Article pubs.acs.org/est
Could Uptake and Acropetal Translocation of PBDEs by Corn Be Enhanced Following Cu Exposure? Evidence from a Root Damage Experiment Shaorui Wang,†,# Yan Wang,‡ Chunling Luo,*,† Longfei Jiang,§ Mengke Song,† Dayi Zhang,∥ Yujie Wang,⊥ and Gan Zhang† †
Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China Key Laboratory of Industrial Ecology and Environmental Engineering (MOE), School of Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China § College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China ∥ Lancaster university, Lancaster Environment Centre, Lancaster, LA1 4YW, United Kingdom ⊥ School of Environmental Science and Engineering, Guangdong University of Technology, Guangzhou 510006, China # Graduate University of Chinese Academy of Sciences, Beijing 100039, China ‡
S Supporting Information *
ABSTRACT: Cocontamination by heavy metals and persistent organic pollutants (POPs) is ubiquitous in the environment. Fate of POPs within soil/water-plant system is a significant concern and an area where much uncertainty still exists when plants suffered cotoxicity from POPs and metals. This study investigated the fate of polybrominated diphenyl ethers (PBDEs) when copper (Cu) was present within the soil/water-plant system using pot and hydroponic experiments. The presence of Cu was found to induce damage to the root cell membranes of corn (Zea mays L. cv. Nongda 108) with increasing concentration in both shoots and roots. The PBDE congeners BDE209 and BDE47 in shoots were also enhanced with the increasing electrolytic leakage from root, attributed to Cu damage, and the highest shoot BDE209 and BDE47 levels were observed under the highest Cu dosage. In addition, positive correlations were observed between the PBDE content of corn shoots and the electrolytic leakage of corn roots. These results indicated that within a defective root system, more PBDEs will penetrate the roots and are acropetally translocated in the shoots. The potential ecological risk associated with the translocation and accumulation of POPs into plant shoots needs careful reconsideration in media cocontaminated with metals and POPs, whereas often ignored or underestimated in environmental risk assessments.
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INTRODUCTION Polybrominated diphenyl ethers (PBDEs), a group of halogenated chemicals,1,2 some of them have been added to the list of banned Persistent Organic Pollutants (POPs) under Stockholm Convention due to their persistence, toxicity, bioaccumulation, and long-range atmospheric transport.3 Most previous studies regarding PBDEs focused mainly on their physicochemical characteristics, partitioning equilibrium, toxicity, and environmental fate.4−7 The uptake and translocation of PBDEs by plants have been studied intensely over the past decade.8−10 Transpiration stream concentration factor (TSCF) was commonly used to describe the root-to-shoot translocation ability of an organic compound, based on its octanol−water partition coefficient (Kow).11,12 Moderately hydrophobic organic compounds (0.5 < log Kow < 3) could be taken up by plant roots and translocated to shoot tissue.13 Nevertheless, the recent discoveries have © XXXX American Chemical Society
revealed that nonionizable, polar, highly water-soluble compounds, likely methanol (log Kow= −0.77) and pentachlorophenol (log Kow = 5.12) were likely to be taken up by plant root and translocated to shoot.14 PBDEs are hydrophobic compounds with log Kow > 5.0, where BDE47 and BDE209 have the log Kow values of 5.87−6.16 and 8.18−8.27, respectively.15 Their behavior and fate in the soil/water-plant system cannot be successfully described by the theories solely using log Kow, particularly when considering the variety of chemicals, cultivars, and physiology of cultivar being changed under stress.16 Some recent studies have reported the acropetal transposition of PBDEs within plants, such as ryegrass17 and Received: August 21, 2015 Revised: October 31, 2015 Accepted: December 22, 2015
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DOI: 10.1021/acs.est.5b04030 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology corn.10 The uptake, translocation, and metabolism of BDE209 in pumpkin also revealed new evidence on the behavior and fate of PBDEs within the soil/water-plant system.18 The root-soil/water boundary is of critical importance in biotic−abiotic mass-transfer interfaces and is a primary entry of pollutant to the food chain. Root physiology status, such as cellular electrolytic leakage, however, is never involved to be a parameter of the plant uptake of PBDEs. Especially when PBDEs and other pollutants coexisted, likely metals, plant roots suffer from the synergistic toxicity or damage from pollutants and the uptake process is altered.19 For instance, substances with a large structural formula, such as metal-chelating compounds, can be taken up indiscriminately and loaded into the root xylem through breaks in the root Casparian strip.20 Hence, it is hypothesized that the translocation of very hydrophobic PBDEs upward to the shoot can be enhanced in a defective root system under PBDEs and heavy metal cocontamination. High levels of metals or PBDEs were found either singly or to coexist in different environmental media, for instance at ewaste recycling sites where the soil Cu and PBDE concentration ranged from 77.9 mg/kg to 1600 mg/kg21 and 0.19 mg/kg to 9.16 mg/kg,22 respectively. The ability of these environmental pollutants to cross the root membrane presents a big concern for food safety, as terrestrial plants sit at the base of many food chains.23 However, the mechanism and risks associated with POP accumulation within plant tissue under metal-POPs contamination are largely ignored when conducting an environmental risk assessment, due to our limited understanding of the uptake of POPs by plants. The objective of this study is to investigate the potential fate of PBDEs within a soil/water-plant system in the presence of copper (Cu) and to determine the underlying mechanism of PBDEs uptake by corn within a defective root system. The study provides new information regarding the PBDE uptake mechanism in plants and will therefore improve the environmental risk assessment of metal-POPs cocontaminated environments.
nutrient solution was renewed every 2 days and aerated twice each day. After 2 weeks of cultivation, uniform seedlings were pretreated with CuSO4·5H2O solution for 2 days, and the four treatments had the following Cu concentration: 0.32 μmol/L (Control), 100 μmol/L (Cu100), 200 μmol/L (Cu200), and 400 μmol/L (Cu400). All the pretreated plants were then placed in Hoagland solution containing 0.04 mg/L BDE209 or 0.04 mg/L BDE47 for 3 days. To evaluate the impacts of root damage on PBDEs penetration and translocation, another hydroponic treatment was carried out to pretreat the corn seedlings with hot water, as detailed in the Supporting Information (SI). Pot Experiment. Loamy soil (pH = 6.4, organic matter = 1.8%) without detectable PBDEs was air-dried, sieved through a 2 mm mesh and then blended thoroughly with BDE209. Subsequently, the BDE209-spiked soil was dosed with five concentrations of Cu (as Cu2(OH)2CO3), and the four treatments (Control, Cu400, Cu800, and Cu1600) containing Cu concentrations of 0, 400, 800, and 1600 mg/kg soil dry weight (DW) in each pot, respectively. Each treatment was composed of three replicates. Afterward, the soil was covered with aluminum foil, stirred for 30 min every day, and then homogenized for 1 month at room temperature to allow the contaminants to equilibrate. BDE209 in mixed soil was analyzed at the end of equilibration, with a final concentration of 3 mg/kg soil DW. Four corn seedlings were then transplanted into individual ceramic pots containing 2 kg soil. During the cultivation period (60 days), deionized water was sprayed to compensate for water loss, and the soil moisture was maintained at 60% of its water holding capacity. Sampling. Plants were harvested at the end of cultivation. Shoots and roots were separated, washed with tap water, and rinsed with deionized water. A portion of the fresh roots were used to analyze electrolytic leakage. The remaining roots and all shoots were freeze-dried, measured for biomass, ground to a fine powder and stored in a freezer until later analysis. Passive air samplers (PAS), containing a polyurethane foam (PUF) disk (14 cm diameter, 1.2 cm thickness, and 0.035 g/cm3), were used to measure the atmospheric deposition of PBDEs and estimate the evaporation of PBDEs from the soil/ water to air during the entire cultivation period. Two samplers were hung over the ceiling of the greenhouse where the pot and hydroponic experiments were carried out, and another two samplers were placed 400 m away from the greenhouse. Detailed descriptions of the setup have been provided previously.25 Chemical Analysis. PBDE Analysis. Approximately 0.5 g plant samples, prehomogenized in 3.0 g anhydrous sodium sulfate, or PUF disks were spiked with the surrogate standards (polychlorinated biphenyl 30 (PCB30), PCB198, and PCB209, 5 ng/μL, 4 μL) and extracted using hexane/acetone (3:1, v/v) for 72 h. Briefly, the fractionated extracts of plants and PUF disks were concentrated to ∼0.5 mL after solvent exchange to hexane. The extracts of plants (prewashed with sulfuric acid) and PUF disks were cleaned-up using a multilayer column containing, from bottom to top, neutral alumina (3% deactivated), neutral silica gel (3% deactivated), 50% (w/w) sulfuric acid-silica gel, and anhydrous Na2SO4, with an eluent of 20 mL hexane/DCM (1:1, v/v). After evaporating to about 50 μL volume, 13C PCB141 was added as an internal standard before instrumental analysis. A procedural blank, a solvent blank with the surrogate and internal standards, and a duplicated sample were run with each
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EXPERIMENTAL SECTIONS Chemicals. Generally, in most environments matrices, such as sediment, sewage sludge, and air, the dominant PBDE congeners are BDE209 and BDE47. BDE47 is also the predominant congener detected in fish, wildlife, and human samples, including blood, milk, and fat.24 Hence, BDE209 and BDE47 were selected for investigation in this study. Standards (99% purity) of BDE209 and BDE47 were purchased from Sigma (St. Louis, MO, U.S.A.). Stock solutions of BDE209 and BDE47 were prepared in isooctane at 1.0 mg/mL. Working solutions of BDE209 and BDE47 were prepared by gradual dilution of the stock solution with acetone. All standards and solutions of BDE209 and BDE47 were stored in amber glass vials at 4 °C. Analytical reagent grade CuSO4·5H2O and Cu2(OH)2CO3 were obtained from JinKe Chemicals (Shanghai, China). Exposure to PBDEs and Cu. Corn seeds (Zea mays L. cv. Nongda 108) were surface sterilized with 0.5% NaClO, rinsed thoroughly with deionized water and then germinated for 2 days. Hydroponic Experiment. Ten seedlings were placed in a pot (2.5 dm3) containing one-half Hoagland nutrient solution and then changed to total Hoagland nutrient solution after 1 week.20 All of the pots were placed in a greenhouse with natural light and a day/night temperature of 25−30/15−18 °C. The B
DOI: 10.1021/acs.est.5b04030 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
Figure 1. Biomass of corn grown in pot (A, BDE209) and hydroponically (B, BDE47 and C, BDE209). The Cu concentration for Control, Cu100, Cu200 and Cu400 is 0.32, 100, 200, and 400 μmol/L respectively in hydroponic treatment. The Cu concentration of Control, Cu400, Cu800, and Cu1600 is 0, 400, 800, and 1600 mg/kg soil DW in pot treatment. Values are means ± SD (n = 3). Bars with different letters within the same plant tissue indicate a significant difference based on LSD (p-value
