Environ. Sci. Technol. 2009, 43, 324–329
Chemical Hydrophobicity and Uptake by Plant Roots ERIK M. DETTENMAIER,† W I L L I A M J . D O U C E T T E , * ,† A N D BRUCE BUGBEE‡ Utah Water Research Laboratory, and Crop Physiology Laboratory, Utah State University, 8200 Old Main Hill, Logan, Utah 84322
Received June 26, 2008. Revised manuscript received October 24, 2008. Accepted October 24, 2008.
The transpiration stream concentration factor (TSCF), the ratio between a compound’s concentration in the xylem to that in the solution adjacent to the roots, is commonly used to describe the relative ability of an organic compound to be passively transported from root to shoot. Widely cited bellshaped curves relating TSCF to the octanol/water partition coefficient (log KOW) imply that significant root uptake and transfer into shoot tissues occurs only for compounds falling within an intermediate hydrophobicity range. However, recent laboratory and field data for relatively water soluble compounds such as sulfolane, methyl tert-butyl ether (MTBE), and 1,4dioxane suggest that these relationships are not universally applicable, especially for nonionizable, highly polar, water soluble organics. To re-evaluate the relationship between root uptake and chemical hydrophobicity, TSCFs were measured for 25 organic chemicals ranging in log KOW from -0.8 to 5 using a pressure chamber technique. Using the TSCF values measured in this study, a new empirical relationship between TSCF (0 and 1) and log KOW (-0.8 to 5) is presented that indicates that nonionizable, polar, highly water soluble organic compounds are most likely to be taken up by plant roots and translocated to shoot tissue.
Introduction Predicting the uptake of organic chemicals by roots and transport via the xylem to above ground tissues is critical for conducting risk assessments and determining the potential effectiveness of phytoremediation. The uptake of xenobiotic organic chemicals by roots has long been observed to be passive with the chemicals moving into the plant in proportion to the amount of water transpired (1, 2), that is in return related to factors such as humidity, sunlight, and exposure duration (3, 4). The transpiration stream concentration factor (TSCF) is a ratio of the contaminant concentration in the xylem sap to that in the root-zone hydroponic or soil solution, and has been widely used as a descriptor of chemical uptake by roots (2, 5). Chemicals actively taken up by plants have TSCF values greater than 1.0 (N, P, and K), while those that move into plants at the same rate as water have TSCF values of one. Interactions with the lipid bilayer in root membranes reduce the uptake of organic chemicals relative to water resulting in TSCF values of less than one. Values of TSCF have typically been measured using one * Corresponding author e-mail:
[email protected]. † Utah Water Research Laboratory. ‡ Crop Physiology Laboratory. 324
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of two approaches. In the first approach, plants are exposed to a continuously measured root-zone chemical concentration. A hydroponic environment is generally used for ease in measuring and controlling the exposure concentration. The collection of xylem sap is problematic, so TSCFs are generally determined from measured shoot concentrations normalized to the water transpired during the exposure period. Losses due to metabolism or volatilization within the plant should be corrected for, but these loses are difficult to quantify and the correction is not always made. To circumvent the problem of collecting sufficient xylem sap or the need to extract and analyze the plant tissue, the second approach for measuring TSCF involves sealing the roots of a detopped plant (i.e., the above ground tissues (shoot) are removed) in a pressurized chamber containing a solution of a known concentration of the chemical of interest (6–8). Xylem flow is regulated by creating a pressure difference between the roots and the stem that is similar to intact plants (9). As a result of this pressure difference, the solution moves through root membranes, and the xylem exudate is collected as it exits the cut stem. The pressure should be adjusted to match the transpiration rate of the intact plant (8). Upon reaching steady state, the TSCF is calculated from the xylem concentration to the root exposure concentration. The pressure chamber approach provides sufficient quantities of xylem sap, direct measurement of xylem concentrations, minimal losses due to volatilization and metabolism, and shorter experimental durations. Maintaining root health is critical for ensuring normal membrane integrity. It is particularly important to maintain adequate root-zone oxygenandnutrientsandtoavoidtoxicchemicalconcentrations. Relatively few experimental TSCF values exist, due in part to the cost associated with their determinations and the lack of regulatory requirements for such data. Where data exist for chemicals having more than one literature TSCF, the variability is often relatively large due to the lack of standardized or generally accepted methods. Because of the scarcity of experimental values, estimated TSCFs are widely used in risk assessments. The most widely used estimation approaches are based on empirical relationships between TSCF and the logarithm octanol/water partition coefficient (log KOW). These relationships suggest an optimal hydrophobicity for uptake and translocation and infer that compounds that are either highly polar (log KOW < 1) or are highly lipophilic (log KOW > 4) will not be significantly taken up by plants (5, 7, 10). However, reports of significant plant uptake of highly water soluble, low log KOW compounds such as 1,4 dioxane (11) MTBE (12) and sulfolane (13, 14) suggest that the general suitability of these estimation techniques should be re-evaluated, especially for these types of compounds. Polar, nonvolatiles were also predicted to be the most likely type of organic chemicals transferred from soil to fruit in a recently published fruit tree model (15). Thus, the main objective of this study was to evaluate the relationship between TSCF and log KOW using the pressure chamber technique and develop a more generally applicable relationship that encompasses both hydrophobic and hydrophilic neutral organic compounds. An extensive literature compilation of TSCF values was also used to evaluate the applicability of the resulting relationship and examine the impact of experimental measurement methods on variability of reported TSCF values.
Materials and Methods Experimental Overview. Values of TSCF were determined for 25 organic chemicals (Table 1), using a pressure chamber 10.1021/es801751x CCC: $40.75
2009 American Chemical Society
Published on Web 12/10/2008
TABLE 1. Average Measured TSCF, Reported log KOW (Reference) and Method of Analysis for Compounds Investigateda compound water (3H2O) trichloroethanol 1,4-dioxane N-nitrosodimethylamine methanol sulfolane caffeine methyl tert-butyl ether tert-butyl alcohol chloroform toluene 1,2-dichloropropane benzene 1,2-dichloroethene methylene chloride 1,1,1-trichlorethane carbon tetrachloride trichloroethene 1,1,2,2-tetrachloroethane tetrachloroethene nonylphenol tetraethoxylate nonylphenol phenanthrene nonylphenol nonylethoxylate pentachlorophenol pyrene
CAS no. or formula 7732-18-5 115-20-8 123-91-1 62-75-9 67-56-1 126-33-0 58-08-2 1634-04-4 75-65-0 67-66-3 108-88-3 78-87-5 71-43-2 540-59-0 75-09-2 71-55-6 56-23-5 79-01-6 79-34-5 127-18-4 26027-38-3 84852-15-3 85-01-8 26027-38-3 87-86-5 129-00-0
log KOW
average measured number of plants TSCF exposed /compound STD error
-1.38 (33) 1.42 (33) -0.27 (33) -0.57 (33) -0.77 (33) -0.77 (33) -0.07 (34) 0.94 (33) 0.35 (33) 1.97 (33) 2.73 (33) 1.98 (35) 2.13 (33) 2.09 (33) 1.25 (33) 2.49 (33) 2.83 (33) 2.42 (33) 2.39 (33) 3.4 (33) 3.1* 3.2* 4.46 (34) 3.0* 5.12 (33) 4.88 (34)
1.00 0.99 0.98 0.97 0.88 0.86 0.83 0.82 0.80 0.69 0.64 0.63 0.59 0.51 0.46 0.44 0.44 0.43 0.36 0.30 0.21 0.18 0.15 0.07 0.07 0.04
26 1 6 2 4 3 13 12 4 5 2 8 7 7 1 9 6 10 2 7 2 2 1 1 1 2
0.01 N/A 0.013 0.016 0.008 0.121 0.018 0.034 0.024 0.092 0.073 0.063 0.075 0.076 N/A 0.082 0.053 0.064 0.017 0.056 0.003 0.011 N/A N/A N/A 0.015
analysis method LSC HS/GC/MS HS/GC/MS LSC LSC LLE/GC/FID LLE/HPLC and LSC HS/GC/MS LSC HS/GC/MS HS/GC/MS HS/GC/MS HS/GC/MS and LSC HS/GC/MS HS/GC/MS HS/GC/MS HS/GC/MS HS/GC/MS HS/GC/MS HS/GC/MS LSC LSC LSC LSC GC/ECD LSC
a GC ) gas chromatography, MS ) mass spectrometry, ECD ) electro-conductivity detector, FID ) flame ionization detector, HPLC ) high performance liquid chromatography, LSC ) liquid scintillation counter, LLE ) liquid liquid extraction, HS ) headspace, *measured using slow stir method and 14C-labeled compounds.
technique. The chemicals were selected to cover, or extend, the range of log KOW values used in previously reported TSCFlog KOW relationships (from -0.8 to 5) from a list of compounds for which analytical methods had been previously developed in related projects. Analysis methods depended on the physical properties of the chemical. Volatile compounds were analyzed by headspace gas chromatograph mass spectrometry (GC/MS), polar nonvolatiles by high performance liquid chromatography (HPLC), and 14C-labeled compounds by liquid scintillation counting (LSC). Two plant species, soybean (Glycine max) cv. Hoyt and tomato (Lycopersicon lycopersicum) cv. Red Robin, were evaluated based on their previous use in related uptake studies and our experience with their cultivation. Typically, only one exposure concentration for each chemical was evaluated. The exposure concentration was based on analytical constraints (e.g., 0.002 mg/L for 14C-nitrosodimethylamine, 100 mg/L for sulfolane) and root toxicity. Root toxicity was determined by visual discoloration of the normally white root tips or abrupt changes in root hydraulic conductivity (measured as the flow rate exiting the stem). Since the headspace GC/MS method allowed for the simultaneous determination of multiple volatile compounds, some of the TSCFs were determined by exposing plants to mixtures (three to nine compounds). No competitive sorption was expected given the low exposure concentrations, relatively large root mass, and physical properties of the compounds. The TSCF values for trichloroethene and benzene, measured as part of a mixture using headspace GC/MS and individually as 14C labeled compounds using LSC, were statistically equivalent. Germination and Plant Culture. Soybean seeds were obtained from Utah State Crop Physiology Laboratory, Logan, UT. Tomato seeds were obtained from Tomato Growers Supply Company, Fort Myers, FL. To initiate germination, seeds were inserted between damp paper towels and placed into transparent Plexiglas containers with about 2.5 cm of tap water maintained at the bottom. The containers were kept at 26 ( 1 °C, while the seeds were kept moist by the wicking action of the paper towels. No significant microbial
contamination of the seeds was observed. After 5-7 days (soybean) or 7-10 days (tomato), the rooted seedlings were transferred to a greenhouse hydroponic environment (16 h photoperiod, 20/16 ( 1 °C day/night) and grown to a uniform size for 4-6 weeks prior to use in the pressure chamber experiments. A modified Hoagland nutrient solution was used in all hydroponic environments. Pressure Chamber. Immediately prior to the start of a pressure chamber experiment, test plants were removed from the hydroponic solution and cut just below the first cotyledonary node (lowest leaves) to remove all of the shoot tissue except for the stem base. A short length (5 cm) of butyl rubber (tomato) or rigid platinum cured silicone tubing (soybean) was then fit over the cut stem forming a gasket. In the case of tomatoes, the gasket was held in place with a hose clamp, and the gasket-covered cut stem was inserted directly through the stem plate and the roots were immediately immersed in a stainless steel vessel containing oxygen saturated nutrient solution spiked with a known concentration of a compound (See Supporting Information Figure S1). The stem plate was then secured to the vessel with a threaded collar and the tip of a disposable pipet was affixed over the cut stem and under the gasket. Compressed oxygen was slowly (20-40 mL min-1) bubbled into the nutrient solution to build pressure within the chamber and to aerate and mix the root zone. The pressure was gradually increased and the flow rate decreased (5-10 mL min-1) until a xylem sap flow rate of approximately 70% (gravimetrically determined one day prior to exposure in the chamber) of the intact plant maximum transpiration rate was reached (the pressure was usually about 150 kPa). The pressure difference between the roots and xylem used in this experiment falls within the reported range of pressure differences measured between intact plant roots and stem xylem (9). For soybeans, no hose clamp was needed. Instead, the gasket-covered stem was first slipped through a hole in an inverted rubber stopper that was inserted up through the chamber’s stem plate, and sealed into the pressure chamber as previously described for the tomato plants. Because of the VOL. 43, NO. 2, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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woody nature and uniform radius of soybean stems, the use of an inverted rubber stopper helped control the pressure exerted on the stem. As the pressure in the chamber increased, the inverted stopper was forced further into the stem plate, increasing the pressure around the stem in a gentle uniform manner proportional to the pressure applied. Samples of xylem sap exiting the cut stem and the root zone exposure solution were collected every 10-30 min (volume dependent on plant size and analysis method) and analyzed for the compounds of interest. Xylem sap samples were collected using a fraction collector (ISCO, CYGNET, Lincoln, NE) and samples of the root zone exposure solution were collected through a septum-sealed port using a glass syringe. Immediately after collection, the samples were transferred to headspace vials or capped in place. For 14C labeled volatiles, the samples were collected directly in scintillation cocktail to minimize losses. Depending on the physical-chemical properties of each compound (higher log KOW ) longer exposure time), samples were collected for 5-50 h, typically reaching steady state in less than 12 h. For 21 of the 26 compounds evaluated, replicate TSCF determinations (more than one plant per compound) were made. Analysis of Xylem Sap and Exposure Solutions. The methods used to determine the concentrations of the test chemicals in xylem sap and exposure solutions depended on the properties of the compounds. Volatile Compound Analysis. Samples (10 mL) of xylem sap and pressure chamber solutions were immediately transferred to headspace vials containing enough sodium chloride (NaCl), to saturate the 10 mL sample and capped. The NaCl was used to increase the headspace concentrations of the volatile organic compounds. The concentrations in the xylem sap and pressure chamber solution were determined indirectly from the concentrations of the compounds in the headspace. External standards made by spiking known amounts of a commercial standard (Supelco, Bellefonte, PA) into NaCl saturated water, were used to define the relationship between the headspace and the solution concentrations. Headspace samples (2 mL) were introduced into a Hewlett-Packard 6890/5973 GC/MS using a Tekmar 7000HT Headspace Analyzer/Autosampler. The autosampler platen/ sample temperature was set to 80 °C, the sample equilibrium time was 20 min, and the transfer line and sample loop temperatures were 180 °C. Chromatographic conditions were as follows: DB-624, 30 m × 0.25 mm, 1.4 µm film thickness column (J&W Scientific, Folsom, CA); helium carrier gas at 0.7 mL/min (3.52 psi); temperature program 40 °C for 2 min to 230 °C at 10 °C/min; and split ratio of 2:1. Sulfolane and Trichloroethanol. A liquid-liquid extraction method was used for sulfolane and trichloroethanol. Aqueous samples (20 mL) were placed into 50 mL centrifuge tubes and saturated with sodium chloride. The extraction solvents, methylene chloride (4 mL) for sulfolane and methyltert-butyl ether (7 mL) for trichloroethanol, were added and the tubes shaken on an orbital shaker for 20 min at 180 oscillation/min. After shaking, the tubes were centrifuged for 15 min at 7500 rpm to separate the phases, and the solvent layer was transferred into a 25 mL sealed vial. The extraction process was repeated two additional times and the combined extracts were analyzed by GC using a temperature program of 50 °C (2 min hold) to 220 at 10 °C/min. Caffeine Analysis. The concentration of caffeine in aqueous samples was directly measured using an Agilent model 1100 high performance liquid chromatograph equipped with a Lichrospher RP 18 (250 × 4.6 mm, 5 µm particles) column (Supelco, Bellefonte, PA) diode array detector 1100 and autosampler. The elution program was isocratic 70% water, 30% methanol with a flow rate of 1 mL/min. 3 H2O and 14C Analysis by Liquid Scintillation Counting. Liquid scintillation counting (LSC) (Beckman LS 1701, 326
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FIGURE 1. TSCF values versus time for methanol and tritiated water run simultaneously. Results from separate experiments with benzene and pyrene shown for comparison. Solid lines represent Hough Transform exponential fitting of the respective data. Beckman Instruments, Inc., Fullerton, CA) was used to directly determine the concentration of tritiated water (3H2O) and 14C labeled compounds in aqueous samples, after adding appropriately 5 mL of Ready Gel scintillation cocktail to 2 mL of sample. Samples were counted to greater than 1% accuracy. The exact sample mass was determined gravimetrically. Calculation of TSCF. For each compound, the measured chemical concentration in the xylem sap was divided by the concentration in the root zone samples collected over the same time interval and were plotted as a function of time in an approach analogous to column breakthrough studies (Figure 1). The use of paired samples minimizes the influence of analytical extraction efficiencies since they are likely to be similar in both the xylem sap and exposure solutions. The steady state TSCF value was calculated using a Hough Transform approach as described by Feinstein and Holt (16). Compilation of TSCF Values from the Literature. TSCF values from 26 studies (1, 2, 5–8, 10–13, 17–32) were compiled from the literature and entered into a Microsoft Access database developed specifically to record available experimental information such as length of exposure, plant species, exposure concentration, experimental method (e.g., soil/ hydroponics/pressure chamber), in addition to the TSCF value. The database is available at no cost from the authors upon request.
Results and Discussion Pressure Chamber TSCF Measurements. The measured TSCF values for 25 compounds are summarized in Table 1 along with the corresponding log KOW values and the general methods used for analysis of the compounds. The TSCF values ranged from 0.01 to 0.98, and the log KOW values ranged from -0.77 to 5. The increased analytical sensitivity associated with the use of 14C-labeled compounds (10 of 26 compounds) enabled the direct measurement of chemical concentrations in the xylem fluid and root zone samples along with tritiated water (3H2O). The 3H2O was used to provide a direct comparison between water and chemical transport (Figure 1). As expected, the steady state TSCF value of 3H2O was 1.0 in all experiments. The shape of the curves also suggests that the health and integrity of the root membranes was not impacted and no preferential flow paths were formed during root pressurization. The effect of chemical hydrophobicity is illustrated in the TSCF versus time plot (Figure 1) for methanol (log KOW ) -0.77), benzene (log KOW ) 2.13), and pyrene (log KOW )
FIGURE 2. Tomato and Soybean TSCF vs log KOW for 118 measurements of 25 compounds r2 ) 0.68. 4.88). The TSCF for methanol increased more rapidly and reached a higher steady state TSCF value (0.88) than benzene (0.4) and pyrene (0.04). The TSCFs values obtained for the six additional highly polar compounds sulfolane, N-nitrosodimethylamine, 1,4-dioxane, caffeine, tert-butyl alcohol, and methyl tert-butyl ether, provide additional evidence that polar, neutral compounds appear to be rapidly taken up by roots and translocated to shoots. The inverse relationship between the rate of root uptake of xenobiotics in a pressure chamber system and hydrophobicity has been previously observed (7, 8). Figure 2 shows the relationship between TSCF versus log KOW for the 25 compounds (plus water) listed in Table 1. The range of TSCF values shown in Figure 2 for some individual compounds illustrates the variability associated with measurements made using different plant species, analytical techniques, and/or in a few cases, exposure concentration. The analytical precision associated with the use of the 14Clabeled compounds and measurement by LCS was greater than using unlabeled compounds. Unlike previous bell-shaped relationships (5, 7, 10), Figure 2 shows a nearly sigmoidal relationship between TSCF and log KOW with the TSCF data approaching the theoretical bounds of TSCF at 1 and 0, respectively. A sigmoidal fit of the experimental data (SigmaPlot) using a maximum TSCF of one produces eq 1 (r (2) ) 0.68, SE ) 0.16). A linear model (TSCF ) -0.15 log KOW + 0.87, r2 ) 0.66, SE ) 0.16) gives similar statistics but could generate estimated TSCFs outside the theoretical bounds. TSCF )
11 11 + 2.6log Kow
(1)
The trend observed in Figure 2 is also consistent with the increasing number of observations in the literature reporting high root uptake for low log KOW compounds such as sulfolane, MTBE, tert-butyl alcohol (TBA), and 1,4-dioxane (6, 11, 12, 25, 30, 31). The difference between the relationship between TSCF and log KOW obtained in this study and those previously reported is not clear, but could be due to a variety of factors including differences in methods used to generate TSCF (intact vs pressure chamber), plant growth conditions (hydroponic vs soil), plant species, plant age, duration, transpiration, losses due to metabolism and volatilization, and perhaps even nonpassive, compound specific uptake mechanisms. For example, the widely referenced relationship by Briggs et al. (5) reported TSCF values for 18 compounds that were obtained using 10 day old barley plants (root wt 0.1 g) that were exposed hydroponically to the chemicals for 24-48 h. The small volume of transpired water (1 mL/day)
FIGURE 3. TSCF uptake curves for caffeine with and without mercuric chloride addition. The steady state TSCF values for caffeine were 0.83 and 1.0 for nonpoisoned and poisoned experiments, respectively. makes it difficult to determine if the plants were healthy and actively growing during the very short exposure period. The plants used in this study had root masses ranging between 20 and 110 g fresh wt, and the volume of water pushed through the plants ranged from 300 to 3000 mL. While TSCFs are assumed independent of plant size and amount of water transpired it is likely there is a minimum volume of water that needs to move through the plant before a representative TSCF can be determined. Plant health and growth conditions are known to impact root membrane integrity and uptake (3, 36–38). As illustrated in Figure 3, adding mercuric chloride at levels toxic to the roots (5 mM) during several TSCF measurements caused chemical concentrations in the xylem to quickly increase and reach a steady state value approaching that of the exposure solution (TSCF ) 1). This apparent loss of root membrane integrity corresponded to a distinct change in root appearance, emphasizing the importance of root health in maintaining the normal regulation of uptake. Literature TSCF Values and the Relationship with Log KOW. In an attempt to better understand the potential reasons for the difference between the TSCF log KOW relationship reported here and the previous bell-shaped curves, more than 150 refereed publications relating to root uptake of organic contaminants were reviewed. Twenty-one contained reported TSCFs, whereas nine additional publications provided enough information that TSCF values could be calculated (1, 2, 5–8, 10–13, 17–32, 39–43). This resulted in 191 average TSCF values for 115 compounds ranging in log KOW from -1.8 to 5.4. Due to differences in the level of experimental details provided, all TSCF values were assumed to be of equal quality and no values were rejected. Out of the 191 TSCF values, 154 values came from studies where intact plants were used and 37 from pressure chamber studies. Intact plants were typically grown and exposed hydroponically but spiked soils were used in three cases. Soybean, poplar, and barley were the most common species investigated. Corresponding log KOW values were obtained (in preferential order) from the studies themselves, Hansch and Leo (33), EPI Suite PhysProp Database (44), and for compounds with no reported value, estimated using EPI Suite KOWWIN (44). Unlike previous reports where data from a single study was used (5, 7, 10) no apparent relationship (visually or statistically) between TSCF and log KOW was found using the combined data set of 191 average literature values (Figure 4). In addition to the overall scatter in the data (Figure 4), for compounds having TSCF values reported in more than one publication, relatively large variations were observed (e.g., VOL. 43, NO. 2, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 4. One hundred twenty-six study average TSCFs compiled from 30 refereed publications for 115 compounds demonstrating the range of variability in reported values.
corrected for, such losses result in lower TSCF values. Low extraction efficiencies and nonuniform distribution of compound within shoot tissues could also contribute to low TSCF values, especially if subsamples are used to calculate the amount of chemical within the entire foliar tissue. Overall, the TSCF values generated in this study and obtained from the literature suggest that bell-shaped curves between TSCF and log KOW greatly underestimate the potential plant uptake and transport into shoot tissue of highly polar, water soluble, neutral organics. The literature data also suggest that pressure chamber derived TSCF values tend to be greater than those derived from intact plants studies. The pressure chamber approach provides a rapid and reproducible method for generating TSCF values, assuming the same analytical technique is used, that can be used in risk and phytoremediation assessments. The pressure chamber TSCF values may be considered a measurement of the maximum translocation potential. Examining the difference between pressure chamber and intact plant TSCF values may give an indication of the importance of loss mechanisms such as volatilization and metabolism. The lack of a standardized methods or guidelines for TSCF measurement will continue to hamper the development of approaches or models that can be used to accurately predict plant uptake and tissue concentrations for risk assessment purposes.
Acknowledgments We thank Julie Chard for her help in plant cultivation and pressure chamber measurements. Funding was provided in part by a fellowship from the Graduate Assistance in Areas of National Need Program, the Utah Water Research Laboratory (WR-1025), and the Utah Agricultural Experiment Station.
Supporting Information Available FIGURE 5. Sigmoidal relationship of literature TSCF values verses log KOW. Pressure chamber derived values highlighted demonstrating their tendency to be greater than reported values for intact plants r2 ) 0.28, SE ) 0.27. MTBE 0.58-1.3 (25, 32) and TCE 0.1-0.9 (40)). The difference in the experimental approach used (intact vs pressure chamber) to measure TSCF was assumed to be the most important factor; however, differences in key operational variables such as exposure duration, plant age, growth conditions, and plant species could also contribute to the variability, especially for intact plant studies. To examine this possibility, the literature data was separated into two groups: TSCF values generated using intact plants and those generated using a pressure chamber method. Since the pressure chamber technique has fewer operational variables, the approach would be expected to yield more consistent data than intact plant studies. In addition, soybeans of similar age and exposure period (6-48 h) were used in the three literature pressure chamber studies (6-8) further reducing potential sources of variability. As shown in Figure 5, the relationship between the literature pressure chamber TSCF values and log KOW appears to reach a maximum approaching one and a minimum approaching zero very similar to the results reported in this study with neutral, polar organics having the highest potential to be taken up by plant roots. It can also be observed that pressure chamber derived TSCF values are generally higher than those obtained from intact plant studies (Figure 5). Chemical losses due to volatilization and metabolism are likely greater during the longer duration and open exposure experiments typically used for intact plant TSCF determinations. If not completely 328
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Figure S1 A diagram of the pressure chamber system used to measure TSCFs. The diagram specifically illustrates the configuration used for measurements in tomato plants. Table S1 contains the data used to generate Figure 4 including chemical name, TSCF, log KOW, and the reference. This material is available free of charge via the Internet at http:// pubs.acs.org.
Literature Cited (1) Sheets, T. J. Uptake and distribution of simazine by oat and cotton seedlings. Weeds 1961, 9 (1), 1–13. (2) Shone, M. G. T.; Wood, A. V. A comparison of the uptake and translocation of some organic herbicides and a systemic fungicide by barley. J. Exp. Bot. 1974, 25 (85), 390–400. (3) Taiz, L.; Zeiger, E. Plant Physiology; 2nd ed.; Sinauer Associates: Sunderland, MA, 1998. (4) Marschner, H., Mineral Nutrition of Higher Plants. 2nd ed.; Academic Press: New York, NY, 1995. (5) Briggs, G. G.; Bromilow, R. H.; Evans, A. A. Relationships between lipophilicity and root uptake and translocation of non-ionized chemicals by barley. Pestic. Sci. 1982, 13 (5), 495–504. (6) Ciucani, G.; Trevisan, M.; Sacchi, G. A.; Trapp, S. A. J. Measurement of xylem translocation of weak electrolytes with the pressure chamber technique. Pest. Manage. Sci. 2002, 58 (5), 467–473. (7) Hsu, F. C.; Marxmiller, R. L.; Yang, A. Y. S. Study of root uptake and xylem translocation of cinmethylin and related-compounds in detopped soybean roots using a pressure chamber technique. Plant Physiol. 1990, 93 (4), 1573–1578. (8) Sicbaldi, F.; Sacchi, G. A.; Trevisan, M.; Del Re, A. A. M. Root uptake and xylem translocations of pesticides from different chemical classes. Pestic. Sci. 1997, 50, 111–119. (9) Benkert, R.; Zhu, J. J.; Zimmermann, G.; Turk, R.; Bentrup, F. W.; Zimmermann, U. Long-term xylem pressure measurements in the Liana Tetrastigma voinierianum by means of the xylem pressure probe. Planta 1995, 196 (4), 804–813.
(10) Burken, J. G.; Schnoor, J. L. Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ. Sci. Technol. 1998, 32 (21), 3379–3385. (11) Aitchison, E. W.; Kelley, S. L.; Alvarez, P. J. J.; Schnoor, J. L. Phytoremediation of 1,4-dioxane by hybrid poplar trees. Water Environ. Res. 2000, 72 (3), 313–321. (12) Rubin, E.; Ramaswami, A. The potential for phytoremediation of MTBE. Water Res. 2001, 35 (5), 1348–1353. (13) Doucette, W. J.; Chard, J. K.; Moore, B. J.; Staudt, W. J.; Headley, J. V. Uptake of sulfolane and diisopropanolamine (DIPA) by cattails (Typha latifolia). Microchem. J. 2005, 81 (1), 41–49. (14) Chard, B. K.; Doucette, W. J.; Chard, J. K.; Bugbee, B.; Gorder, K. Trichloroethylene uptake by apple and peach trees and transfer to fruit. Environ. Sci. Technol. 2006, 40 (15), 4788–4793. (15) Trapp, S. Fruit tree model for uptake of organic compounds from soil and air. SAR QSAR Environ. Res. 2007, 18 (3-4), 367– 387. (16) Feinstein, D. I.; Holt, F. B. Estimating the parameters for an exponential process via a Hough transform. Acoustics, Speech, Signal Process. 1990, 5, 2475–2478. (17) Yoon, J. M.; Oh, B. T.; Just, C. L.; Schnoor, J. L. Uptake and leaching of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by hybrid poplar trees. Environ. Sci. Technol. 2002, 36 (21), 4649– 4655. (18) Trapp, S.; Pussemier, L. Model-calculations and measurements of uptake and translocation of carbamates by bean-plants. Chemosphere 1991, 22 (3-4), 327–339. (19) Geissbuhler, H.; Haselbach, C.; Aebi, H.; Ebner, L. The fate of N′-(4-chlorophenoxy)-phenyl-NN-dimethylurea (C-1983) in soil and plants. Weed Res. 1963, 3, 181–194. (20) Doucette, W. J.; Bugbee, B.; Wood, J.; Orchard, B.; Hayhurst, S.; Pajak, C Quantification of TCE uptake, translocation and transpiration by plants in hydroponic and soil systems using a high flow sealed system growth chamber. In 18th Annual meeting of the Society of Environmental Toxicology and Chemistry, San Francisco, CA, November 16-20, 1997. (21) Crowdy, S. H.; Jones, R. D.; The translocation of sulphonamides in higher plants, I. J. Exp. Bot. 1956, 7 (21), 335–346. (22) Chard, J. K.; Orchard, B. J.; Pajak, C. J.; Bugbee, B.; Doucette, W. J. Uptake of Trichloroethanol and Trichloroacetic Acid by Hybrid Poplar. In Conference of Hazardous Waste Research, 1998 Snowbird, UT, May 18-21, 1998. (23) Crowdy, S. H.; Pramer, D. The occurrence of translocated antibiotics in expressed plant sap. Ann. Bot. (Oxford, UK) 1955, 19 (73), 79–86. (24) Edwards, N. T.; Ross-Todd, B. M.; Graver, E. G. Uptake and metabolism of 14C anthracene by soybean (glycine max). Environ. Exp. Bot. 1982, 22 (3), 349–357. (25) Hong, M. S.; Farmayan, W. F.; Dortch, I. J.; Chiang, C. Y.; McMillan, S. K.; Schnoor, J. L. Phytoremediation of MTBE from a groundwater plume. Environ. Sci. Technol. 2001, 35 (6), 1231– 1239. (26) Kim, J.; Drew, M. C.; Corapcioglu, M. Y. Uptake and phytotoxicity of TNT in onion plant. J. Environ. Sci. Health, Part A: Toxic/ Hazard. Subst. Environ. Eng. 2004, 39 (3), 803–819. (27) Orchard, B. J.; Doucette, W. J.; Chard, J. K.; Bugbee, B. Uptake of trichloroethylene by hybrid poplar trees grown hydroponically in flow-through plant growth chambers. Environ. Toxicol. Chem. 2000, 19 (4), 895–903.
(28) Thompson, P. L.; Ramer, L. A.; Schnoor, J. L. Uptake and transformation of TNT by hybrid poplar trees. Environ. Sci. Technol. 1998, 32 (7), 975–980. (29) Trapp, S.; McFarlane, C.; Matthies, M. Model for uptake of xenobiotics into plantssValidation with bromacil experiments. Environ. Toxicol. Chem. 1994, 13 (3), 413–422. (30) Yifru, D. D.; Nzengung, V. A. Uptake of N-nitrosodimethylamine (NDMA) from water by phreatophytes in the absence and presence of perchlorate as a co-contaminant. Environ. Sci. Technol. 2006, 40 (23), 7374–7380. (31) Yu, X. Z.; Gu, J. D. Uptake, metabolism, and toxicity of methyl tert-butyl ether (MTBE) in weeping willows. J. Hazard Mater. 2006, 137 (3), 1417–1423. (32) Zhang, Q. Z.; Davis, L. C.; Erickson, L. E. Transport of methyl tert-butyl ether through alfalfa plants. Environ. Sci. Technol. 2001, 35 (4), 725–731. (33) Hansch, C.; Leo, A.; Hoekman, D. H. Exploring QSAR: Hydrophobic, Electronic and Steric Constants; American Chemical Society: Washington DC, 1995. (34) Hansch, C.; Leo, A. Medchem Project; Pomona College: Claremont, CA 1985. (35) Agency for Toxic Substances and Disease Register (ATSDR). Toxicological profile for 1,2-Dichloropropane (Draft); U.S. Public Health Service, U.S. Department of Health and Human Services: Washington, DC, 1989. (36) Cakmak, I.; Marschner, H. Increase in membrane permeability and exudation of roots of zinc deficient plants. J. Plant Physiol. 1988, 132, 356–361. (37) Lee, R. B. Effects of organic acids on the loss of ions from barley roots. J. Exp. Bot. 1977, 28 (3), 578–587. (38) Riveria, C. M.; Penner, D. Effect of calcium and nitrogen on soybean (Glycine max) root fatty acid composition and uptake of Linuron. Weed Sci. 1978, 26, 647–650. (39) Fujisawa, T.; Ichise, K.; Fukushima, M.; Katagi, T.; Takimoto, Y. Improved uptake models of nonionized pesticides to foliage and seed of crops. J. Agric. Food Chem. 2002, 50 (3), 532–537. (40) Davis, L.; Vanderhoof, S.; Dana, J.; Selk, K.; Smith, K.; Gophen, G.; Erickson, L. Movement of chlorinated solvents and other volatile organics through plants monitored by fourier transform infrared (FT-IR) spectrometry. J of. Hazard. Subst. Res. 1998, 1 (4), 1–26. (41) Krstich, M. A.; Schwarz, O. J. In Characterization of Xenobiotic uptake utilizing an isolated root uptake test (IRUT) and a whole plant uptake test (WPUT), ASTM Special Technical Publication; ASTM: West Conshohocken, PA, 1990; p 87. (42) McFarlane, C.; Pfleeger, T.; Fletcher, J. Effect, uptake and disposition of nitrobenzene in several terrestrial plants. Environ. Toxicol. Chem. 1990, 9, 513–520. (43) Doucette, W. J.; Wheeler, B. R.; Chard, J. K.; Bugbee, B.; Naylor, C. G.; Carbone, J. P.; Sims, R. C. Uptake of nonylphenol and nonylphenol ethoxylates by crested wheatgrass. Environ. Toxicol. Chem. 2005, 24 (11), 2965–2972. (44) U.S. EPA. Estimation Programs Interface Suite for Microsoft Windows, v3.20; United States Environmental Protection Agency: Washington, DC, 2008.
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