Environ. Sci. Technol. 2006, 40, 45-52
Plant Uptake of Non-Ionic Organic Chemicals C H R I S C O L L I N S , * ,† M I K E F R Y E R , † A N D ALBANIA GROSSO‡ Department Of Environmental Science and Technology, Imperial College, South Kensington, London, UK SW7 2BP, and Environment Agency of England and Wales, Howbery Park, Wallingford, Oxfordshire, UK, OX10 8BD
Plant uptake of organic chemicals is an important process when considering the risks associated with land contamination, the role of vegetation in the global cycling of persistent organic pollutants, and the potential for industrial discharges to contaminate the food chain. There have been some significant advances in our understanding of the processes of plant uptake of organic chemicals in recent years; most notably there is now a better understanding of the air to plant transfer pathway, which may be significant for a number of industrial chemicals. This review identifies the key processes involved in the plant uptake of organic chemicals including those for which there is currently little information, e.g., plant lipid content and plant metabolism. One of the principal findings is that although a number of predictive models exist using established relationships, these require further validation if they are to be considered sufficiently robust for the purposes of contaminated land risk assessment or for prediction of the global cycling of persistent organic pollutants. Finally, a number of processes are identified which should be the focus of future research.
Introduction It is widely recognized that plants can become contaminated with a range of toxic organic industrial chemicals, e.g., PCBs, PAHs, explosives, and dioxins (1-7). To this end plant uptake submodels have been developed within larger exposure assessment models for the determination of risks posed by the development of sites which contain toxic organic chemicals, e.g., CSOIL (RIVM, Netherlands, see (8)), CLEA (DEFRA and Environment Agency, U.K., see (9)), and CALTOX (California Department of Toxic Control, U.S., see (10)). Plant uptake and storage is also a potentially key component in the global cycling of persistent organic pollutants (11-14). In recent years our understanding of the uptake of organic chemicals by vegetation has increased considerably; most notably the process of plant contamination following aerial deposition (15-17). However, the most widely quoted review for the plant uptake of organic chemicals (16) is now over 16 years old. Ryan et al. (18) proposed a screening framework to identify those chemicals which were most likely to contaminate vegetation rather than a process driven model. The current review considers the plant uptake of organic chemicals and identifies the key processes involved with the emphasis on those where there have been significant developments over the last 16 years. An additional aim of the * Corresponding author e-mail:
[email protected]; tel: +44 207 594 7378; fax: +44 207 594 2246. † Imperial College. ‡ Environment Agency of England and Wales. 10.1021/es0508166 CCC: $33.50 Published on Web 11/17/2005
2006 American Chemical Society
review is to provide information to aid the construction of plant uptake models and improve those that already exist.
Plant Uptake Pathways The uptake of organic chemicals by plants occurs via a number of pathways. These are demonstrated in Figure 1. Passive and Active Uptake from Soil into Plant Roots. Organic chemicals can be taken up by plant roots via the vapor or water phases of soil. The uptake of anthropogenic organic chemicals by plant roots has been shown to be a passive, diffusive process, with the exception of a few hormone-like chemicals such as the phenoxy acid herbicides, for which there is some evidence of active uptake (19). Experiments involving the uptake of nonionized chemicals from hydroponic solution into plant roots have demonstrated that the uptake process consists of two components: (1) “equilibration” of the aqueous phase in the plant root with the concentration in the surrounding solution; and (2) “sorption” of the chemical onto lipophilic root solids (20). Lipophilic root solids include lipids in membranes and cell walls (21). Polycyclic aromatic hydrocarbons (PAHs), chlorobenzenes, polychlorinated biphenyls (PCBs), and polychlorinated dibenzo-p-dioxins/dibenzofurans (PCDD/Fs) have all been found to accumulate significantly in plant roots (22). Briggs et al. determined a linear relationship between the octanolwater partition coefficient (KOW) of nonionized chemicals and the observed root concentration factor (RCF ) chemical concentration in the root/concentration in external solution) from their experiments investigating the uptake of Omethylcarbamoyloximes and substituted phenylureas into barley plants. Lipophilic organic chemicals possess a greater tendency to partition into plant root lipids than hydrophilic chemicals. Wild and Jones (23) categorized nonionized organic chemicals with log KOW > 4 as having a high potential for retention in plant roots. Schwab et al. (24) reported that uptake of naphthalene from solution followed a Freundlich isotherm, the gradient of which was less than one in the roots of vegetative plants indicating that they had become saturated with naphthalene, but was not significantly different from one for older roots indicating that they had not become saturated. Therefore, looking at root uptake purely as a partitioning process may be incorrect as this assumes it is independent of concentration, which it is not if the roots can become saturated. The plant aqueous phase as distinct from the lipid phase is only thought to represent an important storage compartment for organic chemicals with log KOW < 2, and a dimensionless Henry’s law constant (KAW) < 100 (25). In addition to the physicochemical properties of the contaminant, the composition of the plant roots is likely to influence root uptake behavior. Trapp and Pussemeir (26) found that the relationship derived by Briggs et al. (20) overestimated experimentally derived RCFs for carbamates VOL. 40, NO. 1, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
45
FIGURE 1. Principal uptake pathways for the uptake of organic chemicals by plants. in common bean plants. A higher content of solids of a lipidlike nature in barley (Hordeum vulgare) roots compared with bean (Vicia faba) roots has been advanced as a probable explanation for this difference (19). Schwab et al. (24) also found quantitative differences between the uptake of naphthalene in plant roots dependent on their lipid content. There is, however, very little information readily available for the lipid contents of plant compartments for different plant species (see below). The retention in root lipid materials has been further illustrated by the higher retention of organic compounds in the peels of carrot and potato compared to their pulp (27, 28). Transport from the Root to the Shoot. Water and solutes are transported upward from the root into other plant parts through the xylem. This flux is driven by the water potential gradient, created throughout the plant during transpiration. For chemicals taken into plant roots to reach the xylem, they must penetrate a number of layers: the epidermis, cortex, endodermis, and pericycle. At the endodermis all materials must pass through at least one cell membrane. It is the combination of the solubility of chemicals in water and the solubility within the cell membrane, which is rich in lipids, that determines the movement of chemicals into roots and subsequent transport to the plant shoot (29). Briggs et al. (30) derived a relationship for predicting concentrations of chemicals in the transpiration stream of the plant from the concentration in soil solution and the KOW of the chemical. This relationship was based on experiments investigating the uptake of a limited number of nonionized chemicals into barley plants. It was found that the transpiration stream concentration factor (TSCF ) concentration in xylem/concentration in external solution) was at a maximum for chemicals with log KOW ca. 1.8. This relationship has been widely used in both plant modeling (18, 31) and also by some authors to explain their results (6). Hsu et al. (32) found a similar relationship for cinmethylin and related compounds in soybean (Glycine max) plants, as did Burken and Schnoor (33) using a range of industrial organic pollutants with hybrid poplar (Populus deltoides × nigra, DN34) (Figure 2). It can be seen from Figure 2. that there are potentially large differences in the TSCF at high (>4) and low log KOW ( 11 will be particle-bound when they deposit to plant surfaces, so VOL. 40, NO. 1, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
47
desorption from the particle into the leaf would be required to contaminate the plant shoot. It should be noted that McLachlan’s framework derived from an offsite aerial source, for local sources soil volatilization and subsequent gaseous deposition may also play a role for those compounds with log KOA > 11. Both Wang and Jones (55) and Kipopoulou et al. (5) found a linear correlation between log KOA and shoot concentration factor (SCF ) shoot concentration of X/soil concentration of X) when investigating crop uptake of chlorobenzenes (log KOA 4.5-7) and PAHs (log KOA 7.5-13), respectively. Interspecies variability in organic chemical concentrations in plant foliage has been demonstrated by Buckley (56). Schrieber et al. (57) measured cuticular permeabilities for 40 plant species and which ranged over 2 orders of magnitude, in any specific properties. Bohme et al. (15) found a 20-fold variation between 5 different grasses and herbs. Since lipophilic chemicals will tend to partition to leaf lipids, differences in the lipid content of plant foliage would seem the most reasonable explanation for this behavior. For foliar uptake models, such as that of Muller et al. (58), the leaf lipid content represents the most sensitive plant characteristic for the uptake of lipophilic chemicals. A study by Simonich and Hites (59) supports this with interspecies variability in experimental results found to be reduced when PAH concentrations were normalized to leaf lipid contents. Both Bohme et al. (15) and Komp et al. (60) found that interspecies variability in leaf/air bioconcentration factors for a variety of semivolatile organic chemicals, where gaseous uptake was the dominant uptake process, could not be explained by variability in extractable lipid contents. The authors concluded that not just lipid quantity but also lipid quality need to be considered when evaluating interspecies variability in leaf/air bioconcentration factors. Unfortunately neither of these workers specifies what they mean by lipid quality. Schreiber and Schonherr (61) and McCrady and Maggard (62) have found that the exposed surface area of the plant foliage influences the foliar uptake rate for a variety of species. Simonich and Hites (59) suggested that this plant characteristic will be particularly significant if chemical partitioning to foliage does not approach equilibrium, because those plants with a larger exposed area will come into contact with more chemical. Particulate Deposition to Plant Surfaces. Organic chemicals can be transferred from soil by the re-suspension of soil particles, and then subsequently to plant foliage via dry and wet deposition. Other atmospheric aerosols containing organic compounds will also contaminate plant foliage following dry and wet deposition. A study by Kao and Venkataraman (63) found that re-suspended soil dust contributed approximately 4% of the total ambient PCDD/F concentrations measured, but could contribute between 20 and 90% of the deposition to environmental surfaces because of the high deposition velocity of soil particles. The dry deposition of particles suspended in the air to plant surfaces involves diffusion, interception, impaction, and sedimentation processes (64). Once particles have been deposited on plant foliage the chemicals bound to them are subject to removal and degradation. However, during the period of contact between plant leaves and deposited particles, particle-bound organic chemicals may diffuse into the plant cuticle and become adsorbed to lipophilic tissues or may permeate into the leaf interior. The plant cuticle can be divided into an outer skin, made up of cuticular waxes embedded within the cutin matrix, and an inner volume element, which mainly consists of the cutin matrix. Lipophilic chemicals that permeate into the inner volume element of the cuticle can pass through the epidermis into the leaf interior with relative ease (46). The permeability of plant cuticles to organic chemicals in solution has been found to 48
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 1, 2006
be linearly related to the KOW of the chemical and inversely related to its molecular volume (65). However, the situation regarding the uptake of chemicals from ephemeral particulate deposits is far more complex and the extent to which the chemical is reversibly or irreversibly bound to the particle will significantly influence the rate of transfer. Nakajima et al. (66) have investigated the uptake of PAHs from the atmosphere into Azalea leaves. The authors suggest that for benzo[a]pyrene and perylene, dry deposition of suspended particles with subsequent permeation into the cuticle represents the major pathway of contamination. Welsch-Paulsch et al. (67) also determined that the dry deposition of large particles represented an important uptake pathway for hepta- and octo-chlorinated PCDDs into grass leaves. The octanol/air partition coefficient has been suggested as a suitable indicator of the significance of the dry deposition contamination pathway for semivolatile organic chemicals (SVOCs). The interpretative framework of McLachlan (16) identifies particle-bound deposition as the primary process of plant uptake for SVOCs with log KOA > 11. Cousins and Mackay (25) suggest that for chemicals with log KOA > 9, particle-bound deposition becomes relatively more important than gaseous deposition. When plant uptake models were compared for incorporation into the CSOIL model (8), the SCF (stem concentration factor ) stem concentration/soil concentration) between the model and the data were only in reasonable agreement when soil resuspension was included in the model using the relationship proposed by Hetrick and McDowell-Boyer (68). Wet deposition is thought to be the dominant deposition mechanism for chemicals with log KAW < -6 (25). Relatively little information is available regarding the wet deposition of particle-bound and gaseous phase organic chemicals to plant surfaces and this pathway is seldom considered when looking at the contamination of vegetation (17). Cousins and Mackay (25) suggest that the majority of wet deposition is not intercepted and retained by vegetation, but is washed directly to soil. However, it should be noted that wet deposition can nevertheless be an important indirect factor via rain splash. Dreicer et al. (69) investigated the rain splash pathway for tomato plants, and they found that only finer soil particles were retained on plant surfaces. There is some evidence that PAH burdens in soil accumulate preferentially in these finer fractions (70). Kaup et al. (71) sequentially extracted maize leaves and reported that of the particle associated PAH and PCCD/F approximately 20% could potentially be eroded and some 30-60% had desorbed from the particle into the epicuticular waxes. Greater penetration was achieved by the more volatile compounds. Interspecies variability in organic chemical concentrations in plant foliage also occurs for chemicals following particulate deposition. Significant differences between plant species have been observed in mass loadings of soil to plant surfaces, as a result of contact with soil particles (17). Plant characteristics that affect the rate of particle deposition and retention include the exposed surface area of the foliage and the presence or absence of leaf hairs. Little and Wiffen (72) observed that rough or hairy leaf surfaces were more efficient at collecting aerosols than smooth surfaces. This observation was explained by increased surface area and the projection of roughness elements through the leaf-air boundary layer. Pinder et al. (73) found that the largest soil loadings occurred on broad-leaved species growing close to the ground, while Hu ¨ lster and Marschner (74) reported that direct contact between soil particles and plant surfaces was a significant uptake pathway for PCDD/Fs to hay. Influence of Plant Composition on Uptake. As previously stated the composition of the plant is believed to significantly affect the uptake of organic chemicals. There are a number of authors who have reported that the lipid content or lipid
TABLE 1. Details of Water, Lipid, Carbohydrate, and Fiber Content of Crops Relevant to Risk Assessment (69) crop class
water
lipid
carbohydrate
fiber
leaf crops (lettuce, pak choi, cabbage) bulbs, stems and tubers (onion, leek, potato) root crops (carrot, parsnip) fruit crops (tomato, pepper, pea, bean)
94.1 83.6 83.9 88.4
0.16 0.16 0.27 0.36
3.5 13.9 13.7 7.9
1.5 1.8 3.9 2.0
quality is of significance (2, 15, 19, 58). A number of predictive uptake models use lipid content as an input parameter (31, 75, 76). Hung and Mackay (75) and Chiouet al. (76) also require the content of fiber and carbohydrate, respectively. There are, however, very little readily accessible data for these parameters. The best source was found to be the website of the U.S. Department of Agriculture where details of the crop composition of important food staples can be found (77). From Table 1 it can be seen that there was some variability within the major crop classes for water, lipid, carbohydrate, and fiber content. The major differences were the higher water content of leaf crops, the lower carbohydrate content of leaf crops, and the higher lipid content of root and fruit crops. These values are lower than the default values suggested by the models of Trapp and Mathies (31), Hung and Mackay (75), and Chiou et al. (76), but are in agreement with Flindt (78) and Tam et al. (79). Therefore these models may possibly overestimate the accumulation of organic chemicals in plants. However, it should also be noted that other plant components such as waxes, lignin, and suberin may also absorb organic chemicals and these would not be extracted using the normal lipid extraction methods, so using values for lipid alone may underestimate total potential accumulation. It may be the reservoir capacity of these other plant components that are responsible for the differences in uptake reported by Bohme et al. (15) and Komp et al. (59) that could not be related solely to lipid content.
Other Potentially Significant Processes Plant Metabolism. Chemicals accumulated in plants may become metabolized, thus reducing their concentration within the plant’s tissues. A fuller review of this process can be found in Burken (80). The process can be divided into transport, where the uptake will be driven by those processes described above; transformation reactions, e.g., oxidation; conjugation, e.g., with glutathione; and finally sequestration, e.g., into the cell wall. Plant metabolism has been reported for a relatively small number of industrial organic chemicals although more is known of herbicides. Those chemicals where evidence has been reported include trichloroethylene, benzene, and pyrene (81-83); with most success being reported for the explosives (84, 85). Metabolic processes and rates will be specific to particular chemicals and plant species (8587). The toxicity of the metabolites and bound residues from these processes is an area that requires investigation. Photolytic Degradation on Plant Surfaces. Photolytic degradation may reduce chemical concentrations in plants and has been demonstrated to be a significant loss mechanism for 2,3,7,8-TCCD from spruce (Picea abies) foliage (88). Trapp and Matthies (89) found it was the most significant loss process for 2,3,7,8-TCDD in their PLANTX model. Photolytic degradation on plant leaves is enhanced by the tendency of leaves to orient themselves to maximize the interception of sunlight. The extent of photolytic degradation on leaf surfaces will influence the aerial deposition and direct contact plant uptake pathways. Volatilization from Foliage to Air. The plant transpiration flux will move some chemicals to sub-stomatal tissues from which they will subsequently be lost via volatilization, thus reducing plant concentrations (90). Volatilization is likely to be a significant transport pathway for chemicals with high
water solubility and vapor pressure. This pathway was found to be significant for benzene (91) and TCE (92). Phytovolatilization is the principal mechanism in the phytoremediation of MTBE-contaminated groundwaters (93). This process will occur in parallel with the gaseous uptake processes described above. Growth Dilution. The importance of growth dilution for the contamination of vegetation with organic chemicals has not been clearly established. Trapp and Matthies (31) and Hung and Mackay (75) include it in their models, but these assume that plants are in the middle stage of exponential growth, they do not describe the biomass accumulation over a season. There are two scenarios where growth dilution might be potentially important: (1) where there is an acute exposure event and growth subsequently results in dilution of this “spike” of contamination, and (2) where the uptake of the chemical per unit mass is slower than the accumulation of dry matter per unit mass. There is little data regarding the first and it would be critically dependent on the growth stage of the crop; the earlier in the season the greater potential for dilution. The second scenario is highly probable. There is little known about the kinetics of uptake, but it is known that plants with KOA > 8.5 may not become saturated with chemical from aerial deposition gaseous exposure from the McLachlan framework discussed above, and Schwab et al. (24) found that older roots of tall fescue (Festuca arundinacea, Schreber) and alfalfa (Medicago sativa, L.) were not saturated with naphthalene, but young roots were. It would therefore appear that growth will have a significant role.
Focus for Future Research This paper has identified key pathways for the plant uptake of organic chemicals. Where possible, predictive relationships have been presented or referenced to enable the construction of plant uptake models. Future research will need to address those areas where at present the understanding of a potentially important pathway is lacking. There is a significant amount of information on the root uptake and aerial deposition of organic chemicals to plants that allows for the understanding of the potential for the transfer of these chemicals. This is not always at the mechanistic level, but is probably sufficient for an estimation of the potential risk from the ingestion of plant material contaminated by these pathways. Where relationships are proposed (for example, those for the accumulation from the gas phase of Bacci et al. (52) and McLachlan (16)) these have not been subsequently validated by a range of independent experiments as is required for a truly robust model. This absence of validation is also true for the relationship derived by Briggs et al. (30) which was developed for pesticides and is used in a number of models for the uptake of industrial chemicals (18, 94). Such validation would determine if this is a better relationship than that of Hsu et al. (32) or Burken and Schnoor (33). Recent work would also suggest that at low KOW, these relationships do not hold (6, 34). There is therefore a need for high-quality laboratory and field studies to quantify key processes so proposed relationships can be validated and hence be used with confidence. At present the contribution to the foliar contamination from distant aerial sources cannot always be separated from VOL. 40, NO. 1, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
49
that arising from local sources. The former has been well studied, but the information on the latter is lacking. Particulate deposition from local sources may be a particularly significant pathway and is a pressing area for investigation. There are virtually no data to allow for quantification of the gaseous soil-air-plant pathway, which would also arise from a local source. Separation of the local from the off-site is required for a balanced risk assessment for contaminated land. A number of researchers have related uptake of organic chemicals to the lipid content of the plant component to predict the contaminant accumulation. However, few data are easily available for a value to be chosen that would be technically defensible. This data gap needs to be addressed if these parameters are to be used with confidence in models. Species and interspecies variability may play a major role here, but one needs to remember the law of diminishing returns; it may not be practicable to determine the lipid and other accumulating components for a wide range of species particularly if there are significant intra-species differences. Finally, there is little information on the toxicity of the plant metabolites and bound residues formed from the uptake of such chemicals and this may significantly influence the risk prioritization of those chemicals investigated.
Literature Cited (1) Hulster, A.; Muller, J. F.; Marschner, H. Soil-Plant Transfer of Polychlorinated Dibenzo-p-Dioxins and Dibenzofurans to Vegetables of the Cucumber Family (Cucurbitaceae). Environ. Sci. Technol. 1994, 28, 1110-1115. (2) Simonich, S. L.; Hites, R. A. Vegetation-Atmosphere Partitioning of Polycyclic Aromatic Hydrocarbons. Environ. Sci. Technol. 1994, 28, 939-943. (3) Lovett, A. A.; Foxall, C. D.; Creaser, C. S.; Chewe, D. PCB and PCDD/DF congeners in locally grown fruit and vegetable samples in Wales and England. Chemosphere 1997, 34, 14211436. (4) Thomas, G.; Sweetman, A. J.; Ockenden, W. A.; Mackay, D.; Jones, K. C. Air-pasture transfer of PCBs. Environ. Sci. Technol. 1998, 32, 936-942. (5) Kipopoulou, A. M.; Manoli, E.; Samara, C. Bioconcentration of polycyclic aromatic hydrocarbons in vegetables grown in an industrial area. Environ. Pollut. 1999, 106, 369-380. (6) Groom, C. A.; Halasz, A.; Paquet, L.; Olivier, L.; Dubois, C.; Hawari, J. Accumulation of HMX (octahydro-1,3,5,7-tetranitri1,3,5,7-tetrazocine) in indigenous and agricultural plants grown in HMX-contaminated anti-tank firing-range soil. Environ. Sci. Technol. 2002, 36, 112-118. (7) Wu, W. Z.; Schramm, K. W.; Xu, Y.; Kettrup, A. Contamination and distribution of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/F) in agriculture fields in Ya-Er Lake area, China. Ecotoxicol. Environ. Saf. 2002, 53, 141-147. (8) Rikken, M. G. J.; Lijzen, J. P. A.; Cornelese, A. A. Evaluation of Model Concepts on Human Exposure; RIVM (National Institiute for Public Health and the Environment): Bilthoven, The Netherlands, 2001. (9) DEFRA. The Contaminated Land Exposure Assessment Model (CLEA): Technical Basis and Algorithms; WRc, Department for Environment, Food, and Rural Affairs: London, 2002. (10) McKone, T. E.; Maddalena, R. L.; Bennett, D. H. CALTOX Total Exposure Model for Hazardous Waste Sites; California Department of Toxic Substances Control: Sacramento, CA, 2003. http:// www.dtsc.ca.gov/ScienceTechnology/caltox.html (last accessed Jan 2005). (11) Dalla Valle, M.; Dachs, J.; Sweetman, A. J.; Jones, K. C. Maximum reservoir capacity of vegetation for persistent organic pollutants: Implications for global cycling. Global Biogeochem. Cycle 2004, 18. (12) Barber, J. L.; Thomas, G. O.; Kerstiens, G.; Jones, K. C. Current issues and uncertainties in the measurement and modelling of air-vegetation exchange and within-plant processing of POPs. Environ. Pollut. 2004, 128, 99-138. (13) Wegmann, F.; Scheringer, M.; Moller, M.; Hungerbuhler, K. Influence of vegetation on the environmental partitioning of DDT in two global multimedia models. Environ. Sci. Technol. 2004, 38, 1505-1512. 50
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 1, 2006
(14) Scheringer, M.; Salzmann, M.; Stroebe, M.; Wegmann, F.; Fenner, K.; Hungerbuhler, K. Long-range transport and global fractionation of POPs: insights from multimedia modeling studies. Environ. Pollut. 2004, 128, 177-188. (15) Bohme, F.; Welsch-Pausch, K.; McLachlan, M. S. Uptake of airborne semivolatile organic compounds in agricultural plants: Field measurements of interspecies variability. Environ. Sci. Technol. 1999, 33, 1805-1813. (16) McLachlan, M. S. Framework for the interpretation of measurements of SOCs in plants. Environ. Sci. Technol. 1999, 33, 17991804. (17) Smith, K. E. C.; Jones, K. C. Particles and vegetation: implications for the transfer of particle-bound organic contaminants to vegetation. Sci. Total Environ. 2000, 246, 207-236. (18) Ryan, J. A.; Bell, R. M.; Davidson, J. M.; O’Connor, G. A. Plant Uptake of Non-Ionic Organic-Chemicals from Soils. Chemosphere 1988, 17, 2299-2323. (19) Bromilow, R. H.; Chamberlain, K. Principles governing uptake and transport of chemicals. In Plant Contamination: Modelling and Simulation of Organic Chemical Processes; Trapp, S., McFarlane, J. C., Eds.; Lewis Publishers: London, 1995; pp 3864. (20) Briggs, G. G.; Bromilow, R. H.; Evans, A. A.; Williams, M. Relationships between Lipophilicity and the Distribution of NonIonized Chemicals in Barley Shoots Following Uptake by the Roots. Pestic. Sci. 1983, 14, 492-500. (21) Paterson, S.; Mackay, D.; Bacci, E.; Calamari, D. Correlation of the Equilibrium and Kinetics of Leaf Air Exchange of Hydrophobic Organic Chemicals. Environ. Sci. Technol. 1991, 25, 866871. (22) DuarteDavidson, R.; Jones, K. C. Screening the environmental fate of organic contaminants in sewage sludge applied to agricultural soils. 2. The potential for transfers to plants and grazing animals. Sci. Total Environ. 1996, 185, 59-70. (23) Wild, S. R.; Jones, K. C. Organic Chemicals Entering Agricultural Soils in Sewage Sludges - Screening for Their Potential to Transfer to Crop Plants and Livestock. Sci. Total Environ. 1992, 119, 85-119. (24) Schwab, A. P.; Al-Assi, A. A.; Banks, M. K. Adsorption of naphthalene onto plant roots. J. Environ. Qual. 1998, 27, 220224. (25) Cousins, I. T.; Mackay, D. Strategies for including vegetation compartments in multimedia models. Chemosphere 2001, 44, 643-654. (26) Trapp, S.; Pussemeir, L. Model calculations and measurements of uptake and translocation of carbamates by bean plants. Chemosphere 1991, 22, 327-345. (27) Fismes, J.; Perrin-Ganier, C.; Empereur-Bissonnet, P.; Morel, J. L. Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. J. Environ. Qual. 2002, 31, 1649-1656. (28) Wild, S. R.; Jones, K. C. Polynuclear Aromatic Hydrocarbon Uptake by Carrots Grown in Sludge-Amended Soil. J. Environ. Qual. 1992, 21, 217-225. (29) McFarlane, J. C. Plant transport of organic chemicals. In Plant Contamination - Modelling and Simulation of Organic Chemical Processes; Trapp, S., McFarlane, J. C., Eds.; Lewis Publishers: Boca Raton, FL, 1995. (30) 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, 495-504. (31) Trapp, S.; Matties, M. Generic one compartment model for the uptake of organic chemicals by foliar vegetation. Environ. Sci. Technol. 1995, 29, 2333-2338. (32) 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, 1573-1578. (33) Burken, J. G.; Schnoor, J. L. Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ. Sci. Technol. 1998, 32, 3379-3385. (34) 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, 41-49. (35) Barak, E.; Jacoby, B.; Dinoor, A. Adsorption of Systemic Pesticides on Ground Stems and in the Apoplastic Pathway of Stems, as Related to Lignification and Lipophilicity of the Pesticides. Pestic. Biochem. Physiol. 1983, 20, 194-202. (36) Uchida, M. Affinity and Mobility of Fungicidal Dialkyl Dithiolanylidenemalonates in Rice Plants. Pestic. Biochem. Physiol. 1980, 14, 249-255.
(37) McCrady, J. K.; McFarlane, C.; Lindstrom, F. T. The Transport and Affinity of Substituted Benzenes in Soybean Stems. J. Exp. Bot. 1987, 38, 1875-1890. (38) Topp, E.; Scheunert, I.; Attar, A.; Korte, F. Factors Affecting the Uptake of C-14-Labeled Organic Chemicals by Plants from Soil. Ecotoxicol. Environ. Saf. 1986, 11, 219-228. (39) O’Connor, G. A.; Kiehl, D.; Eiceman, G. A.; Ryan, J. A. Plant Uptake of Sludge-Borne PCBs. J. Environ. Qual. 1990, 19, 113118. (40) Smelt, J. H.; Leistra, M. A. E. Hexachlorobenzene in soils and crops after soil treatment with pentachloronitrobenzene. Agric. Environ. 1974, 1, 65-71. (41) Schroll, R.; Scheunert, I. Uptake of the lipophilic model compound hexachlorobenzene by different plant species during the vegetation period. Fresenius’ Environ. Bull. 1992, 1, 334338. (42) White, J. C.; Wang, X. P.; Gent, M. P. N.; Iannucci-Berger, W.; Eitzer, B. D.; Schultes, N. P.; Arienzo, M.; Mattina, M. I. Subspecies-level variation in the phytoextraction of weathered p,p′-DDE by Cucurbita pepo. Environ. Sci. Technol. 2003, 37, 4368-4373. (43) Karickhoff, S. W. Semiempirical Estimation of Sorption of Hydrophobic Pollutants on Natural Sediments and Soils. Chemosphere 1981, 10, 833-846. (44) Chiou, C. T.; McGroddy, S. E.; Kile, D. E. Partition characteristics of polycyclic aromatic hydrocarbons on soils and sediments. Environ. Sci. Technol. 1998, 32, 264-269. (45) Cooke, C. M.; Bailey, N. J.; Shaw, G.; Lester, J. N.; Collins, C. D. Interaction of formaldehyde with soil humic substances: Separation by GFC and characterization by H-1-NMR Spectroscopy Bull. Environ. Contam. Toxicol. 2003, 70, 761-768. (46) Reiderer, M. Estimating partitioning and transport of organic chemicals in the foliage/atmosphere system: Discussion of a fugacity based model. Environ. Sci. Technol. 1990, 24, 829-837. (47) Tolls, J.; McLachlan, M. S. Partitioning of Semivolatile Organic Compounds between Air and Lolium multiflorum (Welsh Ray Grass). Environ. Sci. Technol. 1994, 28, 159-166. (48) Hauk, H.; Umlauf, G.; McLachlan, M. S. Uptake of Gaseous DDE in Spruce Needles. Environ. Sci. Technol. 1994, 28, 23722379. (49) Meneses, M.; Schuhmacher, M.; Domingo, J. L. A design of two simple models to predict PCDD/F concentrations in vegetation and soils. Chemosphere 2002, 46, 1393-1402. (50) Welsch-Pausch, K.; McLachlan, M. S.; Umlauf, G. Determination of the Principal Pathways of Polychlorinated Dibenzo-p-Dioxins and Dibenzofurans to Lolium multiflorum (Welsh Ray Grass). Environ. Sci. Technol. 1995, 29, 1090-1098. (51) Bacci, E.; Gaggi, C. Chlorinated Hydrocarbon Vapors and Plant Foliage - Kinetics and Applications. Chemosphere 1987, 16, 2515-2522. (52) Bacci, E.; Cerejeira, M. J.; Gaggi, C.; Chemello, G.; Calamari, D.; Vighi, M. Bioconcentration of Organic-Chemical Vapors in PlantLeaves - the Azalea Model. Chemosphere 1990, 21, 525-535. (53) Bacci, E.; Calamari, D.; Gaggi, C.; Vighi, M. Bioconcentration of Organic Chemical Vapors in Plant Leaves - Experimental Measurements and Correlation. Environ. Sci. Technol. 1990, 24, 885-889. (54) Komp, P.; McLachlan, M. S. Octanol/air partitioning of polychlorinated biphenyls. Environ. Toxicol. Chem. 1997, 16, 24332437. (55) Wang, M. J.; Jones, K. C. Uptake of Chlorobenzenes by Carrots from Spiked and Sewage Sludge Amended Soil. Environ. Sci. Technol. 1994, 28, 1260-1267. (56) Buckley, E. H. Accumulation of Airborne Polychlorinated Biphenyls in Foliage. Science 1982, 216, 520-522. (57) Schreiber, L.; Riederer, M. Determination of diffusion coefficients of octadecanoic acid in isolated cuticular waxes and their relationship to cuticular water permeabilities. Plant Cell Environ. 1996, 19, 1075-1082. (58) Muller, J. F.; Hawker, D. W.; Connell, D. W. Calculation of Bioconcentration Factors of Persistent Hydrophobic Compounds in the Air/Vegetation System. Chemosphere 1994, 29, 623-640. (59) Simonich, S. L.; Hites, R. A. Organic Pollutant Accumulation in Vegetation. Environ. Sci. Technol. 1995, 29, 2905-2914. (60) Komp, P.; McLachlan, M. S. Interspecies variability of the plant/ air partitioning of polychlorinated biphenyls. Environ. Sci. Technol. 1997, 31, 2944-2948. (61) Schreiber, L.; Schonherr, J. Uptake of Organic Chemicals in Conifer Needles - Surface Adsorption and Permeability of Cuticles. Environ. Sci. Technol. 1992, 26, 153-159.
(62) McCrady, J. K.; Maggard, S. P. Uptake and Photodegradation of 2,3,7,8-Tetrachlorodibenzo-p-Dioxin Sorbed to Grass Foliage. Environ. Sci. Technol. 1993, 27, 343-350. (63) Kao, A. S.; Venkataraman, C. Estimating the Contribution of Reentrainment to the Atmospheric Deposition of Dioxin. Chemosphere 1995, 31, 4317-4331. (64) Chamberlain, A. C. Radioactive Aerosols; Cambridge University Press: Cambridge, 1991; Vol. 3. (65) Riederer, M.; Daiss, A.; Gilbert, N.; Kohle, H. Semi-volatile organic compounds at the leaf/atmosphere interface: numerical simulation of dispersal and foliar uptake. J. Exp. Bot. 2002, 53, 18151823. (66) Nakajima, D.; Yoshida, Y.; Suzuki, J.; Suzuki, S. Seasonal Changes in the Concentration of Polycyclic Aromatic Hydrocarbons in Azalea Leaves and Relationship to Atmospheric Concentration. Chemosphere 1995, 30, 409-418. (67) Welschpausch, K.; McLachlan, M. S.; Umlauf, G. Determination of the Principal Pathways of Polychlorinated Dibenzo-p-Dioxins and Dibenzofurans to Lolium multiflorum (Welsh Ray Grass). Environ. Sci. Technol. 1995, 29, 1090-1098. (68) Hetrick, D. M.; McDowell-Boyer, L. M. A user’s manual for TOXSCREEN: A multimedia screening-level program for assessing the potential fate of chemicals released to the environment; Oak Ridge National Laboratory: Oak Ridge, TN, and U. S. EPA, Office of Toxic Substances: Washington, DC, 1984. (69) Dreicer, M.; Hakonson, T. E.; White, G. C.; Whicker, F. W. Rainsplash as a Mechanism for Soil Contamination of Plant Surfaces. Health Phys. 1984, 46, 177-187. (70) Guggenberger, G.; Pichler, M.; Hartmann, R.; Zech, W. Polycyclic aromatic hydrocarbons in different forest soils: mineral horizons. Z. Pflanz. Bodenk 1996, 159, 565-573. (71) Kaupp, H.; Blumenstock, M.; McLachlan, M. S. Retention and mobility of atmospheric particle-associated organic pollutant PCDD/Fs and PAHs in maize leaves. New Phytol. 2000, 148, 473-480. (72) Little, P.; Wiffen, R. D. Emission and deposition of petrol engine exhaust Pb-I. Deposition of exhaust Pb to plant and soil surfaces. Atmos. Environ. 1977, 11, 437-447. (73) Pinder, J. E., III; McLeod, K. W.; Lide, R. F.; Sherrod, K. C. Mass loading of soil particles on a pasture grass. J. Environ. Radioact. 1991, 13, 341-354. (74) Hulster, A.; Marschner, H. Transfer of PCDD/PCDF from Contaminated Soils to Food and Fodder Crop Plants. Chemosphere 1993, 27, 439-446. (75) Hung, H.; Mackay, D. A novel and simple model of the uptake of organic chemicals by vegetation from air and soil. Chemosphere 1997, 35, 959-977. (76) Chiou, C. T.; Sheng, G. Y.; Manes, M. A partition-limited model for the plant uptake of organic contaminants from soil and water. Environ. Sci. Technol. 2001, 35, 1437-1444. (77) USDA. USDA National Nutrient Database for Standard Reference, Release 16; U.S. Department of Agriculture: Washington, DC, 2005. http://www.nal.usda.gov/fnic/foodcomp/Data/SR16/ reports/sr16page.htm. (78) Flindt, R. Biologie in Zahlen. Eine datensammlung in tabellen mit uber 10 000 Einzelwerten; Gustav Fischer Verlag: Stuttgart/ New York, 1988. (79) Tam, D. D.; Shiu, W. Y.; Qiang, K.; Mackay, D. Uptake of chlorobenzenes by tissues of the soybean plant: Equilibria and kinetics. Environ. Toxicol. Chem. 1996, 15, 489-494. (80) Burken, J. G. Uptake and metabolism of organic compounds the green liver model. In Phytoremediation - Transformation and Control of Contaminants; McCutcheon, S. C., Schnoor, J. L., Eds.; John Wiley and Sons: Hoboken, NJ, 2003; p 987. (81) Huckelhoven, R.; Schuphan, I.; Thiede, B.; Schmidt, B. Biotransformation of pyrene by cell cultures of soybean (Glycine max L.), wheat (Triticum aestivum L.), jimsonweed (Datura stramonium L.), and purple foxglove (Digitalis purpurea L.). J. Agric. Food Chem. 1997, 45, 263-269. (82) Shang, T. Q.; Gordon, M. P. Transformation of C-14 trichloroethylene by poplar suspension cells. Chemosphere 2002, 47, 957-962. (83) Ugrekhelidze, D.; Korte, F.; Kvesitadze, G. Uptake and transformation of benzene and toluene by plant leaves. Ecotoxicol. Environ. Saf. 1997, 37, 24-29. (84) Nepovim, A.; Hubalek, M.; Podlipna, R.; Zeman, S.; Vanek, T. In-vitro degradation of 2,4,6-trinitrotoluene using plant tissue cultures of Solanum aviculare and Rheum palmatum. Eng. Life Sci. 2004, 4, 46-49. VOL. 40, NO. 1, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
51
(85) Hannink, N. K.; Rosser, S. J.; Bruce, N. C. Phytoremediation of explosives. Crit. Rev. Plant Sci. 2002, 21, 511-538. (86) Chekol, T.; Vough, L. R.; Chaney, R. L. Plant-soil-contaminant specificity affects phytoremediation of organic contaminants. Int. J. Phytoremediat. 2002, 4, 17-26. (87) Schnabel, W. E.; Dietz, A. C.; Burken, J. G.; Schnoor, J. L.; Alvarez, P. J. Uptake and transformation of trichloroethylene by edible garden plants. Water Res. 1997, 31, 816-824. (88) Niu, J. F.; Chen, J. W.; Martens, D.; Henkelmann, B.; Quan, X.; Yang, F. L.; Seidlitz, H. K.; Schramm, K. W. The role of UV-B on the degradation of PCDD/Fs and PAHs sorbed on surfaces of spruce (Picea abies (L.) Karst.) needles. Sci. Total Environ. 2004, 322, 231-241. (89) Trapp, S.; Matthies, M. Generic One-Compartment Model For Uptake of Organic Chemicals By Foliar Vegetation. Environ. Sci. Technol. 1995, 29, 2333-2338. (90) McFarlane, C.; Pfleeger, T.; Fletcher, J. Effect, Uptake and Disposition of Nitrobenzene in Several Terrestrial Plants. Environ. Toxicol. Chem. 1990, 9, 513-520.
52
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 1, 2006
(91) Collins, C. D.; Bell, J. N. B.; Crews, C. Benzene accumulation in horticultural crops. Chemosphere 2000, 40, 109-114. (92) Ma, X. M.; Burken, J. G. TCE diffusion to the atmosphere in phytoremediation applications. Environ. Sci. Technol. 2003, 37, 2534-2539. (93) 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, 12311239. (94) Trapp, S., MaFarlane, J. C., Eds. Plant Contamination Modelling and Simulation of Organic Chemical Processes; Lewis Publishers: London, 1995.
Received for review April 28, 2005. Revised manuscript received October 11, 2005. Accepted October 19, 2005. ES0508166
