Abstract
Phthalates are synthetic chemical compounds that are primarily used as plasticizers in various plastics and polymers to improve their physical properties. They are reported as ubiquitous pollutants in different spheres of the environment due to the presence of physical bonding with the polymeric matrix. In animals, including humans, they are known to cause various toxic effects. Nevertheless, less attention has been paid to phthalate induced stress in plants, since plants are equally vulnerable to their exposure as they are immobile and being an important component of the environment cannot be ignored. Moreover, due to their frequent detection in higher amounts in agricultural soils globally, significant concern has been raised about phthalate induced stress in plants over the past decade. The main sources of phthalate in agricultural soils are the use of plastic mulching, irrigation with wastewater, pesticide spraying, use of biosolids for improving soil properties, etc. From the soils, phthalates could enter into plants mainly via roots and undergo biomagnification at different trophic levels in an ecosystem. Phthalates were declared as endocrine disruptors thereby, their accumulation in edible plants raises food security concerns. Moreover, the accumulation of phthalates in plants is observed to affect germination, growth and development as well as reported to interfere with normal plant metabolism which led to modulations in the content of pigments, osmolytes, stress biomarkers and activities of antioxidative enzymes, thus reducing the yield and quality of edible plants.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Phthalates are dialkyl or alkyl aryl esters of 1,2-benzenedicarboxylic acid. They are used as plasticizers to enhance their flexibility, durability, and elasticity of plastics or polymers (Mackintosh et al. 2004). In polymeric and non-polymeric matrices, phthalates are physically incorporated which leads to their easy escape into the environment because of slight alterations in the environmental factors viz., pH, temperature, pressure, and irradiation (Meng et al. 2014; Benjamin et al. 2015; Benjamin et al. 2017). The worldwide production of phthalates is increasing globally and from 2007 to 2017, it was predicted to increase from 2.7 to 6.0 million tons per year (Bauer and Herrmann 1997; Xie et al. 2007). Among all plasticizers, phthalates contribute approximately 84% of total plasticizers in the global market (ECHA 2013). The most abundant phthalates in the environment are diethyl phthalate, di-n-butyl phthalate, benzyl butyl phthalate, di(2-ethylhexyl) phthalate, di-n-octyl phthalate (Gavala et al. 2003). Phthalates have been extensively studied for their toxicities using animal systems. Humans are also prone to the frequent exposure of phthalates due to the extensive use of plastic products on regular basis. The human exposure to phthalates is confirmed by the detection of their metabolites in the body fluids and tissues (Hines et al. 2009; Jensen et al. 2015; Pan et al. 2015). Furthermore, the detected concentrations of phthalates and their metabolites in humans have been reported to be associated with high blood pressure, pregnancy loss, preterm birth, diabetes, enhanced insulin resistance, anti-androgenic effects, cardiovascular disease, hypertension, etc. (Hoppin et al. 2013; Shiue 2014; Sun et al. 2014; Trasande et al. 2014; Whyatt et al. 2014; Bai et al. 2017). As phthalates are reported as potential toxicants to living organisms including humans but little attention has been given to studies on the plant systems. On the other hand, due to immobile nature of plants, they are at high risk to the exposure of phthalates. Thus, a concern regarding the potential toxic effects of phthalates on plants is being investigated by number of researchers. The studies have also demonstrated the negative effects of phthalates on edible plants by adversely affecting the normal metabolic processes. Phthalates are reported to affect seed germination in various edible plants (Ma et al. 2013, 2014; Zhang et al. 2016). Phthalates also declined the growth and development of different plants (Chen et al. 2011; Gao and Wen 2016; Gu et al. 2017). The exposure of phthalates to seedlings as well as plants directly affect the content of pigments, osmolytes, level of oxidative stress biomarkers and also altered the activities of antioxidative enzymes (Huang et al. 2006; Liao et al. 2006; Xu et al. 2010; Cheng and Cheng 2012; Ma et al. 2014; Gu et al. 2017; Duan et al. 2018; Gao et al. 2019; Kumari and Kaur 2019; Sharma et al. 2019; Kumari and Kaur 2020; Singh et al. 2020). The considerable accumulation and translocation of phthalates were observed in vegetables and crop plants (Sun et al. 2015, 2018). The main contributing factor for phthalates accumulation in plants is their lipophilic nature. After their uptake, they are transported to different plant parts and observed to accelerate the generation of reactive oxygen species (ROS) which imparts devastating effects on cellular levels as well as causes membrane disruption via lipid peroxidation (Li et al. 2006; Xu et al. 2010; Cheng 2012; Zhang et al. 2015a; Gao et al. 2019). Plants regulate these processes by switching the enzymatic and non-enzymatic antioxidative defense system. Thus, the elevation in the amounts of phthalates in different environmental media can influence the normal processes of plants which leads to severe damages at cellular components and ultimately reduce their overall productivity. Therefore, this review highlights the adverse effects of phthalates stress in plants, roles of antioxidative defense system, their accumulation and metabolites formation after being accumulated in plants.
Physico-chemical properties of phthalates
The uptake and accumulation of phthalates directly rely on their physico-chemical characteristics. Moreover, behavior and fate of phthalates in the environment and biological systems are also dependent on these properties. Phthalates vary in their physical properties which are responsible for their different chemodynamics in the environment (Staples et al. 1997). They are colorless and odorless liquid at ambient temperature. They are the product of esterification of phthalic acid and aliphatic alcohol.
The alcohol ranged from methanol (C4) to texanol (C27) (Sibali et al. 2013). Phthalates which are commonly used as plasticizers fall in the range of methanol (C4) to tridecanol (C13). The water solubility (WS), vapor pressure (Vp), Henry’s constant (H), air-water partitioning coefficient (KAW) and octanol-water partitioning (KOW) coefficient are the main indices to address the physico-chemical properties of phthalates (Table 1).
Water solubility (WS)
It controls the distribution of phthalates between water, soil or sediment and atmosphere. In case of phthalates, water solubility is low and observed to be decreased with an increase in carbon chain length. Thus, being hydrophobic compounds, they get adsorbed onto suspended solids and colloids in surface water reservoirs. They also get firmly associated with soluble humic materials which change their solubilities (Ogner and Schnitzer 1970).
Vapour pressure (Vp)
Phthalates are semi-volatile in nature irrespective of their low vapour pressure. They are reported to be present in the vapour phase at environmentally relevant temperatures (Tienpont 2004). The vapour pressure of phthalates decreases with increase in alkyl chain length.
Henry’s constant (H)
It indicates the tendency of the pollutants to escape from water into the air and can be calculated from the values of water solubility and vapour pressure. In the case of phthalates, Henry’s constant values approximately equal to 1.01 × 10− 2 indicate negligible volatility. The higher values of Henry’s constant for phthalates with higher alkyl chains (4 to 13) indicates that they can transfer from aqueous phase to gaseous phase (Net et al. 2015).
Air-water partitioning coefficient (KAW)
It reflects the affinity of organic compounds for lipid molecules in living beings. It has been commonly employed to know the potential of contaminants to accumulate or concentrate in aquatic organisms (Lyman et al. 1990). In phthalates, the value of KAW increases with an increase in alkyl chain and is directly proportional to bioconcentration/bioaccumulation.
Octanol–water partitioning coefficient (KOW)
It is the measure of the distribution of a substance between air and water. The low molecular weight phthalates are quite volatile and due to their low log KOW values they can readily volatilize from their pure state but very slowly from aqueous media (Net et al. 2015).
Types of phthalates and their applications
On the basis of carbon chain length, phthalates are categorized into two categories i.e. high molecular weight phthalates (HMWP) and low molecular weight phthalates (LMWP) (Ventrice et al. 2013).
High molecular weight phthalates (HMWP)
These phthalates have 7 to 13 carbon atoms in their carbon chain. The most common high molecular weight phthalates are diisodecyl phthalate (DiDP), diisononyl phthalate (DiNP), di(2-propylheptyl) phthalate (DPHP), diisoundecyl phthalate (DiUP) and ditridecyl phthalate (DTDP). High molecular weight phthalates are primarily used as plasticizers in polyvinyl chloride (PVC). The other plasticized products with high molecular weight phthalates include wires and cables, flooring, truck tarpaulins, wall coverings, self-adhesive films or labels, synthetic leather, coated fabrics, roofing membranes and automotive applications (Wilkes et al. 2005; Cao 2010; ECPI 2014).
Low molecular weight phthalates (LMWP)
These include phthalates with 3 to 6 carbon atoms in their carbon chain backbone. Low molecular weight phthalates are di-n-butyl phthalate (DBP), diisobutyl phthalate (DiBP), benzyl butyl phthalate (BBP) and di(2-ethylhexyl phthalate) (DEHP) (Liao et al. 2018). They are used in various PVC products as well as in medical devices, adhesives, paints, inks and enteric-coated tablets (Wittassek et al. 2011; Czernych et al. 2017). The remaining phthalates such as dimethyl phthalate (DMP), diethyl phthalate (DEP) and diallyl phthalate (DAP) have one, two and three carbon-atoms respectively in their hydrocarbon chain. These are not classified as HMWP or LMWP because they are not used as plasticizers. These are mainly used as solvents and fixatives in fragrances, additives in cosmetics, medical devices, household and personal care products (Schettler 2006; Schlumpf et al. 2010; Philippat et al. 2012; Carlstedt et al. 2013; Frederiksen et al. 2013; ECPI 2014).
Phthalates in soils and sediments
In terrestrial ecosystems, soil acts as a natural sink for different pollutants. From soil, phthalates get a route to enter the plants including edible plants (Cai et al. 2008a). Phthalates are mainly released to the soils owing to their extensive use as agricultural plastic films (He et al. 2015). This can lead to potential human health risks via food chain. The major factors that contribute to phthalate pollution in agricultural soils are shown in Fig. 1.
Similarly, in an aquatic ecosystem, sediments act as a sink and source of phthalates deposition especially, which have low water solubility, melting point and volatility (Mitsunobu and Takahashi 2006). The analysis of five phthalates from the sediments of Gomti river was done using HPLC. The reported mean concentration values of phthalates viz., DEHP, DMP, DBP, DOP, DEP was 31.61, 10.54, 10.41, 5.16, 4.57 µg/kg respectively (Srivastava et al. 2010). A study conducted by Arukwe et al. (2012) reported a higher amount of phthalates from the leachates and sediment. The amount of phthalates sediment samples was 1000 times higher than run-off water samples.
Effects of phthalates on plants
In the last decades, the pollution load of phthalates has become a serious environmental issue and cannot be ignored because of their direct or indirect interference with normal physiological processes of living beings. Although, the adverse effects of phthalates are extensively documented on animals but in case of plants, the scenario is quite different. There are few studies which have examined phthalates induced stress in plants. The stress is a collective term used for both external abiotic or biotic constraints that limit plant growth and development via affecting photosynthesis and reducing carbon assimilation ability of plants (Grime 1977). Presently, people dealing with the production of food are facing number of challenges as the productivity of crops is not enough to meet the food demands (FAO 2009). Abiotic stresses are one of the major factors responsible for low productivity. To deal with such constraints number of strategies are adopted throughout the world. The introduction of mulching into the traditional agricultural practices is one of them. Undoubtedly, it has overcome number of issues but also generated concerns due the presence of high amount of additives. Among additives, main emphasis is laid on phthalates because these are highly preferred plasticizers. Phthalates are also reported to cause phytotoxic consequences among plants. However, under the exposure of pollutants they respond differentially and some of the plant species can withstand the adversities, while some of them are sensitive to the pollutants. Plants provide countless services to mankind as well as also play various important ecological functions (Beare et al. 1995; Kuzyakov and Blagodatskaya 2015). The survey of literature revealed that plants under phthalates stress showed adverse effects on germination, growth & development, biochemical and physiological processes.
Germination, growth and development
Germination is a process that starts with the uptake of water in order to set the metabolic events required to accomplish seed germination (Nonogaki 2008). It is considered as a crucial stage of higher plants as subsequent vegetative and reproductive growth of plant also depends upon it (Ma et al. 2013). The exposure of pollutants is more detrimental during early growth stages like germination and seedling growth in a plant life cycle (Macoustra et al. 2015). The process of germination was adversely affected by the exposure of phthalates in Vigna radiata (mung bean), Cucumis sativus (cucumber), Brassica chinensis (rape) (Ma et al. 2013, 2014; Zhang et al. 2016). The authors revealed little effects on germination of rape and mung bean and it may be related to developmental behavior of seeds. Rape and mung bean are dicotyledonous seeds and during seed germination they mainly rely on their own nutritive material via hypertrophic cotyledons rather than uptake of nutrients from soil (Shu et al. 1999). Whereas, cucumber seeds showed inhibition in germination under DMP stress. Thus, the effect on seed germination may be plant-specific or depends upon type of phthalate exposure. Phthalates may have disturbed the physiological and metabolic processes especially mobilization of food reserves of barley seeds during germination as shown in Supplementary Fig. 2. Moreover, phthalates may have imbalanced the level of plant growth regulators and enzymes which might have led to the reduction in seed germination and also affected the other associated parameters.
Phthalates are also reported to reduce the growth of plants at higher concentrations but at lower concentrations, they show plant hormone like properties (Ma et al. 2013, 2014). The exposure of phthalates was observed to decline the growth of algae, duckweeds, various monocotyledonous and dicotyledonous plants (Melin and Egneus 1983; Dueck et al. 2003; Liao et al. 2009; Gao and Wen 2016; Duan et al. 2018). The stress-induced by phthalates also declined the length of shoots and roots as well as biomass of the plants. The biomass of different plants like Phaseolus vulgaris, Brassica campestris var. chinensis, Picea abies, Trifolium repens, Plantago major and Holcus lanatus was declined under the expsoure of DBP (Dueck et al. 2003). The fresh weight was declined in Raphanus sativus treated with DEP and DEHP and in DBP treated Brassica rapa subsp. chinensis (Saarma et al. 2003; Liao et al. 2006). Thus, due to adverse effects of phthalates on germination, the growth and development of barley seedlings and plants was also affected. Because seed germination determines the subsequent growth quality of the plant.
Phthalates stress induced consequences on germination and growth according to previous studies are listed in Table 2.
Physiological responses
The primary source of phthalates in the agricultural soils is the application of plastic agricultural films (He et al. 2015). From soil, phthalates are reported to accumulate in plants which disturb the normal functioning of plants. The plants under phthalate stress show morphological and physiological responses. They also employ various strategies to maintain homeostasis under stressful environments. These strategies include alterations in morphological and developmental patterns (i.e. growth plasticity) as well as biochemical and physiological processes (Tuteja 2007; Saud et al. 2014). Phthalates are reported to affect the biochemical and physiological processes by affecting the contents of pigments, osmoloytes and stress metabolites.
Pigments
The alteration in the levels of chlorophyll pigment is a well avowed index in plants under stressed environment. The pigments posses an important role among the plants as they regulate photosynthesis rate (Zai et al. 2012). Abiotic stresses are reported to affect the photosynthesis. For crops, reduction in photosynthetic capacity is directly related to their yield. For carbon assimilation, plants have to perform a series of complex reactions to form carbohydrates which are direct or indirect sources of energy for heterotrophs including human beings. The photosynthetic apparatus consists of pigments (Chl a, Chl b, pheophytins, and carotenoids), photosystems (PS), light reactions (for the generation of NADPH and ATP) and dark reactions (for CO2 assimilation) (Singh and Thakur 2018).
Osmolytes
The carbohydrates are the final products of photosynthesis. In carbohydrates, disaccharides viz. sucrose, trehalose, raffinose, and fructans are the main forms of sugar that are observed to be involved in adaptation strategies during stress (Keunen et al. 2013; Song et al. 2019). They are soluble sugars and participate in osmotic adjustment (Kumari et al. 2018). Thus, they provide osmoprotection to stabilize the membrane structures as well as maintain turgidity of the cells (Gil et al. 2011). Proteins are also observed to be accumulated during stress in plants especially heat shock proteins (HSPs). They are commonly referred as ‘molecular chaperones’ and play roles in protein folding and assembly. They are categorized based on molecular weight e.g. Hsp70 family, chaperonins (GroEL and Hsp60), Hsp90 family, Hsp100 family and small Hsp family (Wang et al. 2004). A study showed the induction of the various genes and HSPs which acted together in different cascades to combat the heat stress consequences in rice (Chandel et al. 2013). There are other proteins which participate during stress regulation such as late embryogenesis abundant (LEA) proteins. These proteins are observed to accumulate in plants in response to water stress and are reported to act synergistically with trehalose to prevent protein aggregation during stress especially under water stress (Goyal et al. 2005). The exposure of DEP also observed to enhance the expression of HSP in Spirodela polyrhiza and Raphanus sativus. The accumulation of proline is commonly observed in plants under stressed conditions. It is also reported to act as a signaling molecule to modulate mitochondrial function (Szabados and Savouré 2010). It participates in number of functions like act as an osmolyte, ROS scavenger, and redox buffer. It also acts as a molecular chaperone and stabilizes the proteins and membranes (Krasensky and Jonak 2012; Hossain and Dietz 2016).
Oxidative stress markers
The environmental and biotic stresses trigger a common stress response i.e. oxidative stress in which the generation of reactive oxygen species (ROS) gets enhanced that causes damages to cell components (Demidchik 2015). ROS are the inevitable entities of plant’s life and are produced in cells via different pathways and homeostasis is maintained by the antioxidant defense system. The high level of ROS leads to reversible or irreversible variations in biomolecules like proteins, carbohydrates, polynucleic acids and lipids (Møller et al. 2007; Farmer and Mueller 2013). Among these, oxidation of lipids is considered more damaging because it generates free radicals via chain reactions. Lipid peroxidation is referred as a ‘hallmark’ of oxidative stress in plants (Farmer and Mueller 2013). Malondialdehyde (MDA) and hydrogen peroxide (H2O2) are considered as indicators of oxidative stress among the plants. MDA is considered as a marker of lipid peroxidation of membrane (Hu et al. 2020). Stress mediates the generation of ROS which leads to decrease in membrane integrity due to lipid peroxidation. Moreover, under stress, H2O2 is generated along other with ROS. The generation of H2O2 gets accelerated via glycollate oxidase reaction that occurs in peroxisomes (Anjum et al. 2012). Phthalates are observed to enhance the level of ROS.
Antioxidative defense system
The generation of reactive oxygen species (ROS) is an inevitable response of plants under stressed environments. They are produced in plants via partial reduction of oxygen and referred as a collective term for oxygen species and non-radical oxygen species (Ahmad 2018). The presence of unpaired electrons is responsible for their high reactivity which can even mediate the oxidation of cell structures, biomolecules as well as disturb the cell integrity (Kanojia and Dijkwel 2018). The ROS formation also takes place under normal conditions because of various metabolic processes but their level observed to be accelerated during abiotic or biotic stresses. The cellular organelles like chloroplast, mitochondria, and peroxisome, with high metabolic activity act as main sites for ROS formation. Thus, to combat with the enhanced levels of ROS, plants have a defense grid that relies on endogenous enzymatic and non-enzymatic antioxidants (Yu et al. 2019). The enzymatic antioxidative defense system is intricate, efficient and includes enzymes like superoxide dismutase (SOD), guaiacol peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), etc. (Supplementary Fig. 3).
The non-enzymatic antioxidants include glutathione, ascorbate, carotenoids, tocopherols, and polyphenolic compounds, etc. The effects of phthalates on pigments, osmolytes and oxidative stress markers and activities of antioxidative enzymes in different plants are given in Table 3.
Accumulation of phthalates
The advent of industrialization and other anthropogenic activities are responsible for the release of pollutants into the environment on a regular basis. The irregular or unorganized disposal of wastes on soils leads to potential risks to the biotic components particularly microorganisms, nematodes and plants (Bender and Heijden 2015). Moreover, the use of the untreated or partially reclaimed water for irrigation in some arid or semi-arid areas of the world contributed to soil pollution (Li et al. 2018). Sometimes, biosolids are also employed to improve the properties of the soil. The wastewater and biosolids contain variety of harmful inorganic and organic contaminants. The soil acts as a primary sink for different types of wastes such as chemical, domestic, industrial and agricultural wastes (Teng et al. 2014; Qing et al. 2015). These can also cause alterations in the physical and chemical characteristics of the soils. Plants being primary producers of terrestrial food chains are more prone to the exposure of these contaminants. Plants also have potential to uptake and accumulate such pollutants from soil and participate in their mitigation and transformation (Scheringer et al. 2004). Phthalates are one of such contaminants which are listed as priority pollutants by USEPA and due to their ubiquity throughout the world, they are also referred as world’s second PCBs (polychlorinated biphenyls) (Zhou 1989). In plants, phthalates are reported to induce different morphological and physiological consequences. Furthermore, plants are reported to uptake phthalates mainly via roots from soil or aqueous media (Liao et al. 2006, 2009; Cai et al. 2008a, 2008b). In soil, phthalates are reported to decline the diversity of microbial communities and also affect the quality of crop plants (Kapanen et al. 2007).
Mechanism of uptake and metabolism
Several studies have been carried to explore the mechanisms of organic pollutant’s uptake and translocation. There is number of reports which have revealed that the uptake of these pollutants takes place by the roots. During the process of uptake, firstly the organic pollutant gets enriched at root surface and then enters into the plant via roots along with water (Zhang et al. 2017). The contaminants including phthalates are reported to enter through the cuticle free unsuberized cell wall (Müller and Kördel 1993; Kvesitadze et al. 2006). Furthermore, the cell wall between the cells of root cortex is porous, thereby contaminants can move freely before they reach the endodermis (Trapp and McFarlane 1994). Organic pollutants are reported to be translocated to different plant parts after their uptake (Lin et al. 2007). The two types of organic pollutant transport pathways are reported in higher plants i.e. intracellular and intercellular transport and first method is meant for short-distance transport, whereas the second relies on conducting tissue and meant for long-distance transport (Taiz and Zeiger 2002). The long-distance movement can occur either via apoplastic or symplastic way (Miller et al. 2016). It is general mechanism of contaminant uptake but there are also other factors that regulate the phenomenon of uptake like solubility, molecular mass of contaminant, pH, temperature and phase of plant growth, etc. (Korte et al. 2000; Kvesitadze et al. 2006). In case, if the solubility of contaminants is low, even then they can also be absorbed by the roots via passive or active uptake (Inui et al. 2008). Most studies reported that the uptake of organic contaminants by roots is passive as well as diffusive in nature except in some case like phenoxy acid herbicides, where active uptake is reported rather than passive (Ryan et al. 1988; Bromilow and Chamberlain 1995; Collins et al. 2006). During active uptake, lipid content and plant metabolism play important roles (Paterson et al. 1990; Collins 2008).
After uptake, in plants, phthalates may undergo enzymatic transformation to enhance the hydrophilicity to lower their toxicity. This process of contaminant's transformation in plants is referred as Sandermann’s Green Liver Concept (Sandermann 1994) (Fig. 2).
The oxidation, reduction, hydrolysis, etc. are the main enzymatic reactions which mediate the conversion of hydrophobic contaminants into hydrophilic ones. This step leads to increases in the affinity of formed intermediate towards the enzymes and further transformations occur (Kvesitadze et al. 2009). After functionalization, the phthalates undergo conjugation. The process of conjugation enables them to react with intracellular endogenous components. There is another process that also operates besides conjugation i.e. deep oxidation but the amount of contaminant degraded through this process is very less (0.1 to 5%) and also depends upon the contaminant’s structure (Kvesitadze et al. 2009). The conjugation proceeds towards the compartmentalization. It is the final step and in this, the soluble conjugate of phthalates may be accumulated in cellular compartments especially in vacuole. In plant cell, the soluble conjugates of various contaminants are reported to couple with peptides, amino acids, sugars, etc. On the other hand, the insoluble ones in plant cells get coupled with starch, lignin, xylan, pectin, etc. are carried out of the cell and accumulate mainly in the cell wall (Sandermann 1994). Thus, these insights into phthalates uptake and bioaccumulation can act as a significant cue for their transformation and mitigation in the environment. But the less attention was paid on the possible mechanism of phthalates metabolites in plants. In last few years, researchers explained possible mechanisms of frequently detected phthalates in the environment mainly in monocots. The existing literature have shown that a large proportion of hydrophobic xenobiotics taken up by plants can be transformed and formed transformation intermediates exert different biological activities than their parent form (Sun et al. 2015). Carboxylesterases (CXEs, EC 3.1.1.1) are specific esterases are reported to be involved in the metabolism of phthalates in plants that display hydrolyzing activity against carboxylic esters (i.e. de-esterification) as well as that are also documented to be involved in many functional roles in plants, including xenobiotics detoxification (Haslam et al. 2001; Gershater and Edwards 2007; Sun et al. 2015). Moreover, phthalates are derived from the esterification of phthalic acid and two alcohol molecules, belong to the carboxylic esters. Thus, the chemical structure of phthalates and literature reveals that CXEs play a significant role in the metabolism of phthalates in plants, especially in phase I hydrolysis (Lin et al. 2017). After hydrolysis, these metabolites conjugates rapidly in different components of plants and can be accurately determined via radioactive labeling. However, information about the importance of plant CXEs to phthalates metabolism is still limited. Furthermore, there is less knowledge regarding the activity of CXE in the subcellular fractions of phthalates exposed plants, which might reflect the localization and mechanisms of the enzymes involved in phthalates detoxification. The proposed mechanism for phthalates metabolism in plants is given in Fig. 3.
Conclusions
The present review is the outcome of extensive literature survey which highlighted the consequences of phthalates in plants in detail. This also provided insights into phthalates uptake, accumulation, and mechanism of metabolites formation. Plants have evolved tiered mechanisms for the metabolization and detoxification of pollutants. However, in case of phthalates, the exact mechanism of these processes is still unclear and there are number of lacunae. Therefore, further research is required especially to determine the occurrence of phthalate monoesters with parent contaminant during normal agronomic practices in vegetables and other edible crops under field conditions to know potential health risks. Thus, for better understanding of mechanism of phthalates action in plants, many detailed studies are required and the outcomes of this work will helpful for the generation phthalate tolerant varieties as well as to sustain the agricultural yield.
References
Ahmad R (2018) Introductory chapter: basics of free radicals and antioxidants. In: Ahmad F (ed) Free radicals, antioxidants and diseases. IntechOpen, London, pp 1–4
Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids-A review. Environ Exp Bot 75:307–324
Arukwe A, Eggen T, Moder M (2012) Solid waste deposits as a significant source of contaminants of emerging concern to the aquatic and terrestrial environments—A developing country case study from Owerri, Nigeria. Sci Tot Environ 438:94–102
Bai PY, Wittert G, Taylor AW, Martin SA, Milne RW, Jenkins AJ, Januszewski AS, Shi Z (2017) The association between total phthalate concentration and non-communicable diseases and chronic inflammation in South Australian urban dwelling men. Environ Res 158:366–372
Bauer MJ, Herrmann R (1997) Estimation of the environmental contamination by phthalic acid esters leaching from household wastes. Sci Tot Environ 208:49–57
Beare MH, Coleman DC, Crossley DA, Hendrix PF, Odum EP (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant Soil 170:5–22
Bender SF, van der Heijden MGA (2015) Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J Appl Ecol 52:228–239
Benjamin S, Pradeep S, Sarath Josh M, Kumar S, Masai E (2015) A monograph on the remediation of hazardous phthalates. J Hazard Mater 298:58–72
Benjamin S, Masai E, Kamimura N, Takahashi K, Anderson RC, Faisal PA (2017) Phthalates impact human health: epidemiological evidences and plausible mechanism of action. J Hazard Mater 340:360–383
Bromilow RH, Chamberlain K (1995) Principles governing uptake and transport of chemicals. In: Trapp S, McFarlane JC (eds) Plant contamination. Lewis Publishers, Boca Raton, pp 37–68
Cai QY, Mo CH, Wu QT, Zeng QY (2008a) Polycyclic aromatic hydrocarbons and phthalic acid esters in the soil-radish (Raphanus sativus) system with sewage sludge and compost application. Bioresour Technol 99:1830–1836
Cai QY, Mo CH, Zeng QY, Wu QT, Férard JF, Antizar-Ladislao B (2008b) Potential of Ipomoea aquatica cultivars in phytoremediation of soils contaminated with di-n-butyl phthalate. Environ Exp Bot 62:205–211
Cao XL (2010) Phthalate esters in foods: sources, occurrence, and analytical methods. Compr Rev Food Sci Food Saf 9:21–43
Carlstedt F, Jönsson BAG, Bornehag CG (2013) PVC flooring is related to human uptake of phthalates in infants. Indoor Air 23:32–39
Chandel G, Dubey M, Meena R (2013) Differential expression of heat shock proteins and heat stress transcription factor genes in rice exposed to different levels of heat stress. J Plant Biochem Biotechnol 22:277–285
Cheng TS (2012) The toxic effects of diethyl phthalate on the activity of glutamine synthetase in greater duckweed (Spirodela polyrhiza L.). Aquat Toxicol 124–125:171–178
Cheng LJ, Cheng TS (2012) Oxidative effects and metabolic changes following exposure of greater duckweed (Spirodela polyrhiza) to diethyl phthalate. Aquat Toxicol 109:166–175
Chen WC, Huang HC, Wang YS, Yen JH (2011) Effect of benzyl butyl phthalate on physiology and proteome characterization of water celery (Ipomoea aquatica Forsk.). Ecotoxicol Environ Saf 74:1325–1330
Collins CD (2008) A semi-quantitative approach to deriving a model structure for the uptake of organic chemicals by vegetation. Int J Phytoremediat 10:371–377
Collins C, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45–52
Czernych R, Chraniuk M, Zagożdżon P, Wolska L (2017) Characterization of estrogenic and androgenic activity of phthalates by the XenoScreen YES/YAS in vitro assay. Environ Toxicol Pharmacol 53:95–104
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228
Duan K, Cui M, Wu Y, Huang X, Xue A, Deng X, Luo L (2018) Effect of dibutyl phthalate on the tolerance and lipid accumulation in the green microalgae Chlorella vulgaris Bull Environ Contam Toxicol 101:338–343
Dueck ThA, Van Dijk CJ, David F, Scholz N, Vanwalleghem F (2003) Chronic effects of vapour phase di-n-butyl phthalate (DBP) on six plant species. Chemosphere 53:911–920
ECHA (European Chemicals Agency) (2013) Evaluation of new scientific evidence concerning DINP and DIDP in relation to entry 52 of annex XVII to Reach Regulation (EC) No 1907/2006 (Final Review Report). Available: http://echa.europa.eu/documents/10162/31b4067e-de40-4044-93e8-9c9ff 1960715 (Accessed on 2018)
ECPI (2014) European Council for Plasticizers and Intermediates. The plasticizers information centre. Available: www.plasticisers.org (Accessed on 2019)
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450
Food and Agricultural Organization (FAO) (2009) Land and plant nutrition management service. (Available: www.fao.org/wsfs/forum2050/) (Accessed on 2019)
Frederiksen H, Nielsen JKS, Mørck TA, Hansen PW, Jensen JF, Nielsen O, Andersson AM, Knudsen LE (2013) Urinary excretion of phthalate metabolites, phenols and parabens in rural and urban Danish mother-child pairs. Int J Hyg Environ Health 216:772–783
Gao DW, Wen ZD (2016) Phthalate esters in the environment: A critical review of their occurrence, biodegradation, and removal during wastewater treatment processes. Sci Tot Environ 541:986–1001
Gao M, Liu Y, Dong Y, Song Z (2018) Photosynthetic and antioxidant response of wheat to di(2-ethylhexyl) phthalate (DEHP) contamination in the soil. Chemosphere 209:258–267
Gao M, Liu Y, Dong Y, Song Z (2019) Physiological responses of wheat planted in fluvo-aquic soils to di (2-ethylhexyl) and di-n-butyl phthalates. Environ Pollut 244:774–782
Gavala HN, Alatriste-Mondragon F, Iranpour R, Ahring BK (2003) Biodegradation of phthalate esters during the mesophilic anaerobic digestion of sludge. Chemosphere 52:673–682
Gershater MC, Edwards R (2007) Regulating biological activity in plants with carboxylesterases. Plant Sci 173:579–588
Gil R, Lull C, Boscaiu M, Bautista I, Lidón A, Vicente O (2011) Soluble carbohydrates as osmolytes in several halophytes from a mediterranean salt marsh. Notulae Bot Horti Agrobot Cluj-Napoca 39:9–17
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194. https://doi.org/10.1086/283244
Gu S, Zheng H, Xu Q, Sun C, Shi M, Wang Z, Li F (2017) Comparative toxicity of the plasticizer dibutyl phthalate to two freshwater algae. Aquat Toxicol 191:122–130
Haslam R, Raveton M, Cole DJ, Pallett KE, Coleman JO (2001) The identification and properties of apoplastic carboxylesterases from wheat that catalyse deesterification of herbicides. Pest Biochem Physiol 71:178–189
He L, Gielen G, Bolan NS, Zhang X, Qin H, Huang H, Wang H (2015) Contamination and remediation of phthalic acid esters in agricultural soils in China: a review. Agron Sustain Dev 35:519–534
Hines EP, Calafat AM, Silva MJ, Mendola P, Fenton SE (2009) Concentrations of phthalate metabolites in milk, urine, saliva, and serum of lactating North Carolina women. Environ Health Perspect 117:86–92
Hoppin JA, Jaramillo R, London SJ, Bertelsen RJ, Salo PM, Sandler DP, Zeldin DC (2013) Phthalate exposure and allergy in the US population: results from NHANES 2005–2006. Environ Health Perspect 121:1129–1134
Hossain MS, Dietz KJ (2016) Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front Plant Sci 7:548
Huang Q, Wang Q, Tan W, Song G, Lu G, Li F (2006) Biochemical responses of two typical duckweeds exposed to dibutyl phthalate. J Environ Sci Health Part A 41:1615–1626
Hu QJ, Chen MX, Song T, Cheng CL, Tian Y, Hu J, Zhang JH (2020) Spermidine enhanced the antioxidant capacity of rice seeds during seed aging. Plant Growth Regul. https://doi.org/10.1007/s10725-020-00613-4
Inui H, Wakai T, Gion K, Kim YS, Eun H (2008) Differential uptake for dioxin-like compounds by zucchini subspecies. Chemosphere 73:1602–1607
Jensen MS, Anand-Ivell R, Nørgaard-Pedersen B, Jönsson BA, Bonde JP, Hougaard DM, Cohen A, Lindh CH, Ivell R, Toft G (2015) Amniotic fluid phthalate levels and male fetal gonad function. Epidemiology 26:91–99
Kanojia A, Dijkwel PP (2018) Abiotic stress responses are governed by reactive oxygen species and age. Annu Plant Rev Online 1:1–32
Kapanen A, Stephen JR, Brüggemann J, Kiviranta A, White DC, Itävaara M (2007) Diethyl phthalate in compost: ecotoxicological effects and response of the microbial community. Chemosphere 67:2201–2209
Kaur R, Kumari A, Kaur K, Kaur H (2017) Comparative assessment of phytotoxic responses induced by the exposure of benzyl butyl phthalate and di-n-butyl phthalate to giant duckweed (Spirodela polyrhiza L. Schleiden). J Pharm Sci Res 9:2079–2085
Keunen ELS, Peshev D, Vangronsveld J, Van Den Ende WIM, Cuypers ANN (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255
Korte F, Kvesitadze G, Ugrekhelidze D, Gordeziani M, Khatisashvili G, Buadze O, Zaalishvili G, Coulston F (2000) Organic toxicants and plants. Ecotoxicol Environ Saf 47:1–26
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Kumari A, Kaur R (2017) Germination and early growth toxicity to barley seedlings (Hordeum vulgare L.) under di-n-butyl phthalate (DBP) stress. J Pharm Sci Res 9:2361–2366
Kumari A, Kaur R (2018) Evaluation of benzyl-butyl phthalate induced germination and early growth vulnerability to barley seedlings (Hordeum vulgare L.). Indian J Ecol 45:174–177
Kumari A, Kaur R (2019) Modulation of biochemical and physiological parameters in Hordeum vulgare L. seedlings under the influence of benzyl-butyl phthalate. PeerJ 7:e6742
Kumari A, Kaur R (2020) Di-n-butyl phthalate-induced phytotoxicity in Hordeum vulgare seedlings and subsequent antioxidant defense response. Biol Plant 64:110–118
Kumari A, Kaur R, Kaur R (2018) An insight into drought stress and signal transduction of abscisic acid. Plant Sci Today 5:72–80
Kumari A, Kaur R, Sharma R, Kaur R (2019) Assessment of toxicological effects of di-n-butyl phthalate to a cereal crop (Hordeum vulgare L.). J Adv Agric Technol 6:20–26
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: cncept and review. Soil Biol Biochem 83:184–199
Kvesitadze G, Khatisashvili G, Sadunishvili T, Ramsden JJ (2006) Biochemical mechanisms of detoxification in higher plants: basis of phytoremediation. Springer, New York
Kvesitadze E, Sadunishvili T, Kvesitadze G (2009) Mechanisms of organic contaminants uptake and degradation in plants. World Acad Sci Eng Technol 55(6):458–468
Li FM, Wu M, Yao Y, Zheng X, Zhao J, Wang ZY, Xing BS (2015) Inhibitory effects and oxidative target site of dibutyl phthalate onKarenia brevis. Chemosphere 132:32–39
Liao CS, Yen JH, Wang YS (2006) Effects of endocrine disruptor di-n-butyl phthalate on the growth of Bok choy (Brassica rapa subsp. chinensis) . Chemosphere 65:1715–1722
Liao CS, Yen JH, Wang YS (2009) Growth inhibition in Chinese cabbage (Brassica rapa var. chinensis) growth exposed to di-n-butyl phthalate. J Hazard Mater 163:625–631
Liao C, Liu W, Zhang J, Shi W, Wang X, Cai J, Zou Z, Lu R, Sun C, Wang H, Huang C (2018) Associations of urinary phthalate metabolites with residential characteristics, lifestyles, and dietary habits among young children in Shanghai, China. Sci Tot Environ 616–617:1288–1297
Lin H, Tao S, Zuo Q, Coveney RM (2007) Uptake of polycyclic aromatic hydrocarbons by maize plants. Environ Pollut 148:614–619
Lin Q, Chen S, Chao Y, Huang X, Wang S, Qiu R (2017) Carboxylesterase-involved metabolism of di-n-butyl phthalate in pumpkin (Cucurbita moschata) seedlings. Environ Pollut 220:421–430
Li JH, Guo HY, Mu JL, Wang XR, Yin DQ (2006) Physiological responses of submerged macrophytes to dibutyl phthalate (DBP) exposure. Aquat Ecosyst Health Manage 9:43–47
Li Y, Huang G, Gu H, Huang Q, Lou C, Zhang L, Liu H (2018) Assessing the risk of phthalate ester (PAE) contamination in soils and crops irrigated with treated sewage effluent. Water 10:999
Lyman WJ, Reehl WF, Rosenblatt DH (1990) Handbook of chemical property estimation methods. American Chemical Society, Washington
Mackintosh CE, Maldonado J, Hongwu J, Hoover N, Chong A, Ikonomou MG, Gobas FAPC (2004) Distribution of phthalate esters in a marine aquatic food web: comparison to polychlorinated biphenyls. Environ Sci Technol 38:2011–2020
Macoustra GK, King CK, Wasley J, Robinson SA, Jolley DF (2015) Impact of hydrocarbons from a diesel fuel on the germination and early growth of subantarctic plants. Environ Sci Procese Impacts 17:1238–1248
Ma T, Christie P, Teng Y, Luo Y (2013) Rape (Brassica chinensis L.) seed germination, seedling growth, and physiology in soil polluted with di-n-butyl phthalate and bis(2-ethylhexyl) phthalate. Environ Sci Pollut Res 20:5289–5298
Ma TT, Christie P, Luo YM, Teng Y (2014) Physiological and antioxidant responses of germinating mung bean seedlings to phthalate esters in soil. Pedosphere 24:107–115
Melin C, Egneus H (1983) Effects of di-n-butyl phthalate on growth and photosynthesis in algae and on isolated organelles from higher plants. Physiol Plant 59:461–466
Meng XZ, Wang Y, Xiang N, Chen L, Liu Z, Wu B, Dai X, Zhang YH, Xie Z, Ebinghaus R (2014) Flow of sewage sludge-borne phthalate esters (PAEs) from human release to human intake: implication for risk assessment of sludge applied to soil. Sci Total Environ 476–477:242–249
Millar DJ, Hannay JW (1986) Phytotoxicity of phthalate plasticisers: 1. Diagnosis and commercial implications. J Exp Bot. 37:883–897
Miller EL, Nason SL, Karthikeyan KG, Pedersen JA (2016) Root uptake of pharmaceuticals and personal care product ingredients. Environ Sci Technol 50:525–541
Mitsunobu S, Takahashi Y (2006) Study of the water solubility and sorption on particulate matters of phthalate in the presence of humic acid using 14c labelled di-(2-ethylhexyl)phthalate. Water Air Soil Pollut 175:99–115
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
Müller J, Kördel W (1993) Occurrence and fate of phthalates in soil and plants. Sci Tot Environ 134:431–437
Net S, Sempéré R, Delmont A, Paluselli A, Ouddane B (2015) Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci Technol 49:4019–4035
Nonogaki H (2008) Seed germination and reserve mobilization. In: Encyclopedia of Life Sciences. Wiley, New York
Ogner G, Schnitzer M (1970) Humic substances: fulvic acid-dialkyl phthalate complexes and their role in pollution. Science 170:317–318
Pan Y, Jing J, Dong F, Yao Q, Zhang W, Zhang H, Yao B, Dai J (2015) Association between phthalate metabolites and biomarkers of reproductive function in 1066 Chinese men of reproductive age. J Hazard Mater 300:729–736
Park SS, Bae M-S, Schauer JJ, Kim YJ, Cho Y, Kim J (2006) Molecular composition of PM2.5 organic aerosol measured at an urban site of Korea during the ACE-Asia campaign. Atmos Environ 40:4182–4198
Paterson S, Mackay D, Tam D, Shiu WY (1990) Uptake of organic chemicals by plants: a review of processes, correlations and models. Chemosphere 21:297–331
Philippat C, Mortamais M, Chevrier C, Petit C, Calafat AM, Ye X, Silva MJ, Brambilla C, Pin I, Charles MA, Cordier S (2012) Exposure to phthalates and phenols during pregnancy and offspring size at birth. Environ Health Perspect 120:464–470
Qing X, Yutong Z, Shenggao L (2015) Assessment of heavy metal pollution and human health risk in urban soils of steel industrial city (Anshan), Liaoning, Northeast China. Ecotoxicol Environ Saf 120:377–385
Ryan JA, Bell RM, Davidson JM, O’Connor GA (1988) Plant uptake of non-ionic organic chemicals from soils. Chemosphere 17:2299–2323
Saarma K, Tarkka MT, Itävaara M, Fagerstedt KV (2003) Heat shock protein synthesis is induced by diethyl phthalate but not by di(2-ethylhexyl) phthalate in radish (Raphanus sativus). J Plant Physiol 160:1001–1010
Sandermann JH (1994) Higher plant metabolism of xenobiotics: the ‘green liver’ concept. Pharmacogenetics 4:225–241
Saud S, Li X, Chen Y, Zhang L, Fahad S, Hussain S, Sadiq A, Chen Y (2014) Silicon application increases drought tolerance of kentucky bluegrass by improving plant water relations and morphophysiological functions. Sci World J 2014:1–10
Scheringer M, Salzmann M, Stroebe M, Wegmann F, Fenner K, Hungerbühler K (2004) Long-range transport and global fractionation of POPs: insights from multimedia modeling studies. Environ Pollut 128:177–188
Schettler T (2006) Human exposure to phthalates via consumer products. Int J Androl 29:134–139
Schlumpf M, Kypke K, Wittassek M, Angerer J, Mascher H, Mascher D, Vökt C, Birchler M, Lichtensteiger W (2010) Exposure patterns of UV filters, fragrances, parabens, phthalates, organochlor pesticides, PBDEs, and PCBs in human milk: correlation of UV filters with use of cosmetics. Chemosphere 81:1171–1183
Sharma R, Kaur R (2019) Diallyl phthalate-triggered oxidative stress in Spirodela polyrhiza L. Schleiden: physiological effects and role of antioxidant defence system. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-019-02491-4
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037
Sharma R, Kumari A, Rajput S, Arora S, Rampal R, Kaur R (2019) Accumulation, morpho-physiological and oxidative stress induction by single and binary treatments of fluoride and low molecular weight phthalates in Spirodela polyrhiza L. Schleiden. Sci Rep 9:1–19
Shiue I (2014) Higher urinary heavy metal, phthalate, and arsenic but not parabens concentrations in people with high blood pressure, U.S. NHANES, 2011–2012. Int J Environ Res Public Health 11:5989–5999
Shu G, Pontieri V, Dengler NG, Mets LJ (1999) light induction of cell type differentiation and cell-type-specific gene expression in cotyledons of a C4plant, Flaveria trinervia Plant Physiol 121:731–741
Sibali LL, Okonkwo JO, McCrindle RI (2013) Determination of selected phthalate esters compounds in water and sediments by capillary gas chromatography and flame ionization detector. J Environ Sci Health Part A 48:1365–1377
Singh J, Thakur JK (2018) Photosynthesis and abiotic stress in plants. In: Vats S (ed) Biotic and abiotic stress tolerance in plants. Springer, Singapore, pp 27–46
Singh R, Parihar P, Prasad SM (2020) Sulphur and calcium attenuate arsenic toxicity in Brassica by adjusting ascorbate–glutathione cycle and sulphur metabolism. Plant Growth Regul 91:221–235
Song Y, Lv J, Ma Z, Dong W (2019) The mechanism of alfalfa (Medicago sativa L.) response to abiotic stress. Plant Growth Regul. https://doi.org/10.1007/s10725-019-00530-1
Srivastava A, Sharma VP, Tripathi R, Kumar R, Patel DK, Mathur PK (2010) Occurrence of phthalic acid esters in Gomti River Sediment, India. Environ Monit Assess 169:397–406
Staples CA, Peterson DR, Parkerton TF, Adams WJ (1997) The environmental fate of phthalate esters: a literature review. Chemosphere 35:667–749
Sun Q, Cornelis MC, Townsend MK, Tobias DK, Eliassen AH, Franke AA, Hauser R, Hu FB (2014) Association of urinary concentrations of bisphenol a and phthalate metabolites with risk of type 2 diabetes: a prospective investigation in the Nurses’ Health Study (NHS) and NHSII Cohorts. Environ Health Perspect 122:616–623
Sun J, Wu X, Gan J (2015) Uptake and metabolism of phthalate esters by edible plants. Environ Sci Technol 49:8471–8478
Sun J, Pan L, Tsang DCW, Li Z, Zhu L, Li X (2018) Phthalate esters and organochlorine pesticides in agricultural soils and vegetables from fast-growing regions: a case study from eastern China. Environ Sci Pollut Res 25:34–42
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates, Sunderland
Teng Y, Wu J, Lu S, Wang Y, Jiao X, Song L (2014) Soil and soil environmental quality monitoring in China: a review. Environ Int 69:177–199
Tienpont B (2004) Determination of phthalates in environmental, food and biomatrices: an analytical challenge. Environ Res 134:345–52
Trapp M, Mc Farlane C (1994) Modeling and simulation of organic chemical processes. In: Trapp S, McFarlane JC (eds) Plant contamination. CRC, Boca Raton
Trasande L, Sathyanarayana S, Trachtman H (2014) Dietary phthalates and low-grade albuminuria in US children and adolescents. Clin J Am Soc Nephrol 9:100–109
Tuteja N (2007) Chapter twenty-four—mechanisms of high salinity tolerance in plants. In: Häussinger D, Sies H (eds) Methods in enzymology. Academic Press, Cambridge, pp 419–438
Ventrice P, Ventrice D, Russo E, De Sarro G (2013) Phthalates: European regulation, chemistry, pharmacokinetic and related toxicity. Environ Toxicol Pharmacol 36:88–96
Virgin HI, Holst AM, Mörner J (1981) Effect of di-n‐butyl phthalate on the carotenoid synthesis in green plants. Physiol Plant 53:158–163
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Whyatt RM, Perzanowski MS, Just AC, Rundle AG, Donohue KM, Calafat AM, Hoepner LA, Perera FP, Miller RL (2014) Asthma in inner-city children at 5–11 years of age and prenatal exposure to phthalates: the Columbia Center for Children’s Environmental Health Cohort. Environ Health Perspect 122:1141–1146
Wilkes CE, Summer JW, Daniels CA (2005) PVC handbook. Carl Hanser Verlag GmbH & Co, Germany. https://www.bookdepository.com/PVC-Handbook-Charles-E-Wilkes
Wittassek M, Koch HM, Angerer J, Brüning T (2011) Assessing exposure to phthalates—the human biomonitoring approach. Mol Nutr Food Res 55:7–31
Xie Z, Ebinghaus R, Temme C, Lohmann R, Caba A, Ruck W (2007) Occurrence and air–sea exchange of phthalates in the arctic. Environ Sci Technol 41:4555–4560
Xu G, Liu N, Wu M, Guo R, Zhou J, Shi W, Li F (2010) Aquatic toxicity of di (2-eihylhexyl) phthalate to duckweeds. J Shanghai Univ (English Ed) 14:100–105
Yu Y, Qin W, Li Y, Zhang C, Wang Y, Yang Z et al (2019) Red light promotes cotton embryogenic callus formation by influencing endogenous hormones, polyamines and antioxidative enzyme activities. Plant Growth Regul 87:187–199
Zai XM, Zhu SN, Qin P, Wang XY, Che L, Luo FX (2012) Effect of different light qualities on seedling growth and chlorophyll fluorescence parameters of Dendrobium officinale. Biologia 72:735–744
Zhang Y, Du N, Wang L, Zhang H, Zhao J, Sun G, Wang P (2015) Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. Environ Sci Pollut Res 22:3477–3488
Zhang Y, Tao Y, Zhang H, Wang L, Sun G, Sun X, Erinle KO, Feng C, Song Q, Li M (2015) Effect of di-n-butyl phthalate on root physiology and rhizosphere microbial community of cucumber seedlings. J Hazard Mater 289:9–17
Zhang Y, Zhang H, Sun X, Wang L, Du N, Tao Y, Sun G, Erinle KO, Wang P, Zhou C, Duan S (2016a) Effect of dimethyl phthalate (DMP) on germination, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. Environ Sci Pollut Res 23:1183–1192
Zhang Y, Zhang H, Sun X, Wang L, Du N, Tao Y, Sun G, Erinle KO, Wang P, Zhou C, Duan S (2016b) Effect of dimethyl phthalate (DMP) on germination, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. Environ Sci Pollut Res 23:1183–1192
Zhang C, Feng Y, Liu YW, Chang HQ, Li ZJ, Xue JM (2017) Uptake and translocation of organic pollutants in plants: a review. J Integr Agric 16:1659–1668
Zhou WM (1989) Priority pollutants. China Environmental Science Press, Beijing (in Chinese)
Acknowledgements
The authors are highly thankful to University Grants Commission, New Delhi (India) for financial assistance provided under National Fellowship for Higher Education (NFHE) scheme (vide letter no. F1-17.1/2015-16/NFST-2015-17-ST-HIM-1038/(SA-111/Website)).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kumari, A., Kaur, R. A review on morpho-physiological traits of plants under phthalates stress and insights into their uptake and translocation. Plant Growth Regul 91, 327–347 (2020). https://doi.org/10.1007/s10725-020-00625-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-020-00625-0