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Pichardo, J Bioremed Biodeg 2012, 3:10
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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 Su1 and Fengxiang X. Han1,2*
1
2
Insititute for Clean Energy Technology, Mississippi State University, Oktibbeha County, Mississippi, USA
Department of Chemistry and Biochemistry, Jackson State University, Jackson, Mississippi, USA
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
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
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
*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.
Volume 3 • Issue 10 • 1000e124
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
Page 2 of 4
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
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
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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Volume 3 • Issue 10 • 1000e124
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
Page 3 of 4
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Contaminated Soils. J Bioremed Biodeg 3:e124. doi:10.4172/2155-6199.1000e124
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Volume 3 • Issue 10 • 1000e124