Acquisition and Homeostasis of Iron in Higher Plants and Their Probable Role in Abiotic Stress Tolerance
Durgesh K. Tripathi1,2* 
Shweta Singh3 
Shweta Gaur3 Swati Singh3 
Vaishali Yadav3 Shiliang Liu4 
Vijay P. Singh5* 
Shivesh Sharma2,6 Prateek Srivastava7 
Sheo M. Prasad8 Nawal K. Dubey1 
Devendra K. Chauhan3* Shivendra Sahi9- 1Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, India
- 2Centre for Medical Diagnostic and Research, Motilal Nehru National Institute of Technology, Allahabad, India
- 3D. D. Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Allahabad, India
- 4Division of Plant Sciences, University of Missouri, Columbia, MO, United States
- 5Government Ramanuj Pratap Singhdev Post Graduate College, Baikunthpur, India
- 6Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Allahabad, India
- 7Amity Institute of Environmental Sciences, Amity University Uttar Pradesh, Noida, India
- 8Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Allahabad, India
- 9Department of Biological Sciences, University of the Sciences, Philadelphia, PA, United States
Iron (Fe) is a micronutrient that plays an important role in agriculture worldwide because plants require a small amount of iron for its growth and development. All major functions in a plant's life from chlorophyll biosynthesis to energy transfer are performed by Fe (Brumbarova et al., 2008; Gill and Tuteja, 2011). Iron also acts as a major constituent of many plant proteins and enzymes. The acquisition of Fe in plants occurs through two strategies, i.e., strategy I and strategy II (Marschner and Römheld, 1994). Under various stress conditions, Nramp and the YSL gene families help in translocation of Fe, which further acts as a mineral regulatory element and defends plants against stresses. Iron plays an irreplaceable role in alleviating stress imposed by salinity, drought, and heavy metal stress. This is because it activates plant enzymatic antioxidants like catalase (CAT), peroxidase, and an isoform of superoxide dismutase (SOD) that act as a scavenger of reactive oxygen species (ROS) (Hellin et al., 1995). In addition to this, their deficiency as well as their excess amount can disturb the homeostasis of a plant's cell and result in declining of photosynthetic rate, respiration, and increased accumulation of Na+ and Ca− ions which culminate in an excessive formation of ROS. The short-range order hydrated Fe oxides and organic functional groups show affinities for metal ions. Iron plaque biofilm matrices could sequester a large amount of metals at the soil–root interface. Hence, it has attracted the attention of plant physiologists and agricultural scientists who are discovering more exciting and hidden applications of Fe and its potential in the development of bio-factories. This review looks into the recent progress made in putting forward the role of Fe in plant growth, development, and acclimation under major abiotic stresses, i.e., salinity, drought, and heavy metals.
Introduction
Abiotic stress is a result of several environmental disturbances caused by the continuous encroachment of industrialization, urbanization, and some human interference with the natural ecosystem that influence the quality and quantity of agriculture production per year (Mantri et al., 2012). Abiotic stresses include heat, cold, freezing, drought, salinity, flooding agents, UV, and heavy-metal stresses that have significant impacts on a plant life cycle (Macedo, 2012; Mantri et al., 2012; Singh et al., 2015, 2017; Tripathi et al., 2016c). These stresses not only affect plant biodiversity and productivity but also can interfere with the food web and the ecosystem. Abiotic stresses are worldwide problems as they decline the crop yield (Cramer et al., 2011). Moreover, the presence of heavy metals in food crops causes some severe diseases like cancer and asthma (Brigham et al., 2015). Plants, being the most precious gift of the nature that fulfill several basic requirements of human beings, are severely affected by various abiotic stress factors. Abiotic stress causes significant reduction in growth and yield of plants via inducing oxidative stress through enhanced reactive oxygen species (ROS) production and by lowering the antioxidant activities, level of nutrients, and modification of anatomical structures (Nagajyoti et al., 2010; Nazar et al., 2012; Vaculík et al., 2012; Singh et al., 2015; Tripathi et al., 2016b, 2017a). Hoagland and Arnon (1950) pioneered the most popular and commercial technique for developing plants with their roots in solutions containing mineral nutrients required for the growth of plants.
Various techniques are being used to protect plants from the adverse effects of abiotic stresses, which include exogenous supplementations of silicon, nitric oxide, growth-promoting hormones, enzymes, and nutrient management (Nagajyoti et al., 2010; Nazar et al., 2012; Tripathi et al., 2012, 2016a, 2017a,b,c,d; Vaculík et al., 2012; Saxena and Shekhawat, 2013). Among the remedies for abiotic stress, nutrient regulations or management are considered as the cost effective and eco-friendly techniques (Tripathi et al., 2015; Yadav et al., 2016). It has been reported that plant nutrients (micro and macro) play important roles in growth and development (White and Brown, 2010; Waraich et al., 2011; Tripathi et al., 2014, 2015). Therefore, an adequate and balanced supply of nutrients at the correct time is required for the proper growth and development of plants, maintenance of better soil fertility, and preservation of an intensive cropping system to maintain the global food production, particularly in developing countries (Dordas, 2009; Hansch and Mendel, 2009; Sarwar et al., 2010; Moharana et al., 2012; Waraich et al., 2012). In addition, studies also showed that an exogenous supply of nutrients plays a crucial role in the enhancement of plant tolerance against various abiotic stresses (Pankovic et al., 2000; Hassan et al., 2005; Tlustos et al., 2006; Dheri et al., 2007; Sarwar et al., 2010). Some nutrients such as calcium (Ca), magnesium (Mg), sulfur (S), zinc (Zn), and iron (Fe) have shown significant results when they are examined under salinity, drought, and heavy-metal stresses (Sarwar et al., 2010; Singh et al., 2011; Nazar et al., 2012). Currently, the application of Fe as a nutrient supplement and its role in imparting tolerance to plants against abiotic stresses are gaining attention as an area of research. Some studies suggested that the application of Fe reflects significant and/or potential impacts in alleviating the stress imposed by metal ions (Liu et al., 2007; Yadav et al., 2007; Garnier et al., 2010; Emamverdian et al., 2015).
Iron—the fourth most abundant and essential microelement on the earth's crust—is unavailable to higher plants, largely due to neutral and alkaline soils because of its existence in an insoluble form (Shao et al., 2007). In the plant system, Fe is regarded as an essential element in regulating life-sustaining processes like respiration, photosynthesis, chloroplast development, and chlorophyll biosynthesis where it takes part in electron transportation (Kim and Guerinot, 2007). Inadequate Fe supply in plants causes iron-deficiency, which results in decline in crop yields, interveinal chlorosis in plant leaves, etc. (Kim and Guerinot, 2007; Lan et al., 2011). In addition, excess levels of Fe can be fatal for plant health and productivity (Anjum et al., 2015). Therefore, an appropriate supply of Fe is needed for sustaining plant productivity under stress as well as non-stress conditions. It has been reported that out of the total cultivated areas of the world, one-third has Fe deficiency (Kim and Guerinot, 2007), which is causing significant decline in yield of crops every year. Iron is a chief component of the cell redox systems and also acts as a cofactor of various antioxidant enzymes like catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX) (Marschner, 1995; Sharma et al., 2004; Kumar et al., 2010). Therefore, Fe homeostasis plays a crucial role in the life cycle of plants under stressed conditions (Figure 1) (Gratao et al., 2005; Meda et al., 2007; Sarwar et al., 2010). In addition to overviewing major Fe acquisition strategies in plants, this review briefly appraises the literatures available on the role of Fe in plants exposed to major abiotic stresses like salinity, drought, and heavy metals. Less discussed topics in the current context have also been highlighted.
Figure 1. Different Strategies adopted by higher plant for Iron Acquisition. Strategy I occurs in the members of non-graminaceous plants (Left) and Strategy II occurs in the members of graminaceous plants (Right). Ovals corresponds the transporters and enzymes involved that play significant roles in both the strategies. The expression of these genes shown in the present figure occurs in response to Fe deficiency (Modified from; Kobayashi and Nishizawa, 2012).
Iron Acquisition Strategies in Plants
Despite being categorized as the fourth most abundant element of the earth's crust, the availability of Fe to plants is highly heterogeneous as it has low solubility under aerobic conditions, particularly at high pH and in calcareous soil. Plants firmly regulate the homeostasis of Fe and respond to the shortage as well as the surplus level of Fe (Morrissey and Guerinot, 2009). Therefore, in order to maintain proper ion homeostasis, plants stabilize the uptake, transport, and storage (Grotz and Guerinot, 2006). Hence, for the significant acquisition and agglomeration of Fe, plants have developed two different strategies (strategy I and II) under varied soil conditions (Römheld and Marschner, 1986) (Figure 1). Almost all higher plants except the members of family Gramineae follow Strategy I for Fe uptake (Kobayashi and Nishizawa, 2012) (Figure 1). The uptake and accumulation of Fe is frequently enhanced by three reactions: firstly, the secretion of protons through the plasmalemma P-type ATPase in order to acidify the surrounding solution for augmenting the solubility of Fe3+; secondly, by reducing Fe3+ to the more soluble Fe2+ form through Fe3+ chelate reductase; and thirdly, by plasmalemma transport of Fe2+ through Fe transporters (Figure 1). The dominant gene essential for these processes was first cloned from Arabidopsis thaliana and peas such as FRO2, allelic to the frd1 mutation distressing Fe3+-chelate reductase activity (Robinson et al., 1999), and FRO1, respectively (Waters et al., 2002). Furthermore, reduced form of iron in the plants transported from the root via IRT1 (divalent cation transporter) (Eide et al., 1996; Eckhardt et al., 2001), which is a member of the ZIP family (Guerinot, 2000). In addition, IRT1 is also reported as an essential gene because, in the case of excess supplementation of exogenous iron, it reduces the lethality of seedlings and suppresses the chlorosis in irt 1 mutants (Henriques et al., 2002; Varotto et al., 2002; Vert et al., 2002). Moreover, Vert et al. (2002) and Dinneny et al. (2008) observed that the acquisition of Fe starts from the epidermal layers of the root, which is proven by the expression pattern of IRT1 and FRO2. The transporter gene IRT1, which is responsible for Fe transport, has been cloned from Arabidopsis (Eide et al., 1996; Dubeaux et al., 2015) and its ortholog RIT1 has been cloned from pea and tomato as well (Cohen et al., 1998; Eckhardt et al., 2001). Fe3+-chelate reductases are integral membrane-bound proteins and they belong to the family of proteins that are responsible for the transport of electrons from cytosolic NADPH to FAD and, consequently, through heme groups to electron acceptors located on the outer side of the plasma membrane (Figure 1). In response to Fe deficiency, the up-regulation of the FRO gene has been noted in roots (Robinson et al., 1999; Waters et al., 2002). On the basis of the recent studies, IRT1 has been marked as the major transporter gene responsible for the uptake of Fe from soil solutions (Figure 1). Besides this, IRT1 also plays significant role in the transport of Zn, Mn, Co, and Cd (Rogers et al., 2000). Similarly, PEZ1 is a novel effluxer responsible for the xylem loading of phenolics as well as the remobilization of precipitated apoplasmic Fe in the plant cell. This is due to the fact that FRD3, FRDL1, and PEZ1 are efflux Fe-chelating molecules in their Fe liberated forms and Fe efflux occurs in the xylem sap by more than one transporters (Ishimaru et al., 2011). Morrissey et al. (2009) described the role of ferroportin 1/iron regulated 1 (AtFPN1/AtIREG1) metal efflux protein function in Fe homeostasis in Arabidopsis plants, which is similar to the iron efflux transporter in mammals and are responsible for Fe absorption in the intestines and Fe recycling in macrophages. While the active role of AtFPN1 localized on the plasma membrane has not yet been reported, its promoter activity is prominently seen in the stele region of plants. In addition, its mutant species showed the loss of chlorophyll content in both Fe-sufficient and Fe-deficient media, which signify its indispensable role in acquisition of Fe to shoots (Morrissey et al., 2009) as well as mitochondrial Fe metabolism and trafficking progress via the mitochondrial Fe storage protein (mitochondrial ferritin) and transport (mitoferrin-1 and -2) (Richardson et al., 2010).
Strategy II is exclusively specific to the Gramineae family and is based on the biosynthesis and secretion of mugineic acids (MAs) (Figure 1). The roots of graminaceous plant release phytosiderophores (PSs), which are responsible for the chelation of Fe3+ in the rhizosphere. Specific transporter proteins located on the plasma membrane transport Fe3+ PS complexes in the cytosol (Römheld and Marschner, 1986). In response to Fe deficiency, both processes are enhanced through up-regulation of the underlying genes (Figure 1). Until now, nine different kinds of MAs have been recognized, which have been produced via a conserved pathway from S-adenosyl-L-methionine (Bashir et al., 2006; Ueno et al., 2007; Kobayashi and Nishizawa, 2012). Through sequential enzymatic reaction mediated by the precursors of MAs such as NAS, NAAT, DMAS, and DMA, strategy II enhanced acquisition of Fe in graminaceous plant (Figure 1). Normally, the transportation of Fe in plants may be seen in the anatomical structures of roots when observed under the Phase-contrast microscopy. It can be well observed that the deposition percentage of Fe in root cells is increased by the increased level of Fe concentration.
After the acquisition of Fe inside the root, its translocation occurs across the plasma membrane through several different members of transporter families that are responsible for the transportations of intra- and intercellular ions (Figure 2). Such transporters include Nramp and YSL families (Grotz and Guerinot, 2006). The Nramp family leads the translocation of divalent cations, whereas the members of the YSL family are probably only responsible for the translocation of metal chelates (Conte and Walker, 2011). Members of the NRAMP family are responsible for the transportation of an array of metals across the plasma membranes including Mn2+, Zn2+, Cu2+, Fe2+, Cd2+, Ni2+, and Co2+ in microorganisms, plants, and animals (Nevo and Nelson, 2006). In plants, the expression of Nramp transporters has been located in roots and shoots and is responsible for the transportation of metal ions across plasma membranes and the tonoplast (Krämer et al., 2007). In A. thaliana, NRAMPs facilitate the transport of Fe and Cd. NRAMP1 displays a significant role in the transport and homeostasis of Fe. Besides this, members of the YSL family mediate the acquisition of Fe through the translocation of Fe3+ phytosiderophore complexes (Curie et al., 2001). In addition, CDF transporters have also been recognized recently that lead to the transportation of metal ions (in divalent form) in prokaryotes (Nies, 1992) and also in several eukaryotes (Montanini et al., 2007). The apoplast sometime plays an important role in ion uptake into the cells and also performs some important physiological roles in nutrient transport and storage (Sattelmacher and Horst, 2007).
Figure 2. Hypothetical respesentation of exogenous application of Fe and its accumulation from root to shoot, which ultimately decreases the over production of oxidative stress level in plants caused by abiotic stresses.
In addition to this, Deiana et al. (1992) studied homeostasis, kinetics, and the consequences of mechanisms of Fe uptake in plants. Römheld and Marschner (1983) reported that when Fe was found in very high concentrations, caffeic acid plays a very active role in Fe mobilization at the interface of the soil-root. Caffeic acid is the phenolic compound produced from plants (Whitehead et al., 1981, 1983; Olsen et al., 1982; Wei Jin et al., 2008) that functions in the reduction of Fe3+ and takes part in redox reactions near rhizosphere and free spaces (Brown and Ambler, 1973; Olsen et al., 1981; Deiana et al., 1992). Deiana et al. (1992) reported that the concentration of Fe3+ is directly proportional to the yield of Fe2+, i.e., on increasing the Fe3+ concentration. The yield of Fe2+ also increased the value higher than 9 for Fe(III)/CAF molar ratios. Deiana et al. (1992) also found that one molecule of the phenolic plant product (CAF) is capable of reducing the nine electrons of the Fe3+ ion to the Fe2+ ion, and they also demonstrated that the whole reaction mechanism involves two steps. The first one includes the formation of the Fe3+ ion from organic molecules. This reaction is faster and involves the transfer of five electrons, whereas the second one includes the transfer of four electrons with a comparatively slower reaction (Deiana et al., 1992).
Iron and Abiotic Stress Tolerance in Plants
Iron and Salinity Stress
Salinity is one of the most challenging issues of the present time that poses great constraint to agricultural productivity worldwide (Ashraf, 1994; Khan and Gulzar, 2003; Asraf and Harri, 2004; Parihar et al., 2015). Salinity effects are more pronounced in arid and semiarid regions of the world (Bradbury and Ahmad, 1990). It has been estimated that approximately 20% of the total cultivated land is affected by salt stress annually. Likewise, nearly half of the world's irrigated land is being affected by salinity and water-logging conditions (FAO, 2008; Munns and Tester, 2008; Talei et al., 2012). Furthermore, agricultural practices without appropriate water management are another problem that is responsible for extensive salinization in crop lands (Taiz and Zeiger, 2006).
Plant exposure to high salinity induces several detrimental effects on plants as it triggers a wide range of changes at physiological, biochemical, and molecular levels (Tester and Davenport, 2003; Khan et al., 2009). Ion toxicity, nutrient deficiency, and oxidative and osmotic stresses are among the major physiological changes that are primarily being affected by the salt stress in plants (Flowers et al., 1977). Nonetheless, growth stages of plants also get badly hampered by salinity stress (Sairam and Tyagi, 2004; Jithesh et al., 2006). Furthermore, elevated salt concentration in the soil also reduces the osmotic potential that results in disturbed water availability to the root cell. Therefore, it becomes difficult for the plant to acquire both minerals as well as water from the soil (Talei et al., 2011). Rapid alterations in growth, productivity, and the metabolic processes of plants are being observed because of the hormonal signals produced inside root cells (Munns, 2002; Asraf and Harri, 2004).
In addition, salinity reduces the photosynthetic rate, growth, and development of plants, and is also associated with ionic or nutrient imbalance in plant cells (Nazar et al., 2011). Salinity-induced reductions in photosynthesis might involve the excessive accumulation of leaf Na+ and Cl− ions, the stomatal and non-stomatal limitations, and the hindrance of biochemical processes and oxidative damage due to the formation of ROS (Steduto et al., 2000) (Figure 2). Excess accumulation of ROS in plants produces several deleterious effects such as membrane lipid peroxidation, DNA damage, protein oxidation, chloroplast damage, and inhibited biochemical processes (Gunes et al., 2007; Sharma et al., 2012) (Figure 2). Moreover, extreme salinity leads to the ultimate death of the plant cell (Zhu et al., 1997; Xiong and Zhu, 2002). However, a plant's defense mechanisms against salinity comprise osmotic changes, salt separation functions in the cell, and other morphological modifications.
Data analyses based on previous findings showed that salinity also reduces the acquisition of nutrients inside the plant and affects their partitioning (Rabhi et al., 2007; Heidari et al., 2013). Chlorosis might be the unfortunate consequence of the limited Fe supply in plants under salinity (Yousfi et al., 2007). Several studies showed adverse effects of salinity on Fe acquisition in plants.
Hassan et al. (1970), Dahiya and Singh (1976) and Okcu et al. (2005) showed the adverse effect of salinity on the accumulation of Fe content in the shoots of barley, corn, and pea. Furthermore, Heidari and Sarani (2012) reported adverse effects of salinity in the chamomile plant, including stunted growth and a reduction in biochemical components and ion content. Yousfi et al. (2007) have also reported deleterious effect of salt on the physiological processes of barley due to the disturbance in Fe acquisition in plants caused by reducing the flow of phytosiderophore. Now, it is well documented that salinity and Fe interaction in plants result in reduction of salt toxicity.
In the last few decades, extensive studies have been carried out that showed a significant ameliorative effect of Fe against salinity. In reducing the salt stress, Fe plays a unique role by producing antioxidative enzymes (Sharma et al., 2012; Ghasemia et al., 2014). These antioxidative enzymes include catalase (CAT), peroxidases (PODs), and one isoform of superoxide dismutase (SOD) that act as major scavengers of ROS, thereby enhancing cell defense mechanisms against salinity (Scandalios, 1990). However, Manthey et al. (1996) reported decreased activity of both CAT and SOD enzymes under Fe-deficient conditions in onion, which was associated with increased susceptibility against stress. Ghasemia et al. (2014) suggested defending the role of Fe2+ amino acid chelates in tomato plants against salinity. Hence, from the above studies, it can be concluded that Fe plays a significant role in alleviating the adverse effects of salinity.
Iron and Drought Stress
Due to the scarcity of water resources, drought is recognized as one of the single most critical threats to world food security (Abolhasani and Saeidi, 2004; Lambers et al., 2008; Farooq et al., 2009, 2012; Moghadam et al., 2011; Monjezi et al., 2013; Pourgholam et al., 2013). It harms plant growth and development and reduces the growth rates of crop and biomass accumulation. Generally, in crop plants, drought severely affects cell division and expansion, elongation of root, leaf size, proliferation of root, and inhibition of shoot growth (Sharp and Davies, 1989; Spollen et al., 1993; Sharp et al., 2004; Yamaguchi et al., 2010). Furthermore, it hampers all kinds of physiological and biochemical traits such as mineral elements, carbohydrates, ions, hormones, lipids, and nucleic acids (HongBo et al., 2005; Yasar et al., 2006; Moghadam et al., 2011; Pourgholam et al., 2013). The transportation of nutrients from root to shoot are severely affected by drought as the rate of transpiration is reduced. It consequently hampers the active transport of ions and damages the membrane permeability of cells (Viets, 1972; Alam, 1999; Yasar et al., 2006). Simultaneously, due to decrease in soil moisture, a problem occurs with the low distribution of absorbed nutrients in the root of plants in the soil (Alam, 1999; Yasar et al., 2006). More importantly, ROS are generated more frequently due to drought as a result of alterations in electron transport systems (Smirnoff, 1993; Asada, 2006; Waraich et al., 2011). Drought diminishes photosynthetic carbon fixation primarily through restricting the entrance of CO2 into the leaf or by reducing the metabolism (Smirnoff, 1993; Loggini et al., 1999; Apel and Hirt, 2004; Waraich et al., 2011) (Table 1). In addition, stomatal content oscillations and water use efficiency are affected (Farooq et al., 2009, 2012; Li et al., 2009). Stomatal density also deteriorate under severe drought conditions (Xu and Zhou, 2008; De Micco and Aronne, 2012). Photosynthetic pigments and, consequently, photosynthesis are also severely affected by drought (Iturbe-Ormaetxe et al., 1998; Gong et al., 2005). Drought stress reduces chlorophyll a and chlorophyll b contents in marigold (Asrar and Elhindi, 2011; Farooq et al., 2012). It leads to disturbances in water uptake during the imbibition phase of germination, decreases energy supply, and affects enzyme activities, which diminishes the process of germination (Taiz and Zeiger, 2010; Farooq et al., 2012). Drought stress causes generation of numerous signals such as the production of abscisic acid (ABA) in root tissues (Wang et al., 1999; Aroca and Ruiz-Lozano, 2012) or some hydraulic signals passed through the root axis (Aroca and Ruiz-Lozano, 2012; Ionenko et al., 2012).
Table 1. Iron nutrition and drought stress tolerance.
To survive under drought condition, the nutrient status of plants plays a significant role in increasing plant tolerance to drought stress (Table 1) (Payne et al., 1992; Marschner, 1995; Rizhsky et al., 2004; Samarah et al., 2004; Yasar et al., 2006; Rotaru and Sinclair, 2009; Rotaru, 2011; Waraich et al., 2011). A study showed that sunflower develops drought resistance with the help of application of micronutrients (Rahimizadeh et al., 2007). It has been demonstrated that the application of Fe nutrition to plants under drought condition can enhance tolerance as it leads to production of assimilates (Sultana et al., 2001; Khan et al., 2003; Rotaru, 2011; Pourgholam et al., 2013) (Table 1). It has also been reported that legumes have positive responses to Fe nutrition (Slatni et al., 2008; Rotaru, 2011). Furthermore, Mahmood et al. (1990) demonstrated that the application of Fe increased the yield of wheat plants. Elanz et al. (2011) recommended Fe foliar application on sunflower under drought stress, which showed that Fe foliar application under normal and stressed conditions plays important roles in seed and oil production (Table 1). Fe foliar application improved soybean yield and also leads to the intensification of seed set in the wheat crop (Arif et al., 2006; Kobraee et al., 2011; Afshar et al., 2013). Akbari et al. (2013) suggested that Fe foliar application with Zn diminishes oxidative stress by reducing H2O2 content and lessening lipid peroxidation by enhancing antioxidant enzymes (CAT, GPX, and SOD) under drought stress (Table 1). It was also proposed that over-expression of Fe-SOD helps in the reduction of secondary injury symptoms and leads to enhancement in drought tolerance (McKersie et al., 1999, 2000; Alscher et al., 2002; Samis et al., 2002). Pirzad and Shokrani (2012) applied Fe with Zn to improve the leaf characters (weight, area, and numbers) of Calendula officinalis under drought stress. Reductions in terms of either vegetative growth or oil contents in sunflower due to drought conditions were found to be alleviated by the foliar applications of Fe (Ebrahimian and Bybordi, 2011). Mostafa et al. (2011) examined the effect of Fe application with surface water stress conditions on growth, yield, and nutrient uptake of Sesamum indicum L. plants (Table 1). Iron spraying plays a significant role in improving the protein quality and resistance under drought stress (Parhamfar, 2006; Afshar et al., 2012). It is important to mention that Fe is applicable in controlling drought effects on root growth (Snyder and Schmidt, 1974; Glinski et al., 1992). Under drought stress and Fe-deficient conditions, the application of Fe over turf grasses leads to color enrichment and growth improvement (Deal and Engel, 1965; Minner and Butler, 1984; Glinski et al., 1992). Moreover, in Fe-sufficient condition, Fe has been applied to give a darker green color for cool-season turf grass (Snyder and Schmidt, 1974; Yust et al., 1984; Carrow et al., 1988; Wehner and Haley, 1990; Glinski et al., 1992). There is still much more investigative work required to understand the role of Fe against drought stress (Table 1).
Iron and Heavy Metal Stress
Rapid technical development in different sectors of agriculture, industries, and anthropogenic activities have resulted in an abundant release of heavy metals (Young et al., 2009; Oliveira, 2012; Kumar et al., 2013). Metals in the form of pollutants pose serious threats to our environment. They exhibit toxicity in the natural soil that harbors vegetation (Foy et al., 1978; Yizong et al., 2009). The excessive use of phosphatic fertilizers, industrial wastes, and sewage sludge applications release several toxic heavy metals/metalloid such as Cd, Cr, Pb, and As into agricultural soil (Bell et al., 2001; Schwartz et al., 2001; Passariello et al., 2002; Yadav, 2010). Later, these heavy metals enter into the ecosystem and food chain through absorption and accumulation processes in plants and animals, affecting them severely (Yamagata and Shigematsu, 1970; Cervantes et al., 2001; Vernay et al., 2007; Yizong et al., 2009; Kumar et al., 2013). For example, the havoc of “Itai-Itai disease” in Japan was due to presence of Cd contamination in rice and soybean (Yamagata and Shigematsu, 1970; Yizong et al., 2009; Kumar et al., 2013; Tchounwou et al., 2013).
Plants, undoubtedly, are being affected by heavy metal contaminations as numerous morphological, physiological, and biochemical changes have been noticed in metal toxicity-challenged plants (Pandey et al., 2005; Oliveira, 2012; Kumar et al., 2013; Singh et al., 2016). The major damaging effects of heavy metal stress in plants are lipid peroxidation (which is an indicator of biomembrane deterioration) and a variation in enzymatic and transport activities (De Vos et al., 1989, 1991b; De Vos and Schat, 1991a; Pandolfini et al., 1992; Somashekariah et al., 1992; Sinha et al., 1997; Yadav, 2010). Several metals such as Hg, Cd, and Cu affect the permeability of the plasma membrane in the plant cell, which consequently results in a loss of K ions (De Vos et al., 1989, 1991b; De Vos and Schat, 1991a; Pandolfini et al., 1992; Reddy and Prasad, 1992; Sinha et al., 1997). Due to high affinity toward cellular sulfhydryl groups, heavy metals also give rise to sulfhydryl reactions (De Vos et al., 1989; Sinha et al., 1997). Nonetheless, heavy metals in plants cause overproduction of ROS, which generate oxidative stress (Wojtaszek, 1997; Mithofer et al., 2004; Yadav, 2010). Consequently, oxidative stress creates membrane damage (Srivastava et al., 2004; Yadav, 2010) due to the unbalanced antioxidant defense system in plants (Demiral and Turkan, 2005; Yadav, 2010). Heavy metal stress in plants also deteriorates the metabolism of essential elements and severely affects the electron transport chain (Table 2) (Qadir et al., 2004; Dong et al., 2006; Yadav, 2010; Singh et al., 2016).
Table 2. Iron-mediated up-regulation of antioxidative enzymes (SOD, APX, and CAT) and heavy-metal stress tolerance.
To cope with heavy metal stress, plants adopt several strategies at various levels (Table 2). Of these, the management of mineral nutrients was found to be the most efficient mechanism (Cakmak, 2005). Among mineral nutrients, Fe is being recognized as the most efficient and potentially essential micronutrient that plays a pivotal role in mitigating metal stress (Table 2). Several reports showed the efficacy of Fe in controlling the damaging effects of metal stress (Emamverdian et al., 2015). Iron is considered as a biologically important micronutrient as it serves as the major constituent of the cell redox systems such as heme proteins, including leg hemoglobin, catalase, cytochromes, peroxidase, and Fe-S clusters such as aconitase, ferredoxin, and superoxide dismutase (SOD) (Marschner, 1995; Emamverdian et al., 2015).
Moreover, the formation of aconitase plaque by ferrous oxidation to ferric iron on the root surface of terrestrial and aquatic plants helps in the sequestration of a large number of metal through adsorption or co-precipitation and thereby inhibits the uptake and accumulation of metal inside the plant cell (Armstrong, 1964, 1967; Bacha and Hossner, 1977; Chen et al., 1980; Mendelssohn and Postek, 1982; Davison and Seed, 1983; Taylor and Crowder, 1983; Taylor et al., 1984; Levan and Riha, 1986; Greipsson and Crowder, 1992; Emerson et al., 1999; Hansel et al., 2001; Weiss et al., 2003; Emamverdian et al., 2015).
Garnier et al. (2010) described the role of Fe plaque in a paddy field irrigated with ground water and suggested the significant role of plaque formation in attenuating the uptake and accumulation of As in rice plants (Table 2). Liu et al. (2007) also presented evidence for the role of Fe plaque in Cd adsorption on the root surface of the rice seedling (Table 2). Xin-Bin and Wei-Ming (2007) demonstrated the effect of Fe plaque on Se translocation and also showed its altered accumulation in the aerial part of the plant. Rahmana et al. (2008) used Fe with phosphate for the regulation of As toxicity in the water fern (Table 2). Yizong et al. (2009) have demonstrated that Fe plaque plays an important role in regulating Cd, Cu, and Pb toxicities in rice plants. Yang et al. (2011) showed significance of Fe in Pilea cadierei against phosphorus (P).
Consequences of Iron Toxicity and Redox Regulation in Plants
Plants may undergo Fe toxicity in two conditions: either excessive amount of Fe or Fe deficiency. Iron plays key roles in plant metabolism like electron transport systems (redox reactions of Fe-S proteins and cytochromes), respiration, photosynthesis, and nitrogen fixation processes (Soyder and Schmidt, 1974; Carrow et al., 1988; Taiz and Zeiger, 1991). Furthermore, the deficiency of Fe can affect about one-third of the cultivated land. Deficiency of Fe also causes the declination of photosynthetic components, especially Fad (Fe-S protein ferredoxin) of the chloroplast (Tognetti et al., 2007). Fe deficiency in plants causes interveinal chlorosis (Bienfait and Van der Mark, 1983), poor root development, growth retardation, and the eventual death of the plant (Kobayashi et al., 2003). In addition, Fe deficiency also leads to the alteration in expression of chlorophyll-binding proteins and the down-regulation of many photosynthetic pigment levels (Thimm et al., 2001; Rout and Sahoo, 2015). In the agricultural soils, Fe deficiency may also occur either at extremely high pH or at extremely low pH levels. López Jiménez et al. (1985) demonstrated that the increased levels of chlorosis in young Avocado leaves was correlated with a decline in the level of Fe in leaf parts, chloroplast numbers, and activity of catalase (Rout and Sahoo, 2015). The Fe deficiency is also characterized by interveinal chlorosis in young leaves rather than main veins, a type of symptom known as “iron deficiency chlorosis” (Rout and Sahoo, 2015). Similarly, excessive amounts of Fe also cause toxicity in plants. Tanaka et al. (1966) demonstrated that upon increasing the level of Fe, roots are affected more than leaves. It shows that in the presence of an excess amount of Fe, plant roots increase their capability and translocate the Fe in younger leaves. High level of Fe disturb the basal level of magnesium and potassium in plants and cause nutritional disturbances (Tanaka et al., 1966).
Although high concentrations of Fe can lead to toxic consequences in plants (Anjum et al., 2015). Excess free Fe ions like Fe2+ and Fe3+ can cause ROS generation by participating in the Fenton reaction (Fenton, 1894; Haber and Weiss, 1934; Kehrer, 2000; Mai and Bauer, 2016) and leading to oxidative stress (Mai and Bauer, 2016). Down regulated detoxifying proteins in Fe-deprived conditions, viz. CAT2 (CATALASE 2; AT4G35090) proteins and PA2 (PEROXIDASE 2; AT5G06720) proteins, were reported in some plants (Donnini et al., 2010; Rodríguez-Celma et al., 2011). These are enzymes that help in the conversion of H2O2 (hydrogen peroxide) to H2O (water) and oxygen. In addition, Fe deficiency in the roots of M. truncatula (Rodríguez-Celma et al., 2011) and P. dulcis × P. persica (Rodriguez-Celma et al., 2013) was characterized by the superoxide dismutase, i.e., ATMSD1 (ARABIDOP-SIS MANGANESE SUPEROXIDE DISMUTASE 1; AT3G10920) (Mai and Bauer, 2016). Furthermore, non-enzymatic ROS generation also occurs due to Fe deficiency. In this process, two enzymes reported in the roots (Mai et al., 2015) and shoots (Zargar et al., 2013) of Arabidopsis thaliana were GST1 (ARABIDOPSIS GLUTATHIONE S-TRANSFERASE 1; AT1G02930) and MDAR1 (MONODEHYDROASCORBATE REDUCTASE 1; AT3G52880) (Rodríguez-Celma et al., 2011; Mai et al., 2015). In the case of Fe deficiency, two heme-binding proteins (CAT2 and PA2) were found to decrease the level of peroxidases. Moreover, ATMSD1 is a ROS-eliminating enzyme formed after the up-regulation of ROS-eliminating enzyme and beneficial in compensation of deprivation of Fe-dependent peroxidases and stimulated the ascorbate-glutathione cycle from GPX3 (GLUTATHIONE PEROXIDASE3; AT2G43350) (Mai et al., 2015). GST1 and MDAR1 were reported to detoxify the ROS generated due to Fe deficiency (Apel and Hirt, 2004).
Conclusion and Future Outlook
Increased anthropogenic activities and technologies have rendered a polluted environment. Furthermore, the situation is likely to be much worsened by an immense increase in human population that is expected to reach about 9.1 billion by 2050 according to the report of the FAO (2008), which would result in decreased areas of arable land for future agricultural practices. It is well documented that approximately 50% of the world's agricultural land suffers from adverse effects of complex environmental stress factors such as salinity, drought, and heavy metal. Since plants are restricted in their movements, they are inevitably exposed to such stressful conditions that would cause reduction in their yields. To counteract inhibitory/adverse effects of such stresses, plants employ several efficient and sophisticated biochemical defense mechanisms at multiple levels (morphological, anatomical, biochemical, and molecular). Data analyses based on previous findings showed tremendous progress at various levels against stress factors in plants. Of these strategies, management of mineral nutrient status in plants was found to be the most promising. Among mineral nutrients, Fe is regarded as one of the most efficient and essential micronutrients that acts significantly in a number of cellular processes such as metal detoxification, metabolism of secondary metabolites, and maintenance of the cell redox cycle. Previous findings suggested that Fe regulates adverse effects of salinity, drought, and heavy metal by controlling the redox status of the cell and antioxidant defense system. In addition, the formation of Fe plaque also facilitates the sequestration of a large number of metals on the root surface. Although not much is known about the relevancy of Fe nutrition in the mitigation of different stresses, its exogenous application, however, definitely regulates toxicity of several stresses. Despite major progress achieved in the field of Fe nutrition-mediated alleviation of stress, there are several questions still awaiting for the answers. In conclusion, it may be stated that uptake, accumulation, and metabolism of Fe inside the plant still deserve attention and may shed insight into the process of modifying agricultural productivity in stressful environments.
Author Contributions
DKT, ShwetaS, and SwatiS: designed the manuscript; DKT, ShwetaS, SG, and SwatiS: wrote the manuscript; VS, DC, PS, ShiveshS, VY, ND, SL, ShivendraS and SP: critically evaluated the manuscript.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Acknowledgments
The authors are grateful to the University Grants Commission, New Delhi, for financial assistance. DKT and SG is also grateful to the UGC for providing the Dr. D. S. Kothari Fellowship and National Fellowship for Higher Education (NFHE).
Abbreviations
DMAS, deoxymugineic acid synthase; FRO, ferric-chelate reductase oxidase; HA, H+-ATPase; IRT, iron-regulated transporter; MAs, mugineic acid family phytosiderophores; NA, nicotianamine; NAAT, nicotianamine aminotransferase; NAS, nicotianamine synthase; PEZ, PHENOLICS EFFLUX ZERO; SAM, S-adenosyl-L-methionine; TOM1, transporter of mugineic acid family phytosiderophores 1; YS1/YSL, YELLOW STRIPE 1/YELLOW STRIPE 1–like.
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Keywords: Trace elements, iron (Fe), abiotic stress, plants, reactive oxygen species (ROS), enzymatic antioxidants, proteins, gene families
Citation: Tripathi DK, Singh S, Gaur S, Singh S, Yadav V, Liu S, Singh VP, Sharma S, Srivastava P, Prasad SM, Dubey NK, Chauhan DK and Sahi S (2018) Acquisition and Homeostasis of Iron in Higher Plants and Their Probable Role in Abiotic Stress Tolerance. Front. Environ. Sci. 5:86. doi: 10.3389/fenvs.2017.00086
Received: 29 June 2016; Accepted: 24 November 2017;
Published: 09 February 2018.
Edited by:
Naser A. Anjum, University of Aveiro, PortugalReviewed by:
Vijay Shridhar, Doon University, IndiaCatherine Santaella, UMR7265 Biologie végétale et microbiologie environnementales (BVME), France
Copyright © 2018 Tripathi, Singh, Gaur, Singh, Yadav, Liu, Singh, Sharma, Srivastava, Prasad, Dubey, Chauhan and Sahi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Durgesh K. Tripathi, dktripathiau@gmail.com
Vijay P. Singh, vijaypratap.au@gmail.com
Devendra K. Chauhan, dkchauhanau@yahoo.com