Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals

Biotechnology Advances 29 (2011) 645–653

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Biotechnology Advances j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b i o t e c h a d v

Research review paper

Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals Mohammad Miransari Department of Soil Science, College of Agricultural Sciences, Shahed University, Tehran, Qom Highway, Tehran, 18151/159, Iran

a r t i c l e

i n f o

Article history: Received 2 February 2011 Received in revised form 2 April 2011 Accepted 21 April 2011 Available online 30 April 2011 Keywords: Environment Heavy metals Hyperaccumulator plants Molecular mechanisms AM fungi

a b s t r a c t Use of plants, with hyperaccumulating ability or in association with soil microbes including the symbiotic fungi, arbuscular mycorrhiza (AM), are among the most common biological methods of treating heavy metals in soil. Both hyperaccumulating plants and AM fungi have some unique abilities, which make them suitable to treat heavy metals. Hyperaccumulator plants have some genes, being expressed at the time of heavy metal pollution, and can accordingly localize high concentration of heavy metals to their tissues, without showing the toxicity symptoms. A key solution to the issue of heavy metal pollution may be the proper integration of hyperaccumulator plants and AM fungi. The interactions between the soil microbes and the host plant can also be important for the treatment of soils polluted with heavy metals. © 2011 Elsevier Inc. All rights reserved.

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Bioremediation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Hyperaccumulators. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Arbuscular mycorrhizal fungi . . . . . . . . . . . . . . . . . . . . . . . . . . 5. AM fungi and heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Mechanisms of heavy metal removal from soil by microbes affecting plant growth. 7. How to select the right combination of plant and AM species for bioremediation. . 8. The role of plant-microbe interactions in phytoremediation of heavy metals . . . . 9. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Heavy metals (53 elements) are categorized into one group based on their density (N5 g/cm 3) (Holleman and Wiberg, 1985). Heavy metals including iron (Fe), manganese (Mn), copper (Cu), zinc (Zn) and nickel (Ni) are necessary for plant growth and functioning. They catalyze different enzymatic and redox reactions, carry electron and are the main component of DNA and RNA metabolism (Zenk, 1996). However, some of the heavy metals such as Cd and Pb are not necessary to plant growth and, especially their high levels can adversely affect plant growth. At high concentrations, heavy metals influence the structure of enzymes and hence their functionality by affecting the protein structure

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or substituting a necessary element. As the structure of plasma membrane proteins such as H +−ATPases is sensitive to alteration by heavy metals; the toxic effects of heavy metals can influence the permeability and functioning of plasma membrane. In addition, heavy metals cause oxidative stress (production of reactive oxygen species), adversely affecting different cellular components and hence plant tissues (Sajedi et al., 2010; Schutzendubel and Polle, 2002). At high concentrations of heavy metals, there are different mechanisms, utilized by plants, to keep ion homeostasis, and hence to detoxify their unfavorable effects on plant growth (Clemens, 2001). Root exudates are able to chelate heavy metals and cellular walls can bind heavy metals. Inside the cells, production of compounds such as phytochelatins and metallothioneins with high affinity for heavy metals can bind heavy metals and hence control their cytoplasmic concentration by transporting them across tonoplanst and their subsequent sequestration in the vacuole (Hall, 2002).

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In addition to adversely affecting plant growth, heavy metals have unfavorable effects on the environment. There is a wide range of lands in the world contaminated with different sources of pollution affecting ecosystem health and human food chain. The important sources of heavy metals in soil are industrial activities, mines, polluted water, and sewage sludge (Lebeau et al., 2008). Different methods have been used for the remediation of polluted environment with heavy metals, however, use of biological methods have been proved to be more effective and less expensive (Lynch and Moffat, 2005; Salt et al., 1995a). There are different methods of cleaning the environment from different sources of pollutants (such as heavy metals) including plant bioremediation, using soil as a filtering medium and use of different soil microbes such as AM fungi and plant growth promoting rhizobacteria (PGPR) (Lebeau et al., 2008). There are plants called hyperaccumulators, which are able to absorb high amounts of heavy metals, while their growth is not affected. This ability can be effective for the removal of heavy metals from the polluted soils. Some of these plants belong to the families such as Brassicaseae, in which a limited number of plant species are able to develop mycorrhizal symbiosis with their host plant (Assuncao et al., 2001). In soil there are arbuscular mycorrhizal (AM) fungi developing symbiotic association with most of terrestrial plants. In this symbiosis AM fungi can significantly enhance the host plant ability to absorb water and nutrients in the exchange for carbon (C). AM spores are able to germinate in soil; however, for the symbiosis process to proceed the presence of host plant is necessary, indicating that AM fungi are obligate biothrophs (Smith and Read, 2008). Through communicating signal molecules, AM spores and plant roots can develop their symbiotic association. Germinated spores produce hyphae, which grow toward the host plant roots and eventually enter the cellular cortex. The hyphal network is developed by plant C source, producing a very extensive hyphal network with some unique abilities, indicated in the following. 1) Enhancing plant water and nutrient uptake, 2) alleviating soil stresses including heavy metals, 3) improving soil structure, 4) controlling pathogens, and 5) interacting with other soil microbes. Accordingly, AM fungi are considered to be a very effective component of ecosystem increasing crop production and contributing to the environmental cleanness (Miransari 2011a,b; Smith and Read, 2008). Numerous research works have indicated that AM fungi can significantly enhance their host plant ability to grow in soils polluted with heavy metals. Such effects are due to AM fungi abilities as well as their positive effects on plant growth. AM fungi are morphologically and physiologically unique and hence can perform efficiently under stress. In addition they can increase the growth of their host plant by enhancing water and nutrient uptake (Miransari 2011a,b). In the following parts the bioremediation methods of removing heavy metals from soil and the effects of AM symbiosis on the uptake of heavy metals as well as the related molecular mechanisms are mentioned. 2. Bioremediation Bioremediation or phytoremediation is the process of using plants and soil microbes for the removal and cleaning of pollutants from soil including heavy metals. It includes the following subcategories: 1) phytoextraction: uptake of heavy metals by the harvestable parts of plant, 2) phytodegradation: decomposition of pollutants by plants and microbes, 3) rhizofiltration: absorption of metals from polluted waters, 4) phytostabilization: decreased mobility and immobilization of pollutants in soil by plant roots and microbes, and 5) phytovolatilization: volatilization of pollutant into the atmosphere by plant roots (Chaudhry et al., 1998; Khan, 2005). Plants can use some mechanisms to alleviate the unfavorable effects of stress on their growth up to some extent. Under stress plant

tissues can function singly or together to modify the stress. The allocation of different compounds and ions into different plant tissues is among the strategies, which plants use to alleviate the stress and is called phytoremediation, or specifically phytoextraction. The method is more effective when the concentration of heavy metals does not exceed a certain amount, for example, for Pb the limit is equal to 1500 mg/kg. Phytoremediation of agricultural soils can result in the sustainable production of crop plants by positively affecting soil properties (Audet and Charest, 2007a; Salt et al., 1998). There are different parameters influencing the effectiveness of phytoremediation including soil depth and the translocation rate of heavy metals from roots to shoots. Although at least five years is required for soil remediation, longer time is usually necessary for soil clean-up (Dickinson and Pulford, 2005; Khan et al., 2000). With respect to disadvantages related to non-biological methods of treating polluted soils, use of biological methods including hyperaccumulator plants and soil microbes has been indicated to be promising to alleviate the stress of heavy metals (Glick, 2003; Hernandez-Allica et al., 2006; Kuiper et al., 2004; McGrath et al., 2006). There are two different methods by which soil microbes can assist the plant to alleviate the stress: 1) enhanced metal mobility by microbial production of biosurfactants (Herman et al., 1995), siderophores (Dubbin and Louise Ander, 2003) and organic acids (Di Simine et al., 1998), and/or 2) increasing plant growth by PGPR (Zhuang et al., 2007) and/or AM fungi (Khan, 2006). Under heavy metal stress plant allocates most of heavy metals to their roots so that plant shoots can function more efficiently. Other parameters including the rate of plant growth, and plant morphological and physiological properties can also affect plant performance under stress affecting plant abilities for bioremediation (Audet and Charest, 2008). Bioremediation is the process by which soil pollutants are removed, decreased or transported using biological methods and is essential for sustainable development (BBSRC. 1999). It has been a research subject for microbiologists and molecular biologists. Use of soil microbes or plants with the ability to absorb or degrade the pollutant (phytoremediation) or plants to limit the movement of pollutant (phytostabilization) in soil are the common processes of bioremediation. In the combined use of plant and soil microbes, plant supplies C source for microbes, which absorb, degrade or make the plant absorb the released elements. The energy source, used for such a process is usually up to 40% of plant photosynthates exudated by plant roots (Lynch and Moffat, 2005). Audet and Charest (2007a) indicated that the phytoextraction ability of plants is a very important character significantly affecting the bioremediation process. 3. Hyperaccumulators There are plants, which have the ability to absorb high amounts of heavy metals, while their growth remains unaffected. The technology of using plants for removing heavy metals from soil is called “phytoremediation”. It is rarely common that plants hyperaccumulate heavy metals as only less than 0.2% of angiosperms (450 species with the majority (75%) being Ni hyperaccumulators) are hyperaccumulators of heavy metals. Hyperaccumulators must have the ability of metal homeostasis while growing in a polluted environment (Verbruggen et al., 2009). The Thlaspi family are hyperaccumulating plants among which 23 species hyperaccumulate nickel (Ni), 10 species hyper accumulate Zn, just three species (T. caerulescens, T. praecox and T. goesingense) hyperaccumulate Cd and one species hyperaccumulate Pb (Lombi et al., 2000; Vogel-Mikuš et al., 2005, 2008). T. caerulescens is among the most well known hyperaccumulators (Assunção et al., 2003). Interestingly, this plant is able to grow in serpentine soils, which contain high levels of heavy metals including Zn, Co, Pb, Cr, Cd and Ni,

M. Miransari / Biotechnology Advances 29 (2011) 645–653

being able to absorb up to 30,000 and 1000 mg/kg Zn and Cd, respectively in their shoots, while its growth remains unaffected. Usually 100 mg/kg Zn is foliarly applied as 30 mg/kg is adequate for plant growth and 300 to 500 mg/kg is toxic. For Cd, concentrations higher than 1 mg/kg are toxic. It has been indicated that T. caerulescens Wolfen (Brassicaseae) is able to accumulate up to 1.5% (on the basis of dry weight) Zn, 0.6% Cd and 0.4% Pb at the sites with the highest rate of pollution. Such ability is affected by metal concentration and plant growth stage. The presence of metal transporters enables the plant to absorb and localize high rate of metals in different tissues (Pongrac et al., 2007; Vogel-Mikuš et al., 2005). Cellular compartmentation of Zn is also important in T. caerulescens as epidermal vacuoles can significantly enhance plant ability to absorb higher Zn in different parts of the plant including plant shoot (Kupper et al., 1999; Milner and Kochian, 2008; Pence et al., 2000). The following mechanisms are necessary in a hyperaccumulator plant to tolerate and absorb high rate of heavy metals. 1) Organometallic complexes with donor ligands including organic acids, cystein, glutathione, nicotinamine, hystidine and other thiols with low molecular weight (Callahan et al., 2006; Hernandez-Allica et al., 2006; Küpper et al., 2004), 2) ability to transport, 3) compartmentation potential, and 4) ability to store these complexes in the vacuoles of leaf storage cells (Kupper et al., 1999). The vacuoles of epidermal and mesophyll cells of T. caerulescens are able to store Zn and Cd (Kupper et al., 1999; Wójcik et al., 2005). However, in Brassica juncea and A. thaliana leaf trichomes are able to store Cd (Salt et al., 1995b). Hyper accumulators are not able to produce high biomass limiting their application for bioremediation. Hence, identification of hyperaccumulating genes, which can be used in other plants with high biomass production, can be a practical way to treat heavy metal pollution. Metal hyperaccumulators have some unique properties, which make them appropriate for the evaluation of mechanisms related to the absorption of heavy metals. There are a couple of Zn transporters with high affinity, such as ZNT1 (with high and low affinity for Zn and Cd, respectively), which direct the translocation of Zn across the root cell plasma membrane, xylem and eventually the cells of leaf mesophyll. Plant gene expression of such transporter is also important in the behavior of transporter to accumulate Zn in different parts of plant (Pence et al., 2000). Assuncao et al. (2001) also cloned and isolated the genes including ZTP1 (very similar to Arabidopsis ZAT gene), ZNT1 and ZNT2, responsible for Zn absorption and accumulation in T. caerulescens. ZNT1 is most likely the allele of the transporter gene in T. caerulescens (Pence et al., 2000) and ZNT2 is the homologue of ZNT1. They are highly expressed in T. caerulescens compared with T. arvense indicating that T. caerulescens is a hyperaccumulator for heavy metals. The latter two genes are mostly expressed in the roots; however, ZTP1 is expressed in both root and leaf. Interestingly, in T. arvense expression of ZTP1 and ZTP2 control plant Zn uptake under Zn deficient conditions. Down-regulation of these genes can control the process of Zn accumulation in T. caerulescens induced by enhanced Zn concentration in plant (Assuncao et al., 2001). T. goesingense has also been analyzed for its ability to tolerate and accumulate Zn. It has been indicated that the presence of metal tolerance protein 1(TgMTP1) in the cellular membrane of this plant can significantly control Zn hyperaccumulation. It is accumulated at high concentrations in the vacuolar membrane of the plant shoots affecting the transportation of Zn to the vacuoles and hence increasing plant hyperaccumulation ability as well as tolerance. The expression of TgMTP1 in A. thaliana induces a Zn deficiency response along with the enhanced expression of Zn transporter genes including ZIP3, ZIP4, ZIP5 and ZIP9 in the plant root and shoot, resulting in the increased accumulation of Zn in plant shoots. Interestingly, Zn accumulation in the cellular vacuole resulted in the enhanced expression of TgMTP1 in the vacuolar membrane (Gustin et al., 2009).

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In some interesting field experiments researchers indicated the parameters affecting the metal accumulating performance of T. caerulescens. For example, pH (5–6) and plant growth during winter can significantly enhance the process of heavy metal absorption by plant (McGrath et al., 2006; Milner and Kochian, 2008). However, more research work is necessary to indicate the other parameters affecting the absorbing ability of heavy metals by T. caerulescens. Compared with non-hyper accumulating plants, T. caerulescens may look for heavy metals in soil more efficiently. This may be due to the production of organic acids by plant roots enhancing the availability of heavy metals in the rhizosphere (Knight et al., 1997; McGrath et al., 1997, 2006; Pence et al., 2000). T. caerulescens is not only a metal hyperaccumulator, but it is also suitable to evaluate the behavior and homeostasis of micronutrients in plant. There is also another plant species A. Halleri, which is able to accumulate high amounts of heavy metals relative to A. thaliana. It can absorb up to 2.2% (Zn) and 0.28% (Cd) of the leaf dry weight without showing the toxicity symptoms. The ability to hyperaccumulate heavy metals in A. halleri has been attributed to the presence of 30 genes, which are not present in A. thaliana (Van De Mortel et al., 2008; Verbruggen et al., 2009). Down-regulation of HAM4 (heavy metal ATPase 4) by RNA interference indicated that the hyperaccumulating activity of A. halleri resulted by the presence of the metal pump HAM4. The enhanced expression of HAM4 is due to the presence of a cis-sequence and the related gene. Expression of such a gene in A. thaliana results in similar functioning related to the accumulation of heavy metals in plant. Elucidation of mechanisms, responsible for the hyperaccumulation of heavy metals in plants can be useful for the bioremediation of polluted soils as well as for bio-fortification (Hanikenne et al., 2008; Verbruggen et al., 2009). In brief the process of heavy metal absorption by hyperaccumulators includes: root uptake, xylem loading, xylem unloading, detoxification by chelation, vacuolar sequestration and other mechanisms including homeostasis (Verbruggen et al., 2009). In their research work Vogel-Mikuš et al. (2008) were able to localize Zn and Cd in a T. praecox grown on a mine soil using PIXE (proton-induced X-ray emission). Cd at 820 mg g − 1 dry weight had accumulated in the lower and upper epidermis as well as the in the vascular bundles, however, about half of this amounts was found in the mesophyll. With respect to the large volume of mesophyll relative to the epidermis, mesophyll is able to accumulate higher amounts of Cd, detoxifying and/or diluting the concentration of Cd in plant at the tissue and cellular level. 4. Arbuscular mycorrhizal fungi Arbuscular mycorrhizal (AM) fungi are soil fungi developing nonspecific symbiosis with most of the terrestrial plants. This association is beneficial for both symbionts as the host plant supplies the fungi with C in the exchange for water and nutrients. AM fungi are important components of the ecosystem because they can significantly increase ecosystem efficiency. Numerous researchers have indicated the beneficial effects of AM fungi on plant growth and yield production (Smith and Read, 2008). The communications of signal molecules between the two symbionts is necessary for the onset of symbiosis. Fungal spores germinate and grow toward the roots and eventually form the extensive hyphal network inside the root cortical cells and the surrounding soil. Fungal hyphae also produce arbuscules (hyphal branched like structure as the exchanging interface of nutrients between fungi and host plant) and vesicles (hyphal storage part with high number of vacuoles). AM fungi diversity can considerably influence ecosystem functioning through affecting the plant growth as well as its structural combination. Different AM species differ in their ability to affect plant

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growth and yield production. It has been indicated that AM fungi are also able to enhance plant growth under stress by their unique abilities. AM fungi have the following effects on plant growth and ecosystem efficiency: 1) increase plant water and nutrient uptake, 2) improve soil structure, 3) interact with other soil microbes, 4) control pathogens, and 5) alleviate soil stresses including heavy metals (Smith and Read, 2008). In the second part of this review article the role of AM fungi in the removal of heavy metals and the related mechanisms is discussed. 5. AM fungi and heavy metals Heavy metals are a very important source of pollution resulted by anthropogenic activities (Schachtschabel et al., 1992). Plants growing on polluted soils can influence the behavior of heavy metals by absorbing heavy metals in their tissues affecting the quality of food chain. Use of plant cover on soil can avoid the distribution of heavy metals to other parts by water or wind erosion. The uptake of heavy metals by plant and their toxic effects on plant and soil is determined by soil pH; carbonate concentration, soil colloids including clay and organic matter, root exudates and soil microbes (Adriano, 2001; Wenzel et al., 1999). Soil microbes and organic matter can immobilize heavy metals such as Cd; however root exudates including organic acids can enhance the mobility of heavy metals by forming soluble complexes (Janouskova et al., 2006). Production of H + by plant roots can influence rhizosphere pH affecting the solubility and hence bioavailability of metals in soil (Hinsinger, 1998). Heavy metals such as Cd can adversely affect the activity of proton pump and hence production of H + by roots (Tu et al., 1989). Proton pump supplies energy for the uptake and movement of nutrients across the plasma membrane. Accordingly, as heavy metals alter the rhizosphere pH their solubility and hence their bioavailability is decreased with reducing soil pH (Xian, 1989). The exchangeable Cd and not total Cd concentration, determines Cd uptake and accumulation by plant (Cheng et al., 2004; Wu and Zhang, 2002). AM fungi are able to alleviate the stress of heavy metals on plant growth, by soil bioremediation (bioaugmentation). Janouskova et al. (2006) found that AM fungi are able to alleviate the unfavorable effects of cadmium (Cd) on plant growth by the process of phytostabilization. Compared with non-mycorrhizal plants, significantly lower amounts of Cd were found in the mycorrhizal plants because AM hyphae were able to accumulate 10–20 times higher rates of Cd relative to the plant roots. As previously mentioned, the physiological properties of T. praecox allow it to act as a hyperaccumulator for heavy metals such as Zn, Cd and Pb. However, a very important aspect regarding such ability is how it can be improved. Although T. praecox is from the Brassicaseae family, it is able to develop symbiosis with AM fungi (Leyval et al., 1997; Pawlowska et al., 2000). This can be beneficial to improve the tolerating and hyperaccumulating ability of T. praecox under heavy metal stress. In their research work Vogel-Mikus et al. (2006) examined the effects of AM fungi on AM colonization and uptake of Zn, Cd and Pb by T. praecox in a polluted soil. T. praecox developed symbiosis with AM fungi during the stages of enhanced nutrient uptake such as the reproductive stage. There was positive correlation between root colonization by AM fungi and soil total Zn, Cd and Pb. AM colonization resulted in higher and lower nutrient and heavy metal uptake by plant roots, respectively. The decrease of heavy metal uptake by mycorrhizal T. praecox indicates that this plant can physiologically behave differently under heavy metal stress. This may however, enhance the ability of mycorrhizal plant to alleviate heavy metal stress more efficiently. Interestingly and similar to the results of other researchers (Miransari et al., 2007, 2008, 2010a,b) elevated levels of stress enhanced the effectiveness of AM fungi on stress alleviation, which

was also evident from the increased root colonization (Vogel-Mikus et al., 2006). AM fungi increased plant growth in soils polluted with Zn, however parameters such as plant species, plant tissue (root or shoot) and concentration of Zn in soil can affect plant growth differently (Chen et al., 2003, 2004). The important point about treating polluted soil with mycorrhizal plants is the selection of appropriate AM species. Although experimental results indicate the effectiveness of AM species on the alleviation of heavy metals stress, the most efficient species are the ones, which are selected from areas polluted with heavy metals. Such species have attained the ability to survive under such conditions and hence can act more efficiently relative to the other AM species. Such species have developed mechanisms with time, which can make AM fungi resist or tolerate the heavy metal stress and they can accordingly develop more efficient symbiosis with their host plant under such conditions (Khan, 2005). Chen et al. (2004) indicated that in soils, not polluted with Zn, Glomus caledonium is able to colonize the roots at a rate of more than 70%, however, when the soil was polluted with Zn concentrations at 300 and 600 mg/kg the rate of colonization decreased to 50%. Similar results were also found by Duponnois et al. (2006) as the use of 560 mg/kg Cd decreased the rate of root colonization from 60 to 20%. They also mentioned that the interaction effects between AM fungi and florescent pseudomonas increased the colonization rate of host plant from 32 to 45%. When plant is subjected to high levels of heavy metals, they are translocated and accumulated in the parenchyma cells of the inner root, which is the place of inoculation with different fugal structures including arbuscules, vesicles and hyphae (Kaldorf et al., 1999). It has yet not been likely to differentiate between heavy metals allocation to the roots and fungal hyphae. However, the mechanisms, directing heavy metal movement to plant roots by AM fungi have been indicated. They include: 1) heavy metals may be deposited in the cellular wall or in the fungal vacuoles, 2) sequestration of heavy metals by siderophores may deposit heavy metals in root apoplasm or in soil, 3) metallotioneins or phytochelatins may result in the deposition of heavy metals in fungal or plant cells and 4) the allocation of heavy metals from cytoplasm is performed by metal transporters located at the plasmalemma or tonoplast of both symbionts (Galli et al., 1994; Leyval et al., 1997; Schutzendubel and Polle, 2002). Heavy metal content in roots of mycorrhizal plants is highly altered indicating that the related genes are expressed at transcriptional and translation levels by AM fungi (Ouziad et al., 2005). There are indications that AM fungi result in the expression of some genes in the host plant when subjected to heavy metal stress (Repetto et al., 2003; Rivera-Becerril et al., 2005). When subjected to Zn contamination the Zn transporter gene (GintZnT1) in the hyphae of G. intraradices was expressed indicating its role in the alleviation of Zn stress (Gonzalez-Guerrero et al., 2005). In their other experiment Gonzalez-Guerrero et al. (2006) indicated that Cd and Cu result in the expression of the related transporters (GintABC1), which may detoxify their toxic effects in the fungal hyphae. Experiments have shown the expression of genes in the hyphae of G. intraradices inoculating M. truncatula in soils polluted with Zn. When expressed, the related four genes, which are important in the alleviation of Zn stress, result in the production of gluthatione S-transferase as a Zn transporter (Hildebrandt et al., 2006, 2007). This enzyme is the catalyzer for the combination of gluthatione with some electron receivers resulting in the alleviation of oxidative stress (Moons, 2003; Smith et al., 2004). In their experiment, Punaminiya et al. (2010) investigated the role of vetiver grass [Chrysopogon zizanioides (L.)] in association with G. mosseae in the phytoremidation of soils polluted with lead. The little solubility of Pb in the soil is one of the most important factors limiting Pb bioremediation. Colonization with G. mosseae significantly

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increased plant growth as well as Pb uptake by plant roots and its translocation to the plant shoot. In addition, the mycorrhizal plants had a higher rate of chlorophyll content and thiols with low molecular weight indicated the enhanced tolerance of mycorrhizal plant to the Pb pollution. Zarei et al. (2010) evaluated the diversity of AM fungi in polluted and non polluted soils with Pb and Zn. Using the technique of internal transcribed spacer region of rDNA they were able to identify nine AM species. The AM fungal sequence increased with decreasing the concentration of Pb and Zn and only one species was found in the highly contaminated area. Using multivariate statistical analysis it was indicated that in addition to the concentration of heavy metals in soil, the diversity of AM species in soil is also a function of soil calcium carbonate content and P availability. Accordingly, it can be indicated that the presence of carbonate calcium available in soil can influence the process of bioremediation by affecting both AM fungal growth and activity and the concentration of heavy metals. Rajkumar et al. (2009) indicated the importance of siderophore producing bacteria, which are resistant to heavy metal stress, in the bioremediation of soils polluted with heavy metals. Accordingly, under heavy metal pollution, siderophore producing bacteria are able to increase plant growth and tolerance by the enhanced availability of micronutrients such as iron. Such bacteria can also influence the process of bioremediation through the effects of siderophores on the binding of heavy metals and hence their increased availability. Furthermore, the interactions between the endophyte bacteria, which spend a part of their life cycle in the plant, with their host plant is of significant importance. For example, the production of the enzyme 1-amino-cyclopropane-1-carboxylate (ACC) deaminase by such bacteria can alleviate the effects of different stressors on plant growth including the heavy metal stress (Hardoim et al., 2008). Evaluating the ecology of such bacteria in association with their host plant can be important in the bioremediation of heavy metal stress. Long et al. (2010) investigated the diversity of AM species in the rhizosphere and roots of five plant species including Dysphania ambrosioides, Phytolacca Americana, Perilla frutescens, Rehmannia glutinosa, and Litsea cubeba grown under high concentration of heavy metals. Using the small subunit rRNA technique they indicated the phylogeny of AM species. Glomus species were the dominant species indicating the significance of AM fungal diversity, especially Glomus, in association with their host plant in the bioremediation of soils polluted with heavy metals. Metallothioneins are proteins, which are formed when the plant is subjected to heavy metal stress and are able to bind these metals. Cu can induce the production of metallothioneins in non-AM fungi (Kumar et al., 2005). Expression of the related genes in the presence of Cu and Zn and production of metallothioneins in the hyphae of G. intraradices can detoxify the adverse effects of heavy metals (Lanfranco et al., 2002). 6. Mechanisms of heavy metal removal from soil by microbes affecting plant growth There are two different mechanisms by which microbes can alleviate heavy metal stress in soil, and hence on plant growth. 1) Some soil microbes decrease the concentration of heavy metals in soil, while the others can increase it, and 2) by increasing plant growth (dilution effect) or by enhancing heavy metal concentration in plant (Lebeau et al., 2008). Metal bioavailability determines their extraction by plant. Bioavailability of a metal determines its toxicity and is the fraction of metal in soil or water, available to the utilizing organism (Dong et al., 2007). The factors, which affect the bioavailability of metals include: 1) soil properties including soil pH and redox potential, 2) metal chemical properties, 3) soil biological properties, and 4) climate (Fischerová et al., 2006). Usually the low bioavailability of metals decreases their uptake

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by plant to about 1% of its total concentration in soil (Braud et al., 2006; Whiting et al., 2001). However, this ratio is affected by soil properties including pH, cation exchange capacity (CEC), and organic matter (Kayser et al., 2001). Metal properties and its concentration in soil determine its concentration in plant (Baum et al., 2006; Bi et al., 2003). Whether soil microbes are used for bioremediation or not, usually there is much higher rate (10 times higher) of metals in plants roots than in plant shoots (Malcova et al., 2003). There is a wide range of PGPR, which are able to alleviate the stress of heavy metals in soil by enhancing metal uptake by plant as well as by increasing plant growth. Some of such bacteria are Rhizobium, Pseudomonas, Agrobacterium, Burkholderia, Azospirillum, Bacillus, Azotobacter, Serratia, Alcaligenes (Ralstonia), and Arthrobacter (Carlot et al., 2002; Glick, 2003). Production of siderophores by PGPR such as Pseudomonas can produce metal complexes with high solubility resulting in their higher uptake by plant (Braud et al., 2006; Whiting et al., 2001; Wu, C. et al., 2006; Wu, S., 2006a,b). The other interesting mechanism by which PGPR can alleviate the stress of heavy metals on plant growth, as previously mentioned, is through the production of enzyme 1-amino-cyclopropane-1-carboxylate (ACC) deaminase, catalyzing ACC as ethylene (stress hormone) precursor to ammonia and α-ketobutyrate (Glick et al., 1998). Production of auxin (IAA) by rhizobacteria can also enhance the uptake of heavy metals by plant (Lopez et al., 2005; Zaidi et al., 2006). AM fungi can also be used for bioaugmentation by affecting the uptake of heavy metals by the host plant. Different researchers have indicated that AM fungi increased the rate of heavy metal uptake by the host plant in alfalfa (El-Kherbawy et al., 1989), soybean (Heggo et al., 1990), bean and maize (Guo et al., 1996), and clover (Joner and Leyval, 1997). Experiments with G. intraradices have shown that depending on plant species the effects of mycorrhization on Pb uptake differs as it was reduced in root and leaf of corn (Zea mays, L.) and was increased in root of Agrostis capillaries (Malcova et al., 2003). Lower metal concentration in plant may indicate its bioabsorption by soil microbes. For example Ni was shown to be absorbed by B. subtilis by 244 mg/g cell dry weight (Zaidi et al., 2006). AM fungi may also absorb heavy metals in their tissues, for example in their vacuoles or immobilize them in the mycorhizosphere and hence alleviate their toxic effects on plant growth (Chen et al., 2003; Peter et al., 2004). Bi et al. (2003) indicated that absorption of Zn from soil solution by AM fungi can affect Zn mobility by increasing soil pH and hence decreasing Zn uptake by plant root or shoot. Use of different chemicals such as fungicides can adversely affect AM functioning. Different AM species differed in their resistance to the tested fungicides. The fungicides also affected AM species differently. Accordingly, the right combination of AM species and fungicides may result in the highest efficiency of mycorrhizal plants (Samarbakhsh et al., 2009). Use of a fungicide resulted in the enhanced uptake of Pb by mycorrhizal corn (Burke et al., 2000). In soils with low or medium level of fertility, AM fungi can enhance plant nutrient uptake including micronutrients such as Fe, Zn, Mn, and Cu. However, with increasing the concentration of such micronutrients in a polluted soil, mycorrhizal plants are able to reduce the concentration of these heavy metals in their shoots. This indicates that in combination with plant roots AM fungi are able to use some strategies, which can control the uptake of heavy metals by plant under such conditions. One of these strategies is the increased growth of mycorrhizal plant, although other mechanisms may also be responsible. In addition, AM fungi are able to reduce the concentration of heavy metals in the leaf of non-hyperaccumulators (Joner and Leyval, 2001). It is by stimulating plant roots to produce higher levels of compounds such as cysteine and gluthatione, which are able to chelate heavy metals, and hence reduce their toxicity to the host plant (Galli et al., 1995). However, such ability differs in different AM species and hence

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variable rates of heavy metals are absorbed by AM hyphae and plant tissues (Toler et al., 2005). In brief the following may explain the different results observed for the bioaugmentation of heavy metals by soil microbes in association with plants: 1) the species and concentrations of metals, 2) presence of more than one metal and hence their related competition, 3) soil properties, 4) kind of association between plant and soil microbes, 5) the conditions for plant growth, and 6) root volume and density (Baum et al., 2006; Bi et al., 2003; Chen et al., 2003; Joner and Leyval, 2001; Leyval et al., 1997). Additionally according to Lebeau et al. (2008), the following may also indicate the differences between different experiments related to the bioaugmentation of heavy metals: 1) metal properties, 2) experimental type (laboratory, greenhouse or field), 3) method of soil preparation and contamination, 4) properties of microbes and their inoculums, and 5) plant species. They have also mentioned that the effectiveness of bioaugmentation process is influenced by the following parameters: 1) plant root and shoot growth affecting the rate of phytoextraction as well as the properties of soil microbes, and 2) soil properties influencing heavy metal bioavailability and hence their translocation to the plant. The important point about the experimental soil is that in most experiments it is sterilized affecting the behavior of soil microbes. In other words under sterilized conditions the inoculums may behave differently compared with unsterilized conditions, which is the real conditions in the field. Under, unsterilized conditions the inoculums must be able to compete with the native soil microbes for resources, influencing their performance (Miransari et al., 2007, 2008, 2009a,b). Therefore, the results related to the experiments of bioaugmentation must be interpreted with respect to the experimental conditions. In addition the mobilization of metal can also be affected by soil sterilization (Egli et al., 2006) as there are always interactions between plant and soil microbes in the rhizosphere influencing plant behavior and hence the production of root exudates. AM fungi are able to phytostabilize heavy metals in the rhizosphere by production of different compounds resulting in their precipitation in the soil, and they may also absorb them in their cell walls or chelate them in their cellular structures (Gaur and Adholeya, 2004; Gohre and Paszkowski, 2006). The production of glomalin, the insoluble glycoprotein, by fungal hyphae can also affect the process of phytostabilization by binding heavy metals (Gonzalez-Chavez et al., 2004). By the phytoxtraction process mycorrhizal plants are able to accumulate heavy metals in plant shoots or enhance their absorption by increasing the uptake of heavy metals. 7. How to select the right combination of plant and AM species for bioremediation Although soil microbes usually can enhance plant potential to grow in a polluted soil and in case of hyperaccumulators may improve their heavy metal uptake, the selection of appropriate microbes for the right plant is very important. This would result in a more efficient bioaugmentation strategy, which would bioremediate the polluted soil more efficiently. As previously mentioned, selection of AM species from contaminated areas can be more beneficial, because such species are adapted to high concentrations of heavy metals (Gaur and Adholeya, 2004; Khan, 2005). If the selection of AM species is for symbiosis with hyperaccumulators, the followings are of significant importance: 1) most hyperaccumulators belonging to the Brassicaceae family such as T. caerulescens and B. juncea are not able to develop symbiotic association with AM fungi, although there are some exceptions (Kumar et al., 1995), and 2) AM fungi may not perform efficiently in highly contaminated soils (Audet and Charest, 2007b). Therefore, it is important to evaluate the situation precisely and hence determine the right strategy for bioaugmentation.

Different combinations of AM fungi and the host plant under different concentrations of heavy metals may be tested and the most efficient association may be selected. In other words, it must be recognized how AM fungi may alter plant physiology to deal with the stress of heavy metals. Usually under stress AM fungi are able to alter plant physiology in a way so that the plant can handle the stress (Miransari et al., 2008). Determination of how the host plants respond to the presence of AM species in a soil contaminated with heavy metals can be very useful for selecting the right combination of AM-host plant. In addition to inoculating plants with microbes, the other methods of increasing plant biomass for higher rate of phytoextraction under heavy metals pollution must also be tested. For example, if use of chemical fertilization can also enhance the rate of heavy metal bioremediation. The co-inoculation of soil microbes (Miransari, 2010a,b,c, 2011a,b) including AM species may also be appropriate providing that the right combination of soil microbes is selected being active under the stress. Khan (2005) also suggested the following strategy to enhance the ability of AM fungi for bioremediation; use of inoculums for seed inoculation, and co- or inter-cropping and use of mycorrhizal hosts in the rotation. The most appropriate strategy must be: 1) environmentally and economically sustainable, 2) applicable to a large scale, 3) be useable for a combination of heavy metals, and 4) repeatable (Lebeau et al., 2008). However, it must be noted that the use of different practices in the field including the following can alter soil properties and hence the solubility and bioavailability of heavy metals. Therefore, to enhance the efficiency of bioremediation, appropriate practices must be selected and applied. 1) Fertilization can affect soil pH, 2) irrigation influences soil Eh potential, 3) organic fertilization can affect different soil properties including the activities of soil microbes, 4) soil inoculation with microbes, can increase the population and activities of soil microbes and 5) use of different chemicals can adversely affect soil microbes (Davies et al., 2001). 8. The role of plant-microbe interactions in phytoremediation of heavy metals The other important point regarding the phytoremediation of heavy metals is related to the role of plant-microbe interactions. In other words, how the interactions between soil microbes and plant can affect the process of heavy metal bioremediation (Ma et al., 2011). Soil microbes can affect such a process by affecting plant growth in a symbiotic or non-symbiotic association. The presence of soil microbes in the plant rhizosphere can intensify the process of bioremediation by increasing phytostimulation or rhizodegradation (Nwoko et al., 2007; Nwoko, 2010). The stages of bioremediation include plant–microbe interactions and the related rhizosphere processes, uptake and translocation (including the chelating products) of heavy metals and plant tolerance mechanisms of compartmenting and degrading the pollutants. Soil microbes can affect the process of phytoremediation by promoting plant growth and health in the exchange for the C products by plant roots. The related soil microbial activities include the enhanced growth of plant root through increasing the production of plant growth regulators, and water and nutrient uptake (Glick, 2003; Nwoko, 2010). The role of endophyte bacteria interacting with their host plant is also of significance in the process of phytoremediation. Under the stress of heavy metals, the endophytes with the ability of stress tolerance can alleviate the stress and allocate the metals to the plant shoot (Weyens et al., 2009; Ma et al., 2011). The adverse effects of heavy metals on plant growth can limit the process of phytoextraction. However, soil microbes, which are genetically modified for their tolerance to heavy metals can enhance their host plant ability under heavy metal stress. Such microbes owe some mechanisms such as the

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production of products (citric and acetic acid), which increase the availability of heavy metals and hence their uptake and translocation by plant, as well as the high ability for the absorption of heavy metals (Valls and de Lorenzo, 2002; Hooda, 2007; Weyens et al., 2009). The bacteria, which can enhance the process of phytoremediation by their interactions with the host plant are able to degrade the pollutants, promote plant growth (PGPR) or influence the process of phytoremediation by other methods. It is also very important to make such methods of phytoremidation more applicable under field conditions (Glick, 2010). Belimov et al. (2005) isolated 11 Cd-resistant of bacterial strains from the rhizosphere of Indian mustard, with the ability to resist versus other heavy metals too. The isolated bacteria indicated the ability to produce auxin, siderophores and ACCdeaminase, positively affecting plant growth under the stress of heavy metal. Such kind of interactions between the bacteria and the host plant can be used for the treatment of heavy metals. 9. Conclusion Heavy metal stress can adversely affect plant growth and the environment. Hence, appropriate methods must be used to alleviate the stress. Biological methods including the use of plants and soil microbes are among the most suitable methods, environmentally and economically. In this review the most important physiological properties of plants as well as soil microbes were evaluated to indicate how such potentials can be used singly or in combination to enhance the efficiency of soil bioremediation. Different parameters affecting the efficiency of bioremediation were discussed. Among the most efficient biological methods are hyperaccumulator plants and AM fungi. Their properties were reviewed and some suggestions were made to enhance their performance under polluted conditions when applied singly or in combination. It is important to select the appropriate combination of plants and soil microbes to effectively control the stress of heavy metals on plant growth and the environment. Evaluation of the rate symbiotic association between the hyperaccumulators and AM fungi and the factors, which may affect such association is also of significance. The interactions between soil microbes and plant can also be important for the bioremediation of heavy metal stress. References Adriano DC. Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. New York, Berlin, Heidelberg: Springer-Verlag; 2001. Assuncao AGL, Martins P, Folter S, Vooijs R, Schat H, Aarts G. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 2001;24:217–26. Assunção AGL, Schat H, Aarts MG. Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 2003;159:351–60. Audet P, Charest C. Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 2007a;147:231–7. Audet P, Charest C. Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ Pollut 2007b;147:609–14. Audet P, Charest C. Allocation plasticity and plantemetal partitioning: Meta-analytical perspectives in phytoremediation. Environ Pollut 2008;156:290–6. BBSRC. A Joint Research Council Review of Bioremediation Research in the United Kingdom. Swindon: BBRRC, EPSRC and NERC; 1999. Baum C, Hrynkiewicz K, Leinweber P, Meissner R. Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix _ dasyclados). J Plant Nutr Soil Sci 2006;169:516–22. Belimov, A., Hontzeas, N., Safronova, N., Demchinskaya, S.V., Piluzza, G., Bullitta, S., Glick, B.R. Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.) Soil Biol Biochem 2005;37:241–250. Bi YL, Li XL, Christie P. Influence of early stages of arbuscular mycorrhiza on uptake of zinc and phosphorus by red clover from a low phosphorus soil amended with zinc and phosphorus. Chemosphere 2003;50:831–7. Braud A, Jezequel K, Vieille E, Tritter A, Lebeau T. Changes in extractability of Cr and Pb in a polycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut Focus 2006;6: 261–79. Burke SJ, Angle JS, Chaney RL, Cunningham SD. Arbuscular mycorrhizae effects on heavy metal uptake by corn. Int J Phytorem 2000;2:23–9.

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