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Vol. 19 No. 1 - January 2013

Role of Arbuscular Mycorrhizal Fungi In Phytoremediation

By: Neelima Ratti* and Avinash Upadhyay


Excessive heavy metals contamination in soil have detrimental effect on ecosystems and pose risks to human health (HM) they enter the food chain via agricultural products (Liang et al., 2009). The main source of heavy metal contamination include mining and smelting of metalliferous ores, industrial waste, mineral fertilizers, pesticides, vehicle exhausts and municipal sewage sludge (Qian et al., 2005). When heavy metals particularly copper, zinc, chromium, lead, cadmium are taken up by plants in higher concentrations, they not only inhibit metabolic process but also reduce crop yield in plants. Further, through the incorporation into the food chain they can potentially cause human liver and brain disorders (Bibi et al., 2006). Technologies presently available for the remediation of metal contaminated soils are expensive, time consuming and may produce secondary waste (Fitz and Wenzel, 2002). There is still need of an effective and affordable solution. In addition to sites contaminated by human activity, natural mineral deposits containing particularly large quantities of heavy metals are present in many regions of the globe. These areas often support characteristic plant species that thrive well in these metal enriched environments. Some of these species can accumulate very high concentrations of toxic metals to levels which far exceed the soil levels (Baker and Brooks, 1989). In many ways, living plants can be compared to solar driven pumps which can extract and concentrate several elements from their environment. All plants have the ability to accumulate elements like Mg, Fe, Mn, Zn, Cu, Mo, and Ni (Langille and MacLean, 1976) which are essential for their growth and development, whereas certain plants have the ability to accumulate heavy metals which have no known biological function e.g. Cd, Cr, Pb, Co, Ag, Se, and Hg (Baker and Brooks, 1989). However, excessive accumulation of these heavy metals can be toxic to most plants. The ability to both tolerate elevated levels of heavy metals and accumulate them in very high concentrations has evolved both independently and together in a number of different plant species (Ernst et al., 1992). Several higher plants developed strategies for heavy metal resistance enabling plants to survive in highly metal contaminated sites (Pilon-Smits, 2005). Zn at low concentration is important as micronutrient but in high concentrations this metal becomes toxic to plants. Plants readily accumulate Zn and excess Zn within tissues, inhibiting plant growth and rendering the crop unfit for human and animal consumption (Jeliazkova and Craker, 2003). Heavy metals are toxic at slightly higher levels than those at which they are required. High concentration of heavy metals in the soil has detrimental effects on ecosystems and is a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water.

Role of AM fungi in phytoremediation

Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants including HM from the environment by plants, is burning issue in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Various technologies exist that enable the detoxification/deactivation and removal of toxic compounds from the soil, mostly based on physicochemical extraction method. They are costly and completely destroy soil microorganisms. Bioremediation is the use of organisms for the treatment of soil pollution. Root colonizing symbiotic micro-organisms such as arbuscular mycorrhizal fungi (AMF) are mainly involved in phytoremediation, that uses plants for soil remediation. Phytoremediation refers to the use of green plants and their associated microbiota, soil amendments, and agronomic techniques to extract, sequest and/or detoxify various kinds of environmental pollutants (Salt et et.al 1998). These techniques have received considerable interest in recent years because of potential cost savings compared to conventional non-biological techniques.

An insight into heavy metal detoxification in plant: Role of AM fungi

Mycorrhiza is the mutualistic symbiotic association (non-pathogenic) of a specific group of soil-borne fungi (obligate) with the roots of higher plants (Sieverding, 1991). Plant receives support from AM fungi, with the help of its symbiotic association, in the aspect of uptake of phosphorus and other nutrients, enhancement of growth hormones, increase of protein content, increase of lipid, sugars, amino acid levels, increase of tolerance to heavy metals, increase of salinity tolerance, and resistance to root-borne pathogens. Studies have reported mycorrhizae in plants growing on heavy metal contaminated sites (Shetty et al., 1995) indicating that these fungi have evolved a heavy metal tolerance. AM fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up heavy metal (HM) from an enlarged soil volume.

Plants need appropriate below-ground ecosystems, especially at difficult sites. Mycorrhizal fungi enhance root absorption area up to 47-fold (Smith and Read, 1997). The fungi provide nutrients and water otherwise not accessible for plants (Nadian et al., 1997) and facilitate the establishment and survival of vegetation under stress conditions (Jasper et al., 1989). The fungi also stabilize the tailing material with the net of hyphae and improve its structure, as they produce substances that bind soil particles, leading to the formation of soil aggregates (Jastrow et al., 1998). The compounds produced by the extraradical mycelium can also take part in heavy metal chelation. Fungi are known to be able to accumulate significant amounts of heavy metals (Gadd, 1993) varying from a few percent to 20% of dry mass (Tobin et al., 1984), suggesting that microbial biomass may affect the mobility of metals in the soil system. According to the calculations by Söderström (1979), the surface of interaction between fungi and soil is up to 0.14 m2 in 1 g of soil. They can remove metals from the wastes both by metabolism dependent (bioaccumulation) or independent (biosorption) processes (Gadd, 1993). In the second case, both live and dead biomass can be involved (Volesky and Holan, 1995). The components of the fungal cell wall can be very efficient in binding heavy metals due to the presence of free amino, hydroxyl, carboxyl and other groups (Gadd, 1993). Therefore, saprobic fungi can be commercially grown in bulk culture and their either live or dead biomass used as biosorbents for heavy metals (Fomina et al., 2005). Similar phenomena occur in ectomycorrhizal (Turnau and Dexheimer, 1995), ericoid (Bradley et al., 1982) and arbuscular mycorrhizal fungi (Gonzales-Chavez et al., 2004). Some of these microorganisms can also precipitate heavy metals outside the mycelium e.g. by producing various organic acids or enzymes such as the acid phosphates (Turnau and Dexheimer, 1995) or pigments, which additionally prevents the migration of metals. Arbuscular mycorrhiza (AM), occurring in 80% of plant species and formed by about 120 species of fungi belonging to the Glomeromycota (Schüßler et al., 2001), is the most widespread type of symbiosis between fungi and plants. Besides the formation of the extraradical myceliar net that intensively penetrates the substratum (feature common to all types of mycorrhizas), it forms intraradical hyphae that penetrate intercellular spaces and enter cortical root cells. The formation of comparatively short-lived structures called arbuscules is crucial for the functioning of the whole symbiosis (Smith and Read, 1997). This is the place where the arbuscular cell wall is lined by plant plasmalemma, and the exchange of substances takes place. AMF have not been shown to produce organic acids such as oxalic acid, however, glomalin, a protein produced by these fungi, seems to be efficient in sequestering Cu, Cd, Pb and Mn (Gonzales-Chavez et al., 2004). According to Joner and Leyval (1997), the efficiency of protection depends on the AMF isolate. These authors have also shown that no inhibition of mycelium growth was observed even at 20 mg of NH4NO3 -extractable Cd/kg of substratum. Retention of heavy metals in extraradical mycelium of ectomycorrhizas was first proposed as a tolerance mechanism by Denny and Wilkins (1987). The fungi can detoxify metals by intracellular processes (Blaudez et al., 2000). A variety of membrane transporters controlling the trafficking of metal ions have been identified recently in plants and microorganisms (Clemens, 2001). Intracellular detoxification in fungi and plants is attributed to metal chelation by cysteine-rich peptides such as reduced glutathione, phytochelatins and metallothioneins (MeT) (Cobbett and Goldsbrough, 2002). Cd-MeT was shown to take part in detoxification of heavy metals in the ectomycorrhizal fungus, Paxillus involutus (Courbot et al., 2004), while Cu2+-MeT was extracted from Laccaria laccata and P. involutus and their production was correlated with the tolerance to copper (Howe et al., 1997). Despite the increase of glutathione production, the content of phytochelatin was not increased, suggesting that at least in this fungus the cadmium detoxification mechanism is different from the mechanisms observed in the host plant. MeT-like sequences were identified in the ectomycorrhizal fungus Pisolithus tinctorius (Voiblet et al., 2001) and in the arbuscular fungus Gigaspora rosea (Stommel et al ., 2001), although the metal sequestration capacity and actual MeT-like nature was not determined until recently. The identification and functional characterization of an MeT-encoding gene from Gigaspora margarita was demonstrated by Lanfranco et al. (2002), and in addition the differences in gene expression in symbiotic and pre-symbiotic stages were shown. Mycorrhizal fungi qualitatively and quantitatively influence the microbial population of the mycorrhizosphere. They are usually accompanied by bacteria such as legume symbiotic nodular bacteria, plant growth promoting rhizobacteria (PGPR), mycorrhiza helper bacteria (MHB) and saprobic fungi. As these organisms influence plants either by interactions with abiotic (Turnau and Kottke, 2005) and biotic components of the soil (Azcón-Aguilar and Barea, 1996), or by stimulating plant growth through the production of vitamins and hormones (Barea, 2000), they should be included in the optimization of the restoration processes as well as mycorrhizal fungi.

Conclusion and future prospects:

Phytoremediation is an emerging biobased alternative technology in the clean up of metal contaminated soil. The prospect of symbiont existing in heavy metal contaminated soil has important implication for phytoremediation. Mycorrhizal associations increased the absorptive surface area of the plant due to extra-matrical fungal hyphae exploring rhizosphere beyond the root hair zone, which in turn enhanced water and mineral uptake. The protection and increased mineral uptake results in greater biomass production which is important for successful remediation. The potentials of phytoremediation of metal polluted soil can be enhanced by inoculating hyper accumulator plants with mycorrhizal fungi most appropriate for polluted sites. The studies related to the dynamics of AM symbiosis in heavy metal phytoremediation have showed the existence of compromise between plant growth and heavy metal tolerance indicating the importance of metal binding process in buffering the soil environment. It is hence important to understand the contribution of AM symbionts to soil productivity and enhanced metal uptake at molecular level. Hence a comprehensive molecular and physiological understanding of mycorrhizospere dissecting the role of plant and mycorrhizal gene interaction in the process would be valuable to decipher plant tolerance mechanism under heavy metal stress specially with respect to phytoremediation.

*Hislop School of Biotechnology, Hislop College, Nagpur-440001 (MH), [email protected]

This article has been reproduced from the archives of EnviroNews - Newsletter of ISEB India.

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