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. 2020 Jul 7;26(8):1541–1549. doi: 10.1007/s12298-020-00841-y

Chelators of iron and their role in plant’s iron management

Sangita Dey 1, Preetom Regon 1, Saradia Kar 1, Sanjib Kumar Panda 1,2,✉
PMCID: PMC7415063  PMID: 32801485

Abstract

Proper transport of metal and their homeostasis is very crucial for the growth and development of plants. Plants root are the primary organs which comes in contact with the stress and thus few modifications occurs, often determining the nutrient efficiency or sometimes as a stress tolerance mechanism. Plant utilizes two strategies for the uptake of iron viz, strategy I-reduction based and strategy II-chelation based. In this review we attempted for a better understanding of how the chelators acts in the mechanism of iron uptake from soils to plants and how iron is distributed in the plants.

Keywords: Iron homeostasis, Chelators, Iron uptake strategies, Iron translocation, Gene regulators

Introduction

For the proper growth and development of plants, the proper uptake and transport of metal across the plant system is very crucial. Iron (Fe) is an essential plant nutrient required in a trace quantity, which is responsible for various metabolic processes like photosynthesis, cell wall metabolism, and respiratory electron transport chain and also provides protection to the plants against various oxidative stress (Li et al. 2012; Dey et al. 2019). However, the excess concentration of Fe in plants can deleteriously affect the plant total growth causing phytotoxicity affecting leaf by forming yellow–brown spots on the surface of the leaf causing leaf chlorosis and inhibiting the plant growth as well as delimiting the nutritional values of the plants and via Fenton reaction can generate reactive oxygen species which can harm the total yield of the plants (Wang et al. 2000; Fang et al. 2001; Carrasco-Gil et al. 2018; Kar and Panda 2018). Earlier, it has been reported, toxicity of Fe reduced the chlorophyll content in plants (Li et al. 2012; Carrasco-Gil et al. 2018). Fe is never found in free elemental state but mostly in the form of Iron-oxides (Fe2O3/FeO) (Mengel and Kirkby 2001; Schulte 2002). Fe2+ is the preferred form of Fe for root absorption and it is also absorbed as Fe3+ chelate form (Briat et al. 2007; García et al. 2018). Fe is abundantly present in soil, mainly in its oxidized state i.e., Fe3+ with low solubility found especially in calcareous and alkaline soil where it is present in a low concentration and is too less to meet the plant requirement for various biological processes (Romheld 1987; Grillet et al. 2014). Due to the bioavailability of Fe in soils varies with the soil types, plants have adapted strategies for the mobilization and appropriate uptake of Fe needed in both Fe excess and deficient condition (Kobayashi and Nishizawa 2012). Thus, proper Fe uptake, transport, its acquisition and distribution within the plant is very crucial in maintaining Fe homeostasis in plants. Plants as an oxygenic photosynthetic organism has to face a dual challenge: one is to acquire Fe from an inorganic environment and other is to make it available in organic form which can be taken and utilized by plants to carry out the fundamental biological processes of life. Fe is taken up from soils following two mechanisms i.e., strategy I-reduction based and strategy II-chelation based (Marschner and Römheld 1994; Lingam et al. 2011; Naranjo-Arcos et al. 2017). In this review, we attempted to study how the chelators plays a crucial role in Fe uptake and how they can regulate in plants need for Fe management.

Iron chelation and solubilization at the rhizosphere

Iron uptake strategies

Non-graminaceous plants follow up the strategy I-reduction based, which includes proton release, acidifies the soil to solubilize Fe3+ leading to Fe reduction. FIT (FER-like iron deficiency-induced transcription factor) is known to play a pivotal role in the upregulation of the root-expressed clustered genes involved in the Fe acquisition. Action of FIT is upregulated upon Fe deficiency (Bauer et al. 2004; Ivanov et al. 2012; Naranjo-Arcos et al. 2017). Fe3+ is reduced to Fe2+ upon acidification by membrane bound ferric reductase oxidase (FRO) like FRO2. FRO genes are expressed in different parts of the plants and therefore they have a specific role in respective organs in reduction based Fe transport and are not limited to the root plasma membrane only (Jeong and Guerinot 2009; Kobayashi and Nishizawa 2012; Liang et al. 2017). Once Fe3+ are reduced to Fe2+ which is a substrate for transmembrane transport, they are then transported to the roots by a member of zinc regulated transporter (ZRT)-IRT-like protein (ZIP) family, IRT1. Fe3+-chelate reductase which are the integral membrane protein that transfer electrons from cytosolic NADPH to FAD found in the plasmalemma of the root epidermis (Hell and Stephan 2003). Both FRO2 and IRT1 are specifically expressed in root epidermis responsible for Fe uptake from soils and are important for plant growth (Jeong and Guerinot 2009). Arabidopsis thaliana AtIRT1, first Fe-transporter belonging to ZIP family whose expression is rapidly upregulated upon Fe-deficiency which are probably controlled by both root and shoot derived signals (Gayomba et al. 2015). Belonging to a broad substrate range along with high-affinity for Fe-transport, IRT1 is also able to transport various other divalent cations like Cd2+, Co2+, Zn2+, Mn2+ without disturbing the Fe concentration (Baxter et al. 2008; Naranjo-Arcos et al. 2017). Although marginally, another metal transporter NRAMP1 have also been playing a hidden role in Fe uptake from soils. However, its potential role in Fe uptake mechanism still needs better understanding (Schikora and Curie 2010). Fe is stored readily in non-reactive form in plastids encoded by Ferritin (FER) gene and may also be stored in the vacuole of the plant cell and the mobilization from this organelle is generally mediated by two proteins viz., NRAMP3 and NRAMP4 proteins (Aznar et al. 2015; Naranjo-Arcos et al. 2017). Grasses utilizes strategy II-chelation based, follows the uptake of Fe3+ chelated by mugineic acid-based phytosiderophores, resulting in Fe(III)-PS complex which are then transported via yellow stripe (YS) family into the roots. Grasses are able to take up Fe2+ in addition in Fe(III)-PS complex (Jeong and Guerinot 2009; Lin et al. 2016). YS1, yellow stripe gene from maize was first characterized in Poaceae and its function as Fe-transporter in strategy II for Fe transport (Curie et al. 2001). In Graminaceae, transport of Fe-phytosiderophore complexes helps in the uptake of Fe from the rhizosphere complexes through proteins from the YSL family (Nozoye et al. 2011; Aznar et al. 2015).

Solubilization and uptake of iron

Upon Fe deficiency, many studies have been carried out on root responses towards stress condition. Most of the dicot and fewer monocot species on Fe deficiency has a characteristic, where there is an increase in the activity of NADPH dependent reductase as well as an ATPase-driven proton efflux pump which enhances the rate of solubilization of inorganic Fe(III) in the rhizosphere increasing the reduction of Fe(III) to Fe(II) (Hell and Stephan 2003; Römheld and Marschner 1986). However, the roots of the grasses have an ability to solubilize and uptake Fe from the sparingly soluble inorganic Fe(III) by releasing chelators for Fe. These substances are characterized as non-protein amino acids such as mugineic acid and avenic acid. The chelating substances released by roots are termed as phytosiderophores that chelates Fe(III) in the rhizosphere and forms Fe(III)-PS complex which are imported by specific plasmalemma transporter proteins (Grotz and Guerinot 2006; Kobayashi et al. 2005; Kobayashi and Nishizawa 2012; Kar and Panda 2018). An onset of Fe shortage stimulates the release of phytosiderophores. In the xylem sap, citrate has been known to play a crucial role in chelating Fe and its trafficking (Brown and Chaney 1971; Aznar et al. 2015; Yokosho et al. 2016). FRD3, ferric reductase defective 3, belonging to MATE family facilitates the citrate efflux in the xylem. OsFRDL1 (FRD like gene) in rice also possesses similar functions of citrate efflux in the root pericycle cell, exhibiting its role for the efficient Fe translocation (Yokosho et al. 2009). PEZ1, dramatically lowers the amount of caffeic acid as well as protocatechuic acid in the xylem sap, responsible for the loading of these phenolic compounds facilitating the remobilization of apoplasmic Fe into the plant. FRD3, FRDL1, PEZ1 are the efflux Fe chelators which are present in their free forms (Kobayashi and Nishizawa 2012). By comparing the biochemical pathway of both Fe sufficient and deficient plants, most of the responsible genes were cloned in rice and barley. The secretion of MAs significantly increases in response to Fe deficient condition and the tolerance to this condition is strongly related to the amount of MAs produced and secreted, so that Fe(III)-PS complex can be formed which can be taken up by the roots of the plants. For instance, various crops like sorghum, rice, maize secretes deoxymugineic acid (DMA) in very low amounts and hence they are very susceptible to the Fe-deficiency. However, barley secretes comparatively large amount of numerous kinds of MAs including mugineic acid, 3-hydroxymugineic acid (HMA) and 3-epi-hydroxy-mugineic acid (epi-HMA) and they are relatively more tolerant to the low Fe availability (Negishi et al. 2002). Three molecules of methionine are involved in the biosynthesis that are integrated in one enzymatic step into nicotianamine (NA) which are catalyzed by nicotianamine synthase and it has been reported earlier that in all plant cells, nicotianamine acts as an Fe chelators and it is upregulated in roots of the strategy II plants in low Fe content, and plays a central role in Fe uptake mechanism (Scholz et al. 1992; Schuler et al. 2012). NA is the first intermediate in the process of biosynthesis of phytosiderophores, resulting in the uptake of Fe(III)-PS complex. NA is known to promote high content of Fe and its bioavailability in cereal grains and is produced by NA synthase (NAS) (Lee et al. 2009; Zheng et al. 2010). Any alteration in the activities of NAS gene can affect the NA content in plants which can result in the phenotypical changes related to the uptake as well as distribution of Fe (Takahashi et al. 2003; Klatte et al. 2009). NA is found in the phloem sap as well as it is also detected inside the root tip vacuoles where it functions in Zn chelation. Fe-NA complexes inside the phloem might chelate Fe (von Wirén et al. 1999; Weber et al. 2006; Rellán-Álvarez et al. 2008), it can also prevent precipitation of Fe and deliver it to the target sites. NA can also minimize Fe toxicity as the chelation can prevent ROS production (Becker et al. 1995; Hell and Stephan, 2003). However, the role of NA is still a matter of clarification in strategy I plants. But earlier studies have proved that NA can form more stable complex with Fe2+ than Fe3+. The precise mechanism of secretion of chelators is still unclear and needs better understanding. The cloning of mutant allele ys1 from maize helped in elucidating the uptake of Fe(III)-PS complex. Several YS1-like transporter has been reported to transport NA-iron complex, suggesting it as a ligand for Fe transport (Hell and Stephan 2003; Schuler et al. 2012). Fe2+ which is present inside the cell may be further chelated by NA, which is already present in strategy I and strategy II plants. One of the important mechanism regulating Fe homeostasis is vacuolar sequestration serving as Fe storage strategy. Several genes were reported to regulate Fe trafficking occuring between cytosol and vacuoles. Arabidopsis AtVIT1 (Vacuolar Iron Transporter 1), expressed in seeds serving as a vacuolar sequestration of Fe, indicating that the gene can be potentially used for Fe biofortification (Roschttardtz et al. 2009).

Rice, being a graminaceous species, possesses not only strategy II but involve a partial part of strategy I mechanism of Fe uptake (Ishimaru et al. 2006). It includes OsYSL15 for the uptake of Fe3+-PS complexes as well as it also possess OsIRT1 and OsIRT2 for the uptake of Fe2+ form of Fe, depending on their growth condition. OsYSL15 is the primary transporter which is upregulated during Fe-deficient condition for the uptake of Fe-PS from the rhizosphere. It is also present in the stele and developing seeds, where it plays a vital role in the process of Fe homeostasis (Morrissey and Guerinot 2009). Divalent metal transporter, OsIRT1 and OsIRT2 regulated by FIT is the primary transporter of Fe where Fe2+ is predominantly available (Hindt and Guerinot 2012; Kobayashi et al. 2014; Connorton et al. 2017; Kar and Panda 2018; Dey et al. 2019) (Fig. 1).

Fig. 1.

Fig. 1

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Strategic representaion of iron uptake in rice

Translocation of iron: from rhizosphere to shoots

Once the Fe is taken up from the rhizosphere into the root epidermis or exodermis, it is then transported to vascular bundles, where xylem and phloem plays their respective roles for the translocation of Fe. Both symplastic and apoplastic pathways are involved in this radial transport system. However, in latter pathway, casparian strips in the exodermis and endodermis comes into role for the Fe translocation (Fig. 2).

Fig. 2.

Fig. 2

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Apoplastic and symplastic pathway

Plants by utilizing the Fe uptake mechanism, chelates the major portion of both Fe3+ and Fe2+ to avoid the Fe toxic condition and to facilitate its transport into the plant shoot systems. Under Fe-deficient condition, the enzymes and transporter genes which are responsible for the Fe uptake are induced in the cortex and vascular bundles along with root epidermis and are thought to be involved in the process of Fe transport into the shoots (Kobayashi and Nishizawa, 2012; Ogo et al. 2014). Fe-DMA complex has been reported to be found in the phloem sap as the primary chemical form indicating that DMA can also help in the internal translocation of Fe along with uptake from the rhizosphere (Nishiyama et al. 2012). NA is the precursor of DMA and acts as a potential chelator of Fe and helps in the translocation of Fe by supressing their toxicity in the plants. In rice, the NAS enzymes (OsNAS1, OsNAS2, OsNAS3) are involved in the synthesis of NA. However, expression of OsNAS3 is low in comparison to OsNAS1 and OsNAS2 and is maily found in the vascular bundles, suggesting its potential role in the translocation of Fe in the shoots (Inoue et al. 2003). OsYSL2 transporter is responsible for phloem mediated Fe-distribution and Fe-NA transport across the plasma membrane and NA efllux transporter ENA1 and ENA2 are thought to be responsible for the extrusion of NA for the redistribution of Fe into the apoplast or intracellular compartments (Ishimaru et al. 2010; Ogo et al. 2014). As a principal chelator, NA plays crucial role in Fe transport and acquisition, either Fe is freely available or it bound to any target structures like Heme or stored as phytoferritin (Hell and Stephan 2003) (Table 1).

Table 1.

Functions of genes involved in iron uptake and transport

Type Genes Functions Response References
Fe-uptake FRO2 Transfer electrons across the plasma membrane to reduce Fe3+ to Fe2+ in the rhizosphere Strongly induced by low Fe Connolly et al. (2003)
NAS Chelators for metal cations like Fe II and III Strongly induced by low Fe Murata et al. (2006) and Bashir et al. (2006)
NAAT Transfer of amino group from NA to DMA Strongly induced by low Fe Murata et al. (2006) and Bashir et al. (2006)
AHA2 Generates a proton gradient that drives the active transport of nutrients by H(+)-symport Induced by low Fe Schmidt et al. (2000) and Gruber et al. (2013)
IRT1 Uptake of iron from the rhizosphere across the plasma membrane in the root epidermal layer Strongly induced by low Fe Santi and Schmidt (2009)
PEZ1 Efflux of phenolics to the rhizosphere for Fe III chelation Marschner (1995)
YS1/YSL Yellow strip like protein responsible for uptake of chelated Fe III into root cells Strongly induced by low Fe Römheld and Marschner (1986) and Curie et al. (2001)
TOM1 MAs efflux transporter Strongly induced by low Fe Durrett et al. (2007)
Fe-translocation FRD3 Citrate efflux transporter Induced/constitutive by low Fe Li et al. (2015) and Majerus et al. (2009)
PEZ Phenolics efflux transporter Weekly induced by low Fe Marschner (1995)
TOM MAs efflux transporter Strongly induced by low Fe Durrett et al. (2007)
YS1/YSL Yellow strip like protein responsible for uptake of chelated Fe III into root cells Induced/repressed by low Fe Römheld and Marschner (1986) and Curie et al. (2001)
FRO Ferric chelate reductase for Fe-translocation Induced by low Fe Connolly et al. (2003)
IRT Ferrous ion transporter for Fe-translocation Induced by low Fe Santi and Schmidt (2009)
NRAMP Ferrous ion transporter for Fe-translocation Induced by low Fe Tsukamoto et al. (2009)
Fe-storage Ferritin High capacity iron storage and sequestration Induced by Fe-excess Jin et al. (2010)
Fe-compartmentalization FRO Ferric chelate reductase for chlorophyll Fe transport Constitutive by low Fe Connolly et al. (2003)
NRAMP Fe transporter from vacuole into cytosol Induced by low Fe Tsukamoto et al. (2009)
VIT1 Vacuolar iron influx Constitutive/repressed by low Fe response Tsukamoto et al. (2009)
Gene regulator FER/FIT Positive transcriptional regulator Induced by low Fe Santi and Schmidt (2009)
bHLH038/bHLH039 Positive transcriptional regulator Induced by low Fe Ishimaru et al. (2011)
PYE Negative transcriptional regulator Induced by low Fe Curie et al. (2001)
BTS Putative transcriptional/posttranscriptional regulator Induced by low Fe Curie et al. (2001)
EIN3/EIL1 Ethylene signaling regulator Induced by low Fe Yuan et al. (2005)
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Microbial siderophores in Fe mobilisation in plants

There are low molecular mass biomolecules, less than 10 kDa, released from the microorganisms which acts as chelating agents for metal ions. These secreted molecules are known as microbial siderophores and has been reported to possess higher affinity for Fe3+ as compared to the phytosiderophores like mugineic acids (Sharma et al. 2018). The bacteria producing siderophores mostly resides in the rhizospheric region and increases the mobility and availability of metal ions through their secretions, contributing to phytoremediation (Schalk et al. 2011). In case of Fe, presence of siderophore bearing microbes in the rhizosphere leads to better morphological responses. Sah et al. (2017) has reported that higher amount of siderophore producing Pseudomonas aeruginosa strain when applied experimentally in the rhizosphere of Zea mays has brought better shoot and root growth along with increased cob length and grain number. Few plants develop adaptive responses under Fe limiting conditions by secreting phenolic compounds which in turn attracts the siderophore producing rhizobacteria (Jin et al. 2010). The mechanism of mobilisation of Fe using siderophores is still not clear. In another work, pollutant degrading bacteria, Cupriavidus necator produces siderphore which is named as cuprabactin utilised by the bacteria to overcome Fe limitation (Li et al. 2019). This work can be utilised in future as an approach to inoculate the microbe in rhizosphere for increasing Fe acquisition for plants. Other than Fe, microbes are also responsible in uptake of other important elements like copper, zinc and cadmium. Depending upon their chemical structures, siderophores are classified into different types: hydroxymate siderophore, catecholate siderophore and carboxylate siderophore. Mostly, hydroxymate siderophores are responsible for metal immobilisation of metals in plants (Ahmed and Holmström 2014). Pseudobacter putida producing pseudobactin is responsible for growth and yield of plants (Gamalero and Glick 2011). Although, not much studies have been made on metal transportation in plants through siderophores, few studies suggested ligand exchange between phytosiderophore and microbial siderophore is responsible for the same. It has also been reported about the involvement of soil microorganisms in regulation of signalling processes in plants leading to Fe acquisition (Ferreira et al. 2019).

Conclusion

Fe is an essential nutrient element required for the proper growth and development as well as to carry out various metabolic processes within the plant system. However, its toxicity or deficiency can have deleterious effects on plant growth. Plants have developed strategies to deal with the altered conditions for the Fe uptake so that plants are able to control Fe homeostasis by reacting to both Fe-excess and Fe-deficiency (Marschner and Römheld 1994; Lingam et al. 2011; Verma and Pandey 2017).

Fe uptake mechanism is classically divided into two strategies. Strategy I is predominant in eudicotyledonous and non-poaeceae monocot or non-graminaceous plants which are commonly known as “reduction based strategy”. It was made clear using A. thaliana that this strategy involves 3 step process on plasma membrane protein which are induced in the Fe-deficiency condition: the AHA2, Arabidopsis H+-ATPase releases protons which acidifies the soil surface by lowering soil pH, followed by the reduction of Fe3+ to Fe2+ by ferric reductase oxidase 2, FRO2 and finally the Fe2+ are imported into the root cells of the plant by high affinity ferrous Fe transporter 1, IRT1 (Santi and Schmidt 2009; Hell and Stephan 2003; Brumbarova et al. 2015; Kobayashi et al. 2019). Strategy II, which is commonly known as chelation based strategy has been well described in plant species belonging to the Poaecae family i.e., graminaceous plants. Rice, being a model plant has been used to describe various unknown factors which are involved in strategy II Fe uptake mechanism (Sisó-Terraza et al. 2016; Rajniak et al. 2018). Strategy II involves the secretion of phytosiderophores (PS) belonging to mugineic acid family, with the potential to chelate Fe3+ and forms Fe(III)-MA complexs. Enzymes such as nicotianamine synthase (NAS), nicotianamine aminotransferase (NAAT), deoxymugineic acid synthase (DMAS) are involved in the biosynthesis of all types of MAS from S-adenosyl methionine, resulting in deoxymugineic acid (DMA), which is the precursor of all phytosiderophores. After DMA binds to Fe3+ and forms the complex, they are then imported by the Yellow stripe (YS) or Yellow stripe-like (YSL) family members (Grotz and Guerinot 2006; Kobayashi et al. 2005; Kobayashi and Nishizawa 2012; Brumbarova et al. 2015; Connorton et al. 2017; Kobayashi et al. 2019).

Future prospects

In the context of abiotic stress in plants caused by Fe, thorough studies has been performed in the last decade to illustrate the homeostatic activity under both excess and deficient condition. The knowledge of function of chelators and their respective transporters contribute a major part in understanding Fe uptake in plants. Metabolomic approaches has made successful attempts to report the accumulation of natural Fe complex in xylem and phloem tissues, explaining their apoplastic and symplastic pathways involved in Fe transportation. Under deficient Fe scenario, efforts has always been taken to enhance the Fe quantity in the plants and studies of the chelators regarding the same remains primary. In recent years, extensive studies has been performed on understanding the homeostatic responses by many crop plants under both Fe excess and deficient condition through cellular, biochemical and genetic approaches. In large number of crop plants, next generation sequencing has been performed to understand the uptake strategies, transport and homeostasis aiming for novel genes and hypothesis of their functions (Do Amaral et al. 2016; Wu et al. 2017; Aung et al. 2018). Knowing the chelation and transportation, sets a foundation for further assessment of the processing mechanism. Although, large number of genes and signalling pathways has been reported regarding regulation, there are more steps to uncover the interconnection of signalling pathways in case of transportation of the metal inside the plants. Recent development in site targeted mutagenesis with CRISPR/Cas9 can be a better approach to explain proper functions of reported genes. By utilising functional genomic approach, functionality of the chelators and transporters can be altered in bringing biofortification in crop plants.

Acknowledgements

We sincerely acknowledge fellowship obtained from Department of Science and Technology-Innovation in Science Pursuit for Inspired Research (DST-INSPIRE), Government of India, No. DST/INSPIRE Fellowship/2016/IF160804, Dated 12.02.2018.

Abbreviations

FIT

FER-like iron deficiency-induced transcription factor

FRO

Ferric reductase oxidase

ZRT

Zinc regulated transporter

IRT

Iron regulated transporter

YS

Yellow stripe

YSL

Yellow stripe like

FRD

Ferric reductase defective

FRDL

Ferric reductase defective like

MATE

Multidrug and toxic compound extrusion

NADPH

Nicotinamide adenine dinucleotide phosphate

FAD

Flavin adenine dinucleotide

NRAMP

Natural resistance-associated macrophage protein

PS

Phytosiderophores

PEZ

Phenolic efflux zero

DMA

Deoxymugineic acid

MAs

Mugineic acid

VIT1

Vacuolar iron transporter 1

NAS

Nicotianamine synthase

NAAT

Nicotianamine aminotransferase

DMAS

Deoxymugineic acid synthase

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Footnotes

Publisher's Note

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