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OPEN ACCESS
ROLE OF IRON IN PLANT GROWTH AND
METABOLISM
Gyana R. Rout and Sunita Sahoo
Department of Agricultural Biotechnology, College of Agriculture, Orissa University of Agriculture & Technology, Bhubaneswar 751 003,
Odisha, India
ABSTRACT
Iron is an essential micronutrient for almost all living organisms because of it plays critical role in metabolic processes such
as DNA synthesis, respiration, and photosynthesis. Further, many metabolic pathways are activated by iron, and it is a prosthetic
group constituent of many enzymes. An imbalance between the solubility of iron in soil and the demand for iron by the plant are
the primary causes of iron chlorosis. Although abundant in most well-aerated soils, the biological activity of iron is low because it
primarily forms highly insoluble ferric compounds at neutral pH levels. Iron plays a significant role in various physiological and
biochemical pathways in plants. It serves as a component of many vital enzymes such as cytochromes of the electron transport
chain, and it is thus required for a wide range of biological functions. In plants, iron is involved in the synthesis of chlorophyll, and
it is essential for the maintenance of chloroplast structure and function. There are seven transgenic approaches and combinations,
which can be used to increase the concentration of iron in rice seeds. The first approach involves enhancing iron accumulation in
rice seeds by expressing the ferritin gene under the control of endosperm-specific promoters. The second approach is to increase
iron concentrations in rice through overexpression of the nicotianamine synthase gene (NAS). Nicotianamine, which is a chelator
of metal cations, such as Fe+2 and zinc (Zn+2), is biosynthesized from methionine via S-adenosyl methionine synthase. The third
approach is to increase iron concentrations in rice and to enhance iron influx to seeds by expressing the Fe+2- nicotianamine
transporter gene OsYSL2. The fourth approach to iron biofortification involves enhancing iron uptake and translocation by
introducing genes responsible for biosynthesis of mugineic acid family phytosiderophores (MAs). The fifth approach to enhance
iron uptake from soil is the over expression of the OsIRT1 or OsYSL15 iron transporter genes. The sixth approach to enhanced iron
uptake and translocation is overexpression of the iron homeostasis-related transcription factor OsIRO2. OsIRO2 is responsible for
the regulation of key genes involved in MAs-related iron uptake. The seventh approach to enhanced iron translocation from flag
leaves to seeds utilizes the knockdown of the vacuolar iron transporter gene OsVIT1 or OsVIT2. The present review discusses iron
toxicity in plants with regard to plant growth and metabolism, metal interaction, iron-acquisition mechanisms, biofortification of
iron, plant-iron homeostasis, gene function in crop improvement, and micronutrient interactions.
Keywords:Iron homeostasis, Iron biofortification, Iron tolerance, Iron toxicity, Micronutrient interaction, Plant metabolism
Introduction
Heavy metals are environmental pollutants, and their toxicity
is a problem of increasing significance for ecological, nutritional,
evolutionary, and environmental reasons. The term heavy metal
refers to any metallic element with has a relatively high specific
gravity (typically five times heavier than water) and is often toxic
or poisonous even at low concentrations. This group of heavy
metals includes lead (Pb), cadmium (Cd), nickel (Ni), cobalt (Co),
iron (Fe), zinc (Zn), chromium (Cr), arsenic (As), silver (Ag),
and the platinum group elements (Farlex, 2005). Fifty-three of
the 90 naturally occurring elements are considered heavy metals
(Weast, 1984), but only few are of biological importance. Based
on their solubility under physiological conditions, 17 heavy metals
may be available to living cells, and they could be significant
in plant and animal communities within different ecosystems
(Weast, 1984). Some of the heavy metals (Fe, Cu, and Zn) are
known to be essential for plants and animals (Wintz et al., 2002).
Other heavy metals such as Cu, Zn, Fe, Mn, Mo, Ni, and Co are
Received: January 7, 2015. Accepted: March 1, 2015. Published on line: May 19, 2015.
Correspondence to G.R.R: [email protected]
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essential micronutrients (Reeves and Baker, 2000), excess uptake
of which by plants results in toxic effects (Blaylock and Huang,
2000; Monni et al., 2000 ) ; these are also referred to as trace
elements due to their presence in trace or in ultra-trace (1 µg kg-1
or µg L-1) quantities in environmental matrices. Plants experience
oxidative stress upon exposure to heavy metals that leads to
cellular damage and disturbance of cellular ionic homeostasis.
To minimize the detrimental effects of exposure to heavy metals
and their accumulation, plants have evolved detoxification
mechanisms that are mainly based on chelation and subcellular
compartmentalization. Phytochelatins (PCs) are a principal class
of heavy metal chelators in plants, which are synthesized without
translation from reduced glutathione (GSH) in a transpeptidation
reaction catalyzed by the enzyme phytochelatin synthase (PCS).
Therefore, the availability of glutathione is essential for PCs
synthesis in plants, at least during their exposure to heavy
metals (Yadav, 2010). Iron (Fe) is an essential micronutrient for
plants whose deficiency presents a major worldwide agricultural
problem. Moreover, iron is not easily available in neutral
to alkaline soils, rendering plants iron-deficient despite its
abundance. Thirty percent of global cultivated soils are calcareous
with low iron availability, because iron is present in insoluble
oxidized forms ( Guerinot and Yi, 1994; Mori, 1999 ) . Dicots
and monocots have developed the Strategy I response (proton
extrusion to solubilize Fe+3 in the soil, reduction of the solubilized
Fe+3 by a membrane-bound Fe+3 chelate reductase, and subsequent
transport of the resulting Fe+2 into the plant root cell by an Fe+2
transporter) to iron deficiency stress (Römheld and Marschner,
1986; Marschner and Römheld, 1994). This response includes
acidification of the rhizosphere by releasing protons, subsequent
induction of Fe+3 chelate reductase activity that reduces Fe+3 to
Fe+2, and acquisition of Fe+2 across the plasma membrane of root
epidermal cells (Römheld, 1987).
Two types of causal relationships exist between the high
concentration of heavy metals in soil and the expression of
toxicity symptoms. On one hand, heavy metals compete with
essential mineral nutrients for uptake, thereby disturbing the
mineral nutrition of plants (Clarkson and Luttge, 1989). On the
other hand, after uptake by the plant, it accumulates in plant
tissues and cell compartments and ultimately hampers the general
metabolism of the plant (Thurman and Collins, 1983; Taylor et
al., 1988; Turner, 1997). Heavy metal accumulation in plants has
multiple direct and indirect effects on plant growth, and it alters
many physiological functions ( Woolhouse, 1983 ) by forming
complexes with O, N, and S ligands (Van Assche and Clijsters,
1990). They interfere with mineral uptake (Yang et al., 1998;
Zhang et al., 2002; Kim et al., 2003; Shukla et al., 2003; Drazic
et al., 2004; Adhikari et al., 2006), protein metabolism (Tamas et
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Rout and Sahoo, Reviews in Agricultural Science, 3:1-24, 2015.
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al., 1997), membrane function (Quariti et al., 1997; Azevedo et al.,
2005), water relations (Kastori et al., 1992), and seed germination
(Iqbal and Siddiqui, 1992; Al-Hellal, 1995). The present review
highlights the physiology of plant growth in the context of iron
toxicity, interactions with other micronutrients, interactions with
other heavy metals, and molecular mechanisms of iron toxicity,
membrane transport, plant iron homeostasis, iron biofortification,
and genes responsible for iron tolerance.
Effects of Iron on Plant Growth
Iron is the third most limiting nutrient for plant growth and
metabolism, primarily due to the low solubility of the oxidized
ferric form in aerobic environments ( Zuo and Zhang, 2011;
Samaranayke et al., 2012). Iron deficiency is a common nutritional
disorder in many crop plants, resulting in poor yields and reduced
nutritional quality. In plants, iron is involved in chlorophyll
synthesis, and it is essential for the maintenance of chloroplast
structure and function. Being the fourth most abundant element
in the lithosphere, iron is generally present at high quantities
in soils; however, its bioavailability in aerobic and neutral pH
environments is limited. In aerobic soils, iron is predominantly
found in the Fe+3 form, mainly as a constituent of oxyhydroxide
polymers with extremely low solubility. In most cases, this form
does not sufficiently meet plant needs. The visual symptoms of
inadequate iron nutrition in higher plants are interveinal chlorosis
of young leaves and stunted root growth. In waterlogged soils, the
concentration of soluble iron may increase by several orders of
magnitude because of low redox potential (Schmidt, 1993). Under
such conditions, iron may be taken up in excessive quantities.
However, it is potentially toxic and can promote the formation of
reactive oxygen-based radicals, which are able to damage vital
cellular constituents (e.g., membranes) by lipid peroxidation.
Bronzing (coalesced tissue necrosis), acidity, and/or blackening
of the roots are symptoms of plants exposed to above-optimal
iron levels (Laan et al., 1991). Iron predominantly exists as Fe+3
chelate forms in the soil, and plants ultimately cannot absorb it
under various physiological conditions such as high soil pH in
alkaline soils. Thus, plants growing in high-pH soils are not very
efficient at developing and stabilizing chlorophyll, resulting in the
yellowing of leaves, poor growth, and reduced yield. However,
plants have developed sophisticated mechanisms to take up
small amounts of soluble iron. Non-graminaceous plants release
protons, secrete phenolics, reduce Fe+3, and take up iron (Römheld
and Marschner, 1983; Marschner, 1995a; Jeong and Guerinot,
2009; Cesco et al., 2010). Once iron is solubilized, Fe+3 is reduced
to Fe by a membrane-bound Fe+3 reductase oxidase (Jeong and
Connolly, 2009). Fe is then transported into the root by an ironregulated transporter (IRT1). Ishimaru et al. (2011) reported that
©2015 Reviews in Agricultural Science
When the insoluble ferric (Fe3+) form is reduced, it is converted
to a ferrous form in the soil, and is then absorbed by plants. Even
though iron is hardly present in living matter (50–100 µg·g-1 dry
matter), it is still an essential element that is critical for plant
life (Guerinot and Yi, 1994), as this element is involved in plant
metabolism. As a critical component of proteins and enzymes,
iron plays a significant role in basic biological processes such as
photosynthesis, chlorophyll synthesis, respiration, nitrogen fixation,
uptake mechanisms (Kim and Rees, 1992), and DNA synthesis
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graminaceous plants rely on an Fe+3 chelation system during the
secretion of mugineic acid (MA) family phytosiderophores. MAs
are secreted to the rhizosphere through TOM1, and they then
chelate Fe+3. In rice, the resulting Fe-MA complex is transported
by the yellow stripe family transporters (OsYSL15) (Nozoye et
al., 2011). Rice plants also have the ability to take up the iron
transporter (Ishimaru et al., 2006). Rout et al. (2014) screened
51 varieties of upland and lowland rice using different levels of
iron (0, 50, 100, and 200 mM) in nutrient solution to study the
toxicity effect. Out of 51 varieties, 16 varieties were tolerant
(>200 mM Fe), 11 exhibited medium tolerance (<200 mM Fe),
and 24 varieties were susceptible (<100 mM) to selected iron
concentrations. Total chlorophyll, total proline, total phenol, total
protein, and total carbohydrate content showed variation in both
tolerant and susceptible varieties. The oxidative enzymes also
showed variation among the tolerant and non-tolerant genotypes.
Typically, approximately 80% of iron is found in photosynthetic
cells where it is essential for the biosynthesis of cytochromes
and other heme molecules, including chlorophyll, the electron
transport system, and the construction of Fe-S clusters (Briat et al.,
2007; Hansch and Mendel, 2009). In the photosynthetic apparatus,
two or three iron atoms are found in molecules directly related
to photosystem II (PS-II), 12 atoms in photosystem I (PS-I), five
in the cytochrome complex, and two in the ferredoxin molecule
(Varotto et al., 2002). Such distributions show that iron is directly
involved in the photosynthetic activity of plants and, consequently,
their productivity (Briat et al., 2007). Iron availability is assumed to
affect the natural distribution of species, and it may limit the growth
of fast-growing economically important plants (Chen and Barak,
1982). Iron can also be potentially toxic at high concentrations.
The ability of iron to donate and accept electrons means that if iron
is free within the cell, it can catalyze the conversion of hydrogen
peroxide into free radicals. Free radicals can cause damage to a
wide variety of cellular structures, and they can ultimately kill
the cell (Crichton et al., 2002). To prevent that kind of damage,
life forms have evolved a biochemical protection mechanism by
binding iron atoms to proteins.
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through the action of the ribonucleotide reductase (Reichard, 1993).
It is also an active cofactor of many enzymes that are necessary
for plant hormone synthesis, such as ethylene, lipoxygenase,
1-aminocyclopropane acid-1-carboxylic oxidase ( Siedow,
1991), or abscisic acid (compounds that are active in many plant
development pathways and their adaptive responses to fluctuating
environment conditions). Iron deficiency severely affects plant
development and growth, and excess iron in cells is toxic. Iron
reactivity with reduced forms of oxygen produces radical elements
that can cause a loss of integrity and kill the cell. Therefore, there
is an optimal window for the iron concentration to ensure smooth
plant development. Iron is a constituent of all redox systems in
plants, and the best known examples are enzyme systems (hemeiron structure), including prosthetic groups like cytochromes.
Iron plays a role in the porphyrin structure of chlorophyll, and is
therefore a principal component of chloroplasts. The best-known
functions of cytochrome are electron transport and the involvement
of cytochrome oxidase in the terminal step in the respiration
chain. Iron also interacts with non-heme proteins as an iron-sulfur
protein (e.g., ferredoxin, superoxide dismutase). Iron is a major
component of plant redox systems. Because of its physicochemical
properties, especially its affinity to active metalloprotein sites, it
acts as a cofactor in redox reactions that are necessary for oxygen
production and use. However, its best-known function is its
structural role in the prosthetic groups of enzyme systems such as
cytochromes, catalases, and peroxidases. These enzymes are also
the main components of chloroplasts and mitochondria (Mengel
and Kirby, 1987; Marschner, 1995b). The cytochrome essentially
acts as an electron carrier in the respiratory chain. Iron also interacts
with non-heminic proteins such as those in the iron sulfide group
(e.g., ferredoxin, superoxide dismutase). Moreover, iron is also
active in protein synthesis (Bennet, 1945; Perur et al., 1961). Bashir
et al. (2011) identified and characterized the mitochondrial iron
transporter (MIT) in rice after screening 3993 mutant lines. The
identification of MIT is a significant advance in the field of plant
iron nutrition, and it should facilitate the cloning of paralogs from
other plant species. Iron deficiency-induced chlorosis is a major
problem in plants, and it affects both yield and crop quality. Plants
have evolved multifaceted strategies, such as reductase activity,
protons, and specialized storage proteins to mobilize iron from the
environment and to distribute it within the plant. The activation of
iron uptake reactions requires an overall adaptation of the primary
metabolism because these activities need a constant supply of
energetic substrates (i.e., NADPH and ATP). Vigani (2012) reported
that mitochondria are the energetic centers of the root cell, and they
are strongly affected by iron deficiency. They observed that they
display a high level of functional flexibility, which allows them to
maintain the cell viability. Mitochondria contain a large amount
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of metalloproteins that require iron to carry out their function
(Bertini and Rosato, 2007). In fact, several enzymes belonging
to both the respiratory chain and to the tricarboxylic acid cycle
are iron-containing proteins. Moreover, crucial steps of the Fe-S
cluster assembly for the entire cell take place in the mitochondria,
suggesting an important role for this compartment in iron handling
by the cell. Iron deficiency and mitochondria are strongly linked
because this stress greatly induces Strategy I activities that
demand considerable energy, thereby requiring the participation
of mitochondria. Mitochondria represent a crucial target of studies
on plant homeostasis, and it might be of interest to concentrate
future research on understanding how mitochondria orchestrate
the reprogramming of root cell metabolism under iron deficiency.
Overall, root mitochondria are strongly affected by iron starvation,
because they require at least forty iron atoms per respiratory unit to
function (Vigani et al., 2009). The ABC transporter STA1/AtATM3
has been characterized in Arabidopsis and implicated in the export
of Fe-S clusters (Kushnir et al., 2001). In addition, ferric-chelate
reductases, encoded by FRO genes in plants, might be involved in
mitochondrial iron transport because AtFRO3 and AtFRO8, mainly
located in root and shoot veins, respectively, contain mitochondriatargeting sequences (Mukherjee et al., 2006). This suggests that a
reduction-based uptake could also occur in the invaginated inner
membrane of mitochondria. Moreover, the oxidizing conditions
found in the mitochondrial intermembrane space ( IMS ) are
indicative of the need for a reduction-based mechanism (Hu et al.,
2008; Abadía et al., 2011).
Because of iron's redox properties and its ability to form
complexes with diverse ligands, this element is a constituent
of many electron carriers and enzymes; therefore, it plays an
important role in plant metabolism. On the other hand, low
solubility of inorganic iron at physiological pH levels and its
high reactivity in the presence of oxygen, which generates toxic
hydroxyl radicals, represent a severe difficulty (Hell and Stephan,
2003). Soil conditions that result in insufficient or excess iron
uptake are widespread in nature (Snowden and Wheeler, 1993;
Schmidt and Fuhner, 1998; de la Guardia and Alcantara, 2002a).
Chlorosis of young leaves is often the first visual sign of iron
deficiency. It is not only associated with the loss of chlorophyll,
as several steps of its biosynthesis depend on iron, but also with
changes in the expression and assembly of other components of
the photosynthetic apparatus (Terry and Abadia, 1986). On the
other hand, evidence exists that suggests that iron excess increases
cytochrome b6/f complex in the thylakoid (Suh et al., 2002). In
recent years chlorophyll fluorescence analyses have been applied
as rapid non-destructive tools to obtain information about the state
of photosynthetic apparatuses under iron deficiency or toxicity,
and this is especially true regarding photosystem II (PS II). It has
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been demonstrated that photoprotection through excessive light
dissipation as well as reversible photosynthesis might lead to
down-regulation and sustained photo inhibitory damage (Morales
et al., 2000; Gogorcena et al., 2001; Donnini et al., 2003). Nenova
et al. (2006) found that in pea plants, the excess iron resulted in
increased pigment concentrations of up to 28%. Some changes
in the pigment ratios were also observed, suggesting that their
increased content could not only be attributed to concentration
effects due to inhibited growth. Suh et al. ( 2002 ) also found
evidence of photoinhibition in pea plants. The tendency of iron to
form chelates and to undergo changes (Fe2+  Fe3++e-) are the two
important characteristics underlying its numerous physiological
effects. The best-known function of iron is in the enzyme systems
in which heme or hemin function as prosthetic groups (Mengel
and Kirkby, 1987 ) . Here, iron plays a somewhat similar role
to magnesium in the porphyrin structure of chlorophyll. These
heme enzyme systems include catalase, peroxidase, cytochrome
oxidase, and various cytochromes, but the role of these enzymes
in plant metabolism is not completely understood. Research has
also provided information about the function of cytochromes in
electron transport and the involvement of cytochrome oxidase in
the terminal step of the respiration chain. Catalase brings about the
breakdown of H2O2 to water and ½ O2. This enzyme also plays an
important role in chloroplasts (along with the enzyme superoxide
dismutase), photorespiration, and the glycolytic pathway. Cellwall-bound peroxidases appear to catalyze reactions during
the polymerization of phenol to lignin, and peroxidase activity
seems to be particularly depressed in iron deficient roots. Cellwall formation and lignification were impaired, and phenolics
accumulated in the rhizodermis of iron-deficient sunflower roots
(Romheld and Marschner, 1981). Phenolics can be released into
the external solution, and, in the case of caffeic acid, may bring
about chelation and reduction of inorganic Fe3+ (Olsen et al.,
1981). This reaction is not only favored by the accumulation of
phenolics, but also by an increase in the reducing capacity of the
roots, which accompanies the impairment of lignin synthesis.
Barton ( 1970 ) observed large quantities of phytoferritin in
chloroplasts, which confirmed earlier evidence that chloroplasts are
rich in iron, containing as much as 80% of the total iron in plants.
Like heme iron, Fe-S proteins play a major role in oxidoreduction,
and both binuclear Fe-S clusters (2Fe-2S) and tetranuclear Fe-S
clusters ( 4Fe-4S ) occur. Each cluster is surrounded by four
cysteine residues associated with a polypeptide chain (Sandmann
and Boger, 1983). These clusters are known as ferredoxins if they
act exclusively as electron carriers and are characterized by a very
high negative redox potential. Iron and chlorophyll concentrations
are often well correlated in green plants. The same metabolic
pathway involved in chlorophyll formation also operates during
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Iron uptake by plants is fastest when iron is present in the
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the biosynthesis of heme. Iron appears to control the rate of deltaaminolevulinic acid (ALA) formation, which is the precursor of
porphyrins (Miller et al., 1980). During iron deficiency, a decrease
occurred in the condensation rate of glycine and succinyl-CoA to
form ALA. In iron-deficient leaves, the photosynthetic apparatus
remained intact, but the number of photosynthetic units decreased
(Terry, 1980). Iron is also involved in protein metabolism. During
iron deficiency, the protein fraction decreases simultaneously with
an increase in the level of soluble organic N compounds. Nitric
oxide (NO) is a bioactive molecule that has recently emerged as a
cellular messenger in numerous physiological processes in plants
(Neil et al., 2003). NO is biologically active at a concentration
of 1 nmol L -1, and it participates in signaling cascades that
drive plant growth and developmental processes (Beligni et al.,
2001). It is known that NO displays a high affinity towards, and
reacts with, transition metals. The three redox-related states of
biochemically distinguishable NO species, nitroxyl anion (NO-)
nitric oxide radical (NO), and nitrosodium cation (NO+), can
react with the ferric (Fe3+) and/or ferrous (Fe2+) forms of iron
(Stamler et al., 1996). Indeed, the high affinity of NO for iron is
a well-characterized example of the study of compounds formed
between metal ions and other neutral or charged molecules.
The complexes formed between iron and NO are called ironnitrosyl complexes (Stamler et al., 1992; Stamler et al., 1996),
and these interactions are central in NO biochemistry. NO can
form iron-nitrosyl complexes in vivo with Fe-S and heme protein
centers that are important for the biological activity of NO (Wink
et al., 1998). The Fe-S cluster plays an important role in iron
homeostasis because it can act as an iron sensor that regulates
protein expression associated with iron balance such as ferritin
and the transferring receptor in mammals (Beinert et al., 1999). In
addition, Fe-S proteins are viewed as carrier proteins that avoid
the toxicity associated with free iron and allow its delivery at
lower intracellular concentrations (Mansy et al., 2004). The redoxrelated NO species can have simultaneous effects on cellular
iron metabolism and homeostasis via mechanisms that might
involve S-nitrosylation and/or the ligation of NO to Fe-S clusters
(Richardson et al., 1995). The uptake of iron, translocation, and
regulation in higher plants has been reviewed (Kobayashi and
Nishizawa, 2012 ) , and they reported that higher plants have
developed two distinct strategies to acquire slightly soluble iron
from the rhizosphere. Key molecular components, including
transporters, enzymes, and chelators, have been clarified for both
strategies, and many of these components are now thought to also
function inside the plant to facilitate internal iron transport.
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ferrous form ( Chaney et al., 1972 ) . In anaerobic soils, high
concentrations of ferrous ions may lead to iron toxicity via
excessive iron uptake. Plants may limit iron uptake under those
conditions by the oxidation of ferrous ions with oxygen, which is
transported from the shoot via aerenchyma (Foy et al., 1978). Iron
in aerobic soils is mainly present as the ferric ion in precipitates
(Lindsay et al., 1982) or in soluble chelates (Powell et al., 1980).
Chaney et al. (1972) reported that dicotyledonous plants might
enhance their capacity for iron uptake, in response to a developing
deficiency, by increasing their ability to reduce ferric chelates at
the root surface. Plants have evolved two separate mechanisms
for the acquisition of iron, which can be referred to as Strategy I
and Strategy II. These working hypotheses were first proposed by
R mheld and Marschner (1986). Sharma et al. (2013) reported that
the increase in the iron content of plants shows an enhancement
upon the treatment of rice plants with plant growth-promoting
rhizobacteria. They concluded that application of plant growthpromoting rhizobacteria strains was an important strategy to
combat the problem of iron deficiency in rice crops and humans.
Iron is essential for various cellular events in plants, including
cellular respiration, chlorophyll synthesis, and photosynthetic
electron transport. It also serves as a cofactor for a wide range
of plant functions (e.g., cytochromes, catalase, and peroxidase
isozymes contain iron as a prosthetic group). In Fe-S proteins, iron
is associated with cysteine, inorganic sulfur, or both (Marschner,
1995b). Iron is also required for the synthesis and stabilization of
chlorophyll, which is why the chlorophyll content significantly
decreases in Fe-deficient plants. As a result, iron deficiency has
a marked effect on plant growth and product quality. Subcellular
organelles, such as chloroplasts and mitochondria, depend on
iron for their activities. Iron deficiency significantly affects the
function of mitochondria, and the disturbance in mitochondrial
iron homeostasis adversely affects plant growth and development
( Mori et al., 1991; Bashir et al., 2011 a, b, c; Bashir and
Nishizawa, 2013; Vigani et al., 2013).
Iron is primarily absorbed by plants, and it solubilizes Fe3+ and
then reduces it to Fe2+ for absorption or transport into the root. Tong
et al. (1985) reported that both oxygen and photosynthetic substrates
are required for iron reduction by roots in apples (Rümheld and
Marschner, 1985). Clarkson and Sanderson (1978) observed that the
root tips 1–4 cm from the apical zone absorbed and translocated
more iron than the rest of the root. The roots of grapes under iron
stress displayed enhanced proton release from approximately
the same area (Korcak, 1987). R mheld and Marschner (1985,
1986) proposed that iron uptake occurs by two species-dependent
strategies. Strategy I refer to iron mobilization by dicots and nongramineous monocots in response to iron deficiency stress, and
Strategy II refers to that found only with gramineous monocots. The
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chemotaxonomic boundary for the two strategies is not between
dicotyledons and monocotyledons, but between higher plants
and grasses (Römheld, 1987). Plant species exhibiting Strategy I
show one or more of the following adaptive components: i) iron
deficiency-induced enhancement of Fe3+ reduction to Fe2+ at the
root surface, with preferential uptake of Fe2+ (Chaney et al., 1972);
ii) H+ extrusion (Römheld and Marschner, 1984) that promotes
the reduction Fe3+ to Fe2+; and iii) in certain cases the release of
reducing and/or chelating substances by the roots. Enhanced Fe3+
reduction under iron-deficiency, the most typical feature of Strategy
I, is characterized by the activation of reductases located on the
plasma membrane and presumably in the cell wall (apoplast) of
the apical root zones (Bienfait et al., 1983). Bennett et al. (2011)
reported that reduction of Fe+3 by root ferric chelate reductase
further enhances iron solubility, since Fe+2 is more soluble than
Fe+3. Reduction also prepares iron for uptake by IRT1 types (i.e.,
ferrous transporters), which move Fe+2 across the root epidermal
area to the plasma membrane. All three components of Strategy
I (proton pumping, ferric chelate reductase gene expression and
enzyme activity, and IRT1 expression) increase markedly when
plants are grown in iron-deficient conditions. Strategy I is used by
most plant types, including the model plant Arabidopsis thaliana,
which facilitated the identification of key Strategy I genes such
as ferric reductase oxidase (FRO2) (encodes root ferric chelate
reductase (Robinson et al., 1999)) and IRT1 (encodes the ferrous Fe
transporter (Eide et al., 1996). Strategy II systems are characterized
by an iron deficiency-induced release of specific Fe3+-chelating
compounds phytosiderophores (Takagi et al., 1984) and a high
affinity uptake system (transport protein) for Fe3+ phytosiderophores
(Römheld and Marschner, 1986). As a consequence, gramineous
species exhibiting these two components are highly efficient at
acquiring iron forms sparingly, including soluble inorganic Fe3+
(e.g., iron hydroxide). Chlorotic leaves might send a signal to the
roots inducing them to develop the reactions, but only the roots of
efficient varieties could pick up and interpret the chlorosis signal .
Certain plants, namely the grasses, that include most of the
world's staple grains, have evolved a distinct mechanism to acquire
iron from the soil, which is known as Strategy II. This strategy is
best described as a chelation, which is similar to that used by
many bacteria and fungi (Miethke and Marahiel, 2007), and it may
have arisen as an adaptation to alkaline soils where acidification
of the rhizosphere is difficult to achieve (Ma and Nomoto, 1996).
Strong iron chelators called phytosiderophores (PS) are synthesized
by the plant and secreted into the rhizosphere where they bind Fe+3
(Tagaki, 1976; Tagaki et al., 1984, 1988). The Fe (III)-PS complex
is then taken up into root cells via transporters that are specific
to the complex (Römheld and Marschner, 1986; von Wiren et
al., 1994). Phytosiderophores are chemically quite distinct from
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bacterial and fungal siderophores, and they belong to a class of
compounds called mugineic acids (MAs) (Ma and Nomoto, 1996).
The biosynthetic pathway of MAs, starting from the condensation
of three S-adenosyl-methionine molecules that form the precursor
nicotianamine (NA), is well established (Mori and Nishizawa, 1987;
Kawai et al., 1988; Shojima et al., 1990; Ma et al., 1995; Tkahashi
et al., 1999; Kobayashi et al., 2001). The Fe (III)-phytosiderophore
uptake transporter is called yellow stripe 1 (YS1), after the mutant
phenotype of yellow striped leaves that result from the disruption
of the gene encoding this transporter in maize (von Wiren et al.,
1994; Curie et al., 2001). YS1 proteins are distantly related to the
oligopeptide transporter (OPT) family of transporters (Yen et al.,
2001), and have been identified in several grass species (Curie et
al., 2001; Yen et al., 2001; Murata et al., 2006; Inoue et al., 2009;
Lee et al., 2009). YS1 is a proton-coupled symporter of Fe (III)PS complexes (Schaff et al., 2004). The transport activity and
specificity of YS1 transporters from maize ( ZmYS1 ) , barley
(HvYS1), and rice (OsYSL15) have been examined using yeast
growth complementation and radioactive uptake assays in two
electrode voltage clamp experiments in Xenopus leavis oocytes
(Curie et al., 2001; Roberts et al., 2004; Schaaf et al., 2004; Murata
et al., 2006; Inoue et al., 2009; Lee et al., 2009).
In the case of graminaceous plants, the plants secrete MAs
that bind to and solubilize Fe +3 ( Takagi, 1976; Takagi et al.,
1984), and the resulting Fe (III)-MA complexes are readily taken
up by the yellow stripe-like ( YSL ) family of transporters at
the root surface (Curie et al., 2001). MAs are synthesized from
L-methionine (Shojima et al., 1990). NA synthase (NAS) converts
three molecules of S-adenosyl methionine (SAM) to NA (Higuchi
et al., 1994, 1995, 1999), which is then converted to a 3'-keto
intermediate by NA aminotransferase (NAAT) (Kanazawa et al.,
1993; Takahashi et al., 1999). This 3'-keto intermediate is then
reduced to produce deoxymugineic acid (DMA) by the action of
DMA synthase (DMAS) (Bashir and Nishizawa, 2006; Bashir et
al., 2006). This DMA is then released into the rhizosphere through
the MAs1 transporter (Nozoye et al., 2011, 2013). The genes of
MA biosynthetic pathway have been cloned and characterized in
barley, rice, maize, and wheat (Takahashi et al., 1999; Nakanishi
et al., 2000; Kobayashi et al., 2001; Inoue et al., 2003, 2008;
Bashir et al., 2006; Bashir and Nishizawa, 2006). The expression
of these genes is significantly upregulated by iron deficiency
through transcriptional regulation that is mediated by various
combinations of cis-acting elements and trans-acting factors
(Kobayashi et al., 2003, 2005, 2007, 2009, 2010, 2012; Ogo et al.,
2008, 2011; Kobayashi and Nishizawa, 2012), and the synthesis
and secretion of MAs increases with limited iron availability. A
diagrammatic representation of iron transport in the rice plant
is presented in Figure 1 (Bashir et al., 2013). Iron deficiency
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responsive elements 1 and 2 (IDE1 and IDE2, respectively) were
the first identified cis-acting elements controlling gene expression
in response to micronutrient deficiencies (Kobayashi et al., 2003).
Iron is translocated from roots to shoots as a ferric-citrate
chelate form, and this is transported to actively growing shoot
regions. Morris and Swanson (1981) reported that iron stress
did not change the redox potential of sap as compared to that
of non-stressed trees. Since iron moves as a citrate complex, its
stability during transport would be determined, in part, by the
both pH and redox potential. Thus, under iron stress, movement
as a citrate-chelate should not be affected. Translocation via
citrate in the stem exudates of four soybean genotypes was most
nearly related to the available iron supply (Brown et al., 1958).
The transporters that are responsible for loading iron and citrate
into the xylem have been recently revealed. Citrate appears to be
moved into the xylem, at least in part, via the multidrug and toxic
compound extrusion (MATE) family transporter ferric chelate
reductase defective 3 (FRD3), which has a mutation that was
responsible for the manganese accumulator (man1) phenotype
(Rogers and Guerinot, 2002a, b; Durrett et al., 2007). If high levels
of exogenous citrate are provided in the growth medium, iron
accumulation in the root's vasculature is alleviated, and plants
become phenotypically normal (Durrett et al., 2007). Kannan
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(1980) reported that the absorption of nutrients by plant leaves
may be similar to that by roots, the main step being transport
through the plasmalemma. As transport through the plasmalemma
is an active process, the uptake rate of most plant nutrients is
influenced by the physiological status of the leaf (Mengel and
Kirkby, 1987). In leaf tissues, in contrast to the root, this active
uptake process is usually not the limiting step in ion uptake. The
availability of the micronutrient on the leaf surface is directly
related to the water solubility of applied compounds. The
precipitation for the crystallization of exogenous elements leads
to immobilization, and the higher retention of inorganic iron in
epicuticular waxes may be connected with its low solubility. When
the solubility of Fe+2 extends over a wide pH range, this element
is readily oxidized to Fe3+, which tends to precipitate out in the
form of hydroxide even at low pH levels. The formation of such
an insoluble product would immobilize the element on the leaf
surface. However, chelating improves iron solubility in water, and
this property can explain the lesser degree of superficial retention
and, consequently, the higher uptake with chelates. In the case
of pea plants, iron and zinc cross the cuticle more readily as free
ions (Ferrandon and Chamel, 1989), although an opposite result
occurred with iron in citrus. The penetration of substances through
the cuticle is a diffusive process that is influenced by temperature
Fig.1. Iron transport in rice reported by Bashir et al. (2013).
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and concentration gradient. Water and solutes penetrate both
stomatous and astomatous cuticles. Penetration through stomatous
cuticles is usually more rapid than through astomatous cuticles,
but citrus cuticles show the opposite ( Basiouny and Biggs,
1976). Cuticles are 10–20 times more permeable to urea than to
inorganic ions, and the foliar spray of nitrogen compounds can
also enhance iron uptake. Regarding corn, the addition of urea
and ammonium nitrate increased the effectiveness of foliarapplied FeSO4. Moreover, urea and ammonium nitrate had no
effect on Fe-amino chelate, but they decreased the effectiveness
of Fe-EDTA. In tomatoes and white beans, the transport was not
as efficient, but it involved at least 25% of leaf-absorbed iron.
Translocation of foliar-applied iron may be enhanced by chelation
and by treatment with GA3 or kinetin (6-furfuryl amino purine).
In corn, ferrous sulfate with chelating agents (EDTA or DTPA)
considerably increased the translocation of iron out of the treated
leaf (Ferrandon and Chamel, 1989). These authors suggested that
the metal cation is bound to its ligand within the plant, and that its
high mobility might correspond to a lesser affinity of chelated iron
for the negative sites on cell membranes and along vessels.
Biochemistry of Iron Toxicity in Plants
Iron is an essential nutrient for plants. It accepts and donates
electrons, and it plays important roles in the electron transport
chains associated with photosynthesis and respiration. However,
iron is toxic when high levels accumulate. It can act catalytically
via the Fenton reaction to generate hydroxyl radicals, which can
damage lipids, proteins, and DNA. Therefore, plants must respond
to iron stress in terms of both iron deficiency and iron overload.
Plant species and growth media-related factors such as plant age,
hydrogen sulfide accumulation, organic acids, and other reduction
products also influence the occurrence of iron toxicity (De Datta et
al., 1994; Sharawat, 2004). Some researchers reported that seedlings
may be more sensitive to toxic metals than mature plants (Hodgson,
1972; Tadano, 1975). Moreover, Borggard (1983) observed that
iron-rich substrata (especially Fe3+ solids) can fix dissolved
phosphorous via the formation of insoluble ferric phosphates or
by the adsorption of phosphate onto amorphous ferric solids. This
might be expected to have a particularly adverse effect on Epilobium
hirsutum (a fen plant species), which has a high relative growth rate
and is largely confined to nutrient-rich, productive habitats (Wheeler
and Giller, 1982). High iron concentrations may also cause ironinduced deficiencies of essential nutrients (e.g., Mn, P, K, Ca,
and Mg) in plants (Howeler, 1973, Ottow et al., 1982). However,
shoot analyses provided little evidence for such deficiencies in E.
hirsutum, and direct iron toxicity in a typical wetland plant like
E. hirsutum may seem a surprising possibility, especially in a high
pH environment where iron solubility is likely to be rather low.
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Various disorders have been attributed in rice grown in iron-rich
conditions (pH < 6) in which iron solubility can be very high (e.g.,
6000 mg L-1 in flooded acid soils) (Martin, 1968). However, studies
have shown iron toxicity in some dry land plants in high pH
soils. Soluble organic-iron complexes, which may be available to
plants, might also maintain iron in solution (Marschner and Barber,
1975) in organic substrata, and this may partly account for the high
dissolved-iron concentration (approximately 20 mg L-1). Wheeler
(1985) observed that the iron accumulation in E. hirsutum shoots
and roots grown in iron-rich conditions point to the feasibility of
direct iron toxicity in this plant. Kuraev (1966) reported that the
initial toxic effect of high iron inhibits root development, and this
was observed at higher iron concentrations (200 mg L-1), which
may have been due to possible toxicity mechanisms such as the
iron-induced production of superoxide (O2-). Tanaka et al. (1966)
reported that high iron concentrations may influence the growth
and distribution of various wetland plant taxa. E. hirsutum roots
also have some capacity that is clearly inadequate in high iron
environments. Many researchers have reported iron toxicity as a
problem in plants, particularly rice (Howeler 1973, Snowden and
Wheeler 1993). Furthermore, Batty and Younger (2003) examined
the effects of total iron (added as FeSO4 7H2O) on an aquatic reed
species (Phragmites australis), and they found growth inhibition
above a total iron concentration of 1 mg L-1. However, they believed
that the iron might not directly explain the reduction in growth.
Wang (1986) reported that the effective concentration (EC50) for
duckweed (Lemna minor) was 3.7 mg L-1, and Sinha et al. (1999)
found that relatively low concentrations of iron (0.5–5.0 mg L-1)
resulted in damage to the membranes due to lipid oxidation in the
aquatic plant Hydrilla. Although iron is present in both Fe2+ and
Fe3+ forms in soils, it is only taken up by plants in Fe2+ forms. The
available iron content of tea soils varies from 50 to 100 mg kg-1.
Moreover, since oxygen diffuses in air 103 to 104 times faster than
in water or water-saturated soils, oxygen is rapidly depleted by the
respiration of soil microorganisms and plant roots in waterlogged
soils and continuously wetted soils. With the depletion in oxygen,
Fe3+ can act as electron acceptor for microbial respiration, and it is
subsequently reduced to Fe2+ (Becker and Asch, 2005). Rout et al.
(2014) used different iron concentrations to screen 51 varieties of
upland and low land rice varieties under nutrient culture conditions.
They observed that most of the varieties showed low germination
rates, shoot and root tolerant indices, and leaf bronzing symptoms at
40 mM Fe. The total chlorophyll, proline, polyphenol content, total
protein, and total carbohydrate content showed variation in both
tolerant and susceptible varieties.
Effect of Iron on Plant Morphology
Numerous visible effects associated with high iron concentrations
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were commonly observed, and some species showed several of the
following symptoms (Cook, 1990): growth retardation; reduction in
leaf size; deepening of green leaf color (particularly in the youngest
leaves); reddening or purpling of stems and older leaves; wilting of
shoots; yellowing and dieback of oldest leaves (especially from the
tips or margins); brown or black speckles or larger necrotic patches
on leaves; blackening of leaf tips and stem bases; stiffening of
stems; root stunting (particularly of adventitious roots); lack of root
branching; root flaccidity; root blackening (particularly of the apices);
and formation of precipitates on roots (Snowden and Wheeler, 1993).
Furthermore, Hemalatha and Venkatesan (2011) reported that tea
plants that received higher concentrations of iron in soil developed
toxicity symptoms, and the bottom-most leaves turned coppery red
at later stages. They also reported that the upper most leaves of the
tea plant established in soil containing above 500 mg kg-1 of rice
grown in iron-rich conditions iron showed reddish brown spots on
the upper epidermis. Albano and Miller (1993) reported that a specific
physiological disorder, bronze speckle, was consistently induced in
First Lady and Voyager marigolds with Fe-DTPA concentrations
greater than 0.018 mM Fe-DTPA (1 ppm) applied to a soilless
medium. The disorder was characterized by specific symptomology
that was visually distinguished by speckled patterns of chlorosis and
necrosis as well as a downward curling and cupping of the leaves. The
percentage of total leaf dry weight affected with symptoms generally
increased with increasing Fe-DTPA treatments. Symptomatic
leaf tissue had a greater iron concentration than corresponding
asymptomatic leaf tissue. This disorder that affected African and
French marigolds was reported in the floriculture industries of the
United States and Canada (Biernbaum et al., 1988; Carlson, 1988;
Halbrooks and Alabo, 1990; Albano and Miller, 1993). Furthermore,
symptoms of this disorder include leaf chlorosis, bronze spotting
of the leaf, overall stunting, and delayed flowering (Biernbaum et
al., 1988). Symptoms are initially observed on older, mature leaves,
and then progress to younger growth. Slight chlorotic speckling
progresses to necrotic spotting (pitting), and necrosis of leaf margins
(Vetanovetz and Knauss, 1989). Affected leaf tissue has been reported
to have iron and Mn concentrations of 400–2500 ppm, which is
considered excessive (Biernbaum et al., 1988). Vetanovetz et al. (1989)
have identified this disorder as an iron toxicity of some floriculture
crops, including New Guinea impatiens, Sultana impatiens, cutting
and seed geraniums, vinca, and some species of Brassica. Similar
disorders have been observed in cabbage and tomato transplants as
well as elatior begonias (Vetanovetz and Knauss, 1989). Disorders
attributed to iron toxicity include freckled leaves of sugarcane (Foy
et al., 1978), the grey effect in tobacco (Arnold and Birns, 1987), and
various unnamed disorders in other plants. Visual symptoms of iron
toxicity have been reported to include necrotic pitting, spotting or
speckling, and bronzing (Foy et al., 1978; Albano and Halbrooks,
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1991).
Differential Iron Tolerance
One approach used to overcome iron toxicity is the precise
study of its effects at the cellular level, and to select putative
tolerant cells that are screened in the presence of different iron
concentrations that are lethal to unselected cells (Mandal and
Roy, 2000 ) . Metal tolerance screening for a large number of
species demands a relatively rapid and reliable method (Baker
and Walker, 1989). The germination response of plants potentially
provides rapid screening for metal tolerance, but it has been found
to be unsatisfactory. An important mechanism, which excludes
many dry land plants from the wetland environment, is their
inability to prevent the uptake of reduced toxins such as Fe2+ by
oxidative precipitation (Martin, 1968). It seems likely that similar
mechanisms may also help explain differential tolerance of
wetland plants to available iron (Wheeler et al., 1985; Cook 1990).
Wheeler et al. (1983) showed that monocotyledonous species were
usually more tolerant of iron than were dicotyledonous species.
Monocotyledonous shoots are frequently hollow, which facilitates
oxygen diffusion to the roots ( Etherington, 1983 ) . Justin and
Armstrong (1987) indicated that monocotyledonous species (and
particularly wetland ones) also have more porous root systems
than dicotyledonous species. Although dicotyledonous species
(and particularly wetland ones) seem more able to increase root
porosity upon flooding than monocotyledonous ones, they do
not attain the high values inherent in monocotyledonous roots.
Armstrong and Beckett (1987) pointed out that the many wetland
monocotyledonous species also have additional adaptations
that help conserve oxygen supplies for apical consumption and
oxidative detoxification at the root tip, but these adaptations have
not be found in dicotyledonous species. Hodgson (1972) observed
that high concentrations of extractable manganese and aluminum
were also frequently found in sites supporting iron-tolerant species,
so it is possible that some plants have co-tolerance to these metals.
The lack of correlation between tolerance and mean extractable
potassium and magnesium concentrations is notable because there
is considerable evidence that plants insufficiently supplied with
either of these elements are prone to iron toxicity (Howler, 1973,
Foy et al., 1978; Benckiser et al., 1984). Iron tolerance shows a
negative relationship with extractable phosphorus concentrations
and with soil fertility. The least-tolerant species tend to grow in
the more fertile sites and areas with higher extractable phosphorus
concentrations. This may be partly because many iron sensitive
species have high relative growth rates (Snowden and Wheeler,
1993 ) . The development of adventitious roots is sometimes
regarded as an important adaptation to flood tolerance (Drew,
1987 ) . Snowden and Wheeler ( 1993 ) reported iron tolerance
screening for 43 British native fen plant species. They included
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23 dicotyledons and 20 monocotyledons, and they found evidence
of a clear relationship between the iron tolerance of a species and
the nature of the root precipitate (Cook, 1990). Roy et al. (2003)
examined two rice cultivars IR72 (susceptible) and C14-8
(tolerant), and in vitro screening indicated the detrimental effects
of higher concentrations on plantlet regeneration. However, a few
calli survived on stressed media and regenerated plantlets. Cultivar
C14-8 showed a higher degree of tolerance than IR72 . Prominent
differences, including changes in enzyme activity with respect
to iron-toxicity were noted. The results indicated that the activity
of esterase, malate dehydrogenase, and lactate dehydrogenase
in C14-8 decreased in iron-stressed media. Decreased activity
indicates that the gradual degradation of these enzymes or their
structural modification under increased iron toxicity levels. The
activity of these enzymes increased in IR72 under stressed media.
However, the activity of peroxidase remained almost unaltered in
C14-8 across the stress gradient.
Role of Iron in Enzyme Activity
Iron is an essential mineral for plants that is required for
biological redox systems (Asad and Rafique, 2000), and it is
also a vital component of many enzymes that play important
roles in the physiological and biochemical processes of plants.
It acts as a cofactor of key enzymes involved in plant hormone
synthesis and participates in numerous electron transfer reactions
( Kerkeb and Connoly, 2006 ) . Plants are subjected to varying
differences in iron availability from the environment because of
their immobility. Therefore, either starvation or excess amounts
of this element are believed to generate oxidative stress (AbdelKader, 2007), which subsequently leads to several nutritional
disorders that affect physiology of plant (Becker and Asch, 2005).
The toxicity of reactive oxygen species depends on the presence
of a Fenton's catalyst, such as iron or copper ions, which give rise
to extremely reactive OH- radicals in the presence of H2O2 and
O2- (Chen and Schopfer, 1999). The reactive toxic oxygen species
cause damage to DNA proteins, lipids, chlorophyll, and almost
every other organic constituent of living cells (Becana et al.,
1998). Plants protect cellular and sub-cellular systems from the
cytotoxic effects of these reactive oxygen species with antioxidant
enzymes and metabolites such as carotenoids, ascorbic acid, etc.
(Alscher et al., 1997). Venkatesan et al. (2005, 2006) found that
high concentrations of iron may result in the localized formation
of iron polyphenol complexes. Monteiro and Winterbourn
(1988) found that excess iron amounts must have catalyzed the
generation of active O2 free radical species, which might have
eventually oxidized the chlorophyll and subsequently led to
decreased chlorophyll content. Arunachalam et al. (2009) reported
a decrease in chlorophyll and carotenoid content with increased
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iron concentrations. This trend is due to the uniformity of pigment
synthesis (Wilkinson and Ohki, 1988), and carotenoids also act
as important metabolites that aid in protecting the cellular and
subcellular systems from the cytotoxic effects of these reactive
oxygen species (Agarwal et al., 2006) by quenching the singlet
oxygen (Prasad and Bisht, 2011). Amylase is an enzyme that
participates in carbohydrate metabolism. Hofner (1970) found that
amylase activity decreased with increased iron concentrations,
and this was due to the fact that iron forms complexes in plants
with carbohydrate compounds such as maltose. The assimilation
of NH4+ into amino acids occurs via the joint action of glutamine
synthetase and glutamate synthase. Glutamate synthase catalyzes
the transfer of an amide group from glutamine to alphaketoglutarate to yield two glutamate molecules. This reaction
is agreed to be the primary route of nitrogen assimilation in
plants (Temple et al., 1998). When the activity decreased, the
formation of amino acids also decreased, which led to lack of
nitrogen assimilation in plants. Hemalatha et al. (2011) found that
in tea plants, the amylase invertase, aspartate amino transferase,
and glutamate synthase were also drastically affected by the
excess iron concentrations. They also reported that when iron
concentration decreased, the amount of pigments like chlorophyll
and carotenoid were reduced. The polyphenol content, which
plays a vital role in tea quality, was also affected by the localized
formation of a Fe-polyphenol complex. Bashir et al. (2007) studied
the expression patterns and enzyme activities of glutathione
reductase (GR) in graminaceous plants under iron-sufficient and
iron-deficient conditions by isolating barely cDNA clones for
chloroplastic GR (HvGR1) and cytosolic GR (HvGR2). They
found that the GR1 and GR2 sequences were highly conserved
in graminaceous plants, and based on their nucleotide sequences,
HvGR1 and HvGR2 were predicted to encode polypeptides of
550 and 497 amino acids, respectively. Both proteins showed in
vitro GR activity, and the specific activity for HvGR1 was 3-fold
that of HvGR2. HvGR1, HvGR2, and TaGR2 were upregulated
in response to iron-deficiency ( Romero-Puertas et al., 2006 ) .
Moreover, HvGR1 and TaGR1 were mainly expressed in shoot
tissues, whereas HvGR2 and TaGR2 were primarily observed in
root tissues. The GR activity increased in roots of barley, wheat,
and maize and in the shoot tissues of rice, barley, and maize
in response to iron-deficiency. Furthermore, the researchers
observed that GR was not post-transcriptionally regulated in
rice, wheat, and barley. Kaminaka et al., (1998) reported that
OsGR1 expression was mainly observed in roots and calli, rather
than in leaves. Hence, GR may play a role in the iron-deficiency
response in graminaceous plants and in internal iron homeostasis.
Romero-Puertas et al., (2006) reported that the expression of
PsGR1 and PsGR2 was differentially regulated in response to
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Iron is an important component of enzymes that are involved
in the transfer of electrons (e.g., cytochromes and iron-sulfur
[Fe-S] proteins involved in redox reactions ) . Furthermore, it
is a constituent of non-heme iron proteins that are involved in
photosynthesis, N2 fixation, and respiration (Taiz and Zeiger, 1991).
Iron limitation affects one-third of the cultivable land on Earth,
and it represents a major concern for agriculture. Iron limitation
causes the decline of many photosynthetic components, including
the Fe-S protein ferredoxin (Fd), which is involved in essential
oxidoreductive pathways of chloroplasts (Tognetti et al., 2007). In
this role, it is reversibly oxidized from Fe2+ to Fe3+ during electron
transfer. Characteristic symptoms of iron deficiency involve
interveinal chlorosis, which is similar to Mg deficiency (Bienfait
and Van der Mark, 1983). Iron-deprived plants usually develop
interveinal chlorotic symptoms in young leaves as well as poor
root formation, and when severe, the deficiency leads to growth
retardation, stasis, and death (Kobayashi et al., 2003). Chlorosis
has been attributed to the inhibition of chlorophyll synthesis,
which requires the function of iron-containing enzymes (Reinboth
et al., 2006). However, expression of chlorophyll-binding proteins
and other photosynthetic components is downregulated with
relative independence of pigment levels (Thimm et al., 2001).
Therefore, chloroplasts are primary targets of iron deficiency,
resulting in decreased photosynthetic activity and plastidic
pigments and proteins (Winder et al., 1995). Both the utilization
of ribulose-1, 5-biphosphate by rubisco and its regeneration by
the Calvin cycle appear compromised in iron-starved plants
(Arulanathan et al., 1990; Winder et al., 1995). Iron deficiency
can occur in agricultural soils at both extremes of the pH range.
Moreover, several of the following factors contribute either
individually or in combination to the development of chlorosis:
low iron supply; calcium carbonate in soil; bicarbonate in soil
or irrigation water; over irrigation or water logged conditions;
high phosphate levels; high levels of heavy metals; low or high
temperatures; high light intensities; high levels of nitrate nitrogen;
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Iron Deficiency in Plants
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various stresses such as mechanical wounding and increased
temperature. Lipton et al. (2001) reported that GSH may play an
important role in signal transduction for the regulation of gene
expression in response to different stresses and iron homeostasis.
However, an S-nitrosylated form of GSH has been suggested to
act as a transport molecule for NO, thereby increasing its halflife and allowing for effective biological activity (Lipton 2001).
GSH is also essential for the activity of glutathione S-transferase,
which specifically interacts with the dinitrosyl-diglutathionyl-Fe
complex, and it behaves like a storage protein for this complex
both in vivo and in vitro (Maria et al., 2003; Turella et al., 2003).
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imbalances in cation ratios; poor soil aeration; certain organic
matter additions to soil; viruses; and root damage by nematodes
and other organisms (Wallace and Lunt, 1960; Embleton et al.,
1973 ) . Lindsay and Schwab ( 1982 ) reported that olive plants
growing on calcareous soils faced characteristic problems
regarding iron acquisition. The total iron content in these soils
was high, but the fraction available for the plants was insufficient.
This was caused by the very low solubility of iron oxides at
alkaline pH conditions that were buffered by the presence of
bicarbonate in these soils. Further, Lopez-Jimenez (1985) reported
that in young Avocado leaves, the chlorosis increase was related to
decreased iron content in leaves, chlorophyll, and catalase activity.
Iron deficiency is usually manifested as interveinal chlorosis of
young leaves while the veins remain green, hence termed iron
deficiency chlorosis. The manifestation of the symptoms in
young leaves is due to the inability to redistribute iron within
the plant. However, iron may become more mobile under stress
conditions (Chaney et al., 1992). One of the best alternatives to
prevent iron chlorosis problems is the use of tolerant plant species
or genotypes. Differences in tolerance have been found in many
herbaceous and woody species (Hamze et al., 1986; Kolesh et al.,
1987; Chaney et al., 1992; Cianzio, 1995). Alcantar et al. (2003)
observed that olive trees are widely grown on the calcareous
soils of the Mediterranean without generally showing problems
associated with iron chlorosis, and this species is considered
more tolerant than other fruit species such as peaches or quinces.
Nonetheless, iron chlorosis has been observed in some olive
orchards (Martar et al., 1977; Fernadez-Escobar et al., 1993).
This could be related to different causes including the following:
location specific poor soil or environmental conditions; use of
irrigation, fertilization, or higher plantation density aimed to
increase production; or the introduction of less tolerant varieties.
Soil-based organisms have evolved various adaptive mechanisms
to mitigate the consequences of an iron deficit, and most rely
on the optimization of metal uptake from scarcely available
sources. Dicotyledon plants and non-graminaceous monocots
display the so-called Strategy I response, which is characterized
by the development of root hairs and transfer cells, increased
proton extrusion to the rhizosphere to improve Fe3+ solubility, and
enhanced accumulation of ferric-chelate reductases and broad
range metal transporters in the root cell plasma membrane to favor
Fe2+ intake (Eide et al., 1996; Robinson et al., 1999; Thomine
et al., 2000; Bereczky et al., 2003; Mukherjee et al., 2006;). On
the other hand, grasses, have developed a different response in
which phytosiderophores of the mugineic acid family are released
into the surrounding soil (Mori, 1999). The screening for iron
deficiency in cultivars using hydroponic systems with bicarbonate
has been used for herbaceous (Pissaloux et al., 1995; Ahendawi et
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al., 1997; Campbell and Nishio, 2000; Lucena, 2000) and woody
species (Romera et al., 1991a, b; Shi et al., 1993; Sudahono et al.,
1994; Cinelli et al., 1995; Alcantara et al., 2000; Nikolic et al.,
2000). Moreover, Pestana et al. (2004) studied the effects of iron
deficiency in three citrus rootstocks ( Troyer citrange, Taiwanica
orange and Swingle citrumelo ) using different growth
parameters and physiological characteristics. They observed that
Troyer citrange and Taiwanica orange plants had a similar
degree of tolerance to iron chlorosis, whereas the Swingle
citrumelo rootstock was more sensitive.
Iron Biofortification in Plants
Iron is an essential micronutrient for plants and animals,
and iron deficiency is one of the most prevalent micronutrient
deficiencies globally. It affects an estimated two billion people
(Stoltzfus et al., 1998) and causes 0.8 million deaths annually
worldwide ( WHO, 2002 ) . Iron deficiency is ranked sixth
among the risk factors for death and disability in developing
countries with high mortality rates (WHO, 2002). Micronutrient
supplementation, food fortification, and biofortification are the
three basic approaches used to alleviate micronutrient deficiencies.
Rice is a particularly suitable target for biofortification because
iron deficiency anemia is a serious problem in developing
countries where rice is a major staple crop (WHO 2002; Juliano,
1993 ) . Biofortification can be applied to increase the iron
concentrations in polished seeds and to achieve the target iron
demand for human nutrition. Sperotto et al. (2012) suggested
conventional breeding or directed genetic modification as two
possible ways to develop iron-rich rice plants. Iron concentrations
in rice have a narrow variation, ranging from 6 to 22 g L-1 as
compared to 10 to 160 g L-1 in maize and 15 to 360 g L-1 in wheat
(Gómez-Galera et al., 2010); however, most maize genotypes do
not reach the highest values (Ortiz-Monasterio et al., 2007). Based
on available the literature, there is scanty information on the
development of rice genotypes with iron-enriched grains through
conventional breeding programs. However, the methodology is
well established and genetic variation exists. Masuda et al. (2013)
reported seven transgenic approaches and combinations, which
can be used to increase the concentration of iron in rice seeds. The
first approach involves enhancing iron accumulation in rice seeds
by expressing the ferritin gene under the control of endospermspecific promoters. The iron stored in soybean ferritin is readily
absorbed by the human gastrointestinal tract (Lonnerdal, 2009),
and iron stored in ferritin is an important source that humans can
use to avoid iron deficiency (Theil et al., 2012).
The second approach is to increase iron concentrations in
rice through over expression of the nicotianamine synthase gene
(NAS). Nicotianamine, which is a chelator of metal cations, such
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doi: 10.7831/ras.3.1
as Fe+2 and zinc (Zn+2), is biosynthesized from methionine via
S-adenosyl methionine synthase (SAMS) and NAS (Higuchi et
al., 1994). Hell and Stephan (2003) and Takahashi et al. (2003)
reported that all higher plants synthesize and utilize nicotianamine
for the internal transport of iron and other metals. Rice has three
NAS genes: OsNAS1, OsNAS2, and OsNAS3. These genes are
differentially regulated by iron, and all of them are expressed in
cells involved in the long-distance transport of iron (Inoue et al.,
2003). Masuda et al. (2013) suggested that, in addition to their
roles in phytosiderophore synthesis, NAS and nicotianamine play
important roles in the long-distance transport of iron in rice.
The third approach is to increase iron concentrations in
rice and to enhance iron influx to seeds by expressing the Fe+2nicotianamine transporter gene OsYSL2. Koike et al. ( 2004 )
identified the rice OsYSL2 gene. This gene is preferentially
expressed in leaf phloem cells, the vascular bundles of flowers,
and developing seeds, which suggests a role in internal iron
transport. The iron concentration in OsYSL2 knockdown rice
was 18% lower in brown seeds and 39% lower in polished seeds
compared to non-transgenic rice (Ishimaru et al., 2010). Masuda
et al. (2013) hypothesized that enhanced expression of OsYSL2
could increase the iron concentration in rice seeds.
The fourth approach to iron biofortification involves enhancing
iron uptake and translocation by introducing genes responsible
for biosynthesis of MAs. The iron concentrations in the seeds of
transgenic lines were analyzed after cultivation in the paddy field in
iron-sufficient or low (calcareous) soil (Masuda et al., 2008; Suzuki
et al., 2008). Three transgenic rice lines, which were transformed
with barley genome fragments involving mugineic acid synthase
genes (HvNAS1 or HvNAS1 and HvNAAT-A,-B or IDS3) were
produced (Higuchi et al., 2001b; Kobayashi et al., 2001; Masuda et
al., 2008; Suzuki et al., 2008). Masuda et al. (2008) reported after
cultivation in iron-sufficient soil, the IDS3 rice lines produced iron
concentrations that were 1.4-fold and 1.3-fold higher in the polished
and brown seeds than in non-transgenic rice, respectively.
The fifth approach to enhance iron uptake from soil is the
over expression of the OsIRT1 or OsYSL15 iron transporter
genes. Lee et al. (2009a) produced transgenic rice that expressed
the rice ferric ion transporter gene OsIRT1 under the control of
the ubiquitin promoter. This rice showed a 13% increase in iron
concentration in the brown seeds, while the iron concentration
in the leaves increased 1.7-fold. Lee et al. (2009a) reported that
plants that over expressed OsIRT1 were shorter and had fewer
tillers. As constitutive expression of OsIRT1 may disturb metal
homeostasis in rice, they suggested that targeted expression
of OsIRT1 using specific promoters might solve this problem.
Masuda et al. (2013) concluded that OsIRT1 could be used to
enhance iron levels in rice grains. Lee et al. (2009b) reported that
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OsYSL15 over expression using the OsActin1 promoter increased
the concentration of iron in brown seeds by approximately 1.3-fold
compared with non-transgenic rice. Gómez Galera et al. (2012)
produced transgenic rice that overexpressed the barley Fe (III)MA transporter gene HvYS1 under the control of the CaMV35S
promoter. The concentration of iron in the transgenic leaves was
1.5-fold higher than in the non-transgenic leaves.
The sixth approach to enhanced iron uptake and translocation
is over expression of the iron homeostasis-related transcription
factor OsIRO2. Ogo et al. (2006) identified an iron deficiencyinducible basic helix-loop-helix ( bHLH ) transcription factor,
OsIRO2, in rice. OsIRO2 is responsible for the regulation of
key genes involved in MAs-related iron uptake (e.g., OsNAS1,
OsNAS2, OsNAAT1, OsDMAS1, TOM1, and OsYSL15) (Ogo et
al. 2007; Ogo et al. 2011). Ogo et al. (2007) introduced OsIRO2
under the control of the CaMV35S promoter into rice plants.
Plants with the overexpressed OsIRO2 transcription factor
secreted more DMA than non-transgenic rice, and they exhibited
enhanced iron deficiency tolerance in calcareous soils (Ogo et al.,
2007; Ogo et al., 2011). Moreover, the iron concentration in the
transgenic brown seeds increased 3-fold when the transgenic rice
was cultivated in calcareous soil (Ogo et al., 2011). Therefore, this
approach can be used to increase the iron concentrations of seeds
in soils with low iron availability.
The seventh approach to enhanced iron translocation from
flag leaves to seeds utilizes the knockdown of the vacuolar iron
transporter gene OsVIT1 or OsVIT2. Kim et al. (2006) reported
that the Arabidopsis vacuolar iron transporter, VIT1, is highly
expressed in developing seeds, and it transports Fe and Mn into
the vacuole. Zhang et al. (2012) reported that disruption of the
rice VIT orthologs ( OsVIT1 and OsVIT2 ) increased the iron
concentrations by 1.4-fold in brown seeds, and it decreased the
iron concentrations by 0.8-fold in the source organ flag leaves
because VIT genes are highly expressed in rice flag leaves.
Bashir et al. (2013) reported that an OsVIT2-knockdown mutant
showed 1.3-fold and 1.8-fold increases in iron concentrations in
the brown and polished rice seeds, respectively. They suggested
that disruption of OsVIT1 or OsVIT2 enhanced iron translocation
between the source and sink organs, and proposed this as a novel
strategy for producing iron-biofortified rice. Zhang et al. (2012)
and Bashir et al. (2013) reported that the cadmium concentration
was also increased following VIT knockdown in rice. Therefore,
this approach should be avoided in cadmium-contaminated soils.
The mining of high iron rice varieties or the identification of
novel target genes is important to the iron biofortification of rice.
Anuradha et al. (2012) found seven quantitative trait loci (QTL) and
selection markers related to the iron concentrations in rice seeds.
They mapped the QTL using Madhukar × Swarna indica rice
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varieties, and then identified genes related to iron homeostasis (e.g.,
OsYSLs, OsNASs, OsNRAMP1, OsIRT1, OsZIPs, and APRT)
as candidate genes that effect iron concentrations seeds. Sperotto
et al. (2010) analyzed the gene expression profiles of 25 metalrelated genes, including rice homologues of YSL2, NRAMPs,
ZIPs, IRT1, VIT1, NASs, FROs, and NAC5, in eight rice varieties
with different iron and zinc concentrations in the seeds. They also
identified putative target genes that contributed to increased iron
and zinc concentrations in rice grains. Xiong et al. (2014) indicated
that IRT1 is a key component of iron uptake from the soil in dicot
plants. They introduced the peanut (Arachis hypogaea L.) AhIRT1
into tobacco and rice plants using an iron-deficiency-inducible
artificial promoter. Induced expression of AhIRT1 in tobacco plants
resulted in the accumulation of iron in young leaves under irondeficient conditions. Even under iron-excess conditions, the iron
concentration was also markedly enhanced, which suggests that
the iron status did not affect the uptake and translocation of iron by
AhIRT1 in the transgenic plants. They observed that the transgenic
tobacco plants showed improved tolerance to iron limitation in
culture with two types of calcareous soils. The induced expression
of AhIRT1 in rice plants also resulted in high tolerance to low iron
availability in calcareous soils. Induction of AhIRT1 expression into
tobacco plants also affected zinc and manganese concentrations in
both roots and young leaves of the transgenic plants as compared to
non-transgenic plants during iron starvation. The results suggested
that the accumulation of AhIRT1 in transgenic plants disturbed the
zinc, manganese, and copper uptake and/or translocation (Pedas et
al., 2008).
Interaction of Iron with Other Nutrients
Other nutrients may not only play an important role in reducing
the effects of iron toxicity but also in the expression of iron tolerance
by various rice cultivars (Sahrawat, 2004). Iron toxicity is a complex
nutrient disorder, and the deficiencies of other nutrients (especially
P, K, Ca, Mg, and Zn) are considered when instances of iron toxicity
occur in rice (Ottow et al., 1983). Deficiencies of Ca, Mg, and Mn
are not commonly observed in lowland rice, except in acid sulfate
soils. Therefore, P, K, and Zn deficiencies deserve special attention
(Yoshida, 1981). In aerobic conditions, iron in the soil is usually
found as oxyhydroxide polymers with very low solubility, which
limits the iron supply for plant uptake (especially in calcareous
soils). Therefore, iron deficiency is a yield-limiting factor with major
implications for field crop production in many agricultural regions
of the world (Hansen et al., 2006). The expression of chlorosis may
be due to the deficiency of iron interactions with micronutrients like
Zn and Mn (Dixit and Yamdagni, 1983). Ferrihydrite is the inorganic
compound usually associated with iron accumulation in ferritin
(Chasteen and Harrison, 1999). Ferritins are large proteins with a
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central cavity that can store up to 4500 iron atoms, which can be
released when necessary (Yamashita, 2001). Therefore, these proteins
are believed to play a critical role in the cellular regulation of iron
storage and homeostasis (Zancani et al., 2004), because expression of
some plant ferritin isoforms can be induced by iron overload (FobisLoisy et al., 1995; Petit et al., 2001). Chen et al. (1980) identified
both goethite (α-FeOOH) and lepidocrocite (γ-FeOOH) in rice
root coatings. Furthermore, they found that under iron-deficient
conditions, phosphorous concentrations decreased in the roots of
rice cultivars and increased in the shoots of rice plants, which had
lower Zn concentrations in their roots (Murad and Schwertmann,
1984). Selviera et al. (2007) noted increased calcium concentrations
when the roots were iron-deficient. Several iron transporters are
able to transport iron along with Zn and other metals (Korshunova
et al., 1999; Eckhardt et al., 2001; Gross et al., 2003; Lopez-Millan
et al., 2004). The induction of iron transporters under iron-deficient
conditions resulted in increased zinc uptake. Mn concentrations
decreased under iron deficiency in the roots and shoots of plants,
and Mn can be transported by the plant through iron transporters
(Eckhardt et al., 2001; Lopez-Millan et al., 2004). Iron deficiency
resulted in lower sulfur concentrations in the roots and shoots of plant
varieties, and this is probably a consequence of the iron requirements
for sulfur assimilation (Hell and Stephan, 2003). Furthermore, Cu
concentrations decreased in the roots of both cultivars and in the
shoots of rice plants under iron-deficient conditions. In the Poaceae
family, iron deficiency induces the synthesis and exudation of
phytosiderophores (PS), which bind both iron and copper. The Cu-PS
complex can be transported into root cells by the Fe-PS transporter,
although with lower affinity (Briat et al., 1995). At high iron
concentrations, phosphorus concentrations increased considerably
in the roots. Higher amounts of iron oxides that accumulated in the
roots are capable of absorbing anions such as phosphates (Zhang et
al., 1999). In shoots, the phosphorous amounts decreased in plants
under iron excess, which suggests that there was limited phosphorous
translocation to the shoots. Moreover, there was likely limited uptake
of apoplast phosphorous. Howeler (1973) stated that phosphorous
precipitation in the apoplast of the root results in lower phosphorous
absorption by the plant. Calcium concentrations decreased under the
excess iron treatment in roots and shoots, and Selveira Vivian et al.
(2007) found no reports on manganese deficiency levels in the roots
of rice plants at high iron levels. Precipitation of manganese in the
iron plaque may have resulted in its lower absorption by the sensitive
cultivar, where the highest iron concentrations were found. Negative
interactions between iron and manganese have been reported in
plants (Fageria, 2003), and the potassium concentration decreased in
the shoots under iron excess relative to the control (Neue et al., 1998).
Sulfur concentrations were lower in the shoots of plants exposed to
excess iron.
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Genes Responsible for Crop Productivity
Iron is an essential micronutrient, and the expression of genes
involved in iron transport is regulated by iron availability and
demand. Most previous studies have compared the expression of
genes in response to iron deficiency (Mori, 1999; Kobayashi and
Nishizawa, 2012; Bashir et al., 2013). However, the expression of
genes involved in iron transport is also regulated in response to high
iron demand at different developmental stages. Among the abiotic
stresses, iron deficiency constitutes a major factor leading to a
reduction in crop yield due to the high pH, especially in calcareous
soils with extremely low iron solubility (Kobayashi et al., 2005).
They reported that the expression of genes encoding every step in
the methionine cycle was thoroughly induced by iron deficiency
in roots, and almost thoroughly induced in the leaves. The rice
genes involved in iron acquisition are coordinately regulated by
conserved mechanisms in response to iron deficiency, in which iron
deficiency inducible (IDE)-mediated regulation plays a significant
role. A promoter search revealed that iron deficiency-induced
genes associated with iron uptake possessed sequences that were
homologous to the iron deficiency-responsive cis-acting elements
IDE1 and IDE2 in their promoter regions, which were identified at
a higher rate than those showing no induction under iron deficiency.
Kobayashi et al. (2005) and Paz et al. (2007) reported that two
major mechanisms of iron acquisition studied in plants are based on
either the reduction of organic ferric iron chelates via membraneassociated ferrireductase or the release of phytosiderophores that
bind ferric ions and introduce them into the cell. Plant ferritin is
synthesized as a precursor containing a unique amino acid sequence
composed of over 70 residues at the N-terminal, followed by
a region that is relatively conserved among other ferritins. The
first part of this region is known as transit peptide (TP), which is
responsible for plastid targeting and is processed upon entry into
the plastid. The second part is known as the extension peptide,
which may be lost in the germination process (Ragland et al., 1990).
The first and second ferritins consist of about 40 and 30 amino
acid residues, respectively. The conserved region neighboring
the extension peptide has been shown to have 40–50% sequence
identity with mammalian ferritins.
Genetic improvement of iron content and stress adaptation in
plants using the ferritin gene has been reviewed (Goto et al., 2001),
and the gene transfer technique has been a revolutionary tool
for quickly creating novel varieties. The plants that have had the
ferritin gene introduced possess two particular advantages: 1) the
storage of excess iron and other elements and 2) the cancellation
of oxidative stress. There are two possibilities to create useful
plants using the exogenous ferritin gene in this review. One is
iron-fortified plants used to overcome iron deficiency in humans,
and the other is plants that have resistance to heavy metals,
©2015 Reviews in Agricultural Science
Iron is an essential nutrient that plays a critical role in lifesustaining processes. Due to its ability to gain and lose electrons,
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Conclusions
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pathogens, and other stresses or those that exhibit enhanced
growth. These genetic improvements could lead to increased iron
content or stimulated growth. However, the mechanism of iron
storage and the scavenger system for oxidative stress using ferritin
gene expression have not been determined. An understanding at a
physical and molecular level is now necessary to take advantage
of the ferritin gene at an advanced stage. In non-graminaceous
plants, the Fe II-transporter gene and ferric-chelate reductase
gene have been cloned from A. thaliana, but Fe +2-reductase
has not been cloned. In graminaceous monocots, the genes for
mugineic acid (MAs) synthesis, nicotianamine synthase (nas)
and nicotianamine aminotransferase (naat), have been cloned
form barley, whereas the Fe+3-MAs transporter gene has yet to be
cloned. Transferrin absorption in Dunaliella has been reported,
suggesting a phagocytic (endocytic) iron-acquisition mechanism.
In rice, the overexpression of OsIRO2 resulted in increased MAs
secretion, but the repression of OsIRO2 resulted in lower MAs
secretion and hypersensitivity to iron deficiency. Northern blots
revealed that the expression of genes involved in the Fe (III)MAs transport system was dependent on OsIRO2 (Mori, 1999;
Kobayashi et al., 2005; Ogo et al., 2009). The expression of the
genes for NAS, a key enzyme in MAs synthesis, was notably
affected by the level of OsIRO2 expression. Furthermore, a
microarray analysis demonstrated that OsIRO2 regulates 59 irondeficiency-induced genes in roots. Some of these genes, including
two transcription factors that were upregulated by iron deficiency,
possessed the OsIRO2 binding sequence in their upstream regions.
OsIRO2 possesses a homologous sequence of the iron deficiencyresponsive cis-acting element in its upstream region (Ogo et al.,
2009). Three NAS genes have been identified (OsNAS1-3) in
rice, and they are reported to catalyze the formation of NA (Inoue
et al., 2003). OsNAAT1 converts NA to a 3'-keto intermediate
(Inoue et al., 2008), which is further converted to deoxymugineic
acid (DMA) by OsDMAS1 (Bashir and Nishizawa, 2006; Bashir
et al., 2006). In rice, this is secreted to the rhizosphere by TOM1
(Nozoye et al., 2011), where it binds to Fe+3 and is absorbed by
OsYSL15 (Inoue et al., 2009). The role of YSL family transporters
in iron transport is well characterized. The rice genome contains
18 putative YSL family genes ( Koike et al., 2004 ) , among
which OsYSL2, OsYSL15, OsYSL16, and OsYSL18 have been
characterized (Aoyama et al., 2009; Inoue et al., 2009; Kakei
et al., 2012; Zheng et al., 2012). OsYSL2 is a Mn-NA and FeNA transporter (Koike et al., 2004). These genes will contribute
greatly to an understanding of the regulatory mechanisms.
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iron works as a cofactor for enzymes involved in a wide variety
of oxidation-reduction reactions (i.e., photosynthesis, respiration,
hormone synthesis, DNA synthesis, etc.). This function makes
iron an essential nutrient, and its deficiency causes iron chlorosis,
which seriously constrains normal plant development. Iron
toxicity in plants is indicated by bronzing characteristics, which
have been observed in plants grown in greater than 100 mM iron
solutions. Higher iron uptake by plants reduces protein synthesis
in leaves. Ferritin is considered crucial for iron homeostasis, and
it consists of a multimeric spherical protein called phytoferritin,
which is able to store up to 4500 iron atoms inside its cavity
in non-toxic form. A resistant variety may accumulate a larger
amount of phytoferritin, which forms a complex that reduces iron
toxicity. Large amounts of iron in plants are responsible for protein
degradation, because iron may lead to the formation of reactive
oxygen radicals that are highly phytotoxic and cause protein
degradation. Iron chlorosis is a widespread problem, especially for
regions where the bioavailability of iron in the soil is low. Usual
remediation strategies consist of amending iron to soil, which
is an expensive practice. Thus, genetically improved chlorosisresistant rootstocks and new cultivar combinations offer the best
solution to iron chlorosis, and it is one of the most important
lines of investigation needed to prevent this nutritional problem.
Therefore, there is a need for new methods to diagnose and correct
this nutritional disorder. The use of microarray techniques revealed
the changes in gene expression levels due to iron deficiency,
and it has allowed insights into the transcriptional regulation of
some functions. These studies have extended our knowledge of
stress responses to iron deficiency, and have identified candidate
genes and processes for further experimentation to increase our
understanding of iron deficiency stress. It is likely that more
extensive microarray analyses, coupled with suitable annotations
of completely sequenced genomes, will prove valuable in future
studies of iron stress responses in plants. Novel gene regulation
networks for iron deficiency responses include iron deficiencyinducible basic helix-loop-helix transcription factors (OsIRO2),
iron deficiency-responsive cis-acting elements (IDEs), and the
two transcription factors. The identification of the trans-acting
factors responsible for the pathways will contribute greatly to an
understanding of the regulatory mechanisms, and these factors
will also prove beneficial to plants under iron-deficient conditions.
Acknowledgement
The authors wish to acknowledge to the Department of Science
and Technology, Government of Odisha for financial assistance.
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