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Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic

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DOI: 10.1016/j.chemosphere.2014.01.030 · Source: PubMed

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 Chemosphere 108 (2014) 134–144

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Review

Role of phosphate fertilizers in heavy metal uptake and detoxification

of toxic metals
D.K. Gupta a,⇑, S. Chatterjee b, S. Datta b, V. Veer b, C. Walther a
a
Gottfried Wilhelm Leibniz Universität Hannover, Institut für Radioökologie und Strahlenschutz (IRS), Herrenhäuser Str. 2, Gebäude 4113, D-30419 Hannover, Germany
b
Defence Research Laboratory, DRDO, Post Bag 2, Tezpur 784001, Assam, India

h i g h l i g h t s

 Phosphorus fertilizers in soil.

 Phosphate rock as a major source for phosphate fertilizer.
 Uptake of phosphate and heavy metals.
 Rhizosphere, root exudates and elemental uptake.
 Phosphate starvation and signaling in plants.

a r t i c l e i n f o a b s t r a c t

Article history: As a nonrenewable resource, phosphorus (P) is the second most important macronutrient for plant
Received 19 September 2013 growth and nutrition. Demand of phosphorus application in the agricultural production is increasing fast
Received in revised form 20 January 2014 throughout the globe. The bioavailability of phosphorus is distinctively low due to its slow diffusion and
Accepted 21 January 2014
high fixation in soils which make phosphorus a key limiting factor for crop production. Applications of
Available online 18 February 2014
phosphorus-based fertilizers improve the soil fertility and agriculture yield but at the same time concerns
over a number of factors that lead to environmental damage need to be addressed properly. Phosphate
Keywords:
rock mining leads to reallocation and exposure of several heavy metals and radionuclides in crop fields
Phosphate fertilizer
Heavy metal
and water bodies throughout the world. Proper management of phosphorus along with its fertilizers is
Uptake required that may help the maximum utilization by plants and minimum run-off and wastage. Phospho-
Detoxification rus solubilizing bacteria along with the root rhizosphere of plant integrated with root morphological and
Phytoremediation physiological adaptive strategies need to be explored further for utilization of this extremely valuable
nonrenewable resource judiciously. The main objective of this review is to assess the role of phosphorus
in fertilizers, their uptake along with other elements and signaling during P starvation.
Ó 2014 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
2. Phosphorus fertilizers in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
3. Phosphate rock as a major source for phosphate fertilizer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
4. Uptake of phosphate and heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
5. Mechanism of elemental uptake in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
6. Rhizosphere, root exudates and elemental uptake. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139
7. Phosphate starvation and signaling in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140
8. Transport and sequestration of metals in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140
9. Future prospects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141

⇑ Corresponding author. Tel.: +49 511 762 14324; fax: +49 511 762 17917.
E-mail address: guptadk1971@gmail.com (D.K. Gupta).

http://dx.doi.org/10.1016/j.chemosphere.2014.01.030
0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144 135

1. Introduction residues. Most of the phosphates become incorporated as organic

Phosphorus (P), a non-metallic multivalent chemical element in
group 15 of the periodic table (pnictogen), is one of the most
important macro-nutrient for living systems. It is an essential ele-
ment for plant growth and for a couple of physiological functions
that are concerned with energy transformations. Globally, the
main user of phosphorus is agriculture, accounting for about 90%
of the total world demand. Input of phosphorus is vital for food
production as all plants need an ample supply of it. Being an essen-
tial constituent of cells, P is involved in a number of cellular pro-
cesses, including photosynthesis, respiration, energy storage and
transfer, cell division, and cell enlargement. Sufficient amount of
phosphorus is required for the promotion of early root formation,
development and growth, improvement of crop quality and seed
formation. Plants used to uptake phosphate from soils, which then
enters into the food chain, and returns to soils as decayed organic
compounds by living systems and when they are released into
the environment again, become a part of soil organic matter, which
is then mineralized by soil microorganisms. P may exist in diverse
forms in soils. However, in general, three different P pools (solu-
tion, active and fixed) control the P-cycle in nature. Plants used
to take up phosphate from solution. The solution P pool is com-
prised of P in the orthophosphate form and small amounts of or-
ganic P. This pool contains a very small fraction of the total P in
soil, which needs to be replenished in due course of time as grow-
ing plants deplete the soluble source faster. However, P from the
active P pool is the main source of available P for plants, which is
released to the soil solution simply to the water adjoining soil con-
stituents. Mostly attached or adsorbed to small particles in the soil
along with elements like Ca, Al, the inorganic active P pool easily
mineralizes by the biogenic activities in soil. However, source of
the phosphate is an important issue as different heavy metals

Fig. 1. Schematic representation of the biogeochemical cycle of phosphorus through lithosphere, hydrosphere, and biosphere which is an essential component for plant
growth. Phosphate usually comes from rock phosphate deposits and minerals (apatite). Natural dissolution of phosphate rock is restricted by the rate of release and small
amount of this released phosphorus is taken by biota. To meet the demand of phosphorus, phosphate rock mining is a common practice to produce the fertilizer that enters
the crop and food chain of the ecosystems.
136 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144
may be introduced into the agricultural land along with the fertil-
izer. Again, depending on several factors, soil particles may act
either as a source or a sink of phosphate to the surrounding water.
The fixed pool of phosphate contains mostly insoluble inorganic
phosphate compounds that are resistant to mineralization by
microorganisms in the soil. Phosphate in this pool may remain in
soils for years; however, slow conversion between the fixed P pool
and the active P pool does occur (Busman et al., 2002) (Fig. 1).
There are certain constraints in phosphate bioavailability or
bio-accessibility in soils that necessitate the plants developing var-
ious mechanisms to augment the uptake of inorganic phosphates
(Eckardt, 2005). The availability of phosphorus in most of the soils
is in the range of 1 lmol L1, but in general, plants require
30 lmol L1 to reach their maximum yield. Uptake of phosphate
into plant cells occurs against a steep concentration gradient, as
the concentration within plant cells (1–10 mM) is 10,000-fold
higher than that of the natural soil solution (Rausch and Bucher,
2002). In 1669, a German alchemist Hennig Brand discovered P is
usually present in nature as oxide in minerals (inorganic P: Pi) of
phosphate rocks (white phosphorus and red phosphorus) or organ-
ic form (Po) but hardly found as a free element due to its high reac-
tivity. Present as various forms of phosphate (PO4), the quantity of
P in soils vary from 200 to 6000 lg g1 (mean: 600 lg g1)
(Lindsay et al., 1989). However, concentrations and behavior of
the two chemical forms of P (Pi and Po) differ and their fates in
the soil also vary (Hansen et al., 2004; Shen et al., 2011). Pi consti-
tutes approximately 35–70% of total P in soil with apatites, streng-
ite, and variscite being the major P minerals. However, due to their
stability, release of available P from primary minerals through
weathering is too low for plant life, especially for the development
of crop plants (Oelkers and Valsami-Jones, 2008; Sashidhar and Po-
dile, 2010). Secondary P minerals forms other chemical complexes
forming insoluble phosphate salts with elements like calcium (Ca),
iron (Fe) and aluminum (Al) present in the soil (Lindsay et al.,
1989; Shen et al., 2011). However, dissolution rates of Ca-,
Fe- and Al-salts vary on soil pH and size of minerals. Interestingly,
solubility of Fe and Al phosphates increases with rising soil pH and
decreases in case of Ca phosphate (Hinsinger, 2001; Varadarajan
et al., 2002). Again, Al/Fe oxides of phosphates of various clay par-
ticles may be released through desorption reactions. Thus, equilib-
rium of P in nature is a complex phenomenon signifying the
interrelation of different P pools of very stable to labile forms (Shen
et al., 2011). Oxides and hydroxides of Fe/Al along with the clay
minerals usually have several adsorption sites which dominantly
adsorb P in the acidic soil (Linkohr et al., 2002; Luengo et al.,
2006). However, precipitation reactions dominate P retention
(forming dicalcium phosphate, DCP, CaHPO42H2O, which is acces-
sible by plants) in neutral-to-calcareous soils, but, adsorption of P
on the clay minerals and on the surface of calcium carbonates are
also reported (Devau et al., 2010; Shen et al., 2011). Conversion of
DCP into stable octocalcium phosphate (Ca8H2(PO4)6) and more
stable hydroxyapatite (HAP, Ca10(PO4)6(OH)2) result in a reduced
amount availability of P to plants at alkaline pH (Arai and Sparks,
2007). The main objective of this review is to assess the role of
phosphorus in fertilizers, their uptake along with other elements
and signaling during P starvation.
2. Phosphorus fertilizers in soil
Fertilizers are essential for plant growth that provides nutri-
ents in varying proportions. It is estimated that 30–50% of crop
yields in different parts of the world are attributed to natural or
synthetic commercial fertilizers. Fertilizers normally consist of
six macronutrients, viz., nitrogen (N), phosphorus (P), potassium
(K), calcium (Ca), magnesium (Mg), and sulfur (S); and eight
micronutrients (boron (B), chlorine (Cl), copper (Cu), iron (Fe),
manganese (Mn), molybdenum (Mo), zinc (Zn) and nickel (Ni).
Globally, the application of fertilizers for cultivation has risen
astronomically in the last 60 years. In 2006, as stated by World
Resources Institute that, five countries of the world, viz., China,
United States, India, Brazil, and Indonesia – account for
two-thirds of all fertilizer consumption; China ranks first with a
consumption of 55925.6 thousand metric tons, or 32.9% of the
world total (http://www.rankingamerica.wordpress.com/2010/
06/20/the-u-s-ranks-2nd-in-fertilizer-consumption/ downloaded
on 29-6-2013). Country like India, fertilizer usage has increased
dramatically to 133 kg ha1 in 2011 from 1 kg ha1 in 1951–52
(The Hindu, 2011). Among different group of fertilizers, uses of
phosphate based fertilizers are most common and are a vital
factor in the sustained growth and high productivity of pastoral
farming in many countries in the world. In Asia, the average
use of phosphate fertilizer is around 34 kg ha1 (http://
www.fao.org/docrep/007/y5053e/y5053e0f.htm).
3. Phosphate rock as a major source for phosphate fertilizer
Phosphate rock (PR) is the major source for the production of
most of the world’s phosphate fertilizers. However, properties of
the PR vary widely according to their source and physico-chemical
properties. Phosphorus pentoxide (P2O5) is the commonly reported
constituent of the PR. Grade of PR containing P2O5 varies from 25%
to 37%; higher content of P2O5 is desirable for commercial produc-
tion of the phosphate rich fertilizer. International Fertilizer Devel-
opment Center (IFDC) approximately predicted that world
phosphate rock resources is 290,000 mmt with 60,000 mmt of con-
centrate (Kauwenbergh, 2010). Sedimentary marine PR deposits
are the main resources (approximately 75%) of world’s phosphate
followed by igneous and weathered deposits (15–20%) and bio-
genic resources (1–2%). Primary phosphate minerals include
Fluor-apatite [(Ca10(PO4)6F2), found in igneous and metamorphic
environments, for example, in carbonatites, and mica-pyroxenites],
hydroxy-apatite [(Ca10(PO4)6(OH)2), found in biogenic deposits,
e.g., environments, bone deposits], carbonate-hydroxy-apatites
[(Ca10(PO4, CO3)6(OH)), found in caves, as part of bird and bat
excrements, guano] Francolite [(Ca10xyNaxMgy(PO4)6z(CO3)-
zF04zF22), found mainly in marine environments]. Ores of the PR
also contain various toxic metals and radionuclides in varying con-
centrations which later are transferred to phosphate fertilizers or
tailings in production processes and ultimately to soil. Depending
on the source, harmful heavy metals like cadmium (Cd), arsenic
(As), chromium (Cr), lead (Pb), mercury (Hg), and radionuclides
like uranium (U), radium (Ra), and thorium (Th) may be introduced
into the soil along with the fertilizer, which are then absorbed by
growing crop plants causing significant health related issues
(Mortvedt and Beaton, 1995). However, concentration of such con-
taminants vary considerably especially in case of metals. Reports
suggest that application of P fertilizer at a rate of 20 kg P ha1 in
soil leads to the introduction of approximately up to 0.01 g ha1 -
y1 of Hg and 25 g ha1 y1of Cr (Kongshaug et al., 1992; Kpomble-
kou and Tabatabai, 1994). Again, contamination of Cd in the
environment through phosphate fertilizer is also a major issue in
several western countries and china. It is estimated that 54–58%
of the Cd found in the environment comes from the application
of mineral phosphate fertilizers (Tirado and Allsop, 2012). Though
more refined P fertilizers (like diammonium phosphate (DAP), tri-
ple superphosphate (TSP) are available in the market having a
higher price range.
Phosphogypsum (mostly calcium sulfate) is a by-product of
wet-acid based process during the generation of phosphoric acid
in fertilizer industry. Large quantity of deposits of phosphogypsum
 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144
is a potential source of enhanced natural radiation and heavy met-
als. It is reported that 4½ tons of the by-product phosphogypsum is
produced for the production of one ton of phosphoric acid. Approx-
imately seventy percent of calcium phosphate along with different
impurities like heavy metals and radionuclides are present in the
high grade ores of PR for the production of phosphoric acid those
ultimately end up in the phosphogypsum. USEPA (http://www.
epa.gov/radiation/neshaps/subpartr/about.html) reports suggest
the concentration of 238U (uranium) and 226Ra (radium) in phos-
phogypsum of central Florida were about 10 times the background
levels in soil for uranium and 60 times the background levels in soil
for radium-226. The concentration may vary according to the geo-
graphical area and quality of the PR ore.
PR mining do have several concerns over environmental im-
pacts like transformation of landscapes, extraction and pollution
of huge amount of water from adjoining water bodies and contam-
ination with heavy metals and radioactive materials. As a normal
constituent of earth’s crust, rock phosphate deposits usually con-
tain several million tons of uranium which leads to potential expo-
sure of the environment to radiation. It is estimated that
approximately 9–22 million tons of uranium could be recovered
from the total PR deposits which may control substantially the
price of the uranium in the market. However, conventional tech-
nology is not economical to recover uranium from the PR sources.
Normally, external dose of radiation is derived from 226Ra (radium,
a member of the 238U (uranium) decay series) and 228Ra (a member
of 232Th (thorium) decay series). The most relevant isotope of tho-
rium is 232Th (half-life 1.39  1010 years). Short life isotopes of tho-
rium (Th-227–Th-229, and Th-234) and Th 230 (half-life of
8  104 years), are part of the three natural decay chains. A radio-
nuclide particularly relevant to external and internal exposure of
man is the U-238 progeny 226Ra, (haf-life of 1602 years) (Kathren,
1998). In USA, uranium concentrations in P ores range from 20 to
300 parts per million (or 7–100 pCig1); while 226Ra varies from
5 to 33 pCig1. More than 100 different combinations of fertilizers
are available in the market with varying concentrations of nitro-
gen, phosphorus, and potassium. Interestingly, P-rock (phospho-
rite) mining is the fifth largest mining industry (38 million
metric tons in 1989) in USA with most of the phosphate production
goes into the making of fertilizers (http://www.epa.gov/radiation/
tenorm/fertilizer.html; downloaded on 11th July 2013). Thus, real-
location of naturally occurring radionuclides takes place through
the use of fertilizers at trace levels throughout the environment
and becomes a source of radioactivity, which may lead to radiolog-
ical hazards due to the exposure during resident time in the soil
and intake of foodstuff grown on such fertilizer amended soils
(Alharbi, 2013). Moreover, during handling, packing and transpor-
tation of fertilizers, an additional external exposure (mainly due to
40 K and gamma emitting progenities of 238U) is also evident by
other reports (Alharbi, 2013). Potassium is of concern rather in
K-fertilizers, However the long lived primordial radionuclide 40K
with half-life of 1.28  109 years and an isotopic abundance of
0.0118%, can contribute to the external radiation exposure of
workers (UNSCEAR1988: http://www.unscear.org/unscear/en/
publications/1988.html).
4. Uptake of phosphate and heavy metals
Several factors are responsible for the mobility of non-essential
elements in soil, which include soil composition, metal concentra-
tion and speciation, soil redox and pH conditions, precipitation and
permeability and application of phosphate fertilizers. Arsenic (As)
is likely to have low mobility in shallow soils (Weber and
Hendrickson, 2006). The retention of As (especially arsenate
(AsO43)) appears to be controlled by positive charge of the soil
137
due to the presence of Fe &/or Al oxides. Arsenic mobility may be
augment by either increasing pH or reducing the oxidation state
from arsenate to arsenite or through the application of phosphate
fertilizers (Kabata-Pendias, 2001). It is shown that addition of
phosphate fertilizer considerably increases the mobility of As
which may be due to either exchange of solution-phase orthophos-
phate for solid-phase arsenic (Tokunaga and Hakuta, 2001) or com-
petition for adsorption sites with P in soil (Campos, 2002).
Interestingly, the study by Caoa et al. (2003) on the arsenic hyper-
accumulator Chinese brake fern (Pteris vittata L.) showed that addi-
tion of phosphate in soil considerably enhanced plant As uptake by
approximately 265%. Enhanced mobility of As and subsequent in-
creased plant uptake was due to the replacement of P by As at
the soil binding sites (Caoa et al., 2003). Huang H.G. et al. (2012,
2013) reported that di-hydrogen phosphates (KH2PO4, Ca(H2PO4)2,
NaH2PO4 and NH4H2PO4) salt application at three levels (22, 88 and
352 mg P kg1 soil) on Sedum alfredii growth and metal uptake by
three consecutive harvests on aged Zn/Cd combined contaminated
paddy soil. The addition of phosphates significantly increased the
amount of Zn uptake by S. alfredii due to increased shoot Zn con-
centration and dry matter yield (DMY). The highest phytoextrac-
tion of Zn and Cd was observed in KH2PO4 and NH4H2PO4
treatment at 352 mg P kg1 soil. Phosphate fertilizers (like mono-
ammonium phosphate or monocalcium phosphate) also influence
the leaching/mobility of lead (Pb) (Davenport and Peryea, 1991).
Pb (usually occurs as stable Pb2+ cation) forms complexes with or-
ganic matters or may get precipitated as carbonates, hydroxides,
and phosphates. Pb in lead arsenate (PbHAsO4) is usually
converted into comparatively insoluble lead hydroxide and lead
phosphate minerals (Peryea and Creger, 1994). Pb has one of the
highest soil-water distribution coefficients (i.e., the lowest water
mobility) that led to the formation of stable metal-humic sub-
stances (Allison and Allison, 2005). However, Pb remediation in
Pb-contaminated soils using P fertilizer has adverse effects as it
may help to mobilize other metals like arsenic and antimony
(Sb), as chemically, Sb and As tend to behave similarly (Allison
and Allison, 2005; Gupta et al., 2013b,c).
Cadmium (Cd) is a non-essential trace element that is naturally
present in soils. However, anthropogenic activities including appli-
cation of phosphorus fertilizers play a major role for introduction of
Cd in agricultural soils. Cd contamination level in common P fertil-
izers ranges from trace to 300 ppm of dry product, which usually
gets accumulated at the soil or leached to another area (Jones and
Johnston, 1989; Sheppard et al., 2009). Agricultural crops, in turn,
accumulate Cd from soil affecting adversely to plants health, crop
quality, etc. (Grant, 2011). Several studies indicate that the amount
of Cd uptake by plants also depends upon varied factors like Cd phy-
toavailability and soil Cd concentration, crop genetics and soil char-
acteristics including rhizosphere (He and Singh, 1995; Grant, 2011;
Huang et al., 2011). It is demonstrated that due to the application of
NPK fertilizer, Cd concentrations in carrot (Daucus carota L.), lettuce
(Latuca sativa L.), oat (Avena sativa L.), ryegrass (Lolium multiflorum
L.), and durum wheat (Triticum turgidum L.) were increased, but not
by addition of low-solubility rock phosphate containing a similar
Cd concentration (He and Singh, 1995; Grant et al., 2010). Ionic
strength of the soil solution is also getting affected by the applica-
tion of P fertilizers. With growing ionic strength of soil, Cd sorption
is decreased. Further discharge of ammonium from monoammo-
nium phosphate and diammonium phosphate may dislocate Cd
from its conventional adsorption sites in the soil and hence increase
the bioavailability (Lorenz et al., 1994; Lambert et al., 2007). Again,
Zn in P fertilizers (concentrations ranging from <50 to >1500 ppm)
compete for the same binding sites in soil with Cd leading to in-
creased Cd concentrations in soil solutions (François et al., 2009).
However, as Zn also competes with Cd for uptake and translocation
138 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144
by plants, Zn contamination in P fertilizers may actually reduce Cd
accumulation in crops (Cakmak et al., 2000; Jiao et al., 2004; Huang
et al., 2008; Grant, 2011).
5. Mechanism of elemental uptake in plants
A range of elements are usually present in the soil. Plants have
the capacity to obtain necessary elements from environment as
micronutrients. There are several metals like Zn, Cu, which are
essential for plant growth and sustenance, however, elevated level
of essential or non-essential metals can lead to toxicity and inhibi-
tion of growth in most of the plants (Hall, 2002; Lasat, 2002).
Root zone (rhizosphere) of the plants along with the soil micro-
organisms play important roles in metal availability and uptake by
plants. Metals may be bound to soil particle and/or precipitated
that may make a major portion of the metal insoluble or unavail-
able to plants. Microbial community in the rhizosphere can cata-
lyze the redox reactions in soil that changes the mobility of the
metals and tendency of the plants in the uptake process (Lasat,
2002). In the metal infested soil, plants may perform either as
‘‘accumulators’’ and ‘‘excluders’’ for particular metal(s), where
the excluders restrict metal uptake into their biomass and accumu-
lators accumulate metals or contaminants into their aerial tissues
after biodegradation or biotransformation of the same (Tangahu
et al., 2011). The uptake, translocation, and storage of different
metals including toxic elements into the plant’s body are sup-
ported by several factors including soil microorganisms, plant-pro-
duced chelating agents and exudates, plant induced pH changes
and redox reactions and a group of transporters embedded in the
plant cell plasma membrane. The specialized transporter proteins
involved in metal uptake and translocation include proton pumps
(-ATPases that generate electrochemical gradients and consume
energy), co-and antitransporters proteins that use the electro-
chemical gradients generated by-ATPases, and ion channel pro-
teins that facilitate the transport of ions into the cell (Tangahu
et al., 2011). However, reports suggest that, co-transportation of
cations is a common phenomenon and toxic heavy metals which
do not have any known biological function (viz. As, Cd, Pb) are also
transported through the common transportation system (Manara,
2012).
Immobilization and/or controlled entry of metals into the plants
at the root zone may be performed by the root exudates that che-
late metals to prevent their uptake inside the cell (Ni-chelation) or
binding to the apoplast (Cu, Zn) (Salt et al., 2000; Dietz, 1996).
Thus, it is assumed that chemical properties of the rhizosphere
and the cell wall of the root modulate the plant metal uptake
and tolerance. However, transporter proteins present in the plasma
membrane in plants roots and tonoplast of cytoplasm maintain the
physiological concentrations and stress responses of heavy metals
contributing key roles in homeostasis of metals (Manara, 2012).
ZIP family of metal transporters are the major group of trans-
porters, which are present in most of the plant species and also
in bacteria, fungi and animals and are involved in the translocation
of divalent cations across membranes. These proteins mainly con-
sists of topologically comparable eight transmembrane domains
with N- and C-termini exposed to the apoplast and a histidine-rich
cytoplasmic loop flanked by transmembrane domains III and IV
mostly involved with the binding of metals (Guerinot, 2000; Nish-
ida et al., 2008; Milner et al., 2013). The ZIP transporters (like IRT1,
ZRT1 and ZRT2, etc.) are reported to facilitate transportation and
accumulation of different cations including Fe2+, Mn2+, Zn2+, Ni2+,
Cd2+ (Korshunova et al., 1999; Nishida et al., 2011). It is reported
that uptake and transportation of non-essential metal like Cd from
soil into the root cells to shoot is generally carried out by ZIP trans-
porters (Krämer et al., 2007). It is thought that ZIP transporters are
essential for hyperaccumulator species that augment the capacity
of metals accumulation in plants that correlates along with the le-
vel of ZIP expression (Krämer et al., 2007). Further, recent report
suggests that Arabidopsis ZIP1 and ZIP2 (AtZIP1 and AtZIP2) are in-
volved in translocation of Mn (and possibly Zn) from the root to the
shoot and may contribute in the process of remobilization/distri-
bution at cellular level (Milner et al., 2013).
Another family of metal transporters is NRAMP (for the Natural
Resistance-Associated Macrophage Protein) transporters, which
transport different metals (Mn2+, Zn2+, Cu2+, Fe2+, Co2+, Ni2+, and
Cd2+) across membranes. These transporters are mainly expressed
in roots and shoots and also present in diverse bacteria, fungi,
plants, and animals. NRAMP1 playing a specific role in transport,
homeostasis and resistance to toxic effects of iron. The induction
of the AtNramp1 gene (in Arabidopsis thaliana) is reported under
limiting Fe conditions (Curie et al., 2000). However, along with
Fe, Cd is also being co-transported by NRAMP1 (Thomine et al.
2000; Cailliatte et al., 2010). In in rice (Oryza sativa), the uptake
and accumulation of high concentrations of Mn and Cd is facili-
tated by NRAMP5 (Sasaki et al., 2012).
The Copper Transporters (CTR) family is a group of sequence di-
verse eukaryotic proteins that are involved with Cu uptake in the
plants. This group was first identified in yeast and mammalian sys-
tems, and subsequently in plants. CTR contains three domains:
extracellular metal-binding motif, three predicted transmembrane
domains, and within the putative second transmembrane domain a
conserved and essential MXXXM motif (Puig and Thiele, 2002;
Manara, 2012). Nonessential and toxic elements like arsenic (As)
enter into plants through phosphate transporters. Arsenite, the
predominant form of As in reducing environments is transported
by a group of the aquaporin nodulin26-like intrinsic proteins
(NIPs) (Zhao et al., 2009). Usually arsenate is reduced to arsenite
and effluxed to the external medium. However, hyperaccumula-
tion of As in the above ground tissues in some ferns (family: Pterid-
aceae) is also reported (Gumaelius et al., 2004; Sridokchan et al.,
2005). Studies have also shown that arsenite is taken up by rice
(Oryza sativa) roots through highly efficient silicon (Si) pathway
utilizing two silicon transporters, Lsi1 (the aquaporin NIP2;1)
and Lsi2 (an efflux carrier) (Li et al., 2009; Zhao et al., 2010).
Other transporters include PDR8, belongs to ABC transporter
family that helps in effluxing of Cd and Pb from plasma membrane
in the plasma membrane of A. thaliana root hairs and epidermal
cells (Kobae et al., 2006; Kim et al., 2007) and oligopeptide trans-
porters (OPTs) belong to the YSL subfamily (maize yellow stripe
1 protein (ZmYS1)) that are involved in uptake of Fe by transport-
ing Fe(III)-phytosiderophore complexes (Curie et al. 2000).
Though the soil Pi is normally found in organic forms, however,
organic P must be mineralized to inorganic Pi for the pants to take
up the material. Due to its strong reactions with different compo-
nents of soil, Pi enters to the young root tips by apoplastic diffusion
rather mass flow, where the concentrations of Pi may be 1000-fold
higher than in the external solution (Schachtman et al., 1998). Root
tips, epidermal cells of root hairs and root cortex cells (outer layer)
are mainly involved in the diffusion process. As the root tip grows
into the fresh soil, Pi is rapidly taken up by the plant creating a Pi
depletion zone of 0.2–1.0 mm surrounding the tip. In this process
of P extraction, while root hairs assist by expanding the surface
area, mycorrhizal fungi associated with root cells, transfer Pi to
the root by extending them up to several centimeters into the soil.
Structurally, the apoplast is formed in the cortical cells by the con-
tinuum of root cell walls of adjacent cells. The space consists of
interlaced fibers that form an open latticework in roots that serves
to filter the soil solution (Mikkelsen, 2013). To manage the variable
concentrations of external Pi, plants respond by dual-phasic con-
trol of the Pi uptake. The absorption isotherms follow Michaelis–
Menten kinetics by operating at low or high affinity, depending
 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144 139

on either high or low external ion concentrations, respectively
(Nandi et al., 1987; Mimura et al., 1992). A report on the estimation
of transporter’s affinity (Km) varies greatly; for high-affinity uptake
range Km from 3 to 7 mm, whereas for low-affinity transporters the
Km is 50–330 mm in different tissues and plant species (Ullrich-
Eberius et al., 1984; Schachtman et al., 1998). Interestingly, nega-
tive charge in the cell wall fibers and hydroxyl groups containing
mucilage of the root repels anions like phosphate that in turn
reaches the stele. Thus, the movements of anionic compound
including nutrients through the apoplasm are highest in the root
tip. Uptake of Pi from the soil is based upon the PHT1 transporters,
a family of plant plasma membrane proteins having 12 membrane
spanning domains. PHT1 is a relatively large family (e.g. 09 mem-
bers in Arabidopsis and at least 13 in rice and are H2 PO +
4 /H sym-
porters), where some of them are involved with the Pi uptake at
soil-root level, other mainly helps in translocation to various tissue
systems (Nussaume et al., 2011). However, phosphate transporters
help to move P through the membranes into the plant root cells
through an energy-driven transport mechanism (Mikkelsen,
2013). It was found that activity of an H+-extrusion pump such
as the P-type H+-ATPase takes part in energy-dependent Pi uptake
proceeds via electrochemical proton gradient dependent H+/Pi co-
transport (Ullrich-Eberius et al., 1984; Rausch and Bucher, 2002).
6. Rhizosphere, root exudates and elemental uptake
The term rhizosphere was coined by German agronomist and
plant physiologist Lorenz Hiltner in 1904 describing the plant-root
interface where complex biological and ecological processes occur.
It is the most active portion of soil and has the influence on the
chemical, biological and physical activities especially due to varied
organic discharges and exudates by the plant roots (Jones et al.,
2009). This region usually discharges about 10–40% of plant’s total
photosynthetically fixed carbon as both organic (e.g., low molecu-
lar weight organic acids) and inorganic (e.g., HCO3) forms (McNear,
2013). The root products or Rhizodeposits in the surrounding soil
of the root include sloughed-off root cap and border cells, muci-
lage, and exudates (Rovira, 1969; Dakora and Phillips, 2002). Dur-
ing the growth of root tips, apart from exerting pressure (>7 kg/
cm2 or 100 psi) on the surrounding soil, mucilage (a viscous, high
molecular weight, insoluble, polysaccharide-rich material), is pro-
duced that helps in lubricating the soil, protecting the root from
desiccation, improvement of soil quality and uptake of essential
nutrients and elements (McNear, 2013). Along with the mucilage,
root meristem cells protecting the root tip are automatically dis-
charged (slough-off) that attract different useful microbes at the
rhizosphere region (Bengough and McKenzie, 1997; Hawes et al.,
2000, 2003).
Root exudates include both actively and passively released
compounds which may be of both high and low molecular weight
(HMW and LMW, respectively) components. However, apart from
few HMW compounds (like, mucilage, cellulose), an array of
LMW is released into the soil (e.g. organic acids, amino acids, pro-
teins, sugar, phenolics and other secondary metabolites) that at-
tract and utilize surrounding soil biota and influencing the
rhizosphere processes through colonization (Bacillus subtilis, Pseu-
domonas florescence) or symbiosis (e.g. rhizobia and legumes) on
root surfaces. In turn, acquiring of different nutrients (e.g. acquisi-
tion of Fe and P) is achieved by the root surface (Hawes et al., 2003;
Bais et al., 2004). Furthermore, several bacterial species (Table 1)
have the ability to solubilize insoluble inorganic phosphate com-
pounds (Rodríguez and Fraga, 1999). Interestingly, the extremely
assorted range of plant microbial population is usually maintained
at the rhizosphere level, which may imply a close link in the evo-
lutionary happenings. Further, root exudates may be involved in
a variety of intra-plant and inter-plant interaction, cascading the
complex signaling events (Walker et al., 2003, 2009). Root-medi-
ated rhizospheric biochemical interactions thus may generally be
classified into two categories: positive (interaction with rhizobac-
teria (PGPR), cross species signaling to promote growth regulators,
etc.) and negative (secretion of antimicrobials, phytotoxins, nema-
ticidal, and insecticidal compounds) (Bais et al., 2006; Kumar and
Bais, 2012). To make available essential micronutrients like Fe,
Mn, Zn and Cu in metallic soils, roots also discharge metal chela-
tors that unbind the metals from the soil particle and enhance
the mobility and solubility of the same (Bertin et al., 2003;
Lakshmanan et al., 2012). Among known chelators, phytosidero-
phore molecules are common for Fe chelation in different species
of the grass family (Gramineae or Poaceae). Even if Fe is compara-
tively abundant in soil, it is often present as hardly soluble Fe(III)
precipitates. Siderophores like nonproteinogenic amino acids
(mugenoic and avenic acid) of these grasses bind with ‘‘insoluble’’
Fe(III) making the iron available to the grasses (Sugiura and Nom-
oto, 1984; Bais et al., 2006; Lakshmanan et al., 2012). It is also re-
ported that the siderophore amount secreted by the graminoids is
distinctly greater in Fe-deficient plants (Romheld and Marschner,
1985). In dicots as well, many phenolics are released into the soil
to increase metal bioavailability (Bertin et al., 2003; Jones et al.,
2004).
Different studies have provided the evidences that both water-
soluble (e.g. DAP) and water-insoluble (e.g., apatite) P-compounds
play an important role in (im)mobilizing metals in soils by regulat-
ing the bioavailability for plant uptake. Further, as some of the PR

Table 1
List of prominent phosphate solubilizing bacterial species.

Family Bacteria Characteristics Substrate References

Pseudomonadaceae Pseudomonas sp. Gram-negative, aerobic gammaproteobacteria C Illmer and Schinner (1992)
Pseudomonadaceae Pseudomonas striata Gram-negative, rod-shaped, saprotrophic C, H, P Gainda (2013)
Burkholderiaceae Burkholderia cepacia Gram-negative bacteria C Mullan et al. (2002)
Rhizobiaceae Rhizobium sp. Gram-negative, rod-shaped, motile, non-sporulating H Sridevi and Mallaiah (2009) and Dastager and
Damare (2013)
Rhizobiaceae Sinorhizobium Gram-negative nitrogen-fixing bacterium (rhizobium) H, P Bianco and Defez (2010)
meliloti
Bacillaceae Bacillus Gram-positive, rod-shaped, motile. aerobic C Calvo et al. (2010)
amyloliquefaciens
Bacillaceae Bacillus megaterium Gram-positive, rod-shaped, aerobic, spore forming C, H, P Rodríguez and Fraga (1999)
Paenibacillaceae Paenibacillus telluris Gram-positive, motile, facultative anaerobic, endospore- C, H, P Lee et al. (2011)
forming bacteria
Paenibacillaceae Bacillus polymyxa Gram-positive C, H, P Rodríguez and Fraga (1999)
Enterobacteriaceae Citrobacter freundi Aerobic gram-negative bacilli, rod-shaped C, H, P Qian et al. (2010)

C = calcium phosphate; H = hydroxyapatite; P = phosphate rock.

140 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144
source contains high level of heavy metals, application of such P-
compounds may lead to introduction of different heavy metals into
the field. Even though mobilization by certain P compounds en-
hances the bioavailability of metals, practice of phytoremediation
of any contaminated site, however, needs proper evaluation on
the application of specific P compounds. Thus, amendment of soil
helps in removal and subsequent recovery of metals through phy-
toremediation techniques and the safe disposal of metal contami-
nated plants (Bolan et al., 2003).
7. Phosphate starvation and signaling in plants
Management of nutrient utilization is determined by the rhizo-
sphere through mobilization and acquisition of soil nutrients that
greatly influence plant growth and crop productivity (Zhang
et al., 2010). Due to its low solubility and mobility in soil, P deple-
tion in rhizosphere restricts its availability to plants. Thus, the bio-
availability of P to plants is predominantly controlled by plant root
architecture (root morphology, topology, and distribution pattern),
mycorrhizal association with roots and chemical and biological
constituents at rhizosphere level that helps in bioavailability and
acquisition of P. During the P starvation, plants modify their root
system by increasing the root/shoot ratio, root branching, root
elongation, development root hairs and formation of cluster roots
(Shen et al., 2011). Root symbioses with the arbuscular mycorrhi-
zal fungi (AMF) help to increase the spatial availability of P by
extending the nutrient absorptive surface through the formation
of mycorrhizal hyphae (Brundrett, 2009). Thus, AMF influence
the plant growth through increased uptake of nutrients (e.g. P,
Zn, Cu), and in turn stabilize soil and alleviate plant stresses from
different biotic and abiotic factors (Smith et al., 2010; Gianinazzi
et al., 2010).
Organic acids such as citric, malic, and oxalic acids released as
exudates can form complexes with the Fe or Al phosphates, and
thereby enhance the uptake of plant available phosphates. It is pre-
dicted that these chelators have more important effect on P mobi-
lization than on other elements. Even, P adsorption sites on the soil
particle may be blocked by forming complexes with cations on soil
mineral surfaces by releasing diverse group of organic acids as and
when required by plants (Jones et al., 2004). It is reported that
most plants (e.g. white lupine- Lupinus alba, rape- Brassica napus,
alfalfa- Medicago sativa, Cicer arietinum) increase rhizosecretion
significantly in response to P deficiencies (Lipton et al., 1987;
Hoffland et al., 1992; Johnson et al., 1994; Neumann and Romheld,
1999; Jones et al., 2004; Gupta et al., 2006).
When come across a low-Pi medium, root growth is restrained
due to lower meristem maintenance activity, reduced cell elonga-
tion and less auxin circulation at root tip that may lead to irrevers-
ible damage to root growth blockage (Sanchez-Calderon et al.,
2005; Kramer and Bennett, 2006; Desnos, 2008). This retardation
in growth may be due to Fe content and pH change in the media,
or excess accumulation of intracellular Fe in the plants (Misson
et al., 2005; Hirsch et al., 2006; Desnos, 2008; Fang et al., 2012).
Low-Pi stress may attenuate the extension of primary root and ini-
tiate the formation of a shallow root system along with promotion
of root hair formation. Reports suggest that plants roots can sense
the Pi richness in the ambience and thus, Pi-sensitive checkpoint
for root development and meristem maintenance is genetically
controlled (Ticconi et al., 2004; Thibaud et al., 2010; Abel, 2011).
However, few plants can modify their root structure when they
are in P stress. Lupines are best known, as they form proteoid roots
in response to P deficiency (Kania et al., 2003). Mature proteoid
roots generate much higher levels of organic acid as exudate
(1.16 compared to 0.09 lmol h1 g1) by increasing the organic
acid production and decreasing its metabolism on the other hand.
Thus proteoid roots manage to increase the P uptake by almost 50%
than nonproteoid lupine roots (Neumann and Romheld, 1999; Ka-
nia et al., 2003; Bais et al., 2006).
8. Transport and sequestration of metals in plants
Plant evolved to respond to various natural or edaphic stress
factors due to the change in the physiological concentrations of
the bioactive metals which may influence their growth or produc-
tivity (Schützendübel and Polle, 2002; Chatterjee et al., 2011). In
response to heavy metal toxicity, plants follow the general tactics
like immobilization, exclusion, chelation and compartmentaliza-
tion of the metal ions, and expression of the general stress re-
sponses (Cobbett, 2000) which can be enumerated further in
case of hyperaccumulators like Pteris vittata for As (Gumaelius
et al., 2004), Thlaspi caerulescens for Ni (Freeman et al., 2004), Pilea
sinofasciata and Polygonum hydropiper for P (Xiao et al., 2009), etc.
Several transmembrane nutrient transporters are present in the
root to transport different essential elements. Cytoplasmic homeo-
stasis of pi concentrations is achieved through the mechanism of
membrane transport and different exchange between various
intracellular pools of P. Several compartments in plant cell like
cytoplasm, vacuole, apoplast, and nucleus along with their respec-
tive pH determines the form of Pi used for the pool. It has been
seen by the researchers that, basic (pH 7.2) in cytoplasm help in
partitioning H3PO4 in an equal distribution of H2 PO 4 and HPO4

whereas, acidic vacuoles and apoplast partition species like
HPO 4 . Non-essential metals like Cd compete with these nutrient
transporters and enter the root through the cortical tissue (Curie
et al., 2000; Papoyan and Kochian, 2004). In case of Cd, once it en-
ters into the root, it may either be accumulated at root or trans-
ported to the xylem and above ground parts through an
apoplastic and/or symplastic pathway involving several ligands
like organic acids and/or PCs (Cataldo and Wildung, 1983; Salt
et al., 1995). A list of Cd-hyperaccumulator plants has been re-
ported along with their ecotypes like Noccaea caerulescens (J&C
Presl.) FK Mey, Phytolacca americana L., and Arabidopsis halleri (L.)
O’Kane and Al-Shehbazs, etc. (Watanabe et al., 2007; Lux et al.,
2011). Broadley et al. (2001) reported that the species of the
Caryophyllales and Lamiales group accumulate Cd in shoot in
much higher concentration than other species. However, in most
of the plants Cd concentrations are usually higher in roots than
in shoots, signifying the restricted transportation of Cd to the xy-
lem and phloem in most plants. Concentrations are lowest in
seeds, fruits, and tubers (Seregin and Kozhevnikova, 2008; Conn
and Gilliham, 2010). Plants are able to sense the physiological
stress that lead to explicit activation of metal-responsive genes
to synthesize different proteins and signaling molecules specific
for the metal chelation and subsequent compartmentalization of
the ligand-metal complexes within the cells (Cobbett, 2000;
Maksymiec, 2007).
Vacuolar membrane (tonoplast) is mainly involved in metal
homeostasis by regulating the movements of ions and metals
around the cell. Mostly, the vacuole acts as storage space for the
metal ions (Vögeli-Lange and Wagner, 1990). The tonoplast con-
tains many membrane transporters, like, ABC transporter that
helps in the transportation of xenobiotic compound and heavy me-
tal. The ABC transporter subfamily (MRP and PDR) is mainly ac-
tively involved in sequestration of heavy metals (Manara, 2012).
MRPs are concerned with mediating PC–Cd complex transport
across the tonoplast in plants (Vögeli-Lange and Wagner, 1990).
The CDF transporter family of proteins is involved both in the
pumping of divalent metal cations (like Zn, Cd, Co, Fe, Ni, and
Mn) and transportation from the cytoplasm to the vacuole (Krämer
et al., 2007; Peiter et al., 2007; Montanini et al., 2007; Manara,
 D.K. Gupta et al. / Chemosphere 108 (2014) 134–144
2012). CDF transporters consist of six transmembrane domains, a
C-terminal cation efflux domain, and a histidine-rich region be-
tween transmembrane domains IV and V (Mäser et al., 2001)
which probably act as a sensor for heavy metal concentration
(Kawachi et al., 2008). Again, NRAMP transporters for example
AtNRAMP3 and AtNRAMP4 are localized in the tonoplast and help
in the transportation of Fe from the vacuole (Thomine et al., 2003;
Lanquar et al., 2005). Cd sensitivity gets increase on overexpression
of AtNRAMP3 (Thomine et al. 2000) and prevent the accumulation
of Mn (Thomine et al., 2003), indicating a possible role in the
homeostasis of metals other than Fe.
Vacuole in a plant cell is an appropriate storage reservoir for
heavy metal sequestration and accumulation. Once a heavy metal
enters into the plant cell, it may be removed from the active cellu-
lar compartments and cytosol where sensitive metabolic activities
take place (Dalcorso et al., 2010; Hossain et al., 2012). Proton
pumps in the vacuole, especially, vacuolar proton-ATPase (V-ATP-
ase) and vacuolar proton-pyrophosphatase (V-PPase), help in vac-
uolar uptake of most of solutes. Some well-characterized heavy
metal transporter proteins are zinc-regulated transporter (ZRT),
iron-regulated transporter (IRT) like protein ZIP family, the P-type
metal ATPases, ABC transporters of the mitochondria (ATM), ATP-
binding cassette (ABC) transporters, multidrug resistance-associ-
ated proteins (MRP), the natural resistance-associated macrophage
protein (NRAMP) family, copper transporter (COPT) family pro-
teins, cation diffusion facilitator (CDF) family of proteins, yellow-
stripe-like (YSL) transporter and Ca2+: cation antiporter (CAX),
pleiotropic drug resistance (PDR) transporters, etc. (Lee et al.,
2005; Chiang et al., 2006; Krämer et al., 2007; Huang J. et al.,
2012; Gupta et al., 2013b). It was found through vacuole isolation
or compartmental flux analysis on Cd accumulation in Cd-exposed
tobacco (Nicotiana rustica var Pavonii) seedlings, that vacuoles con-
tained almost all of the Cd-binding peptides (Vögeli-Lange and
Wagner, 1990; Huang J. et al., 2012).
Metal-binding ligands play an important role to plants for the
homeostasis of metals and reducing the toxicity thresholds of non-
essential metals. A number of metal-binding ligands have now
been recognized which help plants to sustain in the hostile envi-
ronments (Rauser, 1999; Callahan et al., 2006). Peptide ligands
are also present in the plants. Among the peptide ligands, like phy-
tochelatins (PCs) and metallothioneins (MTs) are most common.
These cysteine-rich polypeptides provide thiols to bind different
kind of metals that help in cellular metal homeostasis and detoxi-
fication (Rauser, 1995; Cobbett, 2000; Gupta et al., 2013a). How-
ever, synthesis of PCs to alleviate toxic effects of non-essential
heavy metals such as As, or Cd are arguably most sophisticated en-
zyme-catalyzed mechanisms known to protect plants and some al-
gae, fungi and invertebrates (Gupta et al., 2004, 2013a; Rea, 2012).
In plants, Phytochelatins (PCs) are the best-characterized hea-
vy metal chelators especially in the context of Cadmium (Cd) tol-
erance (Cobbett, 2000; Gupta et al., 2002; Manara, 2012). PC–
metal complex is formed to sequester metals in both plant and
yeast systems. Root-to-shoot transport of Cd is another important
activity of PCs (Gupta et al., 2008, 2010). High molecular weight
(HMW) compound with PCs are formed particularly in response
to Cd, and As sequestration in vacuole after incorporation of sul-
fur (S2) (Salt et al., 1998). Cd/H+ antiporters and ATP-dependent
ABC transporters in the tonoplast help the transportation of PC–
Cd complexes into the vacuole (Salt and Wagner, 1993; Salt
and Rauser, 1995). Ortiz et al. (1992) reported that Cd-sensitive
mutant of Schziosaccharomyces pombe (mutation in the gene
hmt1 that encodes for an ABC-type transporter) can synthesize
PCs but not accumulate the Cd–PC–sulfide complexes. Again,
wheat gene TaPCS1 when expressed in transgenic A. thaliana in-
creased transport efficiency of Cd from root to shoot (Gong
et al., 2003).
141
9. Future prospects
Increase in crop production per unit area is obligatory to meet
the food requirement alongside with the decrease in the quantity
and quality of land for agriculture. In 1970s the average growth rate
per acre of crop yields was 3.5 percent year1 which was in advance
of the growth rate of global population. In current time, however,
the growth in crop yields per acre has dropped to about 1.5%, which
is very close to the growth of world population. Use of P-based fer-
tilizer to amend the soil for better crop production is common
among different agricultural practices. However, P is the most crit-
ical element of fertilizer that helps to our capability to produce
food, which is having a finite supply. The natural phosphate cycle
is influenced by human mainly in the form of processing, introduc-
tion and utilization of commercial synthetic fertilizers (super phos-
phate). Mining of P as estimated is approximately five times greater
than the amount of P used as fertilizers and one tenth of P used in
the agriculture system. Globally, the lost P (collectively with nitro-
gen) is a concern for several issues including pollution to water
bodies (eutrophication), exhausting the PR faster and related heavy
metal and radiation related hazards in the soil and surroundings.
Therefore, paradoxically, P symbolizes equally an incredibly
important, scarce, non-renewable resource for the life and equally
a contaminant of the system. P dynamics in the soil and its avail-
ability to plants is a complex phenomenon which needs a better
attention to understand it to improve P-use efficiency in crop pro-
duction including reduction of loss of P from agricultural areas,
and, P recovery and reuse from all type of bio-wastes. It is antici-
pated that about eleven percent of total P is lost from human waste,
of which, ninety percent can be recovered, recycled and reused that
may cater for approximately 22% of global demand of P. The useful
approaches that lead to optimization on the balance of inputs/
outputs of P and to maintain the soil-available P supply include
comprehensive information on the element with respect to soil, rhi-
zosphere of specific plants and plant processes. Exploitation of bio-
logical potential at rhizosphere level may further contribute to
effective P management. This may possibly, in one hand, add signif-
icantly for saving P resources, on the other hand, reducing the appli-
cation of chemical fertilizer, without sacrificing crop yields. Reports
indicate that root zone application of ammonium with P improved
maize (Zea mays) growth by stimulating root proliferation and
rhizosphere acidification (Shen et al., 2011). Further, soil and rhizo-
sphere microorganisms including AMF and plant growth promoting
rhizobacteria (PGPR) help to append plant P acquirement from the
soil (Jones and Oburger, 2011). Further, PGPR, like Pseudomonas
fluorescens, Ps. aeruginosa, Ps. cepacia, Ps. putida, species of Azospir-
illum, Azotobatcer, Bacillus, Bradyrhizobium, Enterobacter, Erwinia,
Rhizobium, who are usually proficient colonizer at the root zone,
may act symbiotically and/or a symbiotically with plants for acquir-
ing plant growth-promoting substances and nitrogen fixation.
Acknowledgements
Authors are thankful to Mrs. Swagata Chatterjee for making
handmade figure. The authors apologize for the many colleagues
who are not referenced in this work due to space limitations.
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