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Journal of Stress Physiology & Biochemistry, Vol. 15, No. 3, 2019, pp. 62-75 ISSN 1997-0838 Original Text Copyright © 2019 by Pirzadah, Malik and Dar
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Phytoremediation Potential of Aromatic and Medicinal Plants: A Way Forward for Green Economy
Tanveer Bilal Pirzadah1, 2*, Bisma Malik1, Fayaz Ahmad Dar1
1 Department of Bioresources, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
2 Department of Bioresources, Amar Singh College, Cluster University, Srinagar 190006, Jammu and Kashmir, India
*E-Mail: [email protected]
Currently, interests in the cultivation of aromatic and medicinal plants gained a rapid momentum worldwide. These find great application in various industries such as; cosmetic, pharmaceutical, perfumery and other industrial sectors. Therefore, product safety issues are of paramount importance for the betterment of the consumer. Presently, heavy metal (HMs) pollution is one of the serious issues for the environment and agriculture as it has a direct impact on the production yield. This situation has worsened in the present era due to the population pressure, industrialization and various anthropogenic activities which in turn lead to oxidative stress in plants and thus disturbs the redox homeostasis and ultimate affects the quality and production yield. However, plants possess a different regulatory system that work in a synergetic manner to combat stress and thus adapts themselves in such contaminated soils. These act as sinks to neutralize the toxic effects of these heavy metals either by chelation, sequestration, intensification of enzyme system. Here we discuss the impact of heavy metals on aromatic and medicinal plants and how they play an essential role as a sustainable phytoremediation crops.
Key words: Aromatic plants, Medicinal plants, Phytoremediation, Lethal effects, Regulatory
Received July 29, 2019
elements
The ever increasing population of the world is projected to reach 10.9 billion by 2050 and would lead to food crises in near future. Presently, agriculture sector is confronted immense challenges to provide adequate food supply, while at the same time maintain high productivity and quality standards. Current population of India is approximately 1.27 billion, thus feeding 1.27 billion mouths would indeed be a huge challenge because of degradation of soil quality due to various factors viz., mal-agricultural practices, anthropogenic activities and natural calamities that in turn affects the agro-industry. These mal-practices disturb the soil microflora by incorporating toxic heavy metals which causes shunted growth and ultimately affects the crop yield. Heavy metal toxicity is indeed a great threat to agriculture sector as it leads to oxidative stress in plants and cause deleterious effects resulting in the decline of production yield. Excessive ROS production disturbs the chemical equilibrium in plants and thus causes various oxidative damages like degradation of polyunsaturated fatty acids, leakage of ions, DNA damage and apoptosis (Rascio and Navari-Izzo, 2011; Pirzadah et al., 2018). Nature has engineered the plants to combat distinct biotic and abiotic stresses and thus acts as sinks for obnoxious chemicals. The plants act as green livers to neutralize the toxicity of the heavy metals either inside the plant matrix or in the rhizosphere. The detoxification of heavy metals by plants involves the co-ordinated approach at the physiological, biochemical or genomic level (Dalcorso et al., 2010). Generally, counteraction to heavy metal toxicity can be either accomplished by "evasion" when plants are capable to hamper metal uptake or by "tolerance" when plants sustain under huge metal concentration. The process of evasion involves the chelation or precipitation of metals in the rhizosphere and thus preventing its entry and translocation to the above ground part. In later situation, heavy metals are intra-cellularly chelated by oozing out organic acids or other metal-binding ligands (phytochelatins and metallothioneins) (Seth et al., 2012). The metal binding ligands such as; MTs and PCs helps the plant to absorb HM ions and sequester them inside vacuoles. The fate of the toxicity of HMs is determined by the regulation of vacuole sequestration capacity and thus it is very
important to unravel its mechanism and impact on transport and sequestration. This ability of plants to extract toxic metals is nowadays been exploited to rejuvenate the soil health contaminated with various obnoxious HMs through phytoremediation process besides, the ores of economically important metals can be extracted by means of phytomining. Classical approaches to remediate heavy metal contaminated soils require a huge capital cost. Therefore, the green approach of phytotechnology for the removal of toxic metals from contaminated sites is regarded as a cost-effective, sustainable and a promising alternative to maintain the health of the soil. Many plants have the capability to grow in metalloferous soils and withstand stress and such plants can be categorized into metallophytes, pseudometallophytes or
hyperaccumulators (Wenzel et al., 1998). However, the use of edible plants as phytoremediation crops possesses some drawbacks because the toxic metals may enter into the food chain and causes some deleterious effects. Therefore, non-edible crops such as aromatic and medicinal plants are the appropriate targets of interests to be used as potential sources of phytoremediation crops. Aromatic plants are important sources of essential oils that have potential market in perfumery, cosmetic industry and aromatherapy. Besides, the essential oils production is free from any toxic metal and thus prevents its entrance into the food chain (Khajanchi et al., 2013). Moreover, animals also do not damage to aromatic plants due to its fragrance and therefore it can be cultivated on large scale. Various aromatic and medicinal plants have the ability to accumulate toxic metals and are currently being exploited in phytoremediation technology. Hence, the cultivation of aromatic and medicinal plants offers a novel approach to remediate contaminated soils. Here we discuss the impact of heavy metals on aromatic and medicinal plants and how they play an essential role as a sustainable phytoremediation crops. Heavy metals and their lethal effects in plants
Heavy metal pollution is currently a great threat to agricultural sector as it directly affects the production yield by interrupting the crop physiology. Generally, plants exhibit numerous symptoms in response to heavy
metal stress which include; shunted growth and root ultrastructure (Sharma and Dubey, 2007; Pirzadah et al., 2018), leaf necrosis, chlorosis, turgor loss, decrease in photosynthetic activity, reduction in germination rate and percentage, apoptosis and finally death of the plant (Dalcorso et al., 2010; Wang et al., 2018). Besides, the toxicity of metal ions also disturbs the homeostasis in plants such as water uptake, transpiration, nutrient metabolism (Poschenrieder and Barcelo, 2004) and also interferes in gated ion channels (Demidchik, 2017). Lead (Pb) is not considered as an essential element besides plants does not possess lead uptake channels. However, this toxic element gets entrapped by organic acids (carboxylic group of mucilage uronic acid) on root surfaces (Sharma and Dubey, 2005), but how lead gets incorporated into the root cells is still unknown. Pb in association with other salts (sulphate and phosphate) gets precipitated thus possesses low solubility and availability to plants. As per several reports, maximum concentration of lead gets accumulated inside the root cells, thus creates a primary obstruction for the Pb translocation to the above-ground parts of the plant (Blaylock and Huang, 2000), acting like an innate barrier. Accumulation of Pb in plants has several lethal effects on their physiology and biochemical parameters (growth, morphology and photosynthesis). The enzymes get inactivated under high Pb concentration by binding with their sulfhydryl (-SH) groups. However, the tolerance of plants to Pb concentration varies depending upon the species and nature of mechanism. Some plants are prone to Pb concentration while as some are tolerant and they have the capability to accumulate high Pb concentration and are considered as hyperaccumulators. Buckwheat has tremendous potential to tolerate and accumulate high Pb concentration in their leaves without showing any significant damage (Horbowicz et al., 2013). On dry weight basis buckwheat accumulates approximately about 1000mg/Kg of Pb in its shoots thus is regarded as an excellent hyperaccumulator (Pirzadah et al., 2014). Reports also revealed that buckwheat accumulates high Pb concentration in various parts of the plant such as in leaves (8000mg/Kg), stem (2000mg/Kg) and roots (3300mg/Kg) on dry weight basis without showing any lethal damage (Tamura et al., 2005). In another study,
Pb is involved to inhibit the elongation of stem and root and expansion of leaf as in observed in Allium species (Gruenhage and Jager, 1985), Raphanus sativus and barley (Juwarkar and Shende, 1986) but the intensity of elongation depends on various parameters such as concentration gradient, ionic composition as well as pH of the medium (Pourrut et al., 2011). Aluminium (Al) which constitutes about 7% of the earth's crusts ranked third most abundant element after oxygen and silicon. Major portion of the Al occurs as oxides and alumino-silicates which are harmless compounds however, when soil becomes acidic due to anthropogenic activities, Al gets solubilized into the lethal form (Al3+). The toxicity of Al inhibits plant growth and thus affects the agricultural yield (Smirnov et al., 2014). Al not only causes shunted growth and development of plants but also inhibits root and shoot elongation thus declines the biomass production. The immediate adverse effects of Al-toxicity is root inhibition and elongation by destroying the root apex (Zheng, 2010), thus interferes in water and mineral uptake. Moreover, Al is also involved to halt the action of proton pumps on endosomes which in turn traps transferrin-bound iron inside these vesicles thus acts as a barrier in stimulation of ferritin synthesis. In addition to this Al also causes an oxidative stress though even it is not a redox metal (Liu et al., 2008). Besides, Al possesses the capacity to form electrostatic bonds preferably with oxygen donor ligands (viz. phosphates), cell wall pectin and outer surface of the plasma membrane (Yamamoto et al., 2001). Some reports also revealed that binding of Al to bio-membranes results in rigidification (Jones et al., 2006) which in turn facilitates the radicle chain reaction by iron ions and thus boosts the peroxidation of lipid as is reported in various species like barley (Guo et al., 2004), triticale (Liu et al., 2008), wheat (Hossain et al., 2005) and green gram (Panda et al., 2003). Higher Al concentration also leads to calcium and magnesium deficiency (Jones et al., 1998). The level of Al toxicity varies from species to species; some plants are very prone to Al-induced stress even at micromolar (|M) concentration while some species exhibits high resistance. Among various plant species, buckwheat, tea, mangroves and certain other grass species have the ability to develop symplastic tolerance mechanism and thus accumulates higher Al
concentration in the above-ground parts. Buckwheat has the large tendency to accumulate approximately about 1500 mg/Kg Al-concentration mainly in the form of Al-oxalates in the leaves without any lethal effect (Ma et al., 1997; Zhang et al., 1998). Mercury (Hg) another most toxic HM that has devastating effect on the agricultural production. It generally occurs in different forms such as mercury sulphide (HgS), Hg2+, Hg0 and methyl-mercury (CHsHg+), but the predominant form of Hg in the agricultural land is ionic form i.e., Hg2+ (Pirzadah et al., 2018). Hg possesses the unique property to remain in solid phase by binding onto the clay particles, sulphides or other organic matter. This toxic metal has the tendency to get accumulated in various plant parts especially higher plant species (Israr et al., 2006), where it causes deleterious effects to the plant cells and tissues. For instance, closure of stomata and blockade of water flow in plants by gets binding with water channel proteins (Zhang and Tyerman, 1999). Besides, Hg toxicity also hamper the mitochondrial activity which is usually considered as a power house of the cell and induces the oxidative stress which in turn leads to the generation of ROS, thus enhances the lipid peroxidation and ultimately disrupts the integrity of bio-membrane (Cargnelutti et al., 2006; Pirzadah et al., 2018). Mechanism of action of toxic metals in plant cells
Plants have developed various ways to detoxify HMs toxicity when accumulated at huge concentration levels. Usually, these heavy metals are categorized into two types which include: redox active (Co, Cr, Cu, Fe etc) and redox inactive (Mn, Pb, Cd, Hg, As, Ni etc). The redox active heavy metals play a direct role in generating ROS through various chemical reactions like Fenton and Haber-Weiss reactions (Schutzendubel and Polle, 2002; Cuypers et al., 2016). The second category of heavy metals plays an indirect role to induce oxidative stress like interference with enzyme defense system, disruption of the electron transport chain and lipid peroxidation initiation due to enhanced lipoxygenase activity. Moreover, heavy metals also possess the capability to bind firmly with atoms such as; nitrogen, sulphur and oxygen that is associated to free enthalpy of the formation of the product of the HM and ligand and reduce their solubility. Besides, these HMs also inactivate the enzymes by binding their thiol-group, for
instance, binding of heavy metal like cadmium (Cd) to sulfhydryl group of structural enzymes and proteins either results in mis-folding and arrest of enzyme action or impede with redox enzymatic regulation (Dalcorso et al, 2008; Hossain et al., 2012; Gill, 2014). Most of the enzymes need cofactors which are regarded as helper molecules to aid in biological activity. These cofactors may be either inorganic (Mg2+, Ca2+, Cu2+, Fe2+) or organic (biotin, FAD, NAD) origin and replacement of any cofactor halts the enzyme action. For instance, displacement of magnesium (Mg2+) in ribulose-1,5-bisphosphate-carboxylase/oxygenase (RuBisCO) by Co2+, Zn2+ and Ni2+ thus halts the activity of enzymes (Sharma and Dubey, 2005; Gill, 2014). Moreover, these HMs are also responsible for disruption of biomembranes by enhancing the lipid peroxidation, oxidation of thiol-group of proteins and blockage of basic membrane proteins (H+-ATPase) (Meharg, 1993; Hossain et al., 2012). Furthermore, these toxic heavy metals also leads to the initiation, production and accumulation of most lethal compounds like methylglyoxal-a cytotoxic chemical due to disruption of glyoxalase system that finally elicits oxidative stress by diminishing the glutathione content (Hossain and Fujita, 2010; Hossain and Hasanuzzaman, 2011). Role of Metallothioneins (MT)
MT's are metal binding low molecular weight cysteine rich proteins that are generally synthesized during mRNA translation (Kagi, 1991). These metalloproteins has got immense potential to sequester numerous HM like Cd/ Pb/ Hg/ Cu/ Zn etc by binding via thiol group (-SH) of cysteine residues thus is involved in the homeostasis and detoxification of heavy metal toxicity (Goldsbrough, 2000; Komal et al., 2014; Pirzadah et al., 2014; Tripathi et al., 2015). The structure of MT revealed that it possesses two metal binding domains which are assembled from cysteine clusters. These include a-domain (N-terminal) which bears three binding sites for divalent ion and p-domain (C-terminal) which has the capability to bind with four divalent ions of heavy metals. In plants, the genes encoded these metallo-proteins are influenced by stress conditions viz., HM, cold stress, drought stress etc. (Berta et al., 2009; Jia et al., 2012). These MT are usually regarded as major transition metal ion binding proteins in cells
because they mainly form the complex compounds with Cu, Zn (essential metals) but bear less capacity to bind with Cd, Hg Pb etc. Besides, some researchers also reported that these metallo-proteins also act as a shielding agent to protect plants from oxidative stress by removing free radicles (Jia et al., 2012). Nowadays researchers are very interested in determining the ROS scavenging activity of these MT besides developing databases containing gene sequences of MT that acts as a repository to generate HM resistant plants (Leszczyszyn et al., 2013). However, the transaction between metal binding and ROS scavenging is still unknown yet. It has been reported that during scavenging of ROS, metal ions would be released when free radicles gets bound to cysteine residues of these metallo-proteins. Few authors suggested that the released metals might be involved in signaling cascade. Various MT-types have been reported from plants like rice, oil palm, hybrid poplar, buckwheat and lichens besides many cDNA encoding MT-genes have been isolated (Backor and Loppi, 2009). It has been reported that buckwheat cDNA clone (PBM290) which encode MT-like proteins was isolated from cDNA library and the reduced amino acid sequence reveals its maximal homology with MT3-like protein isolated from Arabidopsis thaliana. Upon expression analysis it is found that buckwheat MT3 mRNAs seem to be present in tissues of root and leaf during development of seed under normal circumstances and its expression is greatly altered by HM stress (Pirzadah et al., 2014). Role of transcription factors (TFs)
Hyperaccumulating plant species contain several metal TFs that are involved in various regulatory pathways to detoxify HMs and some have been already identified in various plant species that imparts HM tolerance and these TFs belong to different families viz., WRKY, basic leucine zipper (bzip), ethylene-responsive factor (ERF) and Myeloblastosis protein (Myb) (Fusco et al., 2005; Van De Mortel et al., 2008). Van De Mortel et al., (2006) reported that under Zn-sufficient conditions, 131 TFs showed 5-times more expression in T. caerulescens compared to A. thaliana. Similarly, Ban et al., (2011) reported that Cd and Cu cause either up-regulation or down-regulation of dehydration responsive element-binding protein (DREB). Another important
metal transporter known as (natural resistance associated macrophage protein) NRAMP found in fungi, bacteria, animals and plants and is responsible to transport a wide variety of metal ions viz.,Cd2+, Zn2+, Cu2+. Ni2+, Co2+, Fe2+ and Mn2+ across membranes (Nevo and Nelson, 2006). In case of plants there type of transporters are usually expressed in roots and shoots and are engaged to transport metal ions through plasma membrane and tonoplast (Schmidt et al., 2007). It has been reported that NRAMPs in Arabidopsis thaliana play a significant role to transport iron (Fe) and Cadmium (Cd), however NRAMP1 exhibits Fe transport specificity and homeostasis (Thomine et al., 2000). Other transporters involved in sequestration of HMs include ATP-binding cassette (ABC) transporters, cation diffusion facilitator (CDF) transporters, heavy metal ATPases (HMA) transporters etc. These are actually intracellular transporters that are involved to carry out the transport of xenobiotics and toxic heavy metals into the vacuole. Multidrug resistance-associated proteins (MRP) and pleiotropic drug resistance (PDR) transporters are two sub-families involved in sequestration of chelated heavy metals (Lee et al., 2005). In case of plants, vacuoles are considered as dominant sites for accumulation and storage of phytochelatins-Cadmium (PC-Cd) complexes. Usually cytosol is the major site where these complexes are generated and are then translocated by means of ABCtransporters (Yazaki, 2006). HMT1 is the first vacuolar transporter present in the tonoplast and is responsible to transport PC-Cd complexes inside the vacuole in a magnesium-adenosine triphosphate-dependent (Mg-ATP) manner (Yazaki, 2006). Salt and Rauser (1995) reported similar homolog protein (HMT1) in oat roots. Magnesium proton exchanger (MHX) and (Cation exchangers) CAX-transporters are the members of calcium-calmodulin (CaCA) families and are responsible for metal homeostasis. (MHX) first identified in vacuolar vesicles of rubber tree (Hevea brasiliensis) and is magnesium (Mg2+) and zinc (Zn2+)/H+ antiport dominantly expressed in xylem-associated cells. However, overexpression of these transporters enhances sensitivity to Mg and Zn, in spite the titre of the metals in shoots is unchanged (Shaul et al., 1999). Besides, CAX family are considered as Ca2+/H+ antiports helps to
recognize Cd2+-ions, thus is involved in Cd-sequestration inside the vacuoles (Salt and Wagner, 1993). AtCAX2 and AtCAX4 are two CAX proteins reported in A. thaliana and possess an essential role in accumulation of Cd inside the vacuoles. Korenkov et al., (2007) reported that overexpression of AtCAX2 and AtCAX4 leads the accumulation of large concentration of Cd inside the vacuoles. Moreover, AtCAX4 is usually
expressed in primordia and a root tip, besides it is induced by nickel (Ni) and manganese (Mn). Current update on the use of aromatic and medicinal plants in phytoremediation technology
The current update on the use of aromatic and medicinal plants as sustainable phytoremediation crops is illustrated in Table 1.
Table 1. An update on the use of aromatic and medicinal plants as phytoremediation crops
Plant Metal Reference
Cymbopogon citratus Cd, As, Ni, Cu, Fe Jisha et al. (2017)
Vetiveria zizanioides Cd and Pb Ng et al. (2017)
Ocimum basilicum Cd Alamo-Nole et al. (2017)
Mentha arvensis Cu, Zn Malinowska and Jankowski (2017)
Vetiveria zizanioides Cu, Pb, Sn, Zn Vo et al. (2011)
lemongrass Pb, Cd, Zn Hassan et al. (2016)
Euphorbia hirta Cd Hamzah et al. (2016)
Cymbopogon citratus Pb(II), Cd(II), Zn(II) Hassan (2016)
Ocimum basilicum Cr, Cd Zahedifara et al. (2016)
Mentha crispa Pb Sa et al. (2015)
Mentha species Ni, Cr, Cd, Al Manikandan et al. (2015)
Ocimum basilicum Cd and Zn Akoumianaki-Ioannidou et al. (2015)
Lavandula vera Pb, Zn, Cd Angelova et al. (2015)
Rosmarinus officinalis Cd and Pb Ramazanpour (2015)
Cymbopogon flexuosus Cr Patra et al. (2015)
Euphorbia hirta Radioactive waste Hu et al. (2014)
Cymbopogon citratus Pb Sobh et al. (2014)
Ocimum basilicum Cd, Pb, Zn Stancheva et al. (2014)
Vetiveria zizanioides Cd , Ni Gunwal et al. (2014)
Cymbopogon citratus Ni Lee et al. (2014)
Matricaria chamomilla Cd , Pb, Zn Stancheva et al. (2014)
Catharanthus roseus Cd, Pb, Ni, Cr Ahmad and Misra (2014)
Ocimum tenuiflorum As Siddiqui et al. (2013)
M. chamomilla Cd, Pb Voyslavov et al. (2013)
Cymbopogon winterianus Cr Sinha et al. (2013)
Vetiveria zizanioides Cu, Zn, Pb Chen et al. (2012)
Chrysopogon zizanioides Hg Mangkoedihardjo and Triastuti (2011)
Aloe vera Cr Sharma and Adholeya (2011)
Ocimum basilicum Cr, Cd, Pb, Ni Prasad et al. (2010)
Pelargonium sps. Pb Abdullah and Sarem (2010)
Hypericum sp. Cd Tirillini et al. (2006)
Ocimum tenuiflorum Cr Rai et al. (2004)
Hypericum perforatum Cd Schneider and Marquard (1996)
Senecio coronatus Ni Przybylowics et al. (1995)
Table 2. Observed phyto-technologies in some aromatic plants.
Name of plant Observed Phyto-technologies Possible heavy metals to be remediated
Vetiver Phytostabilizer Cd, Pb, Cu, As, Hg, Cr, Ni, Sn, Zn
Lemongrass Phytostabilizer Cd, Hg, Pb, Cu, Ni, Cr
Palmarosa Phytostabilizer Cr, Cd, Pb, Ni, Fe, Zn, Cu
Citronella Phytostabilizer Cd, Cr
Ocimum Phytostabilizer Cr, Cd, Ni, Pb, As, Zn
Salvia Hyper accumulator for certain heavy metals Cd, Pb, Cr
Mint Phytostabilizer Cr, Pb, Ni, Cd, Cu, Zn,
Rosemary Potential bio-monitor, Phytostabilizer as well as hyper accumulator of Ni. Hg, Pb, Cu, Zn, Cd, Ni, Fe, As, Sb
Chamomile Facultative metallophytes or metal excluders, Cd accumulating species. Cd, Zn, Cu, Pb, Ni
Geranium Hyper accumulator for certain heavy metals. Cd, Ni, Pb, Zn
Lavender Hyper accumulator for certain heavy metals Cd, Pb, Cu, Zn, Fe
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Figure 1 Graphical representation showing benefits of aromatic plants for phytoremediation
Aromatic and medicinal plants as sustainable phytoremediation crops
Remediation of soil health contaminated with toxic metals by utilizing aromatic plants than non-aromatic edible crops is a promising and sustainable approach.
Till date, few data is available where aromatic and medicinal plants were utilizing as prominent phytoremediation crops (Gupta et al., 2013). Vamerali et al., (2010) carried out a metadata analysis and reported that few data is available regarding the utilization of
aromatic plants as phytoremediation crops. Metadata analysis revealed that an edible oil crop Brassica juncea was mostly cited (148 citations) followed by Helianthus annuus (57 citations), B. napus, and Zea mays (both 39 citations). This indicates that aromatic and medicinal plants were given a least significance as phytoremediation crops. However the use of non-aromatic crops for phytoremediation is not viable because the toxic heavy metals may accumulate into their edible parts and thus enter the food chain either consumed by animals or humans. Therefore, the main thrust was currently focused on aromatic plants which are used for the production of essential oils. These are non-edible and are not being consumed directly like vegetables and staple foods besides they possess efficient check points to reduce toxic metal translocation from soil to essential oils or carried out any alteration in its chemical composition (Zheljazkov et al., 2006) which is due to the process used for oil extraction (Scora and Chang, 1997; Bernstein et al., 2009; Pandey and Singh, 2015). It has been proved that there is least risk of heavy metal contamination in essential oil obtained through steam distillation process as heavy metals remain in the extracted plant. Hence, it can be acceptable in the market (Scora and Chang, 1997; Zheljazkov and Nielsen, 1996). Majority of the promising aromatic plants for phytoremediation of toxic metal contaminated sites have been identified from families -Poaceae, Lamiaceae, Asteraceae and Geraniaceae. Utilizing aromatic and medicinal plants is a novel approach to rejuvenate contaminated soils and currently number of plants viz., vetiver (Vetiveria zizanioides), palmarosa (Cymbopogon martinii), lemon grass (Cymbopogon flexuosus), citronella (Cymbopogon winterianus), geranium mint (Mentha sp.), tulsi (Ocimum basilicum) are ecologically feasible and viable. Some aromatic grasses like, lemon grass, palmarosa, citronella, vetiver, etc. are stress tolerant and perennial in nature. Table 2 represents the observed phyto-technologies of various aromatic and medicinal plants. Besides, there is high demand for the essential oils at the international market because of their significant role in different industrial sectors viz., perfumery, aromatherapy and cosmetic industry and it is predicted that the potential market for essential oils would reach to
US$5 trillion by 2050 (Verma et al., 2014). In order to cater the ever increasing demand of essential oil, aromatic grasses possess the huge potential as these can be grown on contaminated sites to restore the soil health besides oil production and eco-tourism (Fig. 1). Conclusion and further perspective
HM contamination is increasing at an alarming rate due to numerous anthropogenic activities which in turn affects plant health thus declines the production yield. Even though several species possess the capacity to hyper-accumulate these HMs thus resists the oxidative stress while some are prone to HM stress. Generally, plants have the innate ability to detoxify HMs by means of several ways like exclusion, chelation and sequestration. Nowadays research must be focused on non-edible crops such as; aromatic plants as they have great potential in remediating soils contaminated with toxic metals, besides reports revealed that the essential oil production gets enhanced under heavy metal stress as these acts as an elucidating agents. Phytoremediation is a sustainable approach in the phyto-management programme to rejuvenate soil health; therefore a comprehensive research is needed for utilizing aromatic and medicinal plants as phytoremediation crops that may lead to green scented technology. This approach of using green scented technology is cost-effective and reduces the risks of food chain contamination. In future, multiple stress factors will be investigated as it happens in real environmental conditions. An interdisciplinary approach is necessary to unravel the molecular mechanisms involved in HM-stress. In addition to above, plant-metal interaction is also indispensible for numerous purposes such as;
(1) Prognosis health hazards caused by metal bioaccumulation in crops failing visible manifestations of phytotoxicity.
(2) Bio-fortification i.e. design plants in such a way that they can accumulate metals indispensable for human health.
(3) Rejuvenate soil health (phytoremediation) and excavation of rare metals through green route (phytomining).
CONCLUSION AND FURTHER PERSPECTIVE
By dint to their antioxidant property, exogenous spermine exert a stimulating effect on several Physiological processes in the tomato plant. As shown in this study, the combination of this polyamine with cadmium makes it possible to reduce the disturbances caused by this metal stress, such as the recovery of weight, and the content of photosynthetic pigments as well as the stimulation of antioxidant enzymes. Nevertheless, because of the expensive price of polyamine, this has further research needed on the treatment time of exogenous spermine application to take advantage of their large-scale.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
REFERENCES
Abdullah S. and Sarem S. M. (2010) The potential of Chrysanthemum and Pelargonium for phytoextraction of lead-contaminated soils. J Civ Eng. 4:409-416. Ahmad R. and Misra N. (2014) Evaluation of phytoremediation potential of Catharanthus roseus with respect to chromium contamination. Am J Plant Sci 5:2378-2388 Akoumianaki-Ioannidou A., Kalliopi P., Pantelis B. and Moustakas N. (2015) The effects of Cd and Zn interactions on the concentration of Cd and Zn in sweet bush basil (Ocimum basilicum L.) and peppermint (Mentha piperita L). Fresenius Environ Bull. 24(1):77-83. Alamo-Nole L. and Su Y. F. (2017) Translocation of cadmium in Ocimum basilicum at low concentration of CdSSe nanoparticles. Appl Mater Today 9:314318.
Angelova V. R., Grekov D. F., Kisyov V. K. and Ivanov K. I. (2015) Potential of lavender (Lavandula vera L.) for phytoremediation of soils contaminated with heavy metals. Int J Biol Biomol Agric Food Biotechnol Eng. 9:465-472. Backor M. and Loppi S. (2009) Interactions of lichens
with heavy metals. Biol Plant 53: 214-222.
Ban Q. Y., Liu G. F. and Wang Y. C. (2011) A DREB gene from Limonium bicolor mediates molecular and physiological responses to copper stress in transgenic tobacco. J Plant Physiol 168: 449-458.
Bernstein N., Chaimovitch D. and Dudai N. (2009) Effect of irrigation with secondary treated effluent on essential oil, antioxidant activity, and phenolic compounds in oregano and rosemary. Agron J 101: 1-10
Berta M., Giovannelli A., Potenza E., Traversi M. L. and Racchi M. L. (2009) Type 3 metallothioneins respond to water deficit in leaf and in the cambial zone of white poplar (Populus alba). J Plant Physiol 166: 521-530.
Blaylock M. J. and Huang J. W. (2000) Phytoextraction of metals in Phytoremediation of Toxic Metals: Using Plants to clean up the environment. In: Raskin I, Ensley BD (ed) JohnWiley & Sons, New York, NY, USA, pp 53-71.
Cargnelutti D., Tabaldi L. A., Spanevello R. M., Jucoski G. O., Battisti V., Redin M., Linares C. E. B., Dressler V. L., Flores M. M., Nicoloso F. T., Morsch V. M. and Schetinger M. R. C. (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65: 999-1006.
Chen K. F., Yeh T. Y. and Lin C. F. (2012) Phytoextraction of Cu, Zn, and Pb enhanced by chelators with vetiver (Vetiveria zizanioides): hydroponic and pot experiments. ISRN Ecol. 2012: Article ID 729693, 12 pages
Cuypers A., Hendrix S., Amaral dos Reis R., De Smet S., Deckers J., Gielen H., Jozefczak M., Loix C., Vercampt H., Vangronsveld J. and Keunen E. (2016) Hydrogen Peroxide, Signaling in Disguise during Metal Phytotoxicity. Front Plant Sci 7:470. 125.
Dalcorso G., Farinati S. and Furini A. (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5(6): 663-667.
DalCorso G., Farinati S., Maistri S. and Furini A. (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integrat Plant Biol 50(10): 1268-1280.
Demidchik V. (2017) ROS-Activated Ion Channels in Plants: Biophysical Characteristics, Physiological Functions and Molecular Nature. Int J Mol Sci 19: 1263. 1-18.
Fusco N., Micheletto L., Dal Corso G., Borgato L. and Furini A. (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 421(56): 3017- 3027.
Gill M. (2014) Heavy metal stress in plants: a review. Int J Adv Res 2(6): 1043-1055.
Goldsbrough P. (2000) Metal tolerance in plants: the role of phytochelatins and metallothioneins. In: N. Terry and G. Banuelos (eds.). Phytoremediation of contaminated soil and water. CRC Press, LLC, 221-233.
Gruenhage L. and Jager I. I. J. (1985) Effect of heavy metals on growth and heavy metals content of Allium Porrum and Pisum sativum. Angew Bot 59: 11-28.
Gunwal I., Singh L. and Mago P. (2014) Comparison of phytoremediation of cadmium and nickel from contaminated soil by Vetiveria zizanioides L. Int J Sci Res Publ. 4(10) :1-7.
Guo T. R., Zhang G. P., Zhou M. X., Wu F. B. and Chen J. X. (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant and Soil 258: 241-248.
Gupta A. K., Verma S. K., Khan K. and Verma R. K. (2013) Phytoremediation using aromatic plants: a sustainable approach for remediation of heavy metals polluted sites. Environ Sci Technol 47: 10115-10116
Hamzah A., Hapsari R. I. and Wisnubroto E. I. (2016) Phytoremediation of cadmium-contaminated agricultural land using indigenous plants. Int J Environ Agric Res (IJOEAR) 2(1): 8-14
Hassan E. (2016) Comparative study on the biosorption of Pb (II), Cd (II) and Zn (II) using Lemon grass (Cymbopogon citratus): kinetics, isotherms and thermodynamics. Chem Int. 2(2): 89-102.
Horbowicz M., Debski H., Wiczkowski W., Szawara-
Nowak D., Koczkodaj D., Mitrus J. and Sytykiewicz H. (2013) The impact of short term exposure to Pb and Cd on flavonoid composition and seedling growth of common buckwheat cultivars. Pol J Environ Stud 22(6): 1723-1730.
Hossain M. A. and Fujita M. (2010) Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiol Mol. Biol. Plants 16(1): 19-29.
Hossain M. A., Hasanuzzaman M. and Fujita M. (2011) Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycine betaine is correlated with salt tolerance in mung bean. Front Agric China. 5(1): 1-14.
Hossain M. A., Hossain A. K. M. Z., Kihara T., Koyama H. and Hara T. (2005) Aluminum-induced lipid peroxidation and lignin deposition are associated with an increase in H2O2 generation in wheat seedlings. Soil Sci Plant Nutr. 51: 223-230.
Hossain M. A., Piyatida J., Teixeira da Silva J. A. and Fujita M. (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany Article ID 872875: 37. 37 p.
Hu N., Ding D., and Li G. (2014) Natural Plant Selection for Radioactive Waste Remediation. In: Gupta D., Walther C. (eds) Radionuclide Contamination and Remediation Through Plants. Springer, Cham pp 33-53.
Israr M. and Sahi S. V. (2006) Antioxidative responses to mercury in the cell cultures of Sesbania drummondii. Plant Physiol Biochem 44(10): 590595.
Jia D. U., Li Y. J. and Cheng-Hao L. I. (2012) Advances in metallotionein studies in forest trees. POJ 5(1): 46-51.
Jisha C. K., Bauddh K. and Shukla S. K. (2017) Phytoremediation and Bioenergy Production Efficiency of Medicinal and Aromatic Plants. In: Bauddh, K., Singh, B., Korstad, J. (Eds.)
Phytoremediation Potential of Bioenergy Plants, pp 287-304.
Jones D. L., Blancaflor E. B., Kochian L. V. and Gilroy S. (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29: 1309-1318.
Jones D. L., Gilroy S., Larsen P. B., Howell S. H. and Kochian L. V. (1998) Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana. Planta 206: 378-387.
Juwarkar A. S. and Shende G. B. (1986) Interaction of Cd-Pb effect on growth yield and content of Cd, Pb in barley. Ind J Environ Heal 28: 235-243.
Kagi J. H. R. (1991) Overview of metallothioneins. Methods Enzymol 205: 613-626.
Khajanchi L., Yadava R. K., Kaurb R., Bundelaa D. S., Khana M. I., Chaudharya M., Meenaa R. L., Dara S. R. and Singha G. (2013) Productivity, essential oil yield, and heavy metal accumulation in lemon grass (Cymbopogon flexuosus) under varied wastewater-groundwater irrigation regimes. Ind Crop Prod 45: 270-278.
Komal T., Mustafa M., Ali Z. and Kazi A. G. (2014) Heavy metal induced adaptation strategies and repair mechanisms in plants. Journal of Endocytobiosis and Cell Research. 25: 33-41.
Korenkov V., Park S. H., Cheng N. H., Sreevidya C., Lachmansingh J., Morris J., Hirschi K. and Wagner G. J. (2007) Enhanced Cd2+ selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225: 403411.
Lee L. Y., Lee X. J., Chia P. C., Tan K. W. and Gan S. (2014) Utilisation of Cymbopogon citratus (lemon grass) as biosorbent for the sequestration of nickel ions from aqueous solution: equilibrium, kinetic, thermodynamics and mechanism studies. J Taiwan Institut Chem Eng. 45(4): 1764-1772.
Lee M., Lee K., Lee J., Noh E. W. and Lee Y. (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138: 827-836.
Leszczyszyn O. I., Imam H. T. and Blindauer C. A.
(2013) Diversity and distribution of plant metallothioneins: A review of structure, properties and functions. Metallomics 5(9): 1146-1169.
Liu Q., Yang J. L., He L. S., Li Y. Y. and Zheng S. J. (2008) Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biologia Plantarum 52: 87-92.
Ma J. F., Zheng S. J., Hiradate S. and Matsumoto H. (1997) Detoxifying aluminum with buckwheat. Nature 390: 569-570.
Malinowska E. and Jankowski K. (2017) Copper and zinc concentrations of medicinal herbs and soil surrounding ponds on agricultural land. Landscape Ecol Eng. 13(1): 183-188.
Mangkoedihardjo S. and Triastuti Y. (2011) Vetiver in phytoremediation of mercury polluted soil with the addition of compost. J Appl Sci Res. 7(4): 465469.
Manikandan R., Sahi S. V. and Venkatachalam P. (2015) Impact assessment of mercury accumulation and biochemical and molecular response of Mentha arvensis: a potential hyperaccumulator plant. The Scientific World Journal 2015: Article ID 715217, 10 pages
Meharg A. A. (1993) The role of plasmalemma in metal tolerance in angiosperm. Physiologia Plantarum. 88 (1): 191-198.
Nevo Y. and Nelson N. (2006) The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta 1763: 609-620.
Ng C. C., Boyce A. N., Rahman M. and Abas R. (2017) Tolerance threshold and phyto-assessment of cadmium and lead in Vetiver grass, Vetiveria zizanioides (Linn.) Nash. Chiang Mai J Sci. 44(4): 1367-1368.
Panda S. K., Singha L. B. and Khan M. H. (2003) Does aluminium phytotoxicity induce oxidative stress in green gram (Vigna radiata)? Bulgarian Journal of Plant Physiology 29: 77-86.
Pandey V. C. and Singh N. (2015) Aromatic plants versus arsenic hazards in soils. J Geochem Explor 157: 77-80
Patra H. K., Marndi D. S. and Mohanty M. (2015)
Chromium toxicity, physiological responses and tolerance potential of lemon grass (Cymbopogon flexuosus Nees ex steud. wats.). Ann Plant Sci. 4(05): 1080-1084.
Pirzadah T. B., Malik B., Tahir I., Irfan Q. M. and Rehman R. U. (2018) Characterization of mercury-induced stress biomarkers in Fagopyrum tataricum plants. Int J Phytoremediation 20(3): 225236.
Pirzadah T. B., Malik B., Tahir I., Kumar M., Varma A. and Rehman R. U. (2014) Phytoremediation: An Eco-Friendly Green Technology for Pollution Prevention, Control and Remediation. In: Hakeem KR, Sabir M, Ozturk M, Mermut AH (ed), Soil Remediation and plants: Prospects and Challenges, Elsevier publications, USA, pp, 107122.
Poschenrieder. and Barcelo J. (2004) Water relations in heavy metal stressed plants. In: Prasad MNV (ed), Heavy Metal Stress in Plants 3rd eds Springer, Berlin, Germany, pp 249-270.
Pourrut B., Shahid M., Dumat C., Winterton P. and Pinelli E. (2011) Lead Uptake, Toxicity, and Detoxification in Plants. Rev Environ Contam Toxicol 213: 113-136.
Prasad A., Singh A. K., Chand S., Chanotiya C. S. and Patra D. D. (2010) Effect of chromium and lead on yield, chemical composition of essential oil, and accumulation of heavy metals of mint species. Commun Soil Sci Plant Anal. 41(18): 2170-2186.
Przybylowics W. J., Pineda C. A., Prozesky V. M. and Mesjasz-przybylowicz J. (1995) Investigation of Ni hyperaccumulation by true elemental imaging. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 104: 176-181.
Rai U. N., Vajpayee P., Singh S. N. and Mehrotra S. (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167: 1159-1169
Ramazanpour H. (2015) Study effect of soil and amendments on phytoremediation of cadmium
(Cd) and lead (Pb) from contaminated soil by rosemary (Rosmarinus Officinalis L.) [doctoral dissertation]. Zabol: University of Zabol.
Rascio N. and Navari-Izzo F. (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180(2): 169-181.
Sa R. A., Alberton O., Gazim Z. C., Laverde Jr A., Caetano J., Amorin A. C. and Dragunski D. C. (2015) Phytoaccumulation and effect of lead on yield and chemical composition of Mentha crispa essential oil. Desalin Water Treat. 53(11): 30073017.
Salt D. E. and Rauser W. E. (1995) MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107: 1293-1301.
Salt D. E. and Wagner G. J. (1993) Cadmium transport across tonoplast of vesicles from oat roots. Evidence for a Cd2+/H+ antiport activity. J Biol Chem 268: 12297-12302.
Schmidt U. G., Endler A., Schelbert S., Brunner A., Schnell M., Neuhaus H. E., Marty-Mazars D., Marty F., Baginsky S. and Martinoia E. (2007) Novel Tonoplast Transporters Identified Using a Proteomic Approach with Vacuoles Isolated from Cauliflower Buds. Plant Physiol 145(1): 216-229.
Schneider M. and Marquard R. (1996) Investigation on the uptake of cadmium in Hypericum perforatum L. (St. John's wort). Acta Hortic 426: 435-442
Schutzendubel A. and Polle A. (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 372 (53): 1351-1365.
Scora R. W. and Chang A. C. (1997) Essential oil quality and heavy metal concentrations of peppermint grown on a municipal sludge-amended soil. J Environ Qual 26: 975-979
Seth C. S., Remans T., Keunen E., Jozefczak M., Gielen H., Opdenakker K., Weyens N., Vangronsveld J. and Cuypers A. (2012) Phytoextraction of toxic metals: a central role for glutathione, Plant Cell Environ 35(2): 334-346.
Sharma P. and Dubey R. S. (2005) Lead toxicity in
plants. Braz J Plant Physiol 17(1): 35-52.
Sharma P. and Dubey R. S. (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Reports. 26 (11): 2027-2038.
Sharma S. and Adholeya A. (2011) Phytoremediation of Cr-contaminated soil using Aloe vera and Chrysopogon zizanioides along with AM fungi and filamentous saprobe fungi: a research study towards possible practical application. Mycorrhiza News 22(4): 16-20
Shaul O., Hilgemann D. W., de-Almeida-Engler J. J., Van Montagu M., Inze D. and Galili G. (1999) Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J 18: 3973-3980.
Siddiqui F., Krishna S. K., Tandon P. K. and Srivastava S. (2013) Arsenic accumulation in Ocimum spp. and its effect on growth and oil constituents. Acta Physiol Plant. 35(4): 1071-1079.
Sinha S., Mishra R. K., Sinam G., Mallick S. and Gupta A. K. (2013) Comparative evaluation of metal phytoremediation potential of trees, grasses, and flowering plants from tannery-wastewater-contaminated soil in relation with physicochemical properties. Soil Sediment Contamin. 22(8): 958983.
Smirnov O. E., Kosyan A. M., Kosyk O. I. and Taran N. Y. (2014) Buckwheat stomatal traits under aluminium toxicity. Modern Phytomorphology 6: 15-18.
Sobh M., Moussawi M. A., Rammal W., Hijazi A., Rammal H., Reda M. and Hamieh T. (2014) Removal of lead (II) ions from waste water by using Lebanese Cymbopogon citratus (lemon grass) stem as adsorbent. Am J Phytomed Clin Ther. 2(9): 1070-1080.
Stancheva I., Geneva M., Boychinova M., Mitova I. and Markovska Y. (2014) Physiological response of foliar fertilized Matricaria recutita L. grown on industrially polluted soil. J Plant Nutr 37(12): 19521964.
Tamura H., Honda M., Sato T. and Kamachi H. (2005) Pb hyperaccumulation and tolerance in common
buckwheat (Fagopyrum esculentum Moench). J Plant Res 118: 355-359.
Thomine S., Wang R., Ward J. M., Crawford N. M. and Schroeder J. I. (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci USA 97: 4991-4996.
Tirillini B, Ricci A, Pintore G, Chessa M, Sighinolfi S (2006) Induction of hypericins in Hypericum perforatum in response to chromium. Fitoterapia 77: 164-170
Tripathi D. K., Singh V. P., Prasad S. M., Chauhan D. K., Dubey N. K. and Rai A. K. (2015) Siliconmediated alleviation of Cr (VI) toxicity in wheat seedlings as evidenced by chlorophyll florescence, laser induced breakdown spectroscopy and anatomical changes. Ecotoxicol Environ Saf 113: 133-144.
Vamerali T., Marianna B. and Giuliano M. (2010) Field crops for phytoremediation of metal-contaminated land A review. Environ Chem Lett 8(1): 1-17.
van de Mortel J. E., Schat H. Moerland et al. (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens, Plant Cell Environ 31(3): 301-324.
van de Mortel J. E., Villanueva L. A., Schat H., Kwekkeboom J., Coughlan S., Moerland P. D., van Themaat E. V. L., Koornneef M. and Aarts M. G. M. (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142(3): 11271147.
Verma S. K., Singh K., Gupta A. K., Pandey V. C., Trevedi P., Verma S. K. and Patra D. D. (2014) Aromatic grasses for phyto management of coal fly ash hazards. Ecol Eng 73: 425-428.
Vo V. M., Nguyen V. K., and Le V. K. (2011). Potential of using vetiver grass to remediate soil contaminated with heavy metals. VNU Journal of Science, Earth Sciences 27(3), 146-150.
Voyslavov T., Georgieva S., Arpadjan S. and Tsekova K. (2013) Phytoavailability assessment of cadmium and lead in polluted soils and accumulation by Matricaria chamomilla (Chamomile). Biotechnol Biotechnol Equip. 27(4): 3939-3943.
Wang S., Zhang Y., Song Q., Fang Z., Chen Z., Zhang Y., Zhang L., Zhang L., Niu N., Ma S., Wang J., Yao Y., Hu Z. and Zhang G. (2018) Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat. Front Plant Sci 8: 2217.
Wenzel W. W. and Jockwer F. (1998) Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Environ Pollut 104: 145-155
Yamamoto Y., Kobayashi Y. and Matsumoto H. (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in Pea roots. Plant Physiol 125: 199-208.
Yazaki K. (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Letters 580: 1183-1191.
Zahedifara M., Moosavib A. A., Shafigh M., Zareib Z. and Karimian F. (2016) Cadmium accumulation and partitioning in Ocimum basilicum as influenced by the application of various potassium fertilizers. Arch Agron Soil Sci 62(5): 663-673 Zhang S. J., Ma J. F. and Matsumoto H. (1998) High aluminium resistance in buckwheat: I. Al induced specific secretion of oxalic acid from root tip tips. Plant Physiol 117: 745-751. Zhang W. H. and Tyerman S. D. (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol. 120(3): 849-857. Zheljazkov V. D. and Nielsen N. E. (1996) Effect of heavy metals on peppermint and cornmint. Plant Soil 178: 59-66 Zheljazkov V. D., Craker L. E. and Baoshan X. (2006) Effects of Cd, Pb and Cu on growth and essential oil contents in dill pepper mint, and basil. Environ. Exp Bot 58: 9-16 Zheng S. J. (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Anal Bot 106: 183-184.
