role of iron in plant growth and metabolism

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Please cite this articles as:Rout and Sahoo, Reviews in Agricultural Science, 3:1-24, 2015.doi: 10.7831/ras.3.1

Received: January 7, 2015. Accepted: March 1, 2015. Published on line: May 19, 2015.Correspondence to G.R.R: [email protected]©2015 Reviews in Agricultural Science

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ROLE OF IRON IN PLANT GROWTH AND METABOLISMGyana R. Rout and Sunita SahooDepartment of Agricultural Biotechnology, College of Agriculture, Orissa University of Agriculture & Technology, Bhubaneswar 751 003, Odisha, India

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IntroductionHeavy 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

ABSTRACTIron 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

Please cite this articles as:Rout and Sahoo, Reviews in Agricultural Science, 3:1-24, 2015.

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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

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 GrowthIron 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 iron-regulated transporter (IRT1). Ishimaru et al. (2011) reported that

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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.

Effects of Iron on Plant MetabolismWhen 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

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 (heme-iron 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 mitochondria-targeting 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

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. Cell-wall-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. Cell-wall 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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the biosynthesis of heme. Iron appears to control the rate of delta-aminolevulinic 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 iron-nitrosyl 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 redox-related 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.

Distribution of Iron in PlantsIron uptake by plants is fastest when iron is present in the

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 Rŭmheld 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 growth-promoting 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). Rŭmheld and Marschner (1985, 1986) proposed that iron uptake occurs by two species-dependent strategies. Strategy I refer to iron mobilization by dicots and non-gramineous 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

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

(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 foliar-applied 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 PlantsIron 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 iron-induced 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.

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 MorphologyNumerous 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,

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 ActivityIron 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 (Abdel-Kader, 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

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 alpha-ketoglutarate 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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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 half-life 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).

Iron Deficiency in PlantsIron 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;

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 PlantsIron 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 endosperm-specific 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

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+2- nicotianamine 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 deficiency-inducible 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

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 metal-related 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 iron-deficient 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 NutrientsOther 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 (Fobis-Loisy 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.

Genes Responsible for Crop ProductivityIron 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 membrane-associated 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,



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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 FeII-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 iron-deficiency-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 deficiency-responsive 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 Fe-NA transporter (Koike et al., 2004). These genes will contribute greatly to an understanding of the regulatory mechanisms.

ConclusionsIron is an essential nutrient that plays a critical role in life-

sustaining processes. Due to its ability to gain and lose electrons,

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 chlorosis-resistant 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 deficiency-inducible 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.

AcknowledgementThe authors wish to acknowledge to the Department of Science

and Technology, Government of Odisha for financial assistance.

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role of iron in plant growth and metabolism

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