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Environmental Processes
Uptake Kinetics, Accumulation and Longdistance Transport of Organophosphate Esters in Plants: Impacts of Chemical and Plant Properties Qing Liu, Xiaolei Wang, Rongyan Yang, Liping Yang, Binbin Sun, and Lingyan Zhu Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b07189 • Publication Date (Web): 03 Apr 2019 Downloaded from http://pubs.acs.org on April 3, 2019
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Uptake Kinetics, Accumulation and Long-distance Transport of
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Organophosphate Esters in Plants: Impacts of Chemical and
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Plant Properties
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Qing Liu, Xiaolei Wang, Rongyan Yang, Liping Yang, Binbin Sun, Lingyan Zhu*
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Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of
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Education), Tianjin Key Laboratory of Environmental Remediation and Pollution
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Control, College of Environmental Science and Engineering, Nankai University,
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Tianjin 300350, P. R. China
10 11 12 13 14 15 16 17 18 19 20 21
To
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+86-22-23500791. Fax: +86-22-23500791.
whom correspondence should be addressed. E-mail:
[email protected]. Phone:
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ABSTRACT
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The uptake, accumulation and long-distance transport of organophosphate esters
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(OPEs) in four kinds of plants were investigated by hydroponic experiments. The
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uptake kinetics (k1,root) of OPEs in plant roots were determined by the binding of
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OPEs with the proteins in plant roots and apoplastic sap for the hydrophobic
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compounds, while correlated well with the transpiration capacity of the plants for the
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hydrophilic compounds. However, the accumulation capacity of OPEs in plant root
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was controlled by the partition of OPEs to plant lipids. As a consequence, OPEs were
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taken up the fastest in wheat root due to its highest protein content, but least
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accumulated due to its lowest lipid content. The translocation factor (TF) of the OPEs
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decreased quickly with the hydrophobicity (log Kow) increasing, suggesting that the
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hydrophobic OPEs were hard to translocate from roots to shoots. The hydrophilic
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OPEs, such as tris(2-chloroisopropyl) phosphate (TCPP) and tris(2-butoxyethyl)
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phosphate (TBOEP) were ambimobile in the plant xylem and phloem, suggesting that
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they could move to the edible parts of plants and enhanced risk to human health.
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KEYWORDS: organophosphate esters (OPEs), uptake, accumulation, translocation,
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different plants
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Introduction
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Organophosphate esters (OPEs) have been widely used as plasticizers and flame
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retardants in many industrial and household products for decades due to their
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excellent physicochemical properties.1 Since brominated flame retardants (BFRs)
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such as polybrominated diphenyl ethers (PBDEs) were regulated all over the world,
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production and consumption of OPEs display a rapid increase trend.2 All OPEs share
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a common phosphoric acid unit with different functional and polar groups (alkoxy-,
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alkyl-, aryl- and halogenated). As a consequence, OPEs have very different
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physiochemical properties and their hydrophobicity (log Kow) spans a wide range of
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1.63 - 9.49.3 OPEs are mainly used as additives in lots of commercial products and are
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liable to escape from the applied products and release to the environment.4 It was
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reported that many OPEs could induce toxic effects on embryonic development,
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thyroid hormone secretion, immune, neurological and metabolic systems of biota and
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human.5-12 The halogenated OPEs, such as tris(2-chloroethyl) phosphate (TCEP),
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tris(2-chloroisopropyl) phosphate (TCPP), and tris(1,3-dichloro-2-propyl) phosphate
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(TDCPP), were considered to be carcinogenic.13 Because of the increasing
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applications and potentially adverse effects, many concerns are raised on the
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occurrence, distribution and behaviors of OPEs in the environment.
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In the past decades, OPEs were detected frequently in various environmental
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compartments such as drinking water,14 sea water,15 sediment,16 soil,17 air,18 dust19
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and biota,20-22 and soil could be one of the major sinks of OPEs in the environment.23,
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24
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matrices, TCPP, triphenyl phosphate (TPHP), tris(2-butoxyethyl) phosphate (TBOEP)
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and tris(2-ethylhexyl) phosphate (TEHP) were among the most frequently detected
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OPE compounds. 18, 19, 25, 26 High concentration of OPEs was reported not only in the
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soil near e-waste treatment plants,27,
Although the most predominant OPEs could vary in different environmental
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but also in urban soils.17 The total
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concentration of eight OPEs in the soil near an e-waste treatment plant, which was
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located in in Hebei Province, China, was 38-1250 ng/g dry weight (dw), and TCPP,
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TPHP, TBOEP and TEHP were also the most predominant OPEs.28 There were
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evidences that OPEs could transfer from the contaminated soil to plants, which could
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finally enter human body via food chain and cause adverse effects to human.28, 29
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Bioaccumulation of non-ionic organic chemicals in plant is mainly depended on
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the lipid content of plant tissues.30-32 Lipid is regarded as the major reservoir for
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non-ionic organic chemicals in plants, especially for strong hydrophobic organic
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compounds.33 There are a few studies investigating plant accumulation of OPEs. One
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of the studies demonstrated that OPEs could bind with non-specific lipid transfer
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proteins (nsLTPs) and then were absorbed by plant roots.34 A positive correlation was
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observed between the bioaccumulation factors (BAFs) of OPEs and the tissue lipid
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contents in adult zebrafish (Danio rerio), suggesting that lipid played a critical role in
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accumulation of OPEs in animals.35 Against this result, other studies demonstrated
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that the accumulation of OPEs was not basically associated with the lipids contents in
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fish.22, 36 It remains unclear the critical roles of proteins and lipids in the uptake and
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accumulation of OPEs in plants. After absorption from soil solution, organic
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pollutants could transport to the above ground parts of plants via xylem.37, 38 It was
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reported that transport via phloem also took place for some organic pollutants, such as
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herbicides chlorsulfuron and clopyralid.39 Phloem carries carbohydrates from leaves
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to roots, and moves proteins and other substances to buds and fruits.40 As a
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consequence, these organic pollutants are ambimobile39 (mobile in both the xylem and
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phloem) and experience long-distance transport in plants, leading to their
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accumulation in the edible parts of plants and enhanced risk to human health. Until
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now, there is very sparse information about the long-range transport of OPEs in
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plants.
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Plant uptake, accumulation and translocation of OPEs could be correlated to the
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properties of both OPEs and plant species. In this study, four OPEs with different
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substituent groups (TCPP, TPHP, TBOEP and TEHP), which are also the most
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frequently detected with high concentration in the environment, were chosen as target
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OPEs. A hydroponic system was set up to explore the uptake, accumulation behaviors
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and long-distance transport of the OPEs in four kinds of plants. Wheat (Triticum
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aestivum L.), mung bean (Vigna radiata L. Wilczek), carrot (Daucus carota L. var.
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sativa Hoffm.), and lettuce (Lactuca sativa L.) were used as test plants, considering
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that carrot and lettuce have different edible parts, and wheat and mung bean are often
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used as model plants for investigating the bioavailability of organic pollutants. Uptake
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and depuration experiments were performed to assess the transport and distribution of
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the OPEs in these plants. Protein and lipid contents, as well as transpiration capacities
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of the plants were determined in order to investigate their critical roles in the plant
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uptake and transport.
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MATERIALS AND METHODS
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Chemicals and Regents
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TPHP (99%) and TBOEP (98%) were purchased from J & K Scientific Ltd.
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(Beijing, China). TEHP (>95%) was bought from Tokyo Chemical Industry Co,. Ltd.
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(Shanghai, China). TCPP (mixtures of isomers, 98%) was obtained from Macklin
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Biochemical Technology Co., Ltd. (Shanghai, China). The properties of OPEs are
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listed in Table S1 of the Supporting Information (SI). Deuterated tributyl phosphate
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(d27-TnBP, 98 - 99%) was obtained from Cambridge Isotope Laboratories
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(Tewksbury, MA, USA). Deuterated tris(2-chloroethyl) phosphate (d12-TCEP, 99%)
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and deuterated triphenyl phosphate (d15-TPHP, 99%) were bought from Toronto
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Research Chemicals Inc. (Toronto, Ontario, Canada). All the deuterated OPEs were
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used as surrogates. Dichloromethane (DCM, HPLC-grade) was purchased from
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Merck Chemicals (Shanghai) Co., Ltd. HPLC-grade hexane, acetonitrile (ACN) and
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methanol came from Fisher Scientific Co. (Fair Lawn, NJ, USA). HPLC-grade
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dimethyl sulfoxide (DMSO), formic acid and GCB/NH2 cartridges (500 mg/500 mg, 6
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mL) were purchased from Anpel (Shanghai, China). Envi-18 cartridges (500 mg, 6
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mL) were purchased from Sigma-Aldrich (St. Louis, MO, USA).
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Plant exposure and depuration experiments
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All the plant seeds were purchased from Tianjin Academy of Agricultural
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Sciences (Tianjin, China). The seeds were sterilized in 6% (w/w) H2O2 solution for 15
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min, then washed with Milli-Q water 3 times, and subsequently germinated on sterile
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moist filter paper in the dark at 22 - 26 °C for 5 d. After germination, seedlings with
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uniform size were selected and transferred to glass beakers containing nutrient
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solution, which was adjusted to pH 6.5 and sterilized at 115 °C for 30 min (25%
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strength modified Hoagland’s nutrient, SI Table S2) for cultivation. The seedlings
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were cultivated with 16 h light/8 h dark cycle at a relative humidity 60 - 70%. After
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appearance of the forth true leaf, all the plants were transferred to 250 mL autoclaved
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glass beakers containing 200 mL of sterile nutrient solution for exposure, with one
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plant per beaker. The individual standard solutions were added to the sterile nutrient
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solution to get a mixed exposure solution with each compound at a nominal
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concentration of 20 μg/L. The initial concentrations of TCPP, TPHP, TBOEP and
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TEHP in the exposure solution were determined with an ultra-high performance liquid
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chromatography
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(UPLC-MS/MS, see details in the below part), and they were 24.2 ± 0.5, 20.9 ± 0.9,
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18.5 ± 2.1, and 16.7 ± 0.2 μg/L (n=3), respectively. Each beaker was covered with a
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lid, and sealed with aluminum foil and parafilm to prevent photolysis of OPEs in the
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solution. The beakers were positioned randomly and re-randomized every day. The
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spiked exposure solution was renewed every 48 h to keep the exposure concentration
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constant, and the exposure lasted for 144 h. Three plants were sampled randomly at 3,
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6, 12, 24, 48, 96 and 144 h. Unplanted control (with OPEs but without seedlings) and
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blank control (with seedlings but without OPEs) were set up in parallel with the test
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groups. At the end of the exposure experiments, all the remaining plants were
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removed from the beakers, and the roots were washed with sterilized Milli-Q water.
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Then, the plants were transferred to clean sterile nutrient solution for depuration
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experiments. The nutrient solution was renewed daily. The plants were sampled at 12,
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24 and 72 h. All the treatments were performed in triplicate. All the plant samples
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were divided into two parts: root, and shoot which contained the stems and leaves.
tandem
electrospray-triple
quadrupole
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Split-root exposure experiments
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Wheat was selected for the split-root test because it is a fibrous root plant among
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the four test plants. The split-root experiment was conducted in two glass tubes (A
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and B) and the set-up is shown in Figure S1. The glass tube A was added with 20 mL
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of sterile 25% strength modified Hoagland’s nutrient, and the glass tube B contained
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the same volume of nutrient solution spiked with the target OPEs at 20 μg/L. The
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roots of wheat were manually separated into two parts and carefully placed in the two
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tubes. The seedlings were harvested at 4, 12, 24, 48 h, and the OPE contents in the
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roots and solutions in both A and B tubes, and the shoots were determined. Similarly,
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unplanted control and blank control were set up simultaneously, and all of the
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treatments were performed in triplicate.
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Sample preparation
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Upon sampling, the plant roots were thoroughly washed with deionized water
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three times and wiped with filter paper. In the split-root experiment, the rinsing water
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was collected and combined with the original solutions. All the sampled plants were
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freeze-dried at -50 °C for 24 h in a lyophilizer, homogenized and weighed, then stored
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at -20 °C before analysis. The solution samples were extracted immediately after
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sampling. The extraction and following cleanup procedures for the plant samples were
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in accordance with a previous study with minor modifications36, 41 and the details are
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described in SI. Briefly, 0.01 g (dw) of root samples and 0.02 g of shoot samples were
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spiked with 20 ng of d27-TnBP, d15-TPHP and d12-TCEP as surrogates. The samples
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were subjected to ultrasonic extraction with ACN. After dried by N2 and re-dissolved
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in 2 mL of hexane, the samples were cleaned up using GCB/NH2 cartridges.
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The solution samples were extracted and cleaned up according to a previous
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work.42 A 200 mL of solution was extracted with Envi-18 cartridge and then eluted
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with 12 mL of DCM/ACN mixture [1:4 (v/v)]. The collected solution was evaporated
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under a gentle stream of N2 to dryness, and reconstituted in 1 mL of ACN.
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The final extracts of both plant and solution samples were centrifuged at 13000
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rpm for 20 min at 4 °C. The supernatant was subjected for analysis by UPLC-MS/MS.
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Instrumental analysis
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The analysis of OPEs was performed according to a previous study.43 The OPEs
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were analyzed on UPLC-MS/MS (Xevo TQ-S, Waters, Milford, MA, U.S.A.) and
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separated on a BEH C18 column (2.1 mm × 50 mm, 1.7 μm, Waters) coupled with a
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VanGuard precolumn (C18 column, 2.1 mm × 5 mm, 1.7 μm) with Milli-Q water (A)
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and ACN (B) both containing 0.1% formic acid as mobile phase. The injection
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volume was 10 μL, the flow rate was 0.4 mL/min, and the column temperature was
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55°C. Electrospray ionization was operated in positive mode, and multiple reaction
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monitoring (MRM) was used for all analysis. More details of the analytical method
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are provided in the SI, and the mass spectrometer operational parameters and
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quantification ion transitions for each OPEs are listed in Table S3.
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Determination of transpiration capacity, protein and lipid contents in plant roots
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and shoots
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The transpiration capacities of the plants were measured by the weight change of
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the nutrient solution after one day, from which the water evaporation in the control
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was subtracted.44 The protein contents in fresh plant roots and shoots were determined
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according to the method of Bradford assay with some modifications.45 The protein
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contents in the root apoplastic solution were measured following a previous study.46
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Lipid contents in the dried roots and shoots were determined by weight difference.47
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More detailed information about the transpiration capacity, protein and lipid
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determination is provided in Table S8.
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Quality assurance and quality control
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To avoid sample contamination, all glass beakers and tubes were soaked in K2Cr2O7 -
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H2SO4 solution, and washed with Milli-Q water and acetone before used. For OPE
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analysis on UPLC-MS/MS, quality control was performed by regular injection of
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solvent blanks and standards, and none of the target OPEs were detected in the solvent
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blanks. External standard method was used to quantify the concentrations of OPEs.
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The R2 of the standard curves of OPEs were all > 0.99. The recoveries of the four
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OPEs and surrogate standards were assessed by spiking the standards in the nutrient
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solution and plant tissue samples at two levels. All of them were in the range of 72.3 -
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124% (n = 3) (Table S4). Recoveries of the surrogate standards were 60.7 - 84.4% for
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d27-TnBP, 63.7 - 93.0% for d15-TPhP, and 70.0 - 104% for d12-TCEP, respectively.
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The method detection limits (MDLs) were defined as 3 times of the signal to noise
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ratio. The concentrations less than the MDLs were labeled as none detectable (ND).
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The MDLs were in the range of 0.013 - 16.5 ng/L for the solutions and 0.07 - 0.306
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ng/g for plant tissues, respectively (Table S4). The OPE concentrations in the spiked
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solution (Table S5) did not show distinct change during the 48 h exposure. Thus, the
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exposure solution was renewed every two days to ensure constant exposure
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concentrations. The concentrations of OPEs in the unspiked plant controls after
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exposure are listed in Table S6. Only TCPP and TBOEP were detected in mung bean
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and lettuce samples, and their concentrations were less than 0.1% of the
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corresponding concentrations in the exposed plants. The blank concentrations were
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subtracted from the exposed groups. In the split-root experiment which lasted only 48
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h, no OPEs were detected in the blank controls (Table S6).Bioaccumulation factors
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and data analysis
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The uptake kinetics of OPEs was fitted with a first-order one-compartment
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model.
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Ctissue(t) = Ctissue,eq(1 - e - k1,tissuet)
(1)
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where Ctissue (t) is the tissue concentration of OPEs at time t (ng/g dw), Ctissue, eq is
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the tissue concentration (ng/g dw) at accumulation equilibrium, and k1,tissue is the tissue
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uptake rate constant (h-1). The k1,root and k1,shoot represent the root and shoot uptake rate
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constants respectively.
234 235
Root depuration kinetics was fitted by a one-phase decay model. (2)
Ctissue(t) = (C0 - Y) × e - k2,tissuet+Y
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where C0 is the root concentration before depuration (ng/g dw), Y is the plateau
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concentration (ng/g dw), and k2,tissue is the tissue elimination rate constant (h-1). The
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k2,root and k2,shoot represent the root and shoot elimination rate constants, respectively.
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Depuration half-life (t1/2) was calculated using the following equation: (3)
t1/2 = ln2/k2, tissue
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RCF ((ng/g root)/(ng/mL solution)), shoot concentration factor (SCF, (ng/g
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shoot)/(ng/mL solution)), and TF ((ng/g shoot)/(ng/g root)) were calculated according
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to Eqs. (4) - (6), respectively.
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logRCF = logCroot, eq/Csolution
(4)
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logSCF = logCshoot, eq/Csolution
(5)
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TFs = Cshoot, eq/Croot, eq
(6)
Where Croot, eq, Cshoot,
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eq
are the tissue concentrations at equilibrium (ng/g dw).
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Csolution is the concentration of OPEs in the exposure solution. All statistical analysis
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were conducted with the software SPSS 19.0. The means and standard deviations
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were calculated based on triplicate measurements. One-way analysis of variance
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(one-way ANOVA) followed by least significant difference (LSD) was used to
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examine significant differences between values. A linear regression was used to
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derive the relationships among variables. Statement of significant difference is based
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on P < 0.05.
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Roots uptake and elimination kinetics of OPEs
RESULTS AND DISCUSSION
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During the exposure period, the OPE concentrations in the plant roots increased
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rapidly and reached equilibrium within 12 - 48 h (Figure 1; Table S7). Among the
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four plants, the uptake rate constant (k1,root) was in the range of 0.11 - 0.54 h-1, and
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TCPP displayed the slowest k1,root value (0.11 - 0.22 h-1), while TEHP displayed the
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fastest uptake rate which was significantly different from other three OPEs (Figure
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S2), the k1,root of which was about 2 - 4 times higher than that of TCPP (Table S7).
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The k1,root values of the four OPEs (Table S7) increased in the order of TCPP, TBOEP,
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TPHP and TEHP, which was in line with the order of their log Kow values. For all the
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plants, there was a significantly positive linear relationship between the k1,root and log
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Kow of the OPEs (Figure S3; P < 0.05). Three main pathways are relevant for root
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uptake: transmembrane (between cells through cell walls and membranes), symplastic
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(between cells through interconnecting plasmodesmata) and apoplastic (along cell
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walls through the intercellular space).48 The quick uptake equilibrium and the fact that
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the accumulation data fitted well the one-compartment model indicated that the plant
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roots took-up OPEs mainly through adsorption of OPEs to root epiderm, and followed
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by an apoplastic absorption.49 Although not in a linear relationship, the log RCFs
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increased distinctly with the log Kow values increasing (Figure S4), which was in
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accordance with previous studies.39,
275
4.70, the log RCF increased rapidly with log Kow increasing; as log Kow increased over
276
4.70, the increasing trend became slower. These results suggested that hydrophobicity
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of a compound was a critical factor determining its accumulation capacity in plants.
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The compounds with higher hydrophobicity might be easier to partition to root
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organic constituents, particularly root lipids.25, 45, 46
45
As the log Kow of the OPEs was lower than
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The uptake and accumulation of OPEs in the plant roots were distinctly
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dependent on the plant categories. For all the four OPEs, although they displayed the
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fastest uptake rates in wheat, they showed the minimum log RCFs in wheat. The
283
different trends in uptake kinetics and accumulation capacities suggested that they
284
were controlled by different properties of the plant roots.
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The transpiration capacity, protein and lipid contents in the plants are shown in
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Table S8. Transpiration is one of the key driving forces for absorption of water and
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solutes by plants. Studies showed that systemic pesticides were passively taken up
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through the transpiration stream,50 and greater transpiration led to increased uptake
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and accumulation of non-ionic compounds.51 To illustrate the impacts of transpiration
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capacity, protein and lipid contents on the uptake (Figure 2(a)) and accumulation
291
(Figure 2(b)) of the OPEs in plant roots, principal component analyses (PCA) were
292
performed. The grouping of the different parameters in Figure 2(a) and 2(b) was
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based on the correlations among the various parameters.52 Figure 2(a) shows that the
294
k1,root of TCPP and TBOEP and transpiration capacity of the plants were grouped
295
together, while TPHP and TEHP were in another group with the protein contents.
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Since TCPP and TBOEP are more soluble with relatively lower log Kow values (< 3),
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their grouping with transpiration suggested that transpiration was a key driving force
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for uptake of more hydrophilic compounds by the plant roots (Figure S5). The k1,root
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values of TPHP and TEHP deviated from the transpiration capacity, but were close to
300
the protein contents in the roots and apoplastic sap (Figure 2(a)), which was more
301
significant for TEHP (Figure S6). These indicated that proteins in plant roots and
302
apoplastic sap played an important role in the uptake of hydrophobic OPEs. There are
303
large amount of proteins in plant apoplast, including non-specific lipid transfer
304
proteins (nsLTPs). The plant nsLTPs are extracellular proteins, which can bind with
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phospholipids and promote them to transfer in plants.53 It was reported that OPEs with
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higher hydrophobicity were more liable to bind with TaLTP1.1, which is one of the
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most important nsLTPs in wheat, leading to their great uptake rate in wheat roots.34 In
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Figure 2(b), the log RCFs of the four OPEs grouped with the root lipid contents but
309
deviated from the protein contents and transpiration capacities, indicating that
310
partition to lipid controlled the accumulation of OPEs in plant roots (Figure S7).
311
Based on these results, it was assumed that OPEs were taken up and absorbed by plant
312
roots via two mechanisms. For the compounds with low hydrophobic, they were
313
mainly taken up through the transpiration stream. For the OPEs with greater
314
hydrophobicity, they could be taken up by binding with the proteins such as nsLTPs
315
in plant roots.53 The proteins carried OPEs to root lipid constituents (membrane and
316
storage lipids), where the OPEs were finally accumulated.
317
During the 72 h depuration process, the elimination of the four OPEs followed an
318
exponential decay model, and elimination rate of TEHP was slower than other three
319
OPEs in all the plants (Table S9; Figure S2). There are two major pathways for plant
320
root to eliminate the accumulated contaminants: biodegradation and mass transfer
321
from roots to the surrounding solution or upward.54 It was reported that chlorinated
322
OPEs were difficult to be degraded,34 suggesting that TCPP in the plant roots was
323
eliminated mainly via release to the solution or translocate to above-ground tissues.
324
The half-life of TEHP was in the range of 29.6 to 63.6 h-1, much longer than other
325
OPEs (Table S9). Since TEHP has the strongest hydrophobicity with a log Kow of
326
9.49, it was more liable to partition to root lipid constituents. As a consequence, it was
327
hard for TEHP to desorb and release to the external environment. Hydrolysis and
328
oxidation might take place in plant roots, which perhaps made a partial contribution to
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the elimination of the non-chlorinated OPEs, such as TEHP, TBOEP and TPHP.34
330
Shoot uptake, elimination and accumulation of OPEs
331
There are two main pathways for shoot uptake of organic chemicals: leaf
332
absorption of volatile contaminants from the air, and translocation from plant root.51
333
As listed in Table S1, the four target OPEs all have low vapor pressures, suggesting
334
that they were difficult to volatilize from the exposure solution to the air, and
335
translocation by xylem could be the prevalent source of the OPEs in the shoot. As
336
shown in Figure S8, it took longer time for the OPEs to reach equilibrium in shoots,
337
typically >24 h, than in the corresponding roots. This provided another evidence that
338
the OPEs in the shoots mainly originated from the roots. The k1,shoot, values of the four
339
OPEs in the plant shoots were in the range of 0.18 to 0.51 h-1 (Table S7) with those of
340
TCPP and TBOEP significantly higher than TPHP and TEHP (Figure S2). As shown
341
in SI Figure S9, the transpiration and k1,shoot values of TCPP, TBOEP and TPHP
342
grouped together in the PCA component plot, indicating that OPEs could be
343
transported from roots to shoots by transpiration flow. The plants with stronger
344
transpiration capacity would translocate OPEs more efficiently from roots to shoots.
345
The TFs of TCPP and TBOEP were significant higher than those of TPHP and TEHP
346
in the same plants (Figure 3(a), P = 0.005). There was a negative correlation between
347
the log SCF and log Kow values of the OPEs in the plant aerial parts (Figure 3(b)), and
348
the log SCF of TEHP was extremely low (0.23 - 0.60). These results suggested that
349
OPEs with higher log Kow values were more difficult to transport to above-ground
350
tissues via xylem. Prior to entry in the vascular cylinder, compounds in roots have to
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cross the Casparian strip,48 which is composed of lignin and lamellar suberin,55, 56 and
352
acts as a hydrophobic barrier between the apoplast (the extracellular space in the
353
epidermis) and vascular tissue.57 Compounds taken up solely via apoplastic route
354
cannot cross the Casparian strip, but have to cross at least one lipid bilayer to enter
355
xylem or phloem. Transport is greatest for the compounds with log Kow in the range of
356
1-3, which are more liable to cross the Casparian strip.51 TCPP displayed the highest
357
TF among the four target OPEs, implying that it easily crossed the Casparian strip,
358
and moved to the shoot. Although with extremely low TFs, TPHP and TEHP were
359
still found in the shoots (Table S7), suggesting that they could slightly pass through
360
the root apex and move to the stele, with subsequent transport to the shoots via xylem.
361
The Casparian strip at the root apex was not yet fully developed, allowing a small
362
amount of hydrophobic organic compounds to pass through pericycle and then
363
translocate via xylem.58 In another aspect, xylem sap contains a variety of proteins59,
364
60
365
such as dieldrin (log Kow = 5.4), from roots to shoots.61 Thus, a small portion of TPHP
366
and TEHP may bind with the proteins in xylem sap and transport to the shoots via
367
transpiration stream. The log SCFs of OPEs increased with the increase of shoot lipid
368
contents, but not at significant level (P > 0.05, Figure S10). This implied that
369
accumulation of OPEs in shoots could be affected by other factors besides the shoot
370
lipid contents.
which were evidenced to facilitate translocation of hydrophobic organic pollutants,
371
Elimination of OPEs from the shoots was very fast, and about 50% of the
372
accumulated OPEs in the shoots were eliminated during 72 h depuration process.
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Three major pathways are related to elimination of organic contaminants in plant
374
shoots: volatilization through stomata, biodegradation, and transport downward via
375
phloem. Volatilization might be negligible due to the low-volatility of the OPEs. As
376
discussed above, the compounds with greater hydrophobicity, such as TPHP and
377
TEHP, were hard to translocate in the plants due to their strong partition affinity to
378
lipid materials in the plants.52 Biodegradation might account for their elimination in
379
the plant shoots.34 As a chlorinated OPE, TCPP also displayed a fast elimination rate
380
(t1/2 < 22 h). Thus, it was suggested that TCPP could undergo transport downward
381
from shoot to root via phloem, which is another elimination pathway for organic
382
pollutants in plant shoots.
383
Phloem based transport of OPEs in plants
384
The split-root experiment was used to investigate the long-distance transport of
385
chemical in the plants. The mass balance of the OPEs after 48 h of exposure is shown
386
in Figure 4, and 72.2% (TPHP) to 91.5% (TCPP) were recovered.
387
It was reported that TCPP was observed in strawberry fruits (Fragaria
388
ananassa),62 which provided an evidence that TCPP could transport via phloem. As
389
shown in Figure 4(a) and (b), TCPP (about 5.2%) and TBOEP (about 3.9%) were
390
found in the wheat roots in the unspiked solution after 48 h. Since no TCPP or
391
TBOEP was detected in the blank control samples, this testified that TCPP and
392
TBOEP could experience long distance transport via phloem from the shoot to root. It
393
is reported that phloem represents an important translocation pathway for many
394
herbicides.39 It was extremely hard for TPHP and TEHP to transport from shoots back
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to roots via phloem (Figure 4(c) and (d)) because of their high log Kow and strong
396
binding affinity with lipids. The results suggested that highly hydrophilic compounds
397
were ambimobile (mobile in both xylem and phloem). The direction of phloem
398
transport can be either up or down, depending on where the source and sink are
399
relative to each other.63 In the case of heavily polluted soil, TCPP and TBOEP could
400
be absorbed by plant roots, and translocated to the edible tissues. Interestingly,
401
approximately 3.0% of TCPP was detected in the unspiked nutrient solution,
402
demonstrating that TCPP could easily pass through the Casparian strip and even cell
403
membrane, and release to ambient environment. Similar to its uptake process, TCPP
404
releasing might be mainly driven by passive partitioning process.64
405 406
ASSOCIATED CONTENTS
407
Supporting Information
408
Additional tables, figures and experimental details regarding extraction and
409
analytical methods of OPE congeners, the assay method of plant transpiration, protein
410
and lipid contents, the relationship between different parameters.
411
412 413 414
AUTHOR INFORMATION Corresponding Author *Phone: +86-22-23500791; fax: +86-22-23500791; e-mail:
[email protected].
415
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ACKNOWLEDGMENTS
417
We gratefully acknowledge financial support from the Natural Science
418
Foundation of China (NSFC 21737003, 21577067 and 21677081), the 111 program,
419
Ministry of Education, China (T2017002), Tianjin Municipal Science and Technology
420
Commission (16PTSYJC00020, 17JCYBJC23200) and Yangtze River scholar
421
program.
422 423
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Figure Captions:
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Figure 1. Uptake and depuration kinetics of the OPEs in the roots (a) carrot, (b) mung
656
bean, (c) lettuce and (d) wheat during 216 h experiments. Error bars
657
represent standard deviation values (n = 3). The dotted line represents the
658
switch between uptake and depuration phases.
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Figure 2. Principal component analysis (PCA) loading plots of (a) root uptake rate
660
constant (h-1); (b) log RCF and different parameters in the roots. K1 - K4
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and R1 - R4 represent root uptake rate constant and log RCF of TCPP,
662
TPHP, TBOEP, and TEHP, respectively. P1 and P2 represent protein
663
content in apoplastic sap and root whole protein content. T1 and L1
664
represent transpiration capacity and root lipid content.
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Figure 3. Relationships between the (a) TF; (b) log SCF values and log Kow values of OPEs in different plant treatments. Figure 4. Mass balance of the OPEs in the 48 h split-root experiment. (a) - (d) represent TCPP, TBOEP, TPHP, and TEHP, respectively.
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Figure 1
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Figure 2
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Figure 3
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Figure 4
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Table 1. The root concentration factors (RCFs), shoot concentration factors (SCFs) and translocation factors (TFs) of the OPEs in the four plants. Carrot Compounds
Log
Log
RCF
SCF
TCPP
1.88
1.42
TPHP
3.08
TBOEP TEHP
Mung bean Log
Log
RCF
SCF
3.3×10-1
1.90
1.54
1.02
9.0×10-3
3.33
2.21
1.35
1.4×10-1
3.43
0.23
6.0×10-4
TF
Lettuce Log
Log
RCF
SCF
4.4×10-1
2.15
1.45
1.23
1.0×10-2
3.25
2.66
1.49
7.1×10-2
3.51
0.60
1.2×10-3
TF
Wheat Log
Log
RCF
SCF
2.0×10-1
1.44
1.18
5.5×10-1
1.10
7.2×10-3
2.74
0.57
7.0×10-3
2.38
1.50
7.9×10-2
1.78
1.61
5.4×10-1
3.37
0.37
1.0×10-3
3.07
0.23
1.4×10-3
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TF
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