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Uptake and translocation of organic pollutants in plants: A review
Journal of Integrative Agriculture 2017, 16(8): 1659–1668 Available online at www.sciencedirect.com
ScienceDirect
REVIEW
Uptake and translocation of organic pollutants in plants: A review ZHANG Cheng1, FENG Yao1, LIU Yuan-wang1, CHANG Hui-qing2, LI Zhao-jun1, XUE Jian-ming3 1
Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture/China-New Zealand Joint Laboratory for Soil Molecular Ecology, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China 2 Henan University of Science and Technology, Luoyang 471003, P.R.China 3 Scion, Christchurch 29-237, New Zealand
Abstract Organic pollutants, such as polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/Fs), polychlorinated biphenyls (PCBs), antibiotics, herbicides, and bisphenol A (BPA), are commonly found in agricultural environments. They are released into the environment as a result of their use for human health purposes and farm management activities, and are often discharged as waste-water effluents. Most of these organic pollutants are taken up by plants through roots and leaves, and when they enter the tissue, they cause serious damage to the plants. Although the toxicity of organic pollutants to plants, especially to plant cells, has been intensively studied, a systematic review of these studies is lacking. Here we review researches on the toxicity of organic pollutants, their uptake, and translocation in plants. Our objective is to assemble existing knowledge concerning the interaction of organic pollutants with plants, which should be useful for the development of plant-based systems for removing pollutants from aquatic and agricultural environments. Keywords: organic pollutants, plant, uptake, cytotoxicity
1. Introduction Normal development and productivity of plants depends upon internal and external factors. Natural and man-made chemicals are important external factors that exert detrimental effects on plants. Some organic pollutants, such as hormones and persistent organic pollutants (POPs), including polychlorinated dibenzo-p-dioxins and polychlori-
Received 8 November, 2016 Accepted 6 March, 2017 Correspondence LI Zhao-jun, Tel: +86-10-82108657, E-mail: [email protected] © 2017 CAAS. Publishing services by Elsevier B.V. All rights reserved. doi: 10.1016/S2095-3119(16)61590-3
nated dibenzofurans (PCDD/Fs), polychlorinated biphenyls (PCBs), and antibiotics, herbicides and bisphenol A (BPA), have drawn significant attention in environmental science and engineering research. Several countries and international organizations have published lists of harmful pollutants, which need to be controlled urgently. For example, the World Wildlife Fund listed 67 types of environmental hormones in 1997 that were considered harmful (Karissa 2002). Under the Stockholm Convention, countries agreed to reduce or eliminate the production, use, and/or release of 12 key POPs, and as specified under the Convention, a scientific review process led to the addition of other POP chemicals of global concern in 2001 (Anonymous 2008). Although most of these chemicals are beneficial, they may have unforeseen effects on the environment (Myöhänen et al. 2009). Many studies have been conducted on the toxicity of organic pollutants to plants cells and on the up-
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take of organic pollutants by plants. Here we review these studies, focusing primarily on (1) the uptake of organic pollutants by plants and their detrimental effects on plant cells, particularly irreversible cytotoxicity and (2) recent progress on the negative impacts of PCDD/Fs, PCBs, antibiotics, herbicides, and BPA on plant growth, reproduction, and crop productivity. This review could be useful in the development of plant based systems for removing organic pollutants from environments.
2. Uptake and translocation of organic pollutants by plants The uptake pathway of organic pollutants in plants Most organic pollutants are absorbed by plants either from soil or air. As shown in the Table 1 and Fig. 1, the organic pollutants, including PCBs and PCDD/Fs can be absorbed by plants from soil (through roots) or air (through leaves directly from the air or after these pollutants evaporate from
Table 1 Pathway of plant uptake of organic pollutants Organic pollutant1) PCBs (PCB3, PCB15, PCB28, PCB52, PCB73) PCDD/Fs
Tissue tested Root Foliage Root
Foliage Antibiotics (tetracyclines, polyether, semisynthetic and macrolides, aminoglycosides, sulfa, and β-lactams antibiotics)
Root
BPA
Root
Herbicides (sulfonylurea, imidazolinone, triazines, phenylureas, uracilsand, and sulfonamide families)
1)
Root and foliage
Species Hybrid poplar Bluegrass, Luzula, and Betula Cucurbita, rouzi grass (Thylacospermum caespitosum), lettuce, potato, apple, pear, rice, pea, and oilseed rape Rice and radish
Reference Liu and Jerald (2008) Pier et al. (2002) Engwall and Hjelm (2000); Zhang et al. (2009); Li et al. (2014)
Stefan and Michael (1997); Wu et al. (2002) Spinach, lettuce, carrot, radishes, Migliore et al. (2003); Alistair potatoes, onion and garlic, wheat, et al. (2006); Grote et al. cucumber, pinto beans (2007); Bassil et al. (2013); Kang et al. (2013); David et al. (2016) Rice, tobacco Nakajima et al. (2002); Noureddin et al. (2004) Pea, coffee plant, orange plant Sterling (1994); Jurado et al. (1999); Papiernik et al. (2012); Goncalves (2016)
PCBs, polychlorinated biphenyls; PCDD/Fs, polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans; BPA, bisphenol A.
1. Toxicity of organic pollutants to leave cells: (1) Abnormal cell ultrastructure; (2) Disturbed cell biosynthesis;
2. Pollutants uptake by plant from air: (1) PCBs;
(3) Disturbed DNA, etc.
(2) PCDD/Fs; (3) Herbicides, etc.
3. Factors influncing uptake/ translocation:
Translocation
(1) Organic pollutant factors; (2) Plant biological characteristics factors; (3) Environmental media factors.
4. Pollutants uptake by plants from soil: (1) PCBs; (2) PCDD/Fs; (3) Antibiotics; (4) BPA, etc. 5. Toxicity of organic pollutants to root cells: Inordinate mitotic division.
Fig. 1 Uptake and translocation of organic pollutants in plants, factors influencing uptake, and the toxic effects of organic pollutants in plants. PCBs, polychlorinated biphenyls; PCDD/Fs, polychlorinated dibenzofurans; BPA, bisphenol A.
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soil). Herbicides can also be taken up by plants from soil through roots and air after plant leaves come in contact with them. The other organic pollutants, such as antibiotics and BPA, are only absorbed by plants from the soil through roots. This may be because most organic pollutants have low volatility and are mainly exposed to plants through soil or water. The plant root is usually the first tissue that comes in contact with organic pollutants and therefore absorption via roots is the most common method of uptake. Factors influencing uptake of organic pollutants by plants Uptake and translocation of organic pollutants by plants are affected by the physical and chemical properties of the organic pollutants, the biological characteristics of the plants, and the environmental media (Table 2 and Fig. 1). The physical and chemical properties of organic pollutants influencing plant uptake include molecular mass and hydrophobicity with the parameters KOW and KOA. KOW is the partition coefficient between octanol and water, and KOA is the partition coefficient between octanol and air. When the molecular mass of an organic pollutant is below 1 000, it is easily taken up by plant roots. Similarly, organic pollutants with high KOW values are easily absorbed by plant roots and a positive correlation has been found between KOW value and the concentration of organic pollutants in plants. In addition, organic pollutants with low KOA values are easily absorbed by plants from air. Among all the biological features of plants, the root extractable lipid content has the strongest influence on the uptake of organic pollutants. Regarding environmental media factors, indirect factors, including the background electrolyte type, dissolved organic carbon (DOC) concentration, pH, and organic matter content are more important than temperature. These factors mainly impact on uptake of organic pollutants by influencing the adsorption of organic pollutants on soils or the formation of chelates. Therefore, particular attention should be paid to the physical and chemical properties of organic pollutants, such as molecular mass, KOW, and KOA, and the biological characters of the plants such as the root extractable lipid content, when we consider the removal of organic pollutants from the environment. There are some factors, such as the solubility and concentration of organic pollutants, which have real effects on their uptake and translocation by plants, but they are of minor importance when compared with the above factors. Generally, organic compounds dissolved in soil water are easily absorbed by plant roots. However, even when their solubility is low, they can be absorbed by plant roots by passive or active uptake (Inui et al. 2008). In passive uptake, the absorption of organic pollutants is a concentration-dependent process and hence uptake is influenced by the concentration of organic pollutants (Vanier et al. 2001). Most studies show that uptake of organic chemicals by plant
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roots is a passive and diffusive process, except for the uptake of a few hormone-like chemicals, such as the phenoxy acid herbicides, for which there is evidence of active uptake (Ryan et al. 1988; Bromilow and Chamberlain 1995; Collins et al. 2006). Most active uptake processes are affected by plant lipid content and plant metabolism (Paterson et al. 1990; Collins 2008). The modes and mechanisms of uptake and translocation of organic pollutants by plants Many studies have been carried out to determine the modes and mechanisms of uptake and translocation of organic pollutants by plants. In recent years, most researchers have focused on the uptake of organic pollutants by plant roots. These studies have shown that the organic pollutants are first enriched at the root surface and they pass into the roots together with water. They pass through the cuticle-free unsuberized cell walls of young root hairs that are located closely behind the tip of the root ((5±50) mm). After penetration, they move towards the xylem transport tissue in the root along free intercellular space (apoplastic way) or cells (symplastic way) (Sitte and Ziegler 1991; Kvesitadze et al. 2015). In the root cortex, the cell-wall between the cells is porous, and chemicals can move freely from solution to the interior before they reach the endodermis (Trapp and Mc Farlane 1994). After uptake by plants, organic pollutants such as POPs are translocated to different parts of the plants (Lin et al. 2007). Generally, two kinds of organic pollutant transport pathways in higher plants have been reported: (i) intracellular and intercellular transport (short distance transport) and (ii) conducting tissue transport (long distance transport) (Taiz and Zeiger 2002). The mechanism for the transportation of specific organic pollutants varies with the physicochemical properties of organic pollutants. Su and Zhu (2007) reported that dinitrotoluene and dinitrobenzene are transported into plants via the symplastic pathway, whereas phenanthrene and pyrene are transported via the apoplastic pathway. The transportation of organic pollutants in plant phloem and xylem depends upon the size of the molecule. For example, organic pollutants with small molecule size can easily permeate the membrane and hence, easily come in and go out of the phloem and xylem. On the other hand, organic pollutants with large molecule size have low permeability in membranes and therefore cannot be effectively transported in the phloem (Kvesitadze et al. 2015).
3. Toxicity of organic pollutants to plants cells Organic pollutants may have toxic effects on plant cell ultrastructure, biosynthesis, membrane stability and DNA (Fig. 1).
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Table 2 Factors influencing uptake and translocation of organic pollutants by plants Factor Organic pollutant factors Molecular mass
Hydrophobicity KOW (the partition coefficient between octanol and water)
KOA (the partition coefficient between octanol and air)
Plant biological characteristics factors Root extractable lipid content (associated with Klip)
Carbohydrate content of plant cell walls
Transpiration stream concentration factor (TSCF) Permeability of biomembranes, pH of membranes, and electrical gradients across plant cell membranes Epicuticular waxes Environmental media factors Background electolyte type Concentration of dissolved organic carbon (DOC) PH of environmental media PH of environmental media Organic matter content of soil
Temperature
Example or explanation Organic pollutants, which have low-molecular mass and volatility, can be absorbed by roots and foliage. However, high-molecular mass organic pollutants, which are nonvolatile and possess strong hydrophobic properties, can only be absorbed by roots (Fismes et al. 2002). Molecular mass of organic pollutants is the leading factor influencing the plant-uptake process. Compounds with molecular mass below 1 000 can be easily absorbed by plant roots (Kvesitadze et al. 2015). Polychlorinated biphenyls (PCBs) with higher KOW values were bound strongly to root tissues and were prevented from entering the transpiration stream (Liu and Jerald 2008). There was a positive correlation between the concentration of organic pollutant in barley and KOW of PCB (Briggs et al. 1982; Moeckel et al. 2008). PCB with KOA>60 entered plants mainly from air rather than from soil (Cousins and Mackay 2001). Semi-volatile organic pollutants with KOA<85 entered plant foliage mainly as gas and established a distribution equilibrium between foliage and air. Semi-volatile organic pollutants with 85110 entered plant foliage mainly as sediment particles (Mclachlan 1999). There was a positive correlation between organic pollutant content and lipid content in plant roots (Gao et al. 2005). Root uptake of polychlorinated dibenzofurans (PCDD/Fs) from nutrient solution was dominated by lipophilic adsorption, and root accumulation of PCDD/Fs from soil solutions could be predicted by extractable lipid content in plant root (Zhang et al. 2009). Most polycyclic aromatic hydroxys (PAHs) were detected in plant cell walls which consist mostly of carbohydrate. Therefore, the carbohydrate content of plant cells played a leading role in the uptake of PAHs by plants (Chen et al. 2009; Zhang and Zhu 2009). The TSCF can show the capacity of organic pollutant translocation from roots to aboveground parts (Dettenmaier et al. 2009). These membrane characteristics can be used to predict accumulation concentrations of organic pollutants (Sitte and Ziegler 1991; Sterling 1994). The amount and composition of epicuticular waxes greatly affected the capacity of PCB plant-uptake from air (Moeckel et al. 2008). Increased plant uptake of chlor-tetracycline (CTC) and tylosin in the presence of Ca2+ ion compared with Na+ (Lee et al. 2014). Increased plant uptake of CTC by DOC, which may be explained by competition between DOC and CTC for sorption sites of soils (Tao et al. 2010; Lee et al. 2014). The transfer capacity of organic pollutants in soil is good in acidic or alkaline media but poor in media with intermediate pH (Sithole and Guy 1987). The concentration of antibiotics in plants was greater when the pH of the nutrient solution was 6 than when the pH was 4 and 8 (Min 2012). Increased organic matter content of soil decreased the plant uptake of organic pollutants because some organic pollutants (ionized compounds) might be strongly bound to soil organic matter which is a strong anion/cation exchanger (Trapp and McFarlane 1994). Higher temperature coefficient for diffusion processes of organic pollutants can accelerate passive absorption by the plant. On the other hand, temperature rise stimulated transpiration stream rate and enzyme activity of plants (Korte et al. 2000).
3.1. Toxicity of organic pollutants to plant cell ultrastructure The cell ultra-structure or micro structures cannot be distin-
guished clearly by optical microscope. These micro structures include the cell membranes, endoplasmic reticulum, retinal and nuclear membranes, ribosomes and microtubules (MT) or microfilaments. The essential function of a cell is
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controlled by these ultra-structures. Plant cells will become abnormal or even die if the cell’s ultra-structures are damaged or destroyed (Gunning and Steer 1975; Agarwal 2006). When organic pollutants are absorbed into plant cells, they can cause disorder of the cell ultrastructure. For example, tobacco cells were destroyed when tobacco was exposed to WHO98-TEQ of PCDD/Fs at the concentration of 10 000 mg kg–1. The surface of cell walls became coarse and wrinkled, the cytoplasm began to leak, and the shape of the chloroplast transverse section was changed from round to hexagonal (Zhang et al. 2012). Some organic pollutants, such as diphenylether and bipyridylium often induce cell membrane disruption which, in turn, damage the plant tissues (Gunsolus and Curran 1991; Boczkowski and Hoet 2010; Ramadass et al. 2015). Microtubes are formed by the assembly of α- and β-tubulins and MT-associated proteins and can be damaged by organic pollutants (Nancy et al. 2014). Exposure of Allium cepa meristematic root cells to fungicides, such as thiabendazole (TBZ) or griseofulvin (GF) at the concentration of 100 μg mL–1 can cause microtubular damage such as abnormal arrays. Griseofulvin can induce a high frequency of abnormal pre-prophasic bands, mitotic spindles, phragmoplasts, and abnormal tripolar spindles. Other organic pollutants such as BPA can induce microtubule array disruption in pea (Pisum sativum L.) meristematic root-tip cells. Microtubules of pea meristematic root-tip cells can be loosened by BPA, causing the mean diameter to increase from (23±0.70) nm in untreated cells to (32±0.14) nm in cells treated with BPA and then to be completely depolymerized (Adamakis et al. 2013).
3.2. Toxicity of organic pollutants to cell biosynthesis Recent research on the impact of organic pollutants on plant cell biosynthesis has mainly focused on the detrimental effects on photosynthesis, and synthesis of proteins, amino acids, nucleic acids, lipids, and hormones. For example, PCBs and herbicides have been found to be detrimental to cell biosynthesis (Moore and Harriss 1974; Moore and Roberts 1998; Brain et al. 2010). Similarly, it was found that PCBs, antibiotics, and herbicides can inhibit photosynthesis in plants cells. Photosynthesis is an essential process in plants, which is responsible for supporting growth, nutrient uptake and resistance to abiotic or biotic stresses (Xia et al. 2004; Yang et al. 2008; Bassil et al. 2013). PCBs were found to inhibit photosynthetic carbon assimilation in both natural phytoplankton communities and unialgal cultures at the concentration of 10.0 μg L–1 (Engwall and Hjelm 2000). PCBs may also affect the photosynthetic light reactions as it has been shown that photosynthesis-irradiance curves decrease in the presence of PCBs (Harding and Phillip 1978; Liu et al. 2010). The impacts of oxytetracycline (OTC) on wheat photosynthesis resembled stresses caused by salt, alkali,
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and heavy metals. The photosynthesis rates, transpiration rates, and stomatal conductance significantly decreased in all OTC-treated plants of a sensitive cultivar (Li et al. 2011). Similarly, photosynthesis inhibitors were also found in herbicide families such as the triazines, phenylureas, uracils, benzothiadiazoles, and nitriles. These photosynthesis inhibitors shut down the photosynthetic process in susceptible plants by binding organic pollutants to specific sites within the plants chloroplasts (Bunce 2008). Herbicides could also prevent plants from forming photosynthetic pigments, causing green leaves and stems of plants to become white and translucent (Kaspary et al. 2014). It has been reported that RNA, protein, and lipid synthesis could be significantly inhibited by prolonged exposure to hexazinone and chlorsulfuron (Fisher 1975; Yang et al. 2010). Some herbicides, such as sulfonylurea, imidazolinone, and sulfonamide have been found to suppress the synthesis of three essential branch-chain amino acids, which inhibit one key enzyme in plants (Aubert et al. 1997), while herbicides made mainly from an amino acid derivative inhibited the production of three essential aromatic amino acids (Amaia et al. 2013). All these organic pollutant effects can be ascribed to restraining the activities of key enzymes in plants. For example, glyphosate and imazamox could inhibit the biosynthesis of aromatic and branched-chain amino acids, respectively, by inducing the ubiquitin-26S protein system and papain-like cysteine proteases (Zobiole et al. 2009). Although these herbicides inhibit different pathways, they have been found to have common physiological effects, such as increasing free amino acid contents and decreasing soluble protein contents (Amaia et al. 2013). Currently, studies on how new contaminants such as antibiotics affect cell function, are still lacking. Their mechanism is likely to be far more complex than other organic pollutants such as herbicides.
3.3. Toxicity of organic pollutants to membrane stability Unsaturated lipids become rancid due to oxidative deterioration when they react directly with the oxygen molecule (Zward et al. 1999; Chen et al. 2016). This process is called lipid peroxidation (LPO). The insertion of an oxygen molecule is catalyzed by free radicals (non-enzymatic lipid peroxidation) or enzymes (enzymatic lipid peroxidation). It has been shown that LPO induces disturbance of fine structures, alteration of integrity, fluidity, and permeability, and functional loss of biomembranes, and modifies low density lipoprotein to proatherogenic and proinflammatory forms, and generates potentially toxic products (Greenberg et al. 2008). Malondialdehyde (MDA) provides an analytical index to indicate lipid peroxidation of membranes. The larger the content of MDA, the less stable the membranes becomes.
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It has been found that the toxic effect and oxidative stress caused by PCDD/Fs can be indicated by an increase in MDA content (Zhang et al. 2012). There are some reports showing that oxidative stress can be induced by oxytetracycline in water solution (Li et al. 2011). MDA contents were positively correlated with the inhibition rates of antioxidative enzyme activities. It has also been shown that tetracycline may significantly augment MDA content when the levels of tetracycline exceed 5 mg L–1 (Xie et al. 2011b).
3.4. Organic pollutant damage to DNA in plants cells PCBs and herbicides have been found to cause damage to DNA of plant cells. DNA was significantly damaged in leaf nuclei of tobacco plants when they were grown in PCB-polluted soil. When measured by the comet assay, the tail moment (TM) value in leaf nuclei of plants cultivated for 8 weeks in PCB polluted soil ((10.0±1.4) μm), was significantly higher than the corresponding value in nuclei of control plants ((2.3±0.4) μm) (Tomáš et al. 2007). When the root tip cells of soybeans were cultivated in glyphosate for 8 h, the cometic rate, comet tail length, DNA content of tail, tails and olive-tailed margins, and other indicators were significantly different from the control, and there were clear dose-response relationships for all the indicators (Li et al. 2012). DNA fragmentation increased in a dose-dependent manner with dicamba (3,6-dichloro-2-methoxybenzoicacid) (Suleyman et al. 2010). However, it is worth noting that maleic hydrazide (MH) did not cause DNA damage to Arabidopsis thaliana when the alkaline denaturation and neutral gel electrophoresis protocol was used for the comet assay (Merten et al. 2001). Some studies have revealed that DNA damage can be caused by polycyclic aromatic hydrocarbons (PAHs). Tail moment values from the comet assay increased from 46.41 μm (control) to 122.04 μm when plants were treated with phenanthrene at the concentration of 50 mg kg–1. The degree of DNA damage increased with the increase of pyrene concentrations (0–50 mg kg–1). It was also found that pyrene treatment at the concentration of 50 mg kg–1 caused significant damage to the DNA of Vicia faba root tip cells. The TM value increased from 44.3 μm in the control treatment to 110.36 μm in pyrene treated plants (Gao et al. 2014a). DNA damage to Vicia faba root tip cells caused by phenanthrene was also investigated using the comet assay. DNA damage was aggravated with an increase in phenanthrene concentrations from 0 to 0.6 mg L–1 (Gao et al. 2014b).
3.5. Responses of inordinate mitotic division to organic pollutants Reports on damage to inordinate mitotic division induced
by PCBs have mainly focused on algal species (Goel et al. 2006; Song et al. 2006). PCBs have been found to affect cell division rates in several algal species. For example, cell division of Thalassiosira pseudonana strain 3H, Chaetoceros socialis, Skeletonema costatum, Thalassiosira pseudonana 13-I, Monochrysis lutheri, and Isochrysis galbana was found to be significantly inhibited by PCB at low concentration (Fisher 1975). Cell division of Porphyra haitanensis was also found to be significantly affected by PCBs; division rates decreased with increase in PCB concentration (Wang et al. 2006). In higher plants, chlortetracycline may also prevent cells from entering cell division. A possible reason for this could be the depression of protein synthesis and enzyme activities and the disruption of normal organelle function, which may result in inhibition of mitotic division in plant root tip cells (Luciana et al. 2003). Xie et al (2010, 2011a, b) conducted a series of studies on toxicity of chlortetracycline and tetracycline to plant cells. They found that chlortetracycline and tetracycline slightly increased the frequencies of micronucleus and chromosomal aberration, and sister chromatid exchange in plant root tips at the lowest concentration (0.0625–250 mg L–1 of chlortetracycline and 0.25–10 mg L–1 of tetracycline). However, the chromosomal aberration frequency was significantly raised as the concentration of tetracycline increased from 0.5 to 300 mg L–1. At higher concentrations (250–300 mg L–1 of chlortetracycline and 50–300 mg L–1 of tetracycline), the frequencies of micronucleus aberration, chromosomal aberration, and sister chromatid exchange were reduced because of acute cell toxicity (Xie et al. 2010, 2011a, b). Furthermore, genotoxicity occurred early and then influenced mitotic activity when the plants were under the stress of organic pollutants. Tetracycline could stimulate root cell mitotic division of wheat when concentrations ranged from 0.5 to 10 mg L–1. It was also found that tetracycline at high concentrations (>50 mg L–1) could significantly inhibit mitotic index in a concentration-dependent manner (Xie et al. 2011a). Tetracycline could stimulate mitotic cell division of wheat when the tetracycline concentrations ranged from 0.25 to 1 mg L–1. However, it could cause a concentration-related decrease in mitotic index (MI) when the concentrations ranged from 50 to 300 mg L–1. These results indicate that antibiotics, such as tetracyclines and chlortetracycline might be genotoxic to plants cells, and pose a genotoxic risk to living organisms (Xie et al. 2011b). Similarly, Andrioli and Mudry (2011) found that TBZ can lead to disorder in mitotic cell division (Andrioli and Mudry 2011). In another study, TBZ also inhibit onion meristematic root cells mitosis. Onion (Allium cepa) meristematic root cells were exposed to a TBZ-containing pharmaceutical formulation at concentrations of 10–250 mg L–1. The inhibition of mitotic index and induction of C-metaphases, lagging chromosomes, polyploidy and binucleated
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cells, which possibly result in the alteration of chromosomal segregation and cytokinesis, were investigated (Andrioli and Mudry 2011). The effects of pharmaceutical formulations containing the microtubule disruptors TBZ and griseofulvin (GF) on the mitotic machinery of Allium cepa meristematic cells have also been characterized (Nancy et al. 2014). Griseofulvin inhibited mitotic index and caused genotoxic impacts, including increased chromosome fragmentation, bridging and lagging, C-metaphases, tripolar cell division, disorganized anaphases, and nuclear abnormalities in interphase cells of plants. Effects of these organic pollutants on the mitotic machinery were studied by using the method of direct immune fluorescence with β-tubulin labeling and by DNA counter-staining with 4’,6-diamidino-2-phenylindole (DAPI). The results suggested that GF could induce abnormalities in spindle symmetry/polarity. TBZ could also cause chromosome mis-segregation, polyploidy, and lack of cytokinesis (Nancy et al. 2014). Furthermore, a study of the genotoxicity of BPA on onion root meristematic cells showed that exposure to 50, 100, 150, and 200 mg L–1 BPA for five days increased the proportion of CA (break) from 0.4 to 7.2% and CA (fragments) from 0.3 to 3.2% (Jadhav et al. 2012). When the root tips of young seedlings of Pisum sativum L. were exposed to BPA at the concentration of 20, 50, and 100 mg L–1 for 1, 3, 6, 12, and 24 h, the BPA at all concentrations affected normal chromosome segregation, hampered the completion of cytokinesis and deranged the interphase. This suggests that BPA exerted acute anti-mitotic effects on meristematic root-tip cells of P. sativum (Adamakis et al. 2013).
4. Conclusion Currently, many investigations have shown that toxic chemicals not only harm people, but also affect plants. Organic pollutants can be taken up by plants through both roots and foliage. Molecular mass, hydrophobicity, root extractable lipid content, background electrolyte type, dissolved organic carbon, pH, and soil organic matter content are the main factors that influence the uptake and translocation process of organic pollutants in plants. Cell walls and membranes, chloroplasts, and microtubules can show the potential toxicity of pollutants to cell ultrastructure. To explore the damage to cell function caused by organic pollutants, we have summarized pollutant effects on cell biosynthesis and membrane stability, including the synthesis of RNA, lipids, proteins, and photosynthetic pigments. Furthermore, we have clearly segregated the DNA damage and inordinate mitotic division to illustrate genotoxic effects, which are a major issue of this paper. Based on the results, we conclude that these pollutants harm plant genes, which may lead to gene mutation and variation. Although research
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has improved our knowledge about pollutants and stringent regulations aiming to protect public health have already been undertaken, some pollutants, such as antibiotics and herbicides cannot be banned entirely, because they are necessary for human and animal health as well as for crop production. Thus, monitoring these organic chemicals is important for public health and improving the biotic environment, and the presence and trends of these pollutants in the atmosphere, soil, and plants has been the subject of many environmental studies all over the world. We consider that there should be more studies undertaken to determine precise transfer pathways and their temporal pattern, and to pinpoint genotoxicity more precisely in plants cells. An improved understanding of these factors will allow improved control of cumulative toxic effects on plants and reduce harmful impacts of pollutants.
Acknowledgements This work was jointly supported by the special projects foundation of the National Natural Science Foundation of China (31572209), the Beijing Municipal Sciences and Technology Commission, China (Z141105000614012), the Shanxi Province Science and Technology Research Project, China (20140311008-4).
References Adamakis I D S, Emmanuel P, Anna C, Eleftherios P. 2013. Effects of bisphenol A on the microtubule arrays in root meristematic cells of Pisum sativum L. Mutation Research, 750, 111–120. Agarwal U P. 2006. Raman imaging to investigate ultrastructure and composition of plant cell walls: Distribution of lignin and cellulose in black spruce wood (Picea Mariana). Planta, 224, 1141–1153. Alistair B, Paul J, Edward J S, Chris J S, Edward S, Len S L. 2006. Uptake of veterinary medicines from soils into plants. Journal of Agricultural and Food Chemistry, 54, 2288–2297. Amaia Z, Miriam G M, Villamor J G, Zabalza A, Hoorn R A, Royuela M. 2013. Proteolytic pathways induced by herbicides that inhibit amino acid biosynthesis. PLOS ONE, 8, e73847. Andrioli N B, Mudry M D. 2011. Cytological and cytogenetic effects induced by thiabendazole on Allium cepa root meristems. Journal of Basic and Applied Genetics, 2, 17–23. Anonymous. 2008. Text of the stockholm convention. Amended in 2009, 2011, 2013 and 2015. [2016-10-12]. http://chm. pops.int/TheConvention/Overview/TextoftheConvention/ tabid/2232/Default.aspx Aubert S, Bligny R, Day D A, Whelan J, Douce R. 1997. Induction of alternative oxidase synthesis by herbicides inhibiting branched-chain amino acid synthesis. The Plant Journal, 11, 649–657.
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Bassil R J, Bashour II, Sleiman F T, Abou-Jawdeh Y A. 2013. Antibiotic uptake by plants from manure-amended soils. Journal of Environmental Science and Health (Part B: Pesticides Food Contaminants and Agricultural Wastes), 48, 570–574. Boczkowski J, Hoet P. 2010. What’s new in nanotoxicology? Implications for public health from a brief review of the 2008 literature. Nanotoxicology, 4, 1–14. Brain R A, Solomon K R, Brooks B W. 2010. Targets, effects and risks in aquatic plants exposed to veterinary antibiotics. ACS Symposium Series, 1018, 169–189. Briggs G G, Bromilow R H, Evans A A. 1982. Relationships between lipophilicity and root uptake and translocation of non-ionised chemicals by barley. Pesticide Science, 13, 495–504. Bromilow R H, Chamberlain K. 1995. Principles governing uptakeand transport of chemicals. In: Trapp S, Mc Farlane J C, eds., Plant Contamination: Modellingand Simulation of Organic Chemical Processes. Lewis Publishers, London. pp. 38–64. Bunce J A. 2008. Acclimation of photosynthesis to temperature in Arabidopsis thaliana and Brassica oleracea. Photosynthetica, 46, 517–524. Chen L, Zhang S, Huang H, Wen B, Christie P. 2009. Partitioning of phenanthrene by root cell walls and cell wall fractions of wheat (Triticum Aestivum L.). Environmental Science & Technology, 43, 9136–9141. Chen X N, Qiu D Y, Lin H M. 2016. Botanical characteristics and medicinal value of five Glycyrrhiza species cultivated in the Hexi region of Gansu. Acta Prataculturae Sinica, 25, 246–253. (in Chinese) Collins C, Fryer M, Grosso A. 2006. Plant uptake of non ionic organic chemicals. Environmental Science and Technology, 40, 45–52. Collins D C. 2008. A semi-quantitative approach to deriving a model structure for the uptake of organic chemicals by vegetation. International Journal of Phytoremediation, 10, 371–377. Cousins I T, Mackay D. 2001. Strategies for including vegetation compartments in multimedia models. Chemosphere, 44, 643–654. David A, Christiana M, Godfred D, Johan J W, Bjame S, Robert C A. 2016. Uptake of antibiotics from irrigation water by plants. Chemosphere, 157, 107–114. Dettenmaier E M, Doucette W J, Bugbee B. 2009. Chemical hydrophobicity and uptake by plant roots. Environmental Science & Technology, 43, 324–329. Engwall M, Hjelm K. 2000. Uptake of dioxin-like compounds from sewage sludge into various plant species-assessment of levels using a sensitive bioassay. Chemosphere, 40, 1189–1195. Fisher N S. 1975. Chlorinated hydrocarbon pollutants and photosynthesis: A reassessment. Science, 189, 463–464. Fismes J, Perrin G C, Empereur B P, Morel J L. 2002. Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial
contaminated soils. Journal of Environmental Quality, 31, 1649–1656. Gao X, Sheng Y H, Gao Y Z. 2014a. Oxidative stresses and DNA damages in cells of Vicia faba exposed to phenanthrene and pyrene. Journal of Agro-Environment Science, 33, 1873–1881. Gao X, Sheng Y H, Gao Y Z, Chen Z Y, Hu X J. 2014b. Analysis of phenanthrene-caused DNA damage on the root tip cells of Vicia faba with comet assay. Journal of Ecology and Rural Environment, 30, 515–520. Gao Y, Zhu L, Ling W. 2005. Application of the partition-limited model for plant uptake of organic chemicals from soil and water. Science of the Total Environment, 336, 171–182. Goel A, Mcconnell L L, Torrents A, Scudlark J R, Simonich S. 2006. Spray irrigation of treated municipal wastewater as a potential source of atmospheric PBDEs. Environmental Science & Technology, 40, 2142–2148. Goncalves C G. 2016. Selectivity of saflufenacil applied singly and in combination, with glyphosate on coffee and citrus crops. Revista Caatinga, 29, 45–53. (in Portuguese) Greenberg M E, Li X M, Gugiu B G, Gu X, Qin J, Salomon R G, Hazen S L. 2008. The lipid whisker model of the structure of oxidized cell membranes. Journal of Biological Chemistry, 283, 2385–2396. Grote M, Schwake A C, Michel R, Stevens H, Heyser W, Langenkämper G, Betsche T, Freitag M. 2007. Incorporation of veterinary antibiotics into crops from manured soil. Land Bauforschung Volkenrode, 57, 25–32. Gunning B E S, Steer M W. 1975. In: Ultrastructure and the Biology of Plant Cells. Edward Arnold, London. pp. 312-395 Gunsolus J L, Curran W S, 1991. Herbicide mode of action and injury symptoms. In: Cooperative Extension Service. U.S. Department of Agriculture, Washington D.C. pp.1–21. Harding Jr L W, Phillip Jr J H. 1978. Polychlorinated biphenyl effects on marine phytoplankton photosynthesis and cell division. Marine Biology, 49, 93–101. Inui H, Wakai T, Gion K, Kim Y S, Eun H. 2008. Differential uptake for dioxin-like compounds by Zucchini subspecies. Chemosphere, 73, 1602–1607. Jadhav V V, Jadhav A S, Chandagade C A, Raut P D. 2012. Genotoxicity of bisphenol A on root meristem cells of Allium cepa: A cytogenetic approach. Water Environment Pollution, 9, 39–43. Jurado Exposito M, Munoz Castejon M, Garcia-Torres L. 1999. Uptake and translocation of imazethapyr in peas as affected by parasitism of Orobanche crenata and herbicide application methods. Weed Research, 39, 129–136. Kang D H, Gupta S, Rosen C, Fritz V, Singh A, Chander Y, Murray H, Rohwer C. 2013. Antibiotic uptake by vegetable crops from manure-applied soils. Journal of Agricultural and Food Chemistry, 61, 9992–10001. Karissa K. 2002. Persistent organic pollutants: A global issue, a global response. This page was created in 2002 and updated in December 2009. [2016-10-12]. http://www2.epa. gov/international-cooperation/persistent-organic-pollutantsglobal-issue-global-response
ZHANG Cheng et al. Journal of Integrative Agriculture 2017, 16(8): 1659–1668
Kaspary T E, Lamego F P, Cutti L, Aguiar A C M, Bellas C. 2014. Determination of photosynthetic pigments in fleabane biotypes susceptible and resistant to the herbicide glyphosate. Planta Daninha, 32, 417–426. Korte F, Kvesitadze G, Ugrekhelidze D, Gordeziani M, Khatisashvili G, Buadze O, Zaalishvili G, Coulston F. 2000. Organic toxicants and plants. Ecotoxicology & Environmental Safety, 47, 1–26. Kriton K H, Celestia M H. 1982. Influence of the herbicides hexazinone and chlorsulfuron on the metabolism of isolated soybean leaf cells. Pesticide Biochemistry and Physiology, 17, 207–214. Kvesitadze G, Khatisashvili G, Sadunishvili T, Kvesitadze E. 2015. Plants for remediation: Uptake, translocation and transformation of organic pollutants. In: Öztürk M, Ashraf M, Aksoy A, Ahmad M S A, Hakeem K R, eds., Plants, Pollutants and Remediation. Springer Netherlands, USA, pp. 241–305. Lee J, Seo Y, Essington M E. 2014. Sorption and transport of veterinary pharmaceuticals in soil - a laboratory study. Soil Science Society of America Journal, 78, 1531–1543. Li G L, Liu Y J, Guan W F, Chen X L. 2012. Study on the comet assay detects glyphosate-induced DNA damages in soybean root tip cells. Journal of Henan Institute of Science and Technology, 40, 18–21. (in Chinese) Li L, Wang Q, Qiu X H, Dong Y, Jia S L, Hu J X. 2014. Field determination and QSPR prediction of equilibrium-status soil/vegetation partition coefficient of PCDD/Fs. Journal of Hazardous Materials, 276, 278–286. Li Z J, Xie X Y, Zhang S Q, Liang Y C. 2011. Wheat growth and photosynthesis as affected by oxytetracycline as a soil contaminant. Pedosphere, 21, 244–250. Lin H, Tao S, Zuo Q, Coveney R M. 2007. Uptake of polycyclic aromatic hydrocarbons by maize plants. Environmental Pollution, 148, 614–619. Liu J Y, Jerald L S. 2008. Uptake and translocation of lesser-chlorinated polychlorinated biphenyls (PCBs) in whole hybrid poplar plants after hydroponic exposure. Chemosphere, 73, 1608–1616. Liu Y Y, Sun H B, Chen G Z, Zhao B. 2010. Influence of polychlorinated biphenyls on photosynthesis characteristics and relative growth rate of two mangrove seedlings. Marine Environmental Science, 29, 317–320. Luciana M, Salvatore C, Maurizio F. 2003. Phytotoxicity to and uptake of enrofloxacin in crop plants. Chemosphere, 52, 1233–1244. Mclachlan M S. 1999. Framework for the interpretation of measurements of SOCs in plants. Environmental Science & Technology, 33, 1799–1804. Merten M, I-Peng C, Karel J, Angelis I S. 2001. DNA damage and repair in Arabidopsis thaliana as measured by the comet assay after treatment with different classes of genotoxins. Mutation Research, 493, 87–93. Migliore L, Cozzolino S, Fiori M. 2003. Phytotoxicity to and uptake of enrofloxacin in crop plants. Chemosphere, 52, 1233–1244.
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Min L. 2012. Study on uptake and accumulation of three sulfonamides in plants. MSc thesis, Anhui Agricultural University, China. (in Chinese) Moeckel C, Nizzetto L, Di G A, Steinnes E, Freppaz M, Filippa G. 2008. Persistent organic pollutants in boreal and montane soil profiles: Distribution, evidence of processes and implications for global cycling. Environmental Science and Technology, 42, 8374–8380 Moeckel C, Thomas G, Barber J L, Jones K C. 2008. Uptake and storage of PCBs by plant cuticles. Environmental Science & Technology, 42, 100–105. Moore K, Roberts L J. 1998. Measurement of lipid peroxidation. Free Radical Research, 28, 659–671. Moore S A, Harriss R C. 1974. Differential sensitivity to PCB by phytoplankton. Marine Pollution Bulletin, 5, 174–176. Myöhänen T T, García H J A, Tenorio L J, Männistö P T. 2009. Issues about the physiological functions of prolyl oligopeptidase based on its discordant spatial association with substrates and inconsistencies among mRNA, protein levels, and enzymatic activity. Journal of Histochemistry & Cytochemistry, 57, 831–848. Nakajima N, Ohshima Y, Serizawa S, Kouda T, Edmonds J S, Shiraishi F. 2002. Processing of bisphenol a by plant tissues: glucosylation by cultured BY-2 cells and glucosylation/translocation by plants of nicotiana tabacum. Plant and Cell Physiology, 43, 1036–42. Nancy B A, Sonia S, Marcelo L L, Marta D M. 2014. Induction of microtubule damage in Allium cepa meristematic cells by pharmaceutical formulations of thiabendazole and griseofulvin. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 772, 1–5. Noureddin M I, Furumoto T, Yamagishi M. 2004. Absorption, translocation and metabolism of bisphenol A, a possible endocrine disruptor, in rice seedlings. Environment Control in Biology, 42, 31–40. Papiernik S K, Koskinen W C, Barber B L. 2012. Low sorption and fast dissipation of the herbicide saflufenacil in surface soils and subsoils of an eroded prairie landscape. Journal of Agricultural & Food Chemistry, 60, 10936–10941. Paterson S, Mackay D, Tam D, Shiu W Y. 1990. Uptake of organic chemicals by plants: A review of processes, correlations and models. Chemosphere, 21, 297–331. Pier M D, Zeeb B A, Reimer K J. 2002. Patterns of contamination among vascular plants exposed to local sources of polychlorinated biphenyls in the Canadian Arctic and Subarctic. Science Total Environment, 297, 215–227. Ramadass K, Megharaj M, Venkateswarlu K, Naidu R. 2015. Toxicity and oxidative stress induced by used and unused motor oil on freshwater microalga, Pseudokirchneriella subcapitata. Environmental Science and Pollution Research, 22, 8890–8901. Ryan J A, Bell R M, Davidson J M, O’Connor G A. 1988. Plant uptake of non-ionic organic chemicals from soils. Chemosphere, 17, 2299–2323. Sithole B B, Guy R D. 1987. Models for tetracycline in aquatic environments. Water Air & Soil Pollution, 32, 303–314.
1668
ZHANG Cheng et al. Journal of Integrative Agriculture 2017, 16(8): 1659–1668
Sitte P, Ziegler H, Ehrendorfer F, Bresinsky A. 1991. In: Fischer S, ed., Lehrbuch der Botanik für Hochschulen 33. Auflage Bayern, Publikationsserver der Universität Regensburg. (in German) Song M, Chu S G, Letcher R J, Seth R. 2006. Fate, partitioning, and mass loading of polybrominated diphenyl ethers (PBDEs) during the treatment processing of municipal sewage. Environmental Science Technology, 40, 6241– 6246. Stefan T, Michael M. 1997. Modeling volatilization of PCDD/F from soil and uptake into vegetation. Environmental Science & Technology, 31, 71–74. Sterling T M. 1994. Mechanisms of herbicide absorption across plant membranes and accumulation in plant-cells. Weed Science, 42, 263–276. Su Y H, Zhu Y G. 2007. Transport mechanisms for the uptake of organic compounds by rice (Oryza sativa) roots. Environmental Pollution, 148, 94–100. Suleyman C, Mustafa Y, Ibrahim H C, Ahmet B, Hakan T, Evrim S A T. 2010. Evaluation of 2,4-D and dicamba genotoxicity in bean seedlings using comet and RAPD assays. Ecotoxicology and Environmental Safety, 73, 1558–1564. Taiz L, Zeiger E. 2002. Plant Physiology. 3rd. Sinauer Associates, Sunderland. Tao Y Q, Zhang S Z, Xue B. 2010. Bioavailability of polycyclic aromatic hydrocarbons in soils and its evaluation method. Journal of the Graduate School of the Chinese Academy of Sciences, 27, 568–576. (in Chinese) Tomáš G, Petra L, Lucie K, Martina M, Katerina D. 2007. Monitoring toxicity, DNA damage, and somatic mutations in tobacco plants growing in soil heavily polluted with polychlorinated biphenyls. Mutation Research, 629, 1–6. Trapp M, Mc Farlane C. 1994. Modeling and simulation of organic chemical processes. In: Trapp S, Mc arlane J C, eds., Plant Contamination. CRC, USA. Vanier C A, Planas D, Sylvestre M. 2001. Equilibrium partition theory applied to PCBs in macrophytes. Environmental Science & Technology, 35, 4830–4833. Wang J, Dai J X, Yang K F. 2006. The status and prospect of meiosis in Porphyra. Periodical of Ocean University of China, 36, 377–380. (in Chinese) Wu W Z, Schramm K W, Xu Y, Kettrup A. 2002. Contamination and distribution of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/F) in agriculture fields in Ya-Er lake area, China. Ecotoxicology & Environmental Safety, 53, 141–147.
Xia J R, Li Y J, Lu J, Chen B. 2004. Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bulletin of Environmental Contamination and Toxicology, 73, 979–986. Xie X J, Zhou Q, Bao Q, He Z, Bao Y. 2010. Physiological and potential genetic toxicity of chlortetracycline as an emerging pollutant in wheat (Triticum Aestivum L.). Environmental Toxicology and Chemistry, 29, 922–928. Xie X J, Zhou Q, Bao Q, He Z, Bao Y. 2011a. Genotoxicity of tetracycline as an emerging pollutant on root meristem cells of wheat (Triticum aestivum L.). Environmental Toxicology, 26, 417–423. Xie X J, Zhou Q, Lin D, Guo J, Bao Y. 2011b. Toxic effect of tetracycline exposure on growth, antioxidative and genetic indices of wheat (Triticum aestivum L.). Environmental Science and Pollution Research, 18, 566–575. Yang C W, Jianaer A, Li C Y, Shi D C, Wang D L. 2008. Comparison of the effects of salt-stress and alkalistress on photosynthesis and energy storage of an alkaliresistant halophyte Chloris virgate. Photosynthetica, 46, 273–278. Yang X, Guschina I A, Hurst S, Wood S, Langford M, Hawkes T. 2010. The action of herbicides on fatty acid biosynthesis and elongation in barley and cucumber. Pest Management Science, 66, 794–800. Zhang B, Zhang H, Jin J, Ni Y, Jiping C. 2012. PCDD/Fs-induced oxidative damage and antioxidant system responses in tobacco cell suspension cultures. Chemosphere, 88, 798–805. Zhang H, Chen J, Ni Y, Zhang Q, Zhao L. 2009. Uptake by roots and translocation to shoots of polychlorinated dibenzo-p-dioxins and dibenzofurans in typical crop plants. Chemosphere, 76, 740–746. Zhang M, Zhu L. 2009. Sorption of polycyclic aromatic hydrocarbons to carbohydrates and lipids of ryegrass root and implications for a sorption prediction model. Environmental Science & Technology, 43, 2740–2745. Zobiole L H, Kremer R J, Oliveira R S D, Constantin J. 2009. Glyphosate effects on photosynthesis, nutrient accumulation, and nodulation in glyphosate-resistant soybean. Journal of Wuhan University of Technology, 175, 319–330. Zwart D L L, Meerman J H, Commandeur J N, Vermeulen N P. 1999. Biomarkers of free radical damage applications in experimental animals and in humans. Free Radical Biology and Medicine, 26, 202–226. (Managing editor SUN Lu-juan)
ScienceDirect
REVIEW
Uptake and translocation of organic pollutants in plants: A review ZHANG Cheng1, FENG Yao1, LIU Yuan-wang1, CHANG Hui-qing2, LI Zhao-jun1, XUE Jian-ming3 1
Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture/China-New Zealand Joint Laboratory for Soil Molecular Ecology, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China 2 Henan University of Science and Technology, Luoyang 471003, P.R.China 3 Scion, Christchurch 29-237, New Zealand
Abstract Organic pollutants, such as polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/Fs), polychlorinated biphenyls (PCBs), antibiotics, herbicides, and bisphenol A (BPA), are commonly found in agricultural environments. They are released into the environment as a result of their use for human health purposes and farm management activities, and are often discharged as waste-water effluents. Most of these organic pollutants are taken up by plants through roots and leaves, and when they enter the tissue, they cause serious damage to the plants. Although the toxicity of organic pollutants to plants, especially to plant cells, has been intensively studied, a systematic review of these studies is lacking. Here we review researches on the toxicity of organic pollutants, their uptake, and translocation in plants. Our objective is to assemble existing knowledge concerning the interaction of organic pollutants with plants, which should be useful for the development of plant-based systems for removing pollutants from aquatic and agricultural environments. Keywords: organic pollutants, plant, uptake, cytotoxicity
1. Introduction Normal development and productivity of plants depends upon internal and external factors. Natural and man-made chemicals are important external factors that exert detrimental effects on plants. Some organic pollutants, such as hormones and persistent organic pollutants (POPs), including polychlorinated dibenzo-p-dioxins and polychlori-
Received 8 November, 2016 Accepted 6 March, 2017 Correspondence LI Zhao-jun, Tel: +86-10-82108657, E-mail: [email protected] © 2017 CAAS. Publishing services by Elsevier B.V. All rights reserved. doi: 10.1016/S2095-3119(16)61590-3
nated dibenzofurans (PCDD/Fs), polychlorinated biphenyls (PCBs), and antibiotics, herbicides and bisphenol A (BPA), have drawn significant attention in environmental science and engineering research. Several countries and international organizations have published lists of harmful pollutants, which need to be controlled urgently. For example, the World Wildlife Fund listed 67 types of environmental hormones in 1997 that were considered harmful (Karissa 2002). Under the Stockholm Convention, countries agreed to reduce or eliminate the production, use, and/or release of 12 key POPs, and as specified under the Convention, a scientific review process led to the addition of other POP chemicals of global concern in 2001 (Anonymous 2008). Although most of these chemicals are beneficial, they may have unforeseen effects on the environment (Myöhänen et al. 2009). Many studies have been conducted on the toxicity of organic pollutants to plants cells and on the up-
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take of organic pollutants by plants. Here we review these studies, focusing primarily on (1) the uptake of organic pollutants by plants and their detrimental effects on plant cells, particularly irreversible cytotoxicity and (2) recent progress on the negative impacts of PCDD/Fs, PCBs, antibiotics, herbicides, and BPA on plant growth, reproduction, and crop productivity. This review could be useful in the development of plant based systems for removing organic pollutants from environments.
2. Uptake and translocation of organic pollutants by plants The uptake pathway of organic pollutants in plants Most organic pollutants are absorbed by plants either from soil or air. As shown in the Table 1 and Fig. 1, the organic pollutants, including PCBs and PCDD/Fs can be absorbed by plants from soil (through roots) or air (through leaves directly from the air or after these pollutants evaporate from
Table 1 Pathway of plant uptake of organic pollutants Organic pollutant1) PCBs (PCB3, PCB15, PCB28, PCB52, PCB73) PCDD/Fs
Tissue tested Root Foliage Root
Foliage Antibiotics (tetracyclines, polyether, semisynthetic and macrolides, aminoglycosides, sulfa, and β-lactams antibiotics)
Root
BPA
Root
Herbicides (sulfonylurea, imidazolinone, triazines, phenylureas, uracilsand, and sulfonamide families)
1)
Root and foliage
Species Hybrid poplar Bluegrass, Luzula, and Betula Cucurbita, rouzi grass (Thylacospermum caespitosum), lettuce, potato, apple, pear, rice, pea, and oilseed rape Rice and radish
Reference Liu and Jerald (2008) Pier et al. (2002) Engwall and Hjelm (2000); Zhang et al. (2009); Li et al. (2014)
Stefan and Michael (1997); Wu et al. (2002) Spinach, lettuce, carrot, radishes, Migliore et al. (2003); Alistair potatoes, onion and garlic, wheat, et al. (2006); Grote et al. cucumber, pinto beans (2007); Bassil et al. (2013); Kang et al. (2013); David et al. (2016) Rice, tobacco Nakajima et al. (2002); Noureddin et al. (2004) Pea, coffee plant, orange plant Sterling (1994); Jurado et al. (1999); Papiernik et al. (2012); Goncalves (2016)
PCBs, polychlorinated biphenyls; PCDD/Fs, polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans; BPA, bisphenol A.
1. Toxicity of organic pollutants to leave cells: (1) Abnormal cell ultrastructure; (2) Disturbed cell biosynthesis;
2. Pollutants uptake by plant from air: (1) PCBs;
(3) Disturbed DNA, etc.
(2) PCDD/Fs; (3) Herbicides, etc.
3. Factors influncing uptake/ translocation:
Translocation
(1) Organic pollutant factors; (2) Plant biological characteristics factors; (3) Environmental media factors.
4. Pollutants uptake by plants from soil: (1) PCBs; (2) PCDD/Fs; (3) Antibiotics; (4) BPA, etc. 5. Toxicity of organic pollutants to root cells: Inordinate mitotic division.
Fig. 1 Uptake and translocation of organic pollutants in plants, factors influencing uptake, and the toxic effects of organic pollutants in plants. PCBs, polychlorinated biphenyls; PCDD/Fs, polychlorinated dibenzofurans; BPA, bisphenol A.
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soil). Herbicides can also be taken up by plants from soil through roots and air after plant leaves come in contact with them. The other organic pollutants, such as antibiotics and BPA, are only absorbed by plants from the soil through roots. This may be because most organic pollutants have low volatility and are mainly exposed to plants through soil or water. The plant root is usually the first tissue that comes in contact with organic pollutants and therefore absorption via roots is the most common method of uptake. Factors influencing uptake of organic pollutants by plants Uptake and translocation of organic pollutants by plants are affected by the physical and chemical properties of the organic pollutants, the biological characteristics of the plants, and the environmental media (Table 2 and Fig. 1). The physical and chemical properties of organic pollutants influencing plant uptake include molecular mass and hydrophobicity with the parameters KOW and KOA. KOW is the partition coefficient between octanol and water, and KOA is the partition coefficient between octanol and air. When the molecular mass of an organic pollutant is below 1 000, it is easily taken up by plant roots. Similarly, organic pollutants with high KOW values are easily absorbed by plant roots and a positive correlation has been found between KOW value and the concentration of organic pollutants in plants. In addition, organic pollutants with low KOA values are easily absorbed by plants from air. Among all the biological features of plants, the root extractable lipid content has the strongest influence on the uptake of organic pollutants. Regarding environmental media factors, indirect factors, including the background electrolyte type, dissolved organic carbon (DOC) concentration, pH, and organic matter content are more important than temperature. These factors mainly impact on uptake of organic pollutants by influencing the adsorption of organic pollutants on soils or the formation of chelates. Therefore, particular attention should be paid to the physical and chemical properties of organic pollutants, such as molecular mass, KOW, and KOA, and the biological characters of the plants such as the root extractable lipid content, when we consider the removal of organic pollutants from the environment. There are some factors, such as the solubility and concentration of organic pollutants, which have real effects on their uptake and translocation by plants, but they are of minor importance when compared with the above factors. Generally, organic compounds dissolved in soil water are easily absorbed by plant roots. However, even when their solubility is low, they can be absorbed by plant roots by passive or active uptake (Inui et al. 2008). In passive uptake, the absorption of organic pollutants is a concentration-dependent process and hence uptake is influenced by the concentration of organic pollutants (Vanier et al. 2001). Most studies show that uptake of organic chemicals by plant
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roots is a passive and diffusive process, except for the uptake of a few hormone-like chemicals, such as the phenoxy acid herbicides, for which there is evidence of active uptake (Ryan et al. 1988; Bromilow and Chamberlain 1995; Collins et al. 2006). Most active uptake processes are affected by plant lipid content and plant metabolism (Paterson et al. 1990; Collins 2008). The modes and mechanisms of uptake and translocation of organic pollutants by plants Many studies have been carried out to determine the modes and mechanisms of uptake and translocation of organic pollutants by plants. In recent years, most researchers have focused on the uptake of organic pollutants by plant roots. These studies have shown that the organic pollutants are first enriched at the root surface and they pass into the roots together with water. They pass through the cuticle-free unsuberized cell walls of young root hairs that are located closely behind the tip of the root ((5±50) mm). After penetration, they move towards the xylem transport tissue in the root along free intercellular space (apoplastic way) or cells (symplastic way) (Sitte and Ziegler 1991; Kvesitadze et al. 2015). In the root cortex, the cell-wall between the cells is porous, and chemicals can move freely from solution to the interior before they reach the endodermis (Trapp and Mc Farlane 1994). After uptake by plants, organic pollutants such as POPs are translocated to different parts of the plants (Lin et al. 2007). Generally, two kinds of organic pollutant transport pathways in higher plants have been reported: (i) intracellular and intercellular transport (short distance transport) and (ii) conducting tissue transport (long distance transport) (Taiz and Zeiger 2002). The mechanism for the transportation of specific organic pollutants varies with the physicochemical properties of organic pollutants. Su and Zhu (2007) reported that dinitrotoluene and dinitrobenzene are transported into plants via the symplastic pathway, whereas phenanthrene and pyrene are transported via the apoplastic pathway. The transportation of organic pollutants in plant phloem and xylem depends upon the size of the molecule. For example, organic pollutants with small molecule size can easily permeate the membrane and hence, easily come in and go out of the phloem and xylem. On the other hand, organic pollutants with large molecule size have low permeability in membranes and therefore cannot be effectively transported in the phloem (Kvesitadze et al. 2015).
3. Toxicity of organic pollutants to plants cells Organic pollutants may have toxic effects on plant cell ultrastructure, biosynthesis, membrane stability and DNA (Fig. 1).
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Table 2 Factors influencing uptake and translocation of organic pollutants by plants Factor Organic pollutant factors Molecular mass
Hydrophobicity KOW (the partition coefficient between octanol and water)
KOA (the partition coefficient between octanol and air)
Plant biological characteristics factors Root extractable lipid content (associated with Klip)
Carbohydrate content of plant cell walls
Transpiration stream concentration factor (TSCF) Permeability of biomembranes, pH of membranes, and electrical gradients across plant cell membranes Epicuticular waxes Environmental media factors Background electolyte type Concentration of dissolved organic carbon (DOC) PH of environmental media PH of environmental media Organic matter content of soil
Temperature
Example or explanation Organic pollutants, which have low-molecular mass and volatility, can be absorbed by roots and foliage. However, high-molecular mass organic pollutants, which are nonvolatile and possess strong hydrophobic properties, can only be absorbed by roots (Fismes et al. 2002). Molecular mass of organic pollutants is the leading factor influencing the plant-uptake process. Compounds with molecular mass below 1 000 can be easily absorbed by plant roots (Kvesitadze et al. 2015). Polychlorinated biphenyls (PCBs) with higher KOW values were bound strongly to root tissues and were prevented from entering the transpiration stream (Liu and Jerald 2008). There was a positive correlation between the concentration of organic pollutant in barley and KOW of PCB (Briggs et al. 1982; Moeckel et al. 2008). PCB with KOA>60 entered plants mainly from air rather than from soil (Cousins and Mackay 2001). Semi-volatile organic pollutants with KOA<85 entered plant foliage mainly as gas and established a distribution equilibrium between foliage and air. Semi-volatile organic pollutants with 85
3.1. Toxicity of organic pollutants to plant cell ultrastructure The cell ultra-structure or micro structures cannot be distin-
guished clearly by optical microscope. These micro structures include the cell membranes, endoplasmic reticulum, retinal and nuclear membranes, ribosomes and microtubules (MT) or microfilaments. The essential function of a cell is
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controlled by these ultra-structures. Plant cells will become abnormal or even die if the cell’s ultra-structures are damaged or destroyed (Gunning and Steer 1975; Agarwal 2006). When organic pollutants are absorbed into plant cells, they can cause disorder of the cell ultrastructure. For example, tobacco cells were destroyed when tobacco was exposed to WHO98-TEQ of PCDD/Fs at the concentration of 10 000 mg kg–1. The surface of cell walls became coarse and wrinkled, the cytoplasm began to leak, and the shape of the chloroplast transverse section was changed from round to hexagonal (Zhang et al. 2012). Some organic pollutants, such as diphenylether and bipyridylium often induce cell membrane disruption which, in turn, damage the plant tissues (Gunsolus and Curran 1991; Boczkowski and Hoet 2010; Ramadass et al. 2015). Microtubes are formed by the assembly of α- and β-tubulins and MT-associated proteins and can be damaged by organic pollutants (Nancy et al. 2014). Exposure of Allium cepa meristematic root cells to fungicides, such as thiabendazole (TBZ) or griseofulvin (GF) at the concentration of 100 μg mL–1 can cause microtubular damage such as abnormal arrays. Griseofulvin can induce a high frequency of abnormal pre-prophasic bands, mitotic spindles, phragmoplasts, and abnormal tripolar spindles. Other organic pollutants such as BPA can induce microtubule array disruption in pea (Pisum sativum L.) meristematic root-tip cells. Microtubules of pea meristematic root-tip cells can be loosened by BPA, causing the mean diameter to increase from (23±0.70) nm in untreated cells to (32±0.14) nm in cells treated with BPA and then to be completely depolymerized (Adamakis et al. 2013).
3.2. Toxicity of organic pollutants to cell biosynthesis Recent research on the impact of organic pollutants on plant cell biosynthesis has mainly focused on the detrimental effects on photosynthesis, and synthesis of proteins, amino acids, nucleic acids, lipids, and hormones. For example, PCBs and herbicides have been found to be detrimental to cell biosynthesis (Moore and Harriss 1974; Moore and Roberts 1998; Brain et al. 2010). Similarly, it was found that PCBs, antibiotics, and herbicides can inhibit photosynthesis in plants cells. Photosynthesis is an essential process in plants, which is responsible for supporting growth, nutrient uptake and resistance to abiotic or biotic stresses (Xia et al. 2004; Yang et al. 2008; Bassil et al. 2013). PCBs were found to inhibit photosynthetic carbon assimilation in both natural phytoplankton communities and unialgal cultures at the concentration of 10.0 μg L–1 (Engwall and Hjelm 2000). PCBs may also affect the photosynthetic light reactions as it has been shown that photosynthesis-irradiance curves decrease in the presence of PCBs (Harding and Phillip 1978; Liu et al. 2010). The impacts of oxytetracycline (OTC) on wheat photosynthesis resembled stresses caused by salt, alkali,
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and heavy metals. The photosynthesis rates, transpiration rates, and stomatal conductance significantly decreased in all OTC-treated plants of a sensitive cultivar (Li et al. 2011). Similarly, photosynthesis inhibitors were also found in herbicide families such as the triazines, phenylureas, uracils, benzothiadiazoles, and nitriles. These photosynthesis inhibitors shut down the photosynthetic process in susceptible plants by binding organic pollutants to specific sites within the plants chloroplasts (Bunce 2008). Herbicides could also prevent plants from forming photosynthetic pigments, causing green leaves and stems of plants to become white and translucent (Kaspary et al. 2014). It has been reported that RNA, protein, and lipid synthesis could be significantly inhibited by prolonged exposure to hexazinone and chlorsulfuron (Fisher 1975; Yang et al. 2010). Some herbicides, such as sulfonylurea, imidazolinone, and sulfonamide have been found to suppress the synthesis of three essential branch-chain amino acids, which inhibit one key enzyme in plants (Aubert et al. 1997), while herbicides made mainly from an amino acid derivative inhibited the production of three essential aromatic amino acids (Amaia et al. 2013). All these organic pollutant effects can be ascribed to restraining the activities of key enzymes in plants. For example, glyphosate and imazamox could inhibit the biosynthesis of aromatic and branched-chain amino acids, respectively, by inducing the ubiquitin-26S protein system and papain-like cysteine proteases (Zobiole et al. 2009). Although these herbicides inhibit different pathways, they have been found to have common physiological effects, such as increasing free amino acid contents and decreasing soluble protein contents (Amaia et al. 2013). Currently, studies on how new contaminants such as antibiotics affect cell function, are still lacking. Their mechanism is likely to be far more complex than other organic pollutants such as herbicides.
3.3. Toxicity of organic pollutants to membrane stability Unsaturated lipids become rancid due to oxidative deterioration when they react directly with the oxygen molecule (Zward et al. 1999; Chen et al. 2016). This process is called lipid peroxidation (LPO). The insertion of an oxygen molecule is catalyzed by free radicals (non-enzymatic lipid peroxidation) or enzymes (enzymatic lipid peroxidation). It has been shown that LPO induces disturbance of fine structures, alteration of integrity, fluidity, and permeability, and functional loss of biomembranes, and modifies low density lipoprotein to proatherogenic and proinflammatory forms, and generates potentially toxic products (Greenberg et al. 2008). Malondialdehyde (MDA) provides an analytical index to indicate lipid peroxidation of membranes. The larger the content of MDA, the less stable the membranes becomes.
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It has been found that the toxic effect and oxidative stress caused by PCDD/Fs can be indicated by an increase in MDA content (Zhang et al. 2012). There are some reports showing that oxidative stress can be induced by oxytetracycline in water solution (Li et al. 2011). MDA contents were positively correlated with the inhibition rates of antioxidative enzyme activities. It has also been shown that tetracycline may significantly augment MDA content when the levels of tetracycline exceed 5 mg L–1 (Xie et al. 2011b).
3.4. Organic pollutant damage to DNA in plants cells PCBs and herbicides have been found to cause damage to DNA of plant cells. DNA was significantly damaged in leaf nuclei of tobacco plants when they were grown in PCB-polluted soil. When measured by the comet assay, the tail moment (TM) value in leaf nuclei of plants cultivated for 8 weeks in PCB polluted soil ((10.0±1.4) μm), was significantly higher than the corresponding value in nuclei of control plants ((2.3±0.4) μm) (Tomáš et al. 2007). When the root tip cells of soybeans were cultivated in glyphosate for 8 h, the cometic rate, comet tail length, DNA content of tail, tails and olive-tailed margins, and other indicators were significantly different from the control, and there were clear dose-response relationships for all the indicators (Li et al. 2012). DNA fragmentation increased in a dose-dependent manner with dicamba (3,6-dichloro-2-methoxybenzoicacid) (Suleyman et al. 2010). However, it is worth noting that maleic hydrazide (MH) did not cause DNA damage to Arabidopsis thaliana when the alkaline denaturation and neutral gel electrophoresis protocol was used for the comet assay (Merten et al. 2001). Some studies have revealed that DNA damage can be caused by polycyclic aromatic hydrocarbons (PAHs). Tail moment values from the comet assay increased from 46.41 μm (control) to 122.04 μm when plants were treated with phenanthrene at the concentration of 50 mg kg–1. The degree of DNA damage increased with the increase of pyrene concentrations (0–50 mg kg–1). It was also found that pyrene treatment at the concentration of 50 mg kg–1 caused significant damage to the DNA of Vicia faba root tip cells. The TM value increased from 44.3 μm in the control treatment to 110.36 μm in pyrene treated plants (Gao et al. 2014a). DNA damage to Vicia faba root tip cells caused by phenanthrene was also investigated using the comet assay. DNA damage was aggravated with an increase in phenanthrene concentrations from 0 to 0.6 mg L–1 (Gao et al. 2014b).
3.5. Responses of inordinate mitotic division to organic pollutants Reports on damage to inordinate mitotic division induced
by PCBs have mainly focused on algal species (Goel et al. 2006; Song et al. 2006). PCBs have been found to affect cell division rates in several algal species. For example, cell division of Thalassiosira pseudonana strain 3H, Chaetoceros socialis, Skeletonema costatum, Thalassiosira pseudonana 13-I, Monochrysis lutheri, and Isochrysis galbana was found to be significantly inhibited by PCB at low concentration (Fisher 1975). Cell division of Porphyra haitanensis was also found to be significantly affected by PCBs; division rates decreased with increase in PCB concentration (Wang et al. 2006). In higher plants, chlortetracycline may also prevent cells from entering cell division. A possible reason for this could be the depression of protein synthesis and enzyme activities and the disruption of normal organelle function, which may result in inhibition of mitotic division in plant root tip cells (Luciana et al. 2003). Xie et al (2010, 2011a, b) conducted a series of studies on toxicity of chlortetracycline and tetracycline to plant cells. They found that chlortetracycline and tetracycline slightly increased the frequencies of micronucleus and chromosomal aberration, and sister chromatid exchange in plant root tips at the lowest concentration (0.0625–250 mg L–1 of chlortetracycline and 0.25–10 mg L–1 of tetracycline). However, the chromosomal aberration frequency was significantly raised as the concentration of tetracycline increased from 0.5 to 300 mg L–1. At higher concentrations (250–300 mg L–1 of chlortetracycline and 50–300 mg L–1 of tetracycline), the frequencies of micronucleus aberration, chromosomal aberration, and sister chromatid exchange were reduced because of acute cell toxicity (Xie et al. 2010, 2011a, b). Furthermore, genotoxicity occurred early and then influenced mitotic activity when the plants were under the stress of organic pollutants. Tetracycline could stimulate root cell mitotic division of wheat when concentrations ranged from 0.5 to 10 mg L–1. It was also found that tetracycline at high concentrations (>50 mg L–1) could significantly inhibit mitotic index in a concentration-dependent manner (Xie et al. 2011a). Tetracycline could stimulate mitotic cell division of wheat when the tetracycline concentrations ranged from 0.25 to 1 mg L–1. However, it could cause a concentration-related decrease in mitotic index (MI) when the concentrations ranged from 50 to 300 mg L–1. These results indicate that antibiotics, such as tetracyclines and chlortetracycline might be genotoxic to plants cells, and pose a genotoxic risk to living organisms (Xie et al. 2011b). Similarly, Andrioli and Mudry (2011) found that TBZ can lead to disorder in mitotic cell division (Andrioli and Mudry 2011). In another study, TBZ also inhibit onion meristematic root cells mitosis. Onion (Allium cepa) meristematic root cells were exposed to a TBZ-containing pharmaceutical formulation at concentrations of 10–250 mg L–1. The inhibition of mitotic index and induction of C-metaphases, lagging chromosomes, polyploidy and binucleated
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cells, which possibly result in the alteration of chromosomal segregation and cytokinesis, were investigated (Andrioli and Mudry 2011). The effects of pharmaceutical formulations containing the microtubule disruptors TBZ and griseofulvin (GF) on the mitotic machinery of Allium cepa meristematic cells have also been characterized (Nancy et al. 2014). Griseofulvin inhibited mitotic index and caused genotoxic impacts, including increased chromosome fragmentation, bridging and lagging, C-metaphases, tripolar cell division, disorganized anaphases, and nuclear abnormalities in interphase cells of plants. Effects of these organic pollutants on the mitotic machinery were studied by using the method of direct immune fluorescence with β-tubulin labeling and by DNA counter-staining with 4’,6-diamidino-2-phenylindole (DAPI). The results suggested that GF could induce abnormalities in spindle symmetry/polarity. TBZ could also cause chromosome mis-segregation, polyploidy, and lack of cytokinesis (Nancy et al. 2014). Furthermore, a study of the genotoxicity of BPA on onion root meristematic cells showed that exposure to 50, 100, 150, and 200 mg L–1 BPA for five days increased the proportion of CA (break) from 0.4 to 7.2% and CA (fragments) from 0.3 to 3.2% (Jadhav et al. 2012). When the root tips of young seedlings of Pisum sativum L. were exposed to BPA at the concentration of 20, 50, and 100 mg L–1 for 1, 3, 6, 12, and 24 h, the BPA at all concentrations affected normal chromosome segregation, hampered the completion of cytokinesis and deranged the interphase. This suggests that BPA exerted acute anti-mitotic effects on meristematic root-tip cells of P. sativum (Adamakis et al. 2013).
4. Conclusion Currently, many investigations have shown that toxic chemicals not only harm people, but also affect plants. Organic pollutants can be taken up by plants through both roots and foliage. Molecular mass, hydrophobicity, root extractable lipid content, background electrolyte type, dissolved organic carbon, pH, and soil organic matter content are the main factors that influence the uptake and translocation process of organic pollutants in plants. Cell walls and membranes, chloroplasts, and microtubules can show the potential toxicity of pollutants to cell ultrastructure. To explore the damage to cell function caused by organic pollutants, we have summarized pollutant effects on cell biosynthesis and membrane stability, including the synthesis of RNA, lipids, proteins, and photosynthetic pigments. Furthermore, we have clearly segregated the DNA damage and inordinate mitotic division to illustrate genotoxic effects, which are a major issue of this paper. Based on the results, we conclude that these pollutants harm plant genes, which may lead to gene mutation and variation. Although research
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has improved our knowledge about pollutants and stringent regulations aiming to protect public health have already been undertaken, some pollutants, such as antibiotics and herbicides cannot be banned entirely, because they are necessary for human and animal health as well as for crop production. Thus, monitoring these organic chemicals is important for public health and improving the biotic environment, and the presence and trends of these pollutants in the atmosphere, soil, and plants has been the subject of many environmental studies all over the world. We consider that there should be more studies undertaken to determine precise transfer pathways and their temporal pattern, and to pinpoint genotoxicity more precisely in plants cells. An improved understanding of these factors will allow improved control of cumulative toxic effects on plants and reduce harmful impacts of pollutants.
Acknowledgements This work was jointly supported by the special projects foundation of the National Natural Science Foundation of China (31572209), the Beijing Municipal Sciences and Technology Commission, China (Z141105000614012), the Shanxi Province Science and Technology Research Project, China (20140311008-4).
References Adamakis I D S, Emmanuel P, Anna C, Eleftherios P. 2013. Effects of bisphenol A on the microtubule arrays in root meristematic cells of Pisum sativum L. Mutation Research, 750, 111–120. Agarwal U P. 2006. Raman imaging to investigate ultrastructure and composition of plant cell walls: Distribution of lignin and cellulose in black spruce wood (Picea Mariana). Planta, 224, 1141–1153. Alistair B, Paul J, Edward J S, Chris J S, Edward S, Len S L. 2006. Uptake of veterinary medicines from soils into plants. Journal of Agricultural and Food Chemistry, 54, 2288–2297. Amaia Z, Miriam G M, Villamor J G, Zabalza A, Hoorn R A, Royuela M. 2013. Proteolytic pathways induced by herbicides that inhibit amino acid biosynthesis. PLOS ONE, 8, e73847. Andrioli N B, Mudry M D. 2011. Cytological and cytogenetic effects induced by thiabendazole on Allium cepa root meristems. Journal of Basic and Applied Genetics, 2, 17–23. Anonymous. 2008. Text of the stockholm convention. Amended in 2009, 2011, 2013 and 2015. [2016-10-12]. http://chm. pops.int/TheConvention/Overview/TextoftheConvention/ tabid/2232/Default.aspx Aubert S, Bligny R, Day D A, Whelan J, Douce R. 1997. Induction of alternative oxidase synthesis by herbicides inhibiting branched-chain amino acid synthesis. The Plant Journal, 11, 649–657.
1666
ZHANG Cheng et al. Journal of Integrative Agriculture 2017, 16(8): 1659–1668
Bassil R J, Bashour II, Sleiman F T, Abou-Jawdeh Y A. 2013. Antibiotic uptake by plants from manure-amended soils. Journal of Environmental Science and Health (Part B: Pesticides Food Contaminants and Agricultural Wastes), 48, 570–574. Boczkowski J, Hoet P. 2010. What’s new in nanotoxicology? Implications for public health from a brief review of the 2008 literature. Nanotoxicology, 4, 1–14. Brain R A, Solomon K R, Brooks B W. 2010. Targets, effects and risks in aquatic plants exposed to veterinary antibiotics. ACS Symposium Series, 1018, 169–189. Briggs G G, Bromilow R H, Evans A A. 1982. Relationships between lipophilicity and root uptake and translocation of non-ionised chemicals by barley. Pesticide Science, 13, 495–504. Bromilow R H, Chamberlain K. 1995. Principles governing uptakeand transport of chemicals. In: Trapp S, Mc Farlane J C, eds., Plant Contamination: Modellingand Simulation of Organic Chemical Processes. Lewis Publishers, London. pp. 38–64. Bunce J A. 2008. Acclimation of photosynthesis to temperature in Arabidopsis thaliana and Brassica oleracea. Photosynthetica, 46, 517–524. Chen L, Zhang S, Huang H, Wen B, Christie P. 2009. Partitioning of phenanthrene by root cell walls and cell wall fractions of wheat (Triticum Aestivum L.). Environmental Science & Technology, 43, 9136–9141. Chen X N, Qiu D Y, Lin H M. 2016. Botanical characteristics and medicinal value of five Glycyrrhiza species cultivated in the Hexi region of Gansu. Acta Prataculturae Sinica, 25, 246–253. (in Chinese) Collins C, Fryer M, Grosso A. 2006. Plant uptake of non ionic organic chemicals. Environmental Science and Technology, 40, 45–52. Collins D C. 2008. A semi-quantitative approach to deriving a model structure for the uptake of organic chemicals by vegetation. International Journal of Phytoremediation, 10, 371–377. Cousins I T, Mackay D. 2001. Strategies for including vegetation compartments in multimedia models. Chemosphere, 44, 643–654. David A, Christiana M, Godfred D, Johan J W, Bjame S, Robert C A. 2016. Uptake of antibiotics from irrigation water by plants. Chemosphere, 157, 107–114. Dettenmaier E M, Doucette W J, Bugbee B. 2009. Chemical hydrophobicity and uptake by plant roots. Environmental Science & Technology, 43, 324–329. Engwall M, Hjelm K. 2000. Uptake of dioxin-like compounds from sewage sludge into various plant species-assessment of levels using a sensitive bioassay. Chemosphere, 40, 1189–1195. Fisher N S. 1975. Chlorinated hydrocarbon pollutants and photosynthesis: A reassessment. Science, 189, 463–464. Fismes J, Perrin G C, Empereur B P, Morel J L. 2002. Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial
contaminated soils. Journal of Environmental Quality, 31, 1649–1656. Gao X, Sheng Y H, Gao Y Z. 2014a. Oxidative stresses and DNA damages in cells of Vicia faba exposed to phenanthrene and pyrene. Journal of Agro-Environment Science, 33, 1873–1881. Gao X, Sheng Y H, Gao Y Z, Chen Z Y, Hu X J. 2014b. Analysis of phenanthrene-caused DNA damage on the root tip cells of Vicia faba with comet assay. Journal of Ecology and Rural Environment, 30, 515–520. Gao Y, Zhu L, Ling W. 2005. Application of the partition-limited model for plant uptake of organic chemicals from soil and water. Science of the Total Environment, 336, 171–182. Goel A, Mcconnell L L, Torrents A, Scudlark J R, Simonich S. 2006. Spray irrigation of treated municipal wastewater as a potential source of atmospheric PBDEs. Environmental Science & Technology, 40, 2142–2148. Goncalves C G. 2016. Selectivity of saflufenacil applied singly and in combination, with glyphosate on coffee and citrus crops. Revista Caatinga, 29, 45–53. (in Portuguese) Greenberg M E, Li X M, Gugiu B G, Gu X, Qin J, Salomon R G, Hazen S L. 2008. The lipid whisker model of the structure of oxidized cell membranes. Journal of Biological Chemistry, 283, 2385–2396. Grote M, Schwake A C, Michel R, Stevens H, Heyser W, Langenkämper G, Betsche T, Freitag M. 2007. Incorporation of veterinary antibiotics into crops from manured soil. Land Bauforschung Volkenrode, 57, 25–32. Gunning B E S, Steer M W. 1975. In: Ultrastructure and the Biology of Plant Cells. Edward Arnold, London. pp. 312-395 Gunsolus J L, Curran W S, 1991. Herbicide mode of action and injury symptoms. In: Cooperative Extension Service. U.S. Department of Agriculture, Washington D.C. pp.1–21. Harding Jr L W, Phillip Jr J H. 1978. Polychlorinated biphenyl effects on marine phytoplankton photosynthesis and cell division. Marine Biology, 49, 93–101. Inui H, Wakai T, Gion K, Kim Y S, Eun H. 2008. Differential uptake for dioxin-like compounds by Zucchini subspecies. Chemosphere, 73, 1602–1607. Jadhav V V, Jadhav A S, Chandagade C A, Raut P D. 2012. Genotoxicity of bisphenol A on root meristem cells of Allium cepa: A cytogenetic approach. Water Environment Pollution, 9, 39–43. Jurado Exposito M, Munoz Castejon M, Garcia-Torres L. 1999. Uptake and translocation of imazethapyr in peas as affected by parasitism of Orobanche crenata and herbicide application methods. Weed Research, 39, 129–136. Kang D H, Gupta S, Rosen C, Fritz V, Singh A, Chander Y, Murray H, Rohwer C. 2013. Antibiotic uptake by vegetable crops from manure-applied soils. Journal of Agricultural and Food Chemistry, 61, 9992–10001. Karissa K. 2002. Persistent organic pollutants: A global issue, a global response. This page was created in 2002 and updated in December 2009. [2016-10-12]. http://www2.epa. gov/international-cooperation/persistent-organic-pollutantsglobal-issue-global-response
ZHANG Cheng et al. Journal of Integrative Agriculture 2017, 16(8): 1659–1668
Kaspary T E, Lamego F P, Cutti L, Aguiar A C M, Bellas C. 2014. Determination of photosynthetic pigments in fleabane biotypes susceptible and resistant to the herbicide glyphosate. Planta Daninha, 32, 417–426. Korte F, Kvesitadze G, Ugrekhelidze D, Gordeziani M, Khatisashvili G, Buadze O, Zaalishvili G, Coulston F. 2000. Organic toxicants and plants. Ecotoxicology & Environmental Safety, 47, 1–26. Kriton K H, Celestia M H. 1982. Influence of the herbicides hexazinone and chlorsulfuron on the metabolism of isolated soybean leaf cells. Pesticide Biochemistry and Physiology, 17, 207–214. Kvesitadze G, Khatisashvili G, Sadunishvili T, Kvesitadze E. 2015. Plants for remediation: Uptake, translocation and transformation of organic pollutants. In: Öztürk M, Ashraf M, Aksoy A, Ahmad M S A, Hakeem K R, eds., Plants, Pollutants and Remediation. Springer Netherlands, USA, pp. 241–305. Lee J, Seo Y, Essington M E. 2014. Sorption and transport of veterinary pharmaceuticals in soil - a laboratory study. Soil Science Society of America Journal, 78, 1531–1543. Li G L, Liu Y J, Guan W F, Chen X L. 2012. Study on the comet assay detects glyphosate-induced DNA damages in soybean root tip cells. Journal of Henan Institute of Science and Technology, 40, 18–21. (in Chinese) Li L, Wang Q, Qiu X H, Dong Y, Jia S L, Hu J X. 2014. Field determination and QSPR prediction of equilibrium-status soil/vegetation partition coefficient of PCDD/Fs. Journal of Hazardous Materials, 276, 278–286. Li Z J, Xie X Y, Zhang S Q, Liang Y C. 2011. Wheat growth and photosynthesis as affected by oxytetracycline as a soil contaminant. Pedosphere, 21, 244–250. Lin H, Tao S, Zuo Q, Coveney R M. 2007. Uptake of polycyclic aromatic hydrocarbons by maize plants. Environmental Pollution, 148, 614–619. Liu J Y, Jerald L S. 2008. Uptake and translocation of lesser-chlorinated polychlorinated biphenyls (PCBs) in whole hybrid poplar plants after hydroponic exposure. Chemosphere, 73, 1608–1616. Liu Y Y, Sun H B, Chen G Z, Zhao B. 2010. Influence of polychlorinated biphenyls on photosynthesis characteristics and relative growth rate of two mangrove seedlings. Marine Environmental Science, 29, 317–320. Luciana M, Salvatore C, Maurizio F. 2003. Phytotoxicity to and uptake of enrofloxacin in crop plants. Chemosphere, 52, 1233–1244. Mclachlan M S. 1999. Framework for the interpretation of measurements of SOCs in plants. Environmental Science & Technology, 33, 1799–1804. Merten M, I-Peng C, Karel J, Angelis I S. 2001. DNA damage and repair in Arabidopsis thaliana as measured by the comet assay after treatment with different classes of genotoxins. Mutation Research, 493, 87–93. Migliore L, Cozzolino S, Fiori M. 2003. Phytotoxicity to and uptake of enrofloxacin in crop plants. Chemosphere, 52, 1233–1244.
1667
Min L. 2012. Study on uptake and accumulation of three sulfonamides in plants. MSc thesis, Anhui Agricultural University, China. (in Chinese) Moeckel C, Nizzetto L, Di G A, Steinnes E, Freppaz M, Filippa G. 2008. Persistent organic pollutants in boreal and montane soil profiles: Distribution, evidence of processes and implications for global cycling. Environmental Science and Technology, 42, 8374–8380 Moeckel C, Thomas G, Barber J L, Jones K C. 2008. Uptake and storage of PCBs by plant cuticles. Environmental Science & Technology, 42, 100–105. Moore K, Roberts L J. 1998. Measurement of lipid peroxidation. Free Radical Research, 28, 659–671. Moore S A, Harriss R C. 1974. Differential sensitivity to PCB by phytoplankton. Marine Pollution Bulletin, 5, 174–176. Myöhänen T T, García H J A, Tenorio L J, Männistö P T. 2009. Issues about the physiological functions of prolyl oligopeptidase based on its discordant spatial association with substrates and inconsistencies among mRNA, protein levels, and enzymatic activity. Journal of Histochemistry & Cytochemistry, 57, 831–848. Nakajima N, Ohshima Y, Serizawa S, Kouda T, Edmonds J S, Shiraishi F. 2002. Processing of bisphenol a by plant tissues: glucosylation by cultured BY-2 cells and glucosylation/translocation by plants of nicotiana tabacum. Plant and Cell Physiology, 43, 1036–42. Nancy B A, Sonia S, Marcelo L L, Marta D M. 2014. Induction of microtubule damage in Allium cepa meristematic cells by pharmaceutical formulations of thiabendazole and griseofulvin. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 772, 1–5. Noureddin M I, Furumoto T, Yamagishi M. 2004. Absorption, translocation and metabolism of bisphenol A, a possible endocrine disruptor, in rice seedlings. Environment Control in Biology, 42, 31–40. Papiernik S K, Koskinen W C, Barber B L. 2012. Low sorption and fast dissipation of the herbicide saflufenacil in surface soils and subsoils of an eroded prairie landscape. Journal of Agricultural & Food Chemistry, 60, 10936–10941. Paterson S, Mackay D, Tam D, Shiu W Y. 1990. Uptake of organic chemicals by plants: A review of processes, correlations and models. Chemosphere, 21, 297–331. Pier M D, Zeeb B A, Reimer K J. 2002. Patterns of contamination among vascular plants exposed to local sources of polychlorinated biphenyls in the Canadian Arctic and Subarctic. Science Total Environment, 297, 215–227. Ramadass K, Megharaj M, Venkateswarlu K, Naidu R. 2015. Toxicity and oxidative stress induced by used and unused motor oil on freshwater microalga, Pseudokirchneriella subcapitata. Environmental Science and Pollution Research, 22, 8890–8901. Ryan J A, Bell R M, Davidson J M, O’Connor G A. 1988. Plant uptake of non-ionic organic chemicals from soils. Chemosphere, 17, 2299–2323. Sithole B B, Guy R D. 1987. Models for tetracycline in aquatic environments. Water Air & Soil Pollution, 32, 303–314.
1668
ZHANG Cheng et al. Journal of Integrative Agriculture 2017, 16(8): 1659–1668
Sitte P, Ziegler H, Ehrendorfer F, Bresinsky A. 1991. In: Fischer S, ed., Lehrbuch der Botanik für Hochschulen 33. Auflage Bayern, Publikationsserver der Universität Regensburg. (in German) Song M, Chu S G, Letcher R J, Seth R. 2006. Fate, partitioning, and mass loading of polybrominated diphenyl ethers (PBDEs) during the treatment processing of municipal sewage. Environmental Science Technology, 40, 6241– 6246. Stefan T, Michael M. 1997. Modeling volatilization of PCDD/F from soil and uptake into vegetation. Environmental Science & Technology, 31, 71–74. Sterling T M. 1994. Mechanisms of herbicide absorption across plant membranes and accumulation in plant-cells. Weed Science, 42, 263–276. Su Y H, Zhu Y G. 2007. Transport mechanisms for the uptake of organic compounds by rice (Oryza sativa) roots. Environmental Pollution, 148, 94–100. Suleyman C, Mustafa Y, Ibrahim H C, Ahmet B, Hakan T, Evrim S A T. 2010. Evaluation of 2,4-D and dicamba genotoxicity in bean seedlings using comet and RAPD assays. Ecotoxicology and Environmental Safety, 73, 1558–1564. Taiz L, Zeiger E. 2002. Plant Physiology. 3rd. Sinauer Associates, Sunderland. Tao Y Q, Zhang S Z, Xue B. 2010. Bioavailability of polycyclic aromatic hydrocarbons in soils and its evaluation method. Journal of the Graduate School of the Chinese Academy of Sciences, 27, 568–576. (in Chinese) Tomáš G, Petra L, Lucie K, Martina M, Katerina D. 2007. Monitoring toxicity, DNA damage, and somatic mutations in tobacco plants growing in soil heavily polluted with polychlorinated biphenyls. Mutation Research, 629, 1–6. Trapp M, Mc Farlane C. 1994. Modeling and simulation of organic chemical processes. In: Trapp S, Mc arlane J C, eds., Plant Contamination. CRC, USA. Vanier C A, Planas D, Sylvestre M. 2001. Equilibrium partition theory applied to PCBs in macrophytes. Environmental Science & Technology, 35, 4830–4833. Wang J, Dai J X, Yang K F. 2006. The status and prospect of meiosis in Porphyra. Periodical of Ocean University of China, 36, 377–380. (in Chinese) Wu W Z, Schramm K W, Xu Y, Kettrup A. 2002. Contamination and distribution of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/F) in agriculture fields in Ya-Er lake area, China. Ecotoxicology & Environmental Safety, 53, 141–147.
Xia J R, Li Y J, Lu J, Chen B. 2004. Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bulletin of Environmental Contamination and Toxicology, 73, 979–986. Xie X J, Zhou Q, Bao Q, He Z, Bao Y. 2010. Physiological and potential genetic toxicity of chlortetracycline as an emerging pollutant in wheat (Triticum Aestivum L.). Environmental Toxicology and Chemistry, 29, 922–928. Xie X J, Zhou Q, Bao Q, He Z, Bao Y. 2011a. Genotoxicity of tetracycline as an emerging pollutant on root meristem cells of wheat (Triticum aestivum L.). Environmental Toxicology, 26, 417–423. Xie X J, Zhou Q, Lin D, Guo J, Bao Y. 2011b. Toxic effect of tetracycline exposure on growth, antioxidative and genetic indices of wheat (Triticum aestivum L.). Environmental Science and Pollution Research, 18, 566–575. Yang C W, Jianaer A, Li C Y, Shi D C, Wang D L. 2008. Comparison of the effects of salt-stress and alkalistress on photosynthesis and energy storage of an alkaliresistant halophyte Chloris virgate. Photosynthetica, 46, 273–278. Yang X, Guschina I A, Hurst S, Wood S, Langford M, Hawkes T. 2010. The action of herbicides on fatty acid biosynthesis and elongation in barley and cucumber. Pest Management Science, 66, 794–800. Zhang B, Zhang H, Jin J, Ni Y, Jiping C. 2012. PCDD/Fs-induced oxidative damage and antioxidant system responses in tobacco cell suspension cultures. Chemosphere, 88, 798–805. Zhang H, Chen J, Ni Y, Zhang Q, Zhao L. 2009. Uptake by roots and translocation to shoots of polychlorinated dibenzo-p-dioxins and dibenzofurans in typical crop plants. Chemosphere, 76, 740–746. Zhang M, Zhu L. 2009. Sorption of polycyclic aromatic hydrocarbons to carbohydrates and lipids of ryegrass root and implications for a sorption prediction model. Environmental Science & Technology, 43, 2740–2745. Zobiole L H, Kremer R J, Oliveira R S D, Constantin J. 2009. Glyphosate effects on photosynthesis, nutrient accumulation, and nodulation in glyphosate-resistant soybean. Journal of Wuhan University of Technology, 175, 319–330. Zwart D L L, Meerman J H, Commandeur J N, Vermeulen N P. 1999. Biomarkers of free radical damage applications in experimental animals and in humans. Free Radical Biology and Medicine, 26, 202–226. (Managing editor SUN Lu-juan)