 mg kg 1 and 2400 mg kg 1, respectively. Convolvulus arvensis L. could be considered as a potential Cr-hyperaccumulator plant species. Torresdey et al. (2004) reported that Cr concentration in leaves of C. arvensis was up to 2800 mg kg 1 when grown on an agar-based media containing 40 mg l 1 Cr(VI) for 15 days. In addition, Pearsonia metallifera Wild (Papilionoideae) was also reported to contain high concentrations of Cr (Wild, 1974). This species can accumulate up to 20 000 mg kg 1 Cr in the foliage ash when grown on serpentine soils. However, because the Cr concentration in dry leaf tissues is not known, it is difficult to identify whether this species meets the criterion of Cr-hyperaccumulator suggested by Baker and Brooks. Using a nutrient solution culture, Bennicelli et al., 2004 demonstrated that Azolla caroliniana has the capacity to accumulate Cr(III) and Cr(VI), and may be used as a bioaccumulator to remove the Cr from wastewater. But the maximum concentration of Cr(III) and Cr(VI) in the dry tissues of A. caroliniana was merely 964 and 356 mg kg 1, respectively. In the present study, L. hexandra displays an extraordinary accumulation capacity for chromium. Under nutrient solution culture, the Cr concentrations in leaves reached 5608 mg kg 1, which was higher than those in many Cr-hyperaccumulators reported previously. Furthermore, this species has high bioaccumulation coefficients of Cr (Table 2). Treated with Cr(III), the bioaccumulation coefficients of root, stem, and leaf averaged 562.3, 112.9, and 239.6, respectively. It was also found that L. hexandra has a strong ability to accumulate Cr even exposed to low concentrations of Cr. For instance, at the lowest concentration of Cr(III) treatment (5 mg l 1), the Cr
concentration in leaves of L. hexandra was as high as 1359 mg kg 1 DW. Cr is toxic to most high plants at 100 lmol kg 1 dry weight (Davies et al., 2002). Whereas, in this study, when the Cr concentration in the leaves reached 5608 mg kg 1 DW, L. hexandra did not show any obvious symptoms of Cr toxicity, which means that L. hexandra has a high tolerance to Cr. Moreover, it was also found that the effect of Cr(VI) on the growth of L. hexandra is more evident than that of Cr(III), which is in agreement with many previous observations (Skeffington et al., 1976; Zurayk et al., 2001; Becquer et al., 2003; Bennicelli et al., 2004; Torresdey et al., 2005). Cr(VI) is more soluble than Cr(III), and its compounds are also more easier to penetrate through physiological barriers. Therefore, Cr(VI) is more toxic for plants than Cr (III) (Shanker et al., 2005). Additionally, the Cr(III) accumulation in L. hexandra was higher than Cr(VI). It might be attributed to the different uptake mechanism of Cr(III) and Cr(VI) in plants. The use of metabolic inhibitors diminished Cr(VI) uptake in barely whereas it did not affect Cr(III) uptake, indicating that Cr(VI) uptake is an active mechanism depending on metabolic energy and Cr(III) does not (Skeffington et al., 1976). However, in this study, the Cr concentrations in the roots of L. hexandra exposed to Cr(III) were more than 100 times higher than that in culture solution. This phenomenon indicated that an active uptake of Cr(III) possibly occurred in L. hexandra. 5. Conclusions The results of field survey and pot-culture experiment show that L. hexandra is a new Cr hyperaccumulator with an extraordinary accumulation capacity for both Cr(III) and Cr(VI). It often grows rapidly and densely, and easily adapts to artificial cultivation. Moreover, this species can grow in both hygrophytic and terrestrial environments. Therefore, there is great potential for using L. hexandra in the remediation of Cr-contaminated water and soil. In addition, this species has a strong tolerance to Cr, growing normally on higher Cr concentration medium. It can also provide a new resource for exploring the biochemical mechanisms of chromium hyperaccumulation and detoxification. Acknowledgements The authors are grateful to Prof. Wang Dei-ai of Guangxi Institute of Botany Science, Chinese Academy of Science for identifying the plants. This work was cosponsored by the Ministry of Education of China (JiaoKeShi 2006-51), the Natural Science Foundation of China (No. 40663002, 20665003), the Provincial Personnel Department of Guangxi (No. 2004217) and Natural Science Foundation of Guangxi, China (No. 0542006, 0342001-4). The editor and an anonymous reviewer are thanked for a cogent revision of the manuscript.
X.-H. Zhang et al. / Chemosphere 67 (2007) 1138–1143
References Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. Ball, J.W., Izbicki, J.A., 2004. Occurrence of hexavalent chromium in ground water in the western Mojave Desert, California. Appl. Geochem. 19, 1123–1135. Becquer, T., Quantin, C., Sicot, M., Boudot, J.P., 2003. Chromium availability in ultrafamic soils from New Caledonia. Sci. Total Environ. 301, 251–261. Bennicelli, R., Stezpniewska, Z., Banach, A., Szajnocha, K., Ostrowski, J., 2004. The ability of Azolla caroliniana to remove heavy metals (Hg(II), Cr(III), Cr(VI)) from municipal waste water. Chemosphere 55, 141–146. Chen, T.B., Huang, Z.C., Huang, Y.Y., Xie, H., Liao, X.Y., 2003. Cellular distribution of arsenic and other elements in hyperaccumulator Pteris nervosa and their relations to arsenic accumulation. Chin. Sci. Bull. 48, 1586–1591. Davies, F.T., Puryear, J.D., Newton, R.J., Egilla, J.N., Grossi, J.A.S., 2002. Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J. Plant Nutr. 25, 389–407. Huang, M., Wei, C.C., Lu, Y.Q., Zhang, X.H., Wang, D.Q., 2003. The chemical taxonomy treatment of wastewater of chrome plating. J. Guilin Univ. Technol. 23, 85–88 (in Chinese). Kotas, J., Stasicka, Z., 2000. Commentary: chromium occurrence in the environment and methods of its speciation. Environ. Pollut. 107, 263– 283. Liu, X.Y., 1996. Soil quality monitor. In: Xi, D.L., Guo, G.L., Liu, X.Y. (Eds.), Environmental Monitor. Higher Education Press, Beijing, pp. 266–284 (in Chinese). Liu, W., Shu, W.S., Lan, C.Y., 2004. Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin. Sci. Bull. 49, 29–32. Pulford, I.D., Watson, C., 2003. Phytoremediation of heavy metalcontaminated land by trees-a review. Environ. Int. 29, 529–540. Raskin, l., Smith, R.D., Salt, D.E., 1997. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr. Opin. Biotechnol. 8, 221–226. Reeves, R.D., Baker, A.J.M., 2000. Metal-accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment. John Wiley and Sons, New York, pp. 193–229.
1143
Shanker, A.K., Cervantes, C., Loza-Tavera, H., Avudainayagam, S., 2005. Chromium toxicity in plants. Environ. Int. 31, 739–753. Shrivastava, R., Upreti, R.K., Seth, P.K., Chaturvedi, U.C., 2002. Effects of chromium on the immune system. FEMS Immunol. Med. Microbiol. 34, 1–7. Skeffington, R.A., Shewry, P.R., Peterson, P.J., 1976. Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Planta 132, 209–214. Torresdey, J.L.G., Videa, J.R.P., Montes, M., Rosa, G., Diaz, C.B., 2004. Bioaccumulation of cadmium, chromium and copper by Convolvulus arvensis L.: Impact on plant growth and uptake of nutritional elements. Bioresour. Technol. 92, 229–235. Torresdey, J.L.G., Rosa, G., Videa, J.R.P., Montes, M., Jimenez, G.C., Aguilera, I.C., 2005. Differential uptake and transport of trivalent and hexavalent chromium by tumbleweed (Salsola kali). Arch. Environ. Contam. Toxicol. 48, 225–232. Wei, C.Y., Chen, T.B., Huang, Z.C., Zhang, X.Q., 2002. Cretan brake (Pteris cretica L.): an arsenic-accumulating plant. Acta Ecologica Sinica 22, 777–778 (in Chinese). Wei, S.H., Zhou, Q.X., Wang, X., Zhang, K.S., Guo, G.L., Ma, L.N., Qi, Y., 2005. A newly- discovered Cd-hyperaccumulator Solanum nigrum L. Chin. Sci. Bull. 50, 33–38. Wild, H., 1974. Indigenous plants and chromium in Rhodesia. Kiekia 9, 233–241. Xue, S.G., Chen, Y.X., Reeves, R.D., Baker, A.J.M., Lin, Q., Fernando, D.R., 2004. Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ. Pollut. 131, 393–399. Yang, X., Long, X.X., Ni, W.Z., Fu, C.X., 2002. Sedum alfredii H.: A new Zn hyperaccumulating plant first found in China. Chin. Sci. Bull. 47, 1634–1637. Zayed, A.M., Terry, N., 2003. Chromium in the environment: factors affecting biological remediation. Plant Soil 249, 139–156. Zhang, X.H., Wang, D.Q., Huang, M., 2004. Development of electroplating sludge technology. J. Guilin Univ. Technol. 24, 502–506 (in Chinese). Zhang, X.H., Luo, Y.P., Huang, H.T., Liu, J., Chen, J., 2005. Electroplating factory heavy metal pollution in soil and characteristics of plant accumulation. J. Guilin Univ. Technol. 25, 289–292 (in Chinese). Zurayk, R., Sukkariyah, B., Baalbaki, R., 2001. Common hydrophytes as bioindicators of nickel, chromium and cadmium pollution. Water Air Soil Poll. 127, 73–88.