吳啟航， 李伙生， 黃雪夏， 羅定貴， 張 平， 陳永亨， 汪珍春， 周伯春， 孫莉麗， 黃芷瑩， 源韻詩

(廣州大學 a.珠江三角洲水質安全與保護協(xié)同創(chuàng)新中心; b.珠江三角洲水質安全與保護省部共建教育部重點實驗室; c.生命科學學院,廣東 廣州 510006)

利用植物籽粒莧修復鉈污染土壤研究

吳啟航a,b， 李伙生a,b， 黃雪夏b， 羅定貴b， 張 平b， 陳永亨a,b， 汪珍春c， 周伯春c， 孫莉麗c， 黃芷瑩c， 源韻詩c

(廣州大學 a.珠江三角洲水質安全與保護協(xié)同創(chuàng)新中心; b.珠江三角洲水質安全與保護省部共建教育部重點實驗室; c.生命科學學院,廣東 廣州 510006)

近年來，隨著對鉈的強毒性及其對人類健康的高風險認識增加，土壤鉈污染問題越來越多地被關注.植物修復是去除土壤重金屬污染具有低成本和可持續(xù)的技術，適用于鉈污染土壤的修復. 本研究選擇籽粒莧作為測試植物，用于研究鉈污染土壤的修復.土壤中鉈濃度設置為0, 1, 5, 10, 15 和20 mg·kg-1，經(jīng)過100 d的盆栽試驗，結果表明，隨著土壤中鉈的濃度升高，植物的生物量、高度、PSII最大量子效率(Fv/Fm)和植物含鉈總量均有差異，且植物個體組織(根、莖、葉)中鉈的濃度增加；生物富集因子(BCF)在所有實驗設置中均隨著土壤中鉈含量增加而上升，且都大于1；轉移系數(shù)(TF)也有類似的規(guī)律.因此，籽粒莧具有良好的修復鉈污染土壤的潛力.

鉈； 植物修復； 籽粒莧； 生物富集； 轉移

0 Introduction

Thallium (Tl) is an extremely toxic rare element classified as one of the 13 USEPA priority metals[1-3]. It is reported to be highly bioconcentrated[4]and more toxic to living organisms than mercury and cadmium[5]. Although its abundance in earth crust is low (0.75 mg·kg-1)[6], the high release of it into regional environment because of anthropogenic inputs can pose a significant threat to the local ecosystem[7]. The anthropogenic activities, including booming production and consumption of Tl-containing high-tech products, coal combustion, cement production, mining, and smelting, have led to the deterioration of Tl pollution in many regions[8-10]. The increasing public awareness of the high risk of Tl to human health has attracted more and more focus on remediating Tl pollution in recent years.

Recent studies on Tl pollution suggested that the Tl content of the soil in the vicinity of the mining and smelting areas can be extremely high, with a range from 2 to 124 mg·kg-1[9, 11-12], far exceeding the average background concentration. This indicates that most of the soil near the mining and smelting areas is heavily polluted by Tl, and that it is necessary to adopt appropriate measures to remediate the Tl-laden soil. The use of physical and chemical techniques for soil remediation is largely restricted due to huge cost, complex implementation and adverse effects such as destruction of soil structure and secondary pollution[13]. Phytoremediation, which uses high accumulation plants to extract the toxic metals out of soil, is a cost-effective and sustainable technique for heavy metal contamination of soil, and may be effective for Tl removal from soil. Previous investigations showed that some species such asSinapisalba[14],Brassicaoleracea[7, 15],B.napus[16],Biscutellalaevigat[17], andIberisintermedia[18]have good capability to remediate the Tl-laden soil. However, these studied plants are commonly edible vegetables that can be mistakenly consumed by animals and humans, and then causing accumulation of Tl in the food chain[10, 14]. Hence, their application could still be questionable, and more new plants for phytoremediation should be identified.

A.hypochondriacus, is an ornamental plant commonly known as Prince-of-Wales feather or prince’s feather[19]. It is a species of annual flowering plant, originally endemic to Mexico and then spreading in warm areas worldwide[20]. It is usually found well grown in mining wastelands, tailings, barrens and other disturbed habitats[20], implying that it may be a promising bioaccumulator plant. Many recent studies have proven the great potential ofA.hypochondriacusto remediate cadmium (Cd)-polluted soil with fast growth and high biomass as well as high uptake of heavy metals[13, 20-22]. However, there are few reports on the tolerance and bioaccumulation of Tl inA.hypochondriacus. Since Tl is more toxic than Cd, hence, the potential ofA.hypochondriacusfor phytoremediation of Tl-contaminated soil remains enigmatic.

The goal of this study was to examine the capability ofA.hypochondriacusto remediate Tl-laden soil. The response of the biomass, height and photosynthetic activity of the plant to soil loaded with different Tl concentrations was assessed under greenhouse conditions.

1 Materials and methods

1.1 Preparation of pot culture using A. hypochondriacus

The soil used for pot culture was identical with the one previously described by WU, et al[10]. The properties of the soil used in the pot are listed in Table 1. The preparation of pot culture was also the same as that reported by WU, et al[10]except the use ofA.hypochondriacusinstead ofSolanumnigrumas the phytoremediation plant. In brief, the pre-treated soil was blended with appropriate amount of thallous nitrate to create a soil with Tl concentrations of 0 (control), 1, 5, 10, 15, 20 mg·kg-1. Three replicates were performed for each concentration, resulting in 18 pots’ culture in total.A.hypochondriacusgrew from the seeds of the same species collected from Yunfu agricultural site, which is located near the pyrite tailings site own by Yunfu Pyrite Enterprises Group Corporation. The greenhouse conditions for the pot culture were day/night cycle of 16/8 h, day temperature of 22±1 ℃, night temperature of 18±1 ℃, relative humidity of 75%±3 %. The plants were harvested for examination after the greenhouse culture reached 100 d.

Table 1 The soil properties for pot culture (mean±SD, n=3)

ND: Not detected

1.2 Evaluation of photosynthetic activity and growth of A. hypochondriacus

The photosynthetic activity and growth ofA.hypochondriacuswere determined after 100 d pot culture. The maximum quantum efficiency of photosystem II (Fv/Fm) of leaves, which is indicative of the photosynthetic activity of plant, was examined according to WU, et al[10]. Following the measurements of Fv/Fm, the plants were harvested and thoroughly washed with water. Leaves, stems, and roots were separated and weighed fresh. and then dried in oven at 60 ℃ overnight for evaluation of biomass growth after 100 d culture.

1.3 Measurement of Tl concentrations of soil and plants

The determination of Tl content in the soil and plants were performed according to WU, et al[10]. In brief, a mixture of 15 mL nitric acid (15 M) and 5 mL hydrofluoric acid (10 M) was used to digest 0.2 g soil sample, while a mixture of 8 mL nitric acid (15 M) and 2 mL perchloric acid (12 M) was used to digest 0.5 g plant sample. Automatic digestion block (ST40, Beijing Polytech Instrument Ltd., China) was run at 140 ℃ for 3 h for all digestion[10]. Inductively coupled plasma-mass spectrometry (ELAN 6 000, PerkinElmer Instruments, USA) was used to analyze the Tl concentration of samples. The reference test was conducted according to Ref.[10] and showed reliable accuracy.

1.4 Data treatment and statistical analyses

Bioconcentration factor (BCF) was defined as the ratio of the Tl concentration in the whole plant to that in the cultured soil, aiming to estimate the efficiency ofA.hypochondriacusto extract Tl from the soil to the plant. Translocation factor (TF) was defined as the ratio of the Tl concentration in the aboveground part (namely stems and the leaves) of the plants to that of the roots (the belowground part of the plants), aiming to evaluate the efficiency ofA.hypochondriacusto translocate Tl from its roots to its stems and leaves. BCF and TF are given in the following formula (Eq.1～2), which are modified according to YOON, et al[23]. The total Tl mass of the plant was calculated according to Eq.(3).

(1)

(2)

Mtotal=Croots*Mroots+Cstems*Mstems+Cleaves*Mleaves

(3)

WhereCsoil,Cplant,Croots,Cstems,CleavesandCabovegroundare the concentrations of Tl in the soil, the whole plant, roots, stems, and leaves ofA.hypochondriacus, respectively; whileMroots,Mstems,MleavesandMtotalare the mass of roots, stems, leaves and the whole plant ofA.hypochondriacus, respectively.

The statistical analysis of Fv/Fm was conducted according to WU, et al[10]. Briefly, One-way analysis of variance (ANOVA) was applied to examine the impacts of Tl content of soil on Fv/Fm. Normality and homoscedasticity were tested by using Shapiro-Wilk and Levene’s tests, respectively. Logarithmic transformation was applied if either one of the assumptions was violated. Statistical analyses were conducted by software SPSS 22 for Windows.

2 Results and discussion

2.1 Accumulation of Tl in A. hypochondriacus in pot culture

The Tl concentration in different plant organs (roots, stems and leaves) ofA.hypochondriacusgrown in soil loaded with different thallium concentrations (0, 1, 5, 10, 15, 20 mg·kg-1) is depicted in Fig.1. The accumulation of Tl in plant organs and the whole plant (average content of leaves, stems and roots)of accumulation in the plants grew in soils with different Tl concentrations.A.hypochondriacusincreased with the increasing Tl content in soil, as revealed by both the Tl concentration of different organs and the total mass of Tl in the whole plants (Fig.1). The leaves had the lowest accumulation of Tl in the most tests, while the stems had the highest accumulation (over 120 mg Tl·kg-1stems) when soil Tl content reached high up to 20 mg Tl·kg-1soil (Fig.1). It should be noted that at 20 mg Tl·kg-1soil, the Tl concentration of the roots and the leaves slightly decreased as compared with Tl concentration at 15 mg Tl·kg-1soil, while the uptake of Tl in the stems remediation of the identical soil with same Tl content showed a different bioaccumulation pattern, where most Tl was uptaken by the roots and leaves at all exposure levels[10]. UnlikeS.nigrum,A.hypochondriacustends to accumulate Tl in stems at high Tl exposure level. This may be due to the difference in physiological characters between the two plants. For many plants, leaves and stems are more vulnerable to heavy metal toxicity[24, 25], while forA.hypochondriacus, whose main biomass consisted largely of stems, its stems have high tolerance with Tl toxicity even at high exposure levels. So far, the mechanism of detoxification for Tl in plants is not fully understood. The hypothesis about antioxidative defense includes increasing the activities of superoxide dismutase and ascorbate peroxidase is usually used to explain the detoxification response of the corresponding organs of the plants[26-27]. Additional assays should be performed to verify this hypothesis.

Fig.1 The Tl concentration of different plant organs and the whole plant, and the total mass of Tl

At low exposure levels of 1 and 5 mg Tl·kg-1soil, the BCF ofA.hypochondriacuswas similar (1.89 and 1.88, respectively); while at relatively high exposure levels, it was elevated with increasing Tl exposure level (Fig.2). The obvious accumulation of Tl, as indicated by the fact that the BCF at all studies levels was greater than 1, suggests thatA.hypochondriacusis a good extractor for Tl in soil. Although it is not a hyperaccumuting plant in contrast withBiscutellalaevigataandIberisintermediain terms of BCF[28], it has good potential of Tl accumulation and could be further enhanced if agricultural techniques were used. The TF was also significantly affected by Tl exposure level, and generally increased from 0.13 to 1.70 along with increasing Tl exposure level. At 1 mg Tl·kg-1soil, the TF was only 0.13, indicating the low translocation ability ofA.hypochondriacusat low exposure level of Tl. In this case, the harvest of the whole plant including the roots is a must in order to largely extract the Tl. The increase of TF to over 1.0 was observed at exposure levels of 10 and 20 mg Tl/kg soil, implying that the harvest of the above-ground part of the plant may be the most economical way to extract Tl from soil polluted at these levels. Compared withS.nigrum[10], the BCF ofA.hypochondriacuswas relative lower,but the TF was greater. The high efficiency ofA.hypochondriacusto translocate Tl from its roots to its aerial organs could lead to more toxicity to the plant, and thus less accumulation thanSolanum.nigrum. However, for harvesting of the plant, higher TF can be more operationally beneficial since only reaping of the aerial part of the plants is sufficient to extract Tl form soil[29].

Fig.2 The bioconcentration factor (BCF) and translocation factor (TF) of the plants grown in soils with different Tl concentrations

2.2 Impact of Tl on photosynthetic activity of A. hypochondriacus

The maximum quantum efficiency of photosystem II (Fv/Fm) of leaves, an effective indicator of the photosynthetic activity and thus growth of plant, was found significantly affected by the Tl exposure level (Fig.3). The Fv/Fm value of control was at around 0.75, which is slightly lower than the optimal range (0.79～0.84, as suggested by KITAJIMA,et al[30]) for unstressed plants (Fig.3). This is likely due to the heredity of the toxic stress of Tl from the seeds of parents to the offspring seedlings[10]. With the increase in Tl content of soil, the Fv/Fm value decreased to around 0.69 at low levels of 1 and 5 mg Tl/kg soil, and then kept declining to the lowest level of 0.42 at 20 mg Tl/kg soil (Fig.3). When Tl exposure level reached 20 mg Tl/kg soil, leaf senescence and chlorosis began to occur but was not striking. The correlation between Fv/Fm and biomass of leaves was found significantly positive (Pearson correlation coefficient=0.81,P<0.01,n=18), indirectly suggesting that Tl might inhibit the growth of leaves and hence Fv/Fm ofA.hypochondriacus. Similar stress pattern was also found in our previous study on usingS.nigrumto remediate the same Tl-polluted soil[10]. This clearly suggests the high toxicity of Tl.A.hypochondriacuswas found competent for remediation of Cd-polluted soil[13, 20, 21], while for the phytoremediation of Tl, which is more toxic to Cd, its capacity could be slightly compromised when being exposured to high Tl level. It is surmised that the high affinity of Tl to biomolecules and mitochondrial membrane leads to the reduced biosynthesis of chlorophyll even damage to chloroplasts[24, 31, 32], and thus inhibition on the photosystem II reaction with lower Fv/Fm value[10].

Fig.3 The Fv/Fm ratio of the plants grown in soils with different Tl concentrations

2.3 Impact of Tl on growth of A. hypochondriacus

The growth ofA.hypochondriacus, represented by the biomass of different plant organs and by the height of the plant after 100 d pot culture, is demonstrated in Fig.4 and Fig.5, respectively. The plant height gradually decreased from 38 cm for the control to 15 cm for the species growing at soil of 20 mg Tl·kg-1soil (Fig.4). This implies that Tl can inhibit the growth ofA.hypochondriacuswhen it is exposed at high level of Tl. Previous study showed thatA.hybridusL. had good tolerance to Cd at 30 and 60 mg Cd·kg-1soil, with unexpectedly higher plant height as compared with the control (without addition of Cd)[20]. Although its height was still impaired at strongly polluted levels (120, 150 and 180 mg Cd·kg-1soil), its tolerance and adaptability to Cd (below 60 mg Cd·kg-1soil) was already striking. When it comes to Tl, the plant height was shrunk with addition of Tl, suggesting the stronger toxicity of Tl than Cd toA.hypochondriacus.

Unlike the case on plant height, interestingly, the biomass of all the plant organs at low exposure levels (1 and 5 mg Tl·kg-1soil) was higher than that of the control (Fig.5). The plant biomass began to decline when exposure level reached 10 mg Tl·kg-1soil, but became steady when exposure level is at 15 and 20 mg Tl·kg-1soil (Fig.5). In terms of the biomass, the growth ofA.hypochondriacuswas likely stimulated by exposure to low levels of Tl in soil. Similar phenomenon was also observed whenA.hypochondriacuswas used to remediate the Cd-polluted soil, where the plant biomass was greater at relatively low exposure level (30 and 60 mg Cd·kg-1soil)[20]. Our previous study showed that the growth of another plant (S.nigrum) in terms of biomass was constantly compromised by the same level of Tl[10]. This suggests thatA.hypochondriacushas unique adaptability to maintain its biomass when its height (Fig.4) and photosynthetic activity (Fig.3) of leaves were impaired by toxicity of Tl. In addition, LI, et al[13]revealed that the use of agricultural technologies such as appropriate use of fertilizers can substantially enhance the plant biomass and accumulation of Cd inA.hypochondriacus. Therefore, it is likely that the capacity of phytoremediation of Tl may be enhanced if proper fertilizers were used, but this hypothesis requires more investigation.

Fig.4 The height of the plants grown in soils with different Tl concentrations

Fig.5 The biomass of the plants grown in soils with different Tl concentrations

3 Conclusion

During phytoremediation of Tl-laden soil by usingA.hypochondriacus, some inhibition effects such as reduction in plant height, biomass and photosynthetic activity were observed at high exposure levels (over 10 mg Tl·kg-1soil). However, taking the good tolerance and bioconcentration and translocation ability into account,A.hypochondriacushas good potential for phytoremediation of Tl-polluted soil. Further research on enhancing the remediation capacity by using agricultural techniques and other means should be conducted.

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【責任編輯： 孫向榮】

Phytoremediation of thallium-contaminated soil using Amaranthus hypochondriacus

WU Qi-hanga,b, LI Huo-shenga,b, HUANG Xue-xiab, LUO Ding-guib, ZHANG Pingb, CHEN Yong-henga,b, WANG Zhen-chunc, ZHOU Bo-chunc, SUN Li-lic, HUANG Zhi-yingc, YUAN Yun-shic

(a. Collaborative Innovation Center of Water Quality Safety and Protection in Pearl River Delta;b. Key Laboratory of Water Quality Safety and Protection in Pearl River Delta (Ministry of Education); c.School of Life Sciences, Guangzhou University, Guangzhou 510006, China)

The issue of soil contamination by thallium (Tl) has been gaining increasing attention in recent years, due to the increasing awareness of the strong toxicity and high risk of Tl to human health. Phytoremediation is a cost-effective and sustainable means to remove heavy metals from contaminated soil, and may be promising for remediation of Tl-polluted soil. Hence,Amaranthushypochondriacus, which is a highly productive and commonly used phytoremediation plant, was selected to remediate the Tl-polluted soil. In the test of 100 d pot culture, it is shown that although the higher Tl content (0, 1, 5, 10, 15 and 20 mg·kg-1soil) in soil led to lower biomass and height as well as maximal quantum efficiency of photosystem (Fv/Fm) of the plant, the total mass (and average content) of Tl in the whole plant growing in more Tl-polluted soil increased significantly. The Tl accumulated in all different organs (roots, stems and leaves) ofA.hypochondriacusalso increased with the rise in Tl content of soil, indicating the good capability ofA.hypochondriacusto extract Tl from soil. The bioconcentration factor (BCF) at all studied levels of Tl was greater than 1, and increased with increasing Tl content in soil. Similar increasing trend for translocation factor (TF) was found at higher Tl pollution condition. Therefore,A.hypochondriacusis shown to have good potential to remediate Tl-contaminated soil.

thallium; phytoremediation;Amaranthushypochondriacus; bioaccumulation; translocation

ET 471 Document code: A

Foundation items: This project is supported by the National Science Foundation of China (41573119); Collaborative Innovation Major Projects of Guangzhou Education Bureau (13xt02); Educational System Innovation Team Project of Guangzhou Education Bureau (13C02); Young Creative Talent Project for Ordinary Universities of Guangdong Province’s Educational Commission(2015KQNCX115); High Level University Construction Project of Guangdong Province (Regional Water Environment Safety and Water Ecological Protection).

1671- 4229(2016)06-0017-08

X 53

Received date: 2016-09-27; Revised date: 2016-11-06

Biography: WU Qi-hang (1977-), male, associate professor, Ph.D. E-mail: wuqihang@gzhu.edu.cn