Iron toxicity: effects on the plants and detoxification strategies

ABSTRACT

Iron (Fe) is an essential micronutrient for plants, as a cofactor in multi-heme cytochromes and within iron-sulfur clusters. However, Fe can be toxic at high concentrations. Free Fe in cells can disrupt the cell redox balance toward a pro-oxidant state, generating oxidative stress. The focuses of this review were to elucidate the Fe detoxification strategies used by plants, as well as describe the Fe excess effects on the plant body and its impact on the physiological, morphological and metabolic traits. Therefore, we highlight the importance of evaluating Fe toxicity and provide a paper compilation on Fe detoxification strategies and morpho-physiological responses to excess Fe, directing further research in this segment.

Keywords:
antioxidant defense system; Casparian strips; iron histolocalization; iron plaque; ferritin

Introduction

Iron (Fe) is an essential micronutrient for plants (Krohling et al. 2016). This element is present in the form of cofactors in multi-heme cytochromes and within iron-sulfur (Fe-S) clusters (Ferousi et al. 2017). The Fe is required for several key biological functions in plants, such as photosynthesis, mitochondrial respiration, nitrogen fixation and metabolism, sulfur assimilation, and hormone and DNA synthesis (Balk & Pilon 2011; Ibañez et al. 2021). However, although Fe is highly abundant in the earth’s crust, it is poorly available to plants under alkaline and oxidative conditions (Lei et al. 2014). According to Araújo et al. (2014) and Grillet & Schmidt (2014), the solubility of Fe³⁺ (the ferric state) decreases as pH increases, while Fe²⁺ (the ferrous state) is easily oxidized in aerated soils, which can cause Fe deficiency in plants (Kaya et al. 2020).

On the other hand, when occurring in high concentrations in plant tissue (above 500 mg Fe kg^-1 leaf dry mass), Fe can disrupt the cell redox balance toward a pro-oxidant state, inducing alterations in the morphological, metabolic, and physiological traits of the plants and generating oxidative stress (Siqueira-Silva et al. 2012; Jucoski et al. 2013). Under Fe excess, plants adopt different strategies to prevent uptake and the free Fe in the cell from reacting with O₂ (Fig. 1) (Saaltink et al. 2017; Araújo et al. 2020a).

Figure 1
Detoxification strategies (A) and disorder in plant homeostasis (B) in response to iron excess.

Iron toxicity can result from environmental disasters promoted by human activities associated with the Fe processing makes Fe excess an environmental problem (Xing et al. 2010; Araújo et al. 2014; Cordeiro et al. 2019; Valeriano et al. 2019). Furthermore, Fe toxicity is a common problem in some areas susceptible to soil waterlogging, resulting in an exponential increase in Fe availability, especially in acid soils (Lapaz et al. 2020). Soil waterlogging can be caused by inappropriate irrigation, high water tables, after heavy rainfall (mainly on compacted soils with poor natural drainage), and in lowland soils (Frei et al. 2016; Krohling et al. 2016; Maranguit et al. 2017). Additionally, some soils naturally present high concentrations of Fe, such as the ferruginous rocky outcrops (Rocha et al. 2020) and acid sulfate soils with concentrations of up to 5000 mg kg^-1 Fe (Becker & Asch 2005).

The increased availability of Fe in waterlogged soil is due to the activities carried out by microorganisms present in the soil to maintain its metabolism through the oxidation of organic matter and their use as final electron acceptors. In this situation, aerobic microorganisms consume all the molecular O₂ as a final electron acceptor and then die from a lack of O₂. Hence, only anaerobic and facultative anaerobic microorganisms remain in the soil. These microorganisms utilize alternative electron acceptors, preferring those that allow the highest energy yields or that are most readily available, such as Fe³⁺ (Maranguit et al. 2017; Lapaz et al. 2020). Thus, the insoluble Fe³⁺ oxides are reduced into a more soluble form (Fe²⁺), which is released into soil pore water and can result in absorption of excess Fe (Lapaz et al. 2020).

Therefore, this review aimed to elucidate Fe detoxification strategies used by plants and to report the most recent findings involved in these response mechanisms, in order to highlight the importance of studying Fe toxicity and show its effect on physiological, morphological and metabolic traits. This compilation should be useful to guide new research in this field of study.

Iron detoxification strategies used by plants

Inhibition of Fe uptake

Mechanisms for dealing with Fe toxicity in plants may be classified into indirect or direct responses (Saaltink et al. 2017). The indirect response is associated with the inhibition of Fe uptake, while the direct response occurs with accumulation of free Fe in the plant (Krohling et al. 2016; Saaltink et al. 2017). In the indirect response, the iron plaque (IP) is formed on the root surface of plants exposed to Fe excess (Fig. 2F-H) (Araújo et al. 2020a, b), that can inhibit the absorption of Fe on the root surface after oxidation of Fe²⁺ to Fe³⁺ (Krohling et al. 2016; Araújo et al. 2020a). On the other hand, in plants exposed to adequate conditions of Fe availability, the IP is not formed (Fig. 2E). Thus, its available quantity in the soil will decrease, forming a smooth, regular precipitate or irregular plaque coating (Siqueira-Silva et al. 2012; Cheng et al. 2014). It is believed that IP formation is controlled by soil Fe availability and the oxidizing capacity of roots, that is, by oxygen radical loss (Li et al. 2017) and/or microbiological oxidation (Wu et al. 2016).

Figure 2
Iron localization in leaves (A-D) and roots (E-H) of Setaria viridis treated with 0.1 mM (A, E) or 7 mM (B-D, F-H) Fe-Citrate during six days in Hoagland's solution. Fresh organs (C, G) or sections of samples fixed and embedded in resin (A, B, D-F, H) were submitted to Perls staining (C, G, H) or Perls/DAB staining (A, B, D-F). Positive staining for the presence of iron occurred in bundle sheath cells (B, D), chloroplasts (D), ferritin (D, F), vacuole (B), trichome (C), iron plaque (F-G). Source: photos taken by author Talita de Oliveira Araújo.

The components of the IP will depend on the biogeochemical factors in which the plant grows (Tripathi et al. 2014). The IP comprises a mixture of crystalline and amorphous Fe (oxyhydr) oxides, mainly Fe³⁺ minerals such as lepidocrocite, goethite, or ferrihydrite (Pardo et al. 2016). Other minerals have also been reported on the root surface, forming the IP, such as jarosite in Imperata cylindrica (Amils et al. 2007) and siderite and ferric phosphate in Typha latifolia (Hansel et al. 2001).

The Fe hydroxide present in the IP can react with electrolytes, such as metals, metalloids, and nutrients, to form complexes in the IP (Cheng et al. 2014; Zhang et al. 2019). The role of the interaction of the IP with the electrolytes is controversial. Some studies have shown that the IP acts as a buffer (Tripathi et al. 2014). When plants lack nutrients, they are remobilized from the IP so that the roots can capture them. For example, Ye et al. (2001) observed in Typha latifolia that IP can act as a Cu reservoir. In contrast, other studies have reported that the IP acts as a physical barrier or an adsorbent that inhibits the uptake, such as As (Wu et al. 2016) and Cd (Huang et al. 2020) in rice, among others (Tripathi et al. 2014). These results show that further research is needed to understand whether the role of IP may vary between plants and/or is a result of different interactions of electrolytes with IP, since the -OH functional group is present in IP and has a high affinity with metals and with some ions.

Role of Casparian strips in preventing Fe translocation

In some plants, the endoderm forms an apoplastic barrier that can prevent the assimilation of metals (Siqueira-Silva et al. 2019). The endoderm includes the innermost cortical layer surrounding the stele. It is responsible for controlling root waterproofing by undergoing two differentiation states: (I) impregnation of cell walls with lignin (giving rise to Casparian strips), followed by (II) addition of suberin lamellae (Doblas et al. 2017). In hyperaccumulator plants, the importance of apoplastic barriers in preventing Fe uptake has been verified (Fig. 1A). For example, Siqueira-Silva et al. (2019) showed that removal of the root apex negatively influences Fe tolerance and avoidance mechanisms in Paspalum densum and Echinochloa crus-galli. Araújo et al. (2020a) observed that the endodermis plays a central role in the control of Fe excess in the vascular system in P. urvillei and Setaria parviflora, while in O. sativa, the endodermis is not such a barrier for the movement of Fe toward the stele. The different responses in the control of Fe traffic toward the stele may be explained by the fact that not all species and/or cultivars use the same mechanisms to mitigate excess Fe, including the suberization of Casparian strips. Barberon et al. (2016) demonstrated that suberization is substantially reduced in IRT1 mutants with Fe deficiency in Arabidopsis, allowing apoplastic and transcellular Fe pathways. Suberization is mediated by the hormones abscisic acid (ABA) and ethylene, which are positive and negative regulators for this response, respectively (Curie & Mari 2017).

Fe sequestration and compartmentalization

Excess Fe in the plant is a potential oxidative stress inducer (Lapaz et al. 2020). In view of this, internal detoxification mechanisms are used by plants as strategies to prevent Fe from reacting with O₂ without affecting the plant's functional demand (Siqueira-Silva et al. 2012; Darbani et al. 2013). The excess Fe is sequestered in vacuoles (Fig. 2B), plastids (Fig. 2D), and/or apoplastic compartments, away from highly sensitive intracellular sites (Araújo et al. 2020a), followed by compartmentalization between the various kinds of organs, including trichomes (Fig. 2C) (Thomine & Vert 2013) or restriction of the compartmentalization of Fe within the root, in order to limit the translocation of Fe toward the shoots (Müller et al. 2017; Bomfim et al. 2021). On the other hand, in plants exposed to adequate conditions of Fe availability, there was no deposition of Fe in vacuoles (Fig. 2A).

The compartmentalization of free Fe tends to dilute its quantity within plant cells. Due to its potential toxicity, Fe is translocated through the plant body associated with chelating molecules and under the proper control of redox states between the ferrous and ferric forms (Kobayashi & Nishizawa 2012). Fe²⁺-nicotianamine (NA) complex is mainly involved in the subcellular distribution and inter-organ partitioning of Fe by the phloem, while Fe²⁺-citrate is considered the main form in which Fe is transported by the xylem (Kobayashi et al. 2019). Iron was histolocated in all tissues of the lateral roots of Ipomoea pes-caprae and Canavalia rosea: epidermis, including root hair, cortical parenchyma, exodermis, endodermis, pericycle, xylem, and phloem (Siqueira-Silva et al. 2012). In roots of P. urvillei, Fe is strongly histolocalized in the epidermis, aerenchyma, endodermis, pericycle, phloem, and protoxylem, whereas in S. parviflora, Fe is histolocalized in the epidermis, phloem, and xylem cells. The two species also showed a positive reaction for Fe histolocalization in cortex cells and in protoxylem and metaxylem cell walls (Araújo et al. 2015).

High Fe accumulation also occurs in the leaves in different plant tissue like spongy parenchyma cells and parenchyma cells of xylem on leaves of Avicennia schaueriana and Laguncularia racemosa, respectively (Arrivabene et al. 2015) and in epidermal cells of leaves of C. hilariana (Silva et al. 2017), suggests the storage of Fe in these tissues as the detoxification strategy in these species for the Fe excess. In P. urvillei, S. parviflora, S. viridis, and O. sativa, Fe accumulation was observed in different cellular compartments in the leaves. The highest Fe accumulation, common to all species, was found in the bundle sheath cells. Within these cells, Fe is highly accumulated in the central vacuole as ferric oxide (Araújo et al. 2020a). In Arabidopsis, the influx of Fe into the vacuoles is mediated via the FPN2 transporter (Morrissey & Guerinot 2009), while VIT1 has a specific function in the vacuolar transport of Fe into xylem parenchyma of developing embryos (Gollhofer et al. 2014). The NRAMP3 and NRAMP4 transporters, when induced by Fe deficiency, export it out of the vacuoles (Darbani et al. 2013; Thomine & Vert 2013).

Fe sequestration as ferritin complexes

Ferritin has a double function in plants: Fe detoxification and storage (Figs. 2D, 2F). Ferritins contain a hollow spherical shell of 24 subunits that can bind up to 4500 Fe atoms in their nucleus (Briat et al. 2010; Araújo et al. 2020a). They are present in chloroplasts and mitochondria (Nouet et al. 2011), which are quantitatively more important for Fe use (Thomine & Vert 2013), as well as they are also present in others plastids located in different plant tissues (Nouet et al. 2011), which are organelles with the greatest potential for Fe detoxification. In addition, ferritins have been found in cell walls and cytoplasm in I. cylindrica, amplifying the known distribution of this structure within the plant (Fuente et al. 2012). In the chloroplast, the reduction of Fe³⁺ via FRO7 (ferric reductase oxidase) is required for incorporation into chloroplasts (Krohling et al. 2016). PIC1 is the permease that imports Fe into the chloroplast. This permease is likely a member of a larger Fe-import complex together with NiCo transporter, where Fe is bound by NiCo first and subsequently transferred to PIC1 (Duy et al. 2011; Müller et al. 2019), while permease MIT is involved in transporting Fe into mitochondria after reduction of Fe³⁺ (Kobayashi et al. 2019; Malhotra et al. 2020).

Ferritins are encoded by four genes in Arabidopsis (AtFer1 to AtFer4) and are regulated mainly at the transcriptional level (Briat et al. 2010). Fe excess and oxidative stress promote AtFer1 gene expression through two independent and additive pathways (Briat et al. 2010). AtFer3 expression in response to excess Fe is very similar to the AtFer1 gene, while AtFer2 is induced by ABA (Petit et al. 2001). However, ferritin-null mutants in A. thaliana are less affected by Fe excess (Ravet et al. 2009), despite the high Fe-buffering capacity of ferritins. This finding opens up avenues for further research on the role of these proteins in Fe detoxification mechanisms in different crops. Müller et al. (2017) investigated the tolerance responses to excess Fe and suggested that ferritin may contribute to growth and survival after observing a strong increase in OsFER1 expression in the leaves of O. sativa cultivars. Wu et al. (2017) also found an increase in ferritin expression in rice cultivars with contrasting tolerance to Fe, but no genotypic differences were observed. DeLaat et al. (2014), studying Phaseolus vulgaris, found that water deficit combined with excess Fe substantially increased the expression of three ferritin genes (PvFer1, PvFer2, and PvFer3), but with different kinetics.

Some research has reported the role of the cell wall in response to Fe deficiency in the fixation and redistribution of Fe between roots and shoots (Lei et al. 2014; Ye et al. 2015, Zhu et al. 2016). These responses are related to the traits of cell wall components, in particular pectin and hemicellulose, which are highly negatively charged polysaccharides and thus represent a sink for cationic nutrients (Curie & Mari 2017). According to Fuente et al. (2012) and Araújo et al. (2020a), the cell wall contains a large pool of high Fe concentrations in the plant. Fuente et al. (2012) suggested that the deposit of jarosite on the cell wall in I. cylindrica may be related to the degradation of ferritin and phytosiderin. In P. urvillei, S. parviflora, and O. sativa, the chemical form of this pool of Fe in the cell wall has not been identified, whereas S. viridis accumulates Fe in ferritins (Araújo et al. 2020a). Based on reports from the literature, the characterization of biomineralized Fe deposits is limited and the signaling mechanisms involved in this process as a strategy to detoxify excess Fe have not yet been described. Hence, there is a need for further research in this segment, as well as verifying these responses in different species.

Tolerance to the generation of reactive oxygen species (ROS)

When excessive absorption and the accumulation of free Fe occur in plant tissue (Fig. 1A), the cell redox balance can be displaced to a pro-oxidant state and generate oxidative stress (Jucoski et al. 2013; Müller et al. 2017; Lapaz et al. 2020). Therefore, Fe excess could potentially increase the overproduction of ROS (Fig. 1B) (Pinto et al. 2016; Araújo et al. 2020b).

In this context, accumulation of Fe²⁺ becomes highly toxic to plants cells because it catalyzes hydrogen peroxide (H₂O₂) decomposition, generating the hydroxyl radical (HO^•), according to the Fenton reaction: Fe 2+ + 𝐻 2 𝑂 2 → Fe 3+ +HO • + 𝐻𝑂 − . Fe3+ produced by this reaction can be reduced to Fe2+ by the superoxide anion radical (O₂•-) via the Haber-Weiss reaction, allowing Fe2+ to again participate in the Fenton reaction, according to the following reaction: 𝐹𝑒 3+ + 𝑂 2 •− → 𝐹𝑒 2+ + 𝑂 2 (Becana et al. 1998; Lapaz et al. 2020). ROS can lead to peroxidation, including cell collapse and even tissue deterioration. In addition, they cause the oxidation of sugars, proteins, nucleic acids, and lipids, electron transport disruption, and enzyme inhibition/activation (Pereira et al. 2009; Xu et al. 2015).

To contain oxidative stress, plants respond by activating enzymatic antioxidant defense pathways (superoxide dismutase - SOD (EC 1.15.1.1), catalase - CAT (EC 1.11.1.6), peroxidase - POX (EC 1.11.1.7), ascorbate peroxidase - APX (EC 1.11.1.11), glutathione peroxidase - GPX (EC 1.11.1.9), and glutathione reductase - GR (EC 1.6.4.2)) and/or non-enzymatic antioxidant defense pathways (ascorbate - AA, glutathione - GSH, carotenoids, tocopherol, ubiquinol, uric acid, and lipoic acid) (Jucoski et al. 2013, Krohling et al. 2016). The combined SOD and POX enzyme activity has been established to be largely responsible for preventing Fe2+-induced oxidative stress in O. sativa leaves (Becker & Asch 2005). Hence, the increasing antioxidant potential of plants is considered as one of the useful strategies to mitigate the effects of ROS overload (Ahammed et al. 2020). However, there is a threshold of enzyme activity; that is, the protective function of antioxidant enzymes may be limited in the face of an exorbitant production of ROS (Xing et al. 2010).

Fe impacts on physiological, morphological and metabolic traits

The different strategies adopted by Fe-resistant species involve mechanisms to neutralize the damage caused by the Fe presence (Fig. 1A) (Siqueira-Silva et al. 2012; Krohling et al. 2016; Kobayashi et al. 2019; Siqueira-Silva et al. 2019; Araújo et al. 2020a), while sensitive species, in turn, may be strongly impacted by Fe (Fig. 1B) (Neves et al. 2009). Iron ore industries can disturb the nearby vegetation (Silva et al. 2017; Silva et al. 2020) which deserves attention because the exposition of sensitive species to Fe leads to a decrease in biodiversity over the years (Arrivabene et al. 2015). The loss of the structure and function of cell membrane promoted by the lipid peroxidation due to the ROS excess promotes changes in the plant cells (Araújo et al. 2020b), which can compromise the anatomy of organs and their functionality, thus impair key plant processes.

Iron toxicity is a complex phenomenon and dependent on many different aspects, such as the sensitivity of the species, the plant organ, time of Fe exposure, Fe soil concentration, soil pH, exchangeable Fe content and Fe uptake and its translocation in plant body (Becker & Asch 2005; Nagajyoti et al. 2010; Pandey & Verma 2019). In I. pes-caprae roots, Siqueira-Silva et al. (2012) found that Fe promoted morphological changes like growth retarding, flaccidity and decreased branching, necrosis and collapse of the apex of the lateral roots. Santana et al. (2014) described derangement of mesophyll cells, presence of hypertrophied cells alteration on wall shape and differentiation of metaxylem elements, decreased volume of bulliform cells as an anatomical alteration in tolerant grass species to Fe excess.

The Leaf bronzing (i.e., coloration caused by the accumulation of phenols in the vacuole) is commonly indicated as a typical symptom of stress caused by Fe excess (Wu et al. 2014; Pinto et al. 2016). Silva et al. (2017) described chlorosis, necrosis, foliar abscission and spotted necrosis, purplish spots on the leaves and an increase in the emission of new leaves completely purplish as visual symptoms found in C. hilariana and Eugenia uniflora plants growing near a Fe pelletizing factory. Moreover, Zhang et al. (2016) noticed that Fe toxicity can promote a global and progressive disorder in cell protoplasm, generating a deformed and shrunken appearance in the cell, which may lead toward programmed cell death.

The Fe histolocalization in plant tissues through histochemical methods is a complementary tool for studies of Fe toxicity in plants because it allows to spatially characterize the distribution of the element in the different tissues and even organelles of the cell, showing the main sites of accumulation on the plant body (Silva et al. 2006; Sivaprakash et al. 2006). Perls/DAB method (Roschzttardtz et al. 2009) and Prussian Blue (Stevens & Chalk 1996) for instance are used to highlight iron in the plant tissues. Several authors used histolocalization techniques to show Fe accumulation in tissues such as endodermis, epidermal cells, shoots, xylem vessels, and organelles such as chloroplasts (Di Toppi et al. 2012; Arrivabene et al. 2015; Silva et al. 2017; Araújo et al. 2020a).

The impact of Fe toxicity on physiological traits can reflect a decrease in gas exchange traits and chlorophyll content, deactivation of PSII reaction center and a decrease in saturated fatty acids and increase unsaturated fatty acids in chloroplast membrane in Pisum sativum (Xu et al. 2015). Pereira et al. (2013) observed a decrease in photosynthesis rate in O. sativa due to stomatal and non-stomatal limitations, with non-stomatal limitation more severe in the most sensitive cultivar. Müller et al. (2017) studying O. sativa, found that upland cultivars displayed a mechanism to limit Fe translocation from roots to the shoots, minimizing leaf oxidative stress induced by excess Fe, while lowland cultivar invested in the increase of CO₂ production rate, as an alternative drain of electrons. In Ipomoea batatas, it was observed that exposure to excess Fe caused an increase in chlorophyll content and a decline in net CO₂ assimilation rate, as well as a reduction in the production of nicotinamide adenine dinucleotide (NADPH) and adenosine triphosphate (ATP) (Adamski et al. 2011). According to Lapaz et al. (2020), starch and ureide accumulation could be considered efficient biomarkers of phytotoxicity caused by soil waterlogging and Fe excess in Glycine max.

Conclusions and future perspectives

Strategies against Fe toxicity were evolutionarily selected and can provide protection to the plant species to grow on Fe-rich soils. This review discussed the Fe detoxification strategies used by plants: (I) inhibition of Fe uptake through the formation of IP, (II) inhibition of Fe translocation to the stele by Casparian strips, (III) sequestration and compartmentalization of Fe in vacuoles, plastids and apoplastic compartments that can be histolocalized through different histochemical tests, and (IV) tolerance to the generation of ROS.

We also showed that strategies can vary among species and cultivars, being pronounced to different degrees or even not important in some plants. Additionally, plants can have its homeostasis disturbed when dealing with Fe toxicity, affecting physiological, morphological and metabolic traits. In this context, a thorough understanding of Fe-excess effects on plants and their detoxification strategies should facilitate the development of new tools that allow the selection of Fe-tolerant species via conventional breeding or biotechnological strategies.

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Publication Dates

• Publication in this collection
  29 Apr 2022
• Date of issue
  2022

History

• Received
  17 Apr 2021
• Accepted
  02 Dec 2021