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The Potential Effects of Arbuscular Mycorrhizae (AM) on the Uptake of Heavy Metals by Plants from Contaminated Soils | OMICS International
ISSN: 2155-6199
Journal of Bioremediation & Biodegradation

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The Potential Effects of Arbuscular Mycorrhizae (AM) on the Uptake of Heavy Metals by Plants from Contaminated Soils

Sergio T. Pichardo1, Yi Su1and Fengxiang X. Han1,2*
1Insititute for Clean Energy Technology, Mississippi State University, Oktibbeha County, Mississippi, USA
2Department of Chemistry and Biochemistry, Jackson State University, Jackson, Mississippi, USA
Corresponding Author : Fengxiang X. Han
Department of Chemistry and Biochemistry
Jackson State University, 1400 John R Lynch Street Jackson
MS 39217, USA
E-mail: [email protected]
Received: August 26, 2012; Accepted: August 28, 2012; Published: August 31, 2012
Citation: Pichardo ST, Su Y, Han FX (2012) The Potential Effects of Arbuscular Mycorrhizae (AM) on the Uptake of Heavy Metals by Plants from Contaminated Soils. J Bioremed Biodeg 3:e124. doi:10.4172/2155-6199.1000e124
Copyright: © 2012 Pichardo ST. This is an open-a ccess article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Arbuscular mycorrhizal (AM) symbioses have been an integral part of terrestrial ecosystems, since the invasion of land by plants. Description, phylogenetic relationships, and worldwide distribution date back to the late 1800s is documented [1]. AM are the most widespread mutualistic symbiosis between the roots of the vast majority of land plants and fungi belonging to the phylum Glomeromycota, characterized by an extensive intraradical and extraradical hyphal network [2]. Mycorrhizal associations between a fungus and a plant root are ubiquitous in the natural environment [3]. Fungi play a central role in many microbiological and ecological processes, influencing soil fertility, decomposition, cycling of minerals and organic matter, as well as plant health and nutrition. Fungi are heterotrophs, requiring external sources of carbon for energy and cellular synthesis and they have adopted three different trophic strategies to obtain this carbon, occurring as saprotrophs, necrotrophs, and biotrophs [4]. Mycorrhizae are symbiotic non pathogenic associations between plant roots and one or more fungi connecting the soil and the roots [5-7]. Arbuscular mycorrhizal (AM) fungi establish a mutualistic symbiosis with the roots of most plant species. Seven different categories of mycorrhizal symbiosis have been distinguished on the basis of their morphological characteristics and the fungal and plant species involved, but the Arbuscular mycorrhizal is the most ancient and wide spread form [8]. Paleobotanical and molecular sequence data suggest that the first land plant formed associations with Glomalean fungi from the Glomeromycota class since about 460 million years ago [9].
The AM type of mycorrhiza has undergone several name changes from endomycorrhizal to Vesicular – Arbuscular Mycorrhiza (VAM) to Arbuscular mycorrhiza (AM). The shift to VAM from endomycorrhizal followed the recognition that evolutionary and functionally VAM did not resemble other types of endomycorrhizas that penetrated the root cells. The fungi forming VAM were all Zygomycetes in the order Glomales [1]. More recently, the V in VAM was dropped because members of the mycorrhizal fungi included in the family Gigasporaceae do not form vesicles [10]. AM are the dominant form of mycorrhizae for symbiosis with plants. They colonize the roots of most terrestrial plants, including Chinese break fern (Pteris vittata L). The AM are included in the group of endomycorrhizae [11]. The symbiosis is characterized by highly branched fungal structures, arbuscules, which grow intracellularly without penetrating the host plasmalemma [8]. It is documented that over 82% of higher plants are capable of forming symbiosis with AM fungi which have no, or at least very low specificity, improving the growth and nutrient uptake of plants [2,12]. The AM fungi have gained a reputation as broad generalists, but are clear that AM fungal communities are also influenced by the structure of their associated plant communities [4]. Mycorrhizal diversity decrease, and changes in species composition may be induced by anthropogenic activities such as forest harvest, tillage and wildfire [13,14].
Mycorrhizal fungi efficiently contributed to the amelioration of various stresses experienced by hosting plants, including metal toxicity, oxidative stress, water stress, and effects of soil acidification [8]. They provide a greater absorptive surface than root hairs and thus help in the adsorption of the relatively immobile ions in soil such as phosphate, copper and zinc. In addition, mycorrhizal plants have greater tolerance to toxic metals, to root pathogens, to drought, to high soil temperature, to adverse pH and to transplant shock [15]. The endomycorrhizal fungus penetrates the cortical cells of the roots of a vascular plant. The fungus and the plant establish a highly evolved mutualistic relationship found between fungi and plants, which constitute the most prevalent plant symbiosis known [16]. The beneficial effect of mycorrhizae on plant growth has mostly been attributed to an increase in the uptake of nutrients, especially phosphorus [17]. While receiving photosynthates, mycorrhizal fungi improve the mineral nutrition of the plant and can also increase its tolerance towards some pollutants, such as heavy metals. The fungus assist the host plant in the uptake of nutrients (especially relatively immobile nutrients such as P) in exchange for carbon substrates from host plant photosynthesis. The AM fungi can also increase plant resistance to diverse adverse abiotic factors including drought and saline conditions or biotic stresses such as attack by pathogens or insect pests [18]. The chief role of the mycorrhizal fungi appears to be conversion of minerals of the soil and of the decaying organic material into forms accessible to the host. Up to 20% of the host plant’s photosynthate carbon may be transferred to the AM fungi [19]. The host is presumably secreting sugars, amino acids, and other organic materials, making them available to the fungus. An increase in the carbon supplied by the plant to the AM fungi increases the uptake of phosphorus (main benefit) and the transfer of phosphorus from the fungi to plant [20,21]. Phosphorus is an essential mineral element in all living organism because of the role it plays in the structure of nucleic acid and phospholipids, carbon metabolism and enzymes activation/deactivation. This mineral element is quantitatively rated as second most important inorganic mineral element for plant growth after nitrogen [22]. Mycorrhizae can be much more efficient than plant roots at taking up phosphorus. The rate of inflow of phosphorus into mycorrhizae can be up to six times that of the root hairs [17]. In addition, to increasing the absorptive surface area of their host plant roots systems, the hyphae of symbiotic fungi provide an increased surface area for interactions with other microorganisms, and provide an important pathway for the translocation of energyrich plant assimilates (products of photosynthesis) to the soil [17,8]. The increase in plant growth by mycorrhizal association is largely due to increased absorption of nutrients from soil solution [17]. The inoculation of a mixture of AM fungi growing as a community had better effect on plants growth than an individual fungus. Different AM fungi affect their host plant and host soil differently, and further that a community of fungi acting in concert is likely to provide greater benefit to the plant-soil system than a single species [8,23]. AM fungi inoculation can influence soil properties and soil microbial community [2,24]. All of these are speculated to change the speciation, mobility, and bioavailability of mercury in soil, therefore influencing its behavior in soil-plant system [25].
While plants provide important compounds for AMF survival, these fungi expand the contact surface between plants and soil, contributing to an enhanced plant uptake of macronutrients [26]. Heavy metals are one of the main sources of environmental pollution which are not biologically degraded in soil [27]. In general, it is accepted that high concentrations of heavy metals in soil have an adverse effect on micro-organisms and microbial processes [20]. It was determined that the presence of both Glomus claroideum and Glomus intraradices enhanced the uptake and accumulation of zinc (Zn) by Solanum nigrum (up to 83 and 49% higher Zn accumulation, respectively). The main deposits for the metal were found in the intercellular spaces and in the cell walls of the root tissues [28]. AM fungi affect metal uptake by plants from soil and translocation from roots to shoots, however, mycorrhizal effects may depend on elements, plant and fungal species/ ecotypes [29]. AM fungi may enhance the uptake of heavy metals into the plant, or reduce uptake. In the latter case, AM fungi have generally such a strong influence on plant biomass that the mycorrhizal effect on phyto-extraction remains positive [30,31]. The enhancement of phytoaccumulation of heavy metals including Zn, cadmium (Cd), arsenic (As), and selenium (Se) – in plants has been shown by inoculation of roots using AM fungi [32,33]. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus) [27]. The effectiveness of mycorrhizal colonization varied between the fungal isolates introduced [34]. There are contradictory reports on the effectiveness of mycorrhizal fungi on heavy metals uptake by plants. Some reports show that AM increase heavy metal concentration in their host plants, meanwhile, other authors report that Arbuscular mycorrhizal fungi have no or may have a negative effect, but at high metal concentration and low pH they are disadvantageous for the plant, whose growth is depressed [35-39]. Acidification may increase the bioavailability and toxicity of heavy metals in the pedosphere [40], and it is demonstrated that mycorrhizal fungi are able to acidify the rhizosphere by releasing organic acids like citric and oxalic acids [41]. The effect of AM fungi on plant uptake of metals is not clear. Extraradical mycelium of mycorrhizal fungi is of paramount importance not only for metabolism-independent binding of heavy metals to cell walls, but also, and probably more so, for metabolism-dependent intracellular uptake of heavy metals and transport to the associated host plant [20].
High concentrations of heavy metals in soil have an adverse effect on micro-organisms and microbial processes due to their toxicity for living organisms. Among soil microorganisms, mycorrhizal fungi are the only ones providing a direct link between soil and roots, and can therefore be of great importance in heavy metal availability and toxicity to plants [20]. There is evidence that heavy metals affect mycorrhizae [42]. Mycorrhizal infection rate of maize (Zea mays L) was reduced by the addition of heavy metals including Zn, Cu, Ni, Cr, Pb, and Cd [43]. Likewise, high levels of Cu negatively affect AM root colonization rates [30,44], and lead reduced AM colonization of plants in sand culture experiments [42]. It was reported that the development of AM fungi was negatively influenced by the higher Mn concentrations, with significant differences between isolates and cultivation lineages. The lineage of Glomus sp. cultured in inert metal-free substrate tolerated excessive Mn levels to a lesser extent than the lineage kept longterm in the original contaminated soil, but withstood Mn at higher concentrations than the G. intraradices from uncontaminated soil [44]. On the other hand, mycorrhizal colonization and growth of external hyphae were inhibited by sewage sludge-contaminated soil containing Zn, Cd, and Pb [45].
A potential advantage of using mycorrhizal fungi in bioremediation and phytoremediaiton is that they receive a direct supply of carbon from their host to support growth into contaminated substrates [8]. Phytoremediation is the cost-effective remediation technology which is potentially employable for a large area of heavy metal contaminated soils [46-53]. Some of this carbon may subsequently be available to bacteria associated with the mycorrhizal mycelium [54], and this may have consequences for bioremediation in the mycorrhizosphere [8]. Tolerant mycorrhizal fungi may grow and solubilized toxic metal mineral better than non-tolerant strains. Metal dissolution by fungi may take place through proton-promoted or ligand-promoted mechanisms and organic acids provide both a source of protons for solubilization and metal-chelating anions to complex the metal cations [8]. The effect of mycorrhizal fungi on plant responses to drought stress is difficult to separate from nutritional effects since the hyphal contribution to nutrient uptake becomes more important as soil dries. The supply of poorly diffusible nutrients such as P in dry soil will become limited by the increasing tortuosity of the diffusion path and mycorrhizal hyphae will make an increasingly important contribution to P uptake as the soil dries, confounding the effect of water and nutrients [8]. The mycorrhizal fungi increase the surface area of roots and thus help in absorbing some diffusion-limited nutrients (P, Zn, Cu etc.). They also help in water uptake, thereby protecting the plants under mild drought stress and also help to deter the activity of root pathogens. They produce growth-promoting substances such as indole acetic acid (IAA), cytokinins and gibberellin like substances. Arbuscular mycorrhizal fungi enhance the plant growth as a result of the improved phosphate nutrition and water supply of the host plant, likewise the fungus receives fixed carbon [55,56,19]. Plants can be inoculated with commercial inoculum. It is documented that Arbuscular mycorrhizal inoculation enhanced host plants tolerance to metal lead, and also enhanced shoot biomass and shoot P concentration [42]. However, the mechanisms on the interaction between heavy metals and Arbuscular mycorrhizal and the uptake of heavy metals by VM require further study in order to apply AM in bioremediation of contaminated soils.


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