Iron Toxicity and its Management in Rice: A Comprehensive Review

Iron is crucial for all living organisms as it is essential for metabolic functions like respiration, photosynthesis and DNA synthesis. It is also involved in enzymes and chlorophyll synthesis. Lowland rice production is primarily affected by iron toxicity, which occurs in wet soils and is associated with elevated levels of reduced iron (Fe²⁺). This leads to the “bronzing” of rice leaves, resulting in production losses. Iron toxicity has been found in South America, Asia and Africa. Other soil types where iron toxicity can occur include acid sulphate, acid clay, peat, valley-bottom soils, ultisols, oxisols, sandy soils and low to moderately high organic matter content.
 
Symptoms of iron toxicity in rice
 
Fe toxicity symptoms may initially manifest within 1 to 2 weeks after transplantation, although they can also take longer than 2 months to appear. Initially, small brown spots form on the tips of older leaves and gradually spread toward the base. In severe cases, the entire leaf is affected. Leaf bronzing is observed in potassium-deficient rice plants that cannot sustain adequate root oxidation capacity. Limited growth, significantly decreased tillering, a thick, sparse and compromised root system exhibiting a dark brown to black coating on the root surface, along with numerous dead roots (Dobermann and Fairhurst, 2000). As the symptoms progress, the leaf tips in some rice varieties turn orange-yellow and dry out. These effects are especially noticeable in older leaves with higher rates of transpiration (Yamanouchi and Yoshida, 1981). The entire leaf turns orange, reddish brown, or even purple-brown under extreme toxicity situations (Fairhurst and Witt, 2002). According to Abu et al., (1989), toxicity during the vegetative stages reduces plant height and dry matter production; the biomass of the shoots is more negatively affected than that of the roots (Fageria, 1988). A decrease in the number of panicles per hill (Singh et al., 1992), increased spikelet sterility (Virmani, 1977) and delays in blooming and maturity of up to 20-25 days are all associated with iron toxicity during the late vegetative or early reproductive stages. Plant height, panicle length, the number of productive tillers and total yield are all reduced by iron toxicity (Abraham, 1989).
 
Effects of iron toxicity
 
There are two main ways that metal poisoning in agricultural plants presents itself. The first type, known as direct toxicity, is when metals are taken in excess and have fatal effects on the cells of the plant. Indirect toxicity is the second type, which is related to interfering with plant’s ability to absorb and utilize vital nutrients. The plants experience nutritional imbalances as a result of this indirect poisoning.

Interestingly, this form of iron toxicity (indirect toxicity) is more common in lowland rice than direct toxicity (Fageria et al., 2006). Zinc  (Zn), potassium (K) and phosphorus (P) are the three main nutritional deficiencies seen in Brazilian rice that is flooded or irrigated (Barbosa et al., 1983). Furthermore, the effect of iron (Fe) toxicity on rice cultivar production differs according to the cultivar’s tolerance or sensitivity to this toxicity.
 
Fe uptake mechanism
 
Iron is primarily found in oxidized soils in the ferric state (Fe³⁺), which is linked to oxides and hydroxyoxides and causes low solubility. To effectively absorb iron, plants need to transform it into the Fe²⁺ form. To combat iron deficiency, plants have developed two primary defense mechanisms, as shown in the Fig 1. In the first method of iron uptake, roots release of protons (H⁺), which lowers the rhizosphere’s pH, allowing reduced iron to be absorbed through a transport pathway for Fe²⁺ across the plasma membrane. Primarily, dicots and nongraminaceous monocots employ this strategy. Phytosiderophores, substances that bind to Fe³⁺ without changing it into Fe²⁺, are secreted by crop plants as a second method for iron uptake. These chelating chemicals, such as avenic and mugineic acids, are nonprotein amino acids. The greening of chlorotic tomato mutants may be supported by iron transfer within cells due to structural similarities to nicotianamine, a substance found in green plants that helps mobilize iron (Epstein and Bloom, 2005).



Fe uptake mechanism by rice
 
As shown in Figure 2, waterlogging reduces ferric iron (Fe³z ) to the more soluble ferrous iron (Fe²z ) in the soil by creating an anaerobic environment (Aung and Masuda, 2020). There is a notable buildup of Fe²⁺ as a result of this reduction, which mostly takes place in the anaerobic soil layer (2–15 cm depth). This excess Fe²⁺ is absorbed by plant roots, where it may result in iron plaques, Fe (OH)^ƒ on the root surfaces. Iron overload occurs in the plant’s tissues when excessive Fe²⁺ uptake overwhelms the plant, even if these plaques can occasionally serve as a barrier. Fenton reactions are set off inside the plant by Fe²⁺, generating reactive oxygen species (ROS) that cause oxidative stress and harm cellular components like membranes, proteins, and DNA. This manifests as bronzing symptoms on leaves and, in severe cases, leads to reduced growth, poor yield, or crop failure.


 
Factors inducing iron toxicity
 
Iron poisoning in rice rhizosphere occurs when solubility and concentration of iron exceed plant needs. Soil conditions affecting these factors are not fully understood (Fageria et al., 1990), but include iron release, oxidation-reduction potential, low pH, ionic strength, fertility, organic matter, microbial activity, and plant genetic variability.
 
Release of iron into the soil solution from the parent material
 
Goethite, hematite, pyrite, siderite, and magnetite are among the iron minerals found in soils (Fageria, 2013). Iron released into the soil solution by parent materials can be harmful to plants, particularly rice plants. Kosaki and Juo, (1986) found a strong correlation between Fe²⁺ iron levels in Nigerian soil and bronzing, a condition in West African rice plants living in lowlands, inland valley swamps, and hydromorphic settings, indicating iron poisoning as the main cause.
 
Oxidation-reduction potential
 
The chemical process of oxidation-reduction involves the exchange of electrons between substances. The oxidation number of the electron acceptor decreases and becomes decreased when the electron donor loses electrons, increasing its oxidation number. Organic materials provide electrons for biological reduction processes (Ponnamperuma, 1972). The conversion of Fe³⁺  to Fe²⁺  increases absorption, but as Fe²⁺ is converted to Fe³⁺, its concentration decreases, causing plants to absorb less. Submerged soils undergo various reduction processes, including H⁺  to H₂, CO₂ to CH₄, nitrate to dinitrogen, sulphate to H₂S and  Fe³⁺ to Fe²⁺. Redox potential, measured in millivolts, influences these processes.
 
Soil pH
 
Because of the dynamic interactions between plants, microbes and soil processes, the pH of soil varies greatly (Adams, 1984). Iron changes into less soluble forms when pH increases, mostly as the oxide FeO₃ . Acidic soils are more harmful to iron than alkaline ones. While the pH of sodic and calcareous soils lowers when submerged, the amount that the pH of acidic soils changes depends on crop rotation, fertility, organic matter, rice cultivar and soil type. Soils rich in organic matter and reducible iron typically achieve a pH of approximately 6.5 after a few weeks of immersion (Ponnamperuma, 1972).
 
Ionic strength
 
The electrical environment that surrounds ions in a solution is measured by a property called ionic strength. As macro- and micronutrients are released into the soil solution, ionic strength increases in submerged soils, improving rice plant absorption of Fe²⁺ and raising iron toxicity. This rise is associated with the solubilization of phosphorus and the decrease of Fe²⁺ and Mn²⁺ in acidic soils. It happens in alkaline soils when Fe²⁺ iron from reduction processes displaces cations (Patrick and Mikkelsen, 1971).
 
Low soil fertility
 
Iron toxicity in rice can be caused by essential nutrient deficits in wet or depleted soils. Nutrients like potassium, phosphorus, calcium and magnesium can hinder iron absorption, increasing the risk. According to Yamauchi, 1989 increasing potassium levels in shoots can improve rice dry matter output and reduce iron toxicity. According to Trolldenier, (1977), Low potassium and phosphorus levels can exacerbate toxicity. Increased nitrogen levels may promote excess iron absorption. High salinity can also increase iron intake due to chemicals like magnesium or sodium chloride (Breemen and Moormann, 1978).
 
Interaction with other nutrients
 
Iron can interact with other nutrients in a neutral, antagonistic, or synergistic manner, depending on how the plants respond to their growing environment. In rice plants, manganese is an example of an antagonistic connection with iron (Olsen and Watanabe, 1979). The amount of iron that rice absorbs is significantly reduced when manganese is supplied to the soil. Fageria et al., (1981) found that as the iron concentration in the nutritional solution increased from 0 to 160 mg Fe L^-1, the absorption of phosphorus, potassium, calcium and magnesium decreased. Calcium and magnesium absorption decreased linearly as the amount of iron in the nutritional solution increased.
 
Adaptation strategies
 
The three main types of adaptation strategies include" avoidance" and "tolerance" based procedures, as well as  "includer" and "excluder" tactics.
 
Strategy Ia-iron oxidation occurring at the root surface
 
Rice roots need to pass through an oxidation barrier in the rhizosphere before absorbing Fe²⁺ from the soil. This barrier is created by transporting molecular oxygen from the air to the roots via the aerenchyma, a gas-conducting tissue that increases ethylene synthesis (Kawase, 1981). In flooded rice, aerenchyma can occupy up to 50% of root volume (Armstrong, 1980), with effectiveness varying by growth stage. Early and sustained aerenchyma formation is crucial for iron tolerance, especially under iron-toxic soil conditions (Jayawardena et al., 1977).
 
Strategy Ib-selectivity of root membranes
 
Iron, which enters the root apoplast after passing through the rhizosphere’s oxidative barrier, can be rejected by root cell membranes (Tadano, 1976; Green and Etherington, 1977). In healthy plants, up to 87% of iron can be blocked by the endodermal barrier. This process, which depends on energy, can be hindered by high Fe²⁺ concentrations (Tadano, 1975) and dietary deficiencies in Ca, K and P (Yamanouchi and Yoshida, 1981). It is sensitive to environmental conditions and plant growth stages, making it less effective under severe iron toxicity or during seedling-stage toxicity.
 
Strategy IIa-retention within root and stem tissues
 
Iron in plants can be immobilized at storage sites, but it rises with transpiration once it enters the xylem. Root tissues contain "metabolically inactive" iron (Tanaka et al., 1966) and as plants age, their roots store less iron (Tadano, 1976). Fe²⁺ may become immobile in stem or leaf sheath tissues during transit. Iron-tolerant West African rice varieties typically retain more iron in leaf sheaths than blades (Audebert and Sahrawat, 2000). Phytoferritin production may be part of this iron withdrawal (Seckbach, 1982; Smith, 1984), but its efficacy varies with Fe²⁺ transport rates and may decrease in heavy transpiration or growth cycle.
 
Strategy IIb-retention within the leaf apoplast
 
Kosegarten et al., (1999) suggest that iron mobility in leaves is influenced by apoplastic pH, with higher pH causing Fe²⁺ oxidation and acidic pH promoting absorption (Mengel and Kosegarten, 2000; Nicolic and Römheld​, 2001). Non-diffusible polymers inhibit certain polysaccharides and ferric-chelate reductase activity (Schmidt, 1999; Lucena, 2000). In plants without pH regulation, excess Fe²⁺  can accumulate uncontrollably in leaf cells (Welch et al., 1993).
 
Strategy III-tolerance in symplastic tissues
 
Fe²⁺ in plant symplasts can cause oxidative damage, necessitating neutralization for tissue tolerance. Binding Fe²⁺ to phytoferritin helps control oxidation processes. Ascorbate and glutathione reduce oxidative stress. Zinc increases superoxide dismutase (SOD) enzyme activity, enhancing iron tolerance. Hydrogen peroxide requires detoxification by peroxidases or catalases. SOD and peroxidases must work together to manage stress, especially during seedling toxicity and transplanting stress. Genetic variations in these responses are poorly understood and not used for screening in rice breeding.
 
Defense mechanism
 
As shown in the Fig 3. Plants have developed 4 defense mechanisms to control and mitigate iron levels.


 
Defense 1: Fe exclusion by roots
 
The first line of defense is to keep excessive amounts of iron out of the plant’s root system. Genes like OsIRT1, OsNRAMP1, OsYSL2, OsYSL15, TOM1, OsNAS1, OsNAS2, OsDMAS1 and OsNAAT1 mediate iron transfer into the root cells. HRZ functions as a regulatory protein that prevents the activation of the aforementioned Fe uptake genes, hence reducing Fe absorption.
 
Defense 2: Fe retention in roots
 
The second defense activates if Fe enters the roots, aiming to contain and immobilize it within root cells. The genes such as OsFERs, OsVIT2 are help to store iron within root cells, particularly by sequestering it in specific compart-ments where it is less likely to cause harm, OsNAS3 aids in binding Fe to specific molecules, which helps in storing and immobilizing it, OsWRKYs may regulate the retention process and activate other Fe-related defense mechanisms.
 
Defense 3: Fe mitigation in shoots
 
The third defense aims to handle Fe that reaches the shoots, specifically in the leaf cells, by storing it safely and preventing damage. The protein OsFERs helps store Fe in leaf cell compartments like chloroplasts and vacuoles, which are specialized for storage and can contain Fe safely, the OsVIT2 transporter moves Fe into the vacuoles within leaf cells, reducing free Fe that could be toxic and OsNAS3 binds Fe with compounds like nicotianamine (NA), forming stable complexes that reduce Fe reactivity and toxicity.
 
Defense 4: ROS detoxification
 
Reactive oxygen species (ROS), which are harmful byproducts of iron buildup, can be produced by an excess of iron. In order to save plant cells from oxidative damage, this last line of defense neutralizes ROS. Transcription factors known as OsWRKYs regulate and activate genes related to ROS detoxification. The cytochrome 450 enzyme may aid in controlling ROS levels and is engaged in a number of detoxifying procedures. Transcription factors OsNAC4, OsNAC5 and OsNAC6 may activate genes that aid in ROS detoxification and are involved in stress responses. The GSNOR enzyme aids in preserving cellular equilibrium and detoxifying dangerous ROS.
       
By using these techniques, the plant efficiently controls excess iron, avoiding toxicity and preserving the health of its cells throughout all of its tissues.
 
Management practices
 
Using tolerant cultivars like IR8192-200, IR9764-45 and Mahsuri is the most effective and cost-effective way to address this problem (Dobermann and Fairhurst, 2000). Chuvannamodan, an indigenous landrace of Kerala and Varsha, a mid-early, high-yielding redkernelled rice variety, shown tolerance to high iron concentrations (> 600 ppm) (Suma et al., 2022). Although they have a somewhat lower potential yield, African cultivars are often more resistant to this stress than Asian ones. Regarding water management, the effects of drain time and length for 6 and 9 days within 30 days post-transplanting, soil improvement and fertilizer application, the Indragiri variety demonstrated the highest tolerance to iron toxicity. The most efficient way to achieve grain output under Fe toxicity was to combine a 75% seed treatment, 90 kg/ha of P₂O₅ and 100 kg/ha of K₂O. This significantly boosted rice production in the acid sulphate soils of tidal swamplands (Khairullah et al., 2021). By lowering the amount of iron available in the soil solution, efficient irrigation water management successfully decreased the amount of iron toxicity in rice plants cultivated in field circumstances. In 2021, de Campos et al. in acid sulphate soils, leaching every two weeks and adding 2.5 tons of organic matter per hectare are recommended as ways to lower iron toxicity and increase rice output (Nugroho et al., 2022). Iron toxicity and soil acidity in paddy soils derived from laterite can be effectively managed by applying a combined total of 300 kg/ha of limestone powder and 300 kg/ha of phosphogypsum. This joint application enhances nutrient availability, improves nutrient uptake by plants and promotes rice growth and yield (Joseph et al., 2020). Mini and Lekshmi, (2021) were discovered that the best treatment for increasing yield by 23% was a combination of soil test-based RDF + rice husk ash @ lime (based on pH) + foliar spray of 0.5% solution of customized formulation @ 5 kg ha^-1 as foliar application of 0.5% solution in two splits at maximum tillering and panicle initiation stage. The B:C ratio also increased from 1.53 to 1.91. Grain and straw yields increased significantly when 5 tons of organic matter, 90:45:120 kg of N:P:K 150 kg of lime and 100 kg of silica were applied per hectare. Additionally, silica application helps reduce the prevalence of pests (Yadav et al., 2017). In temperate regions where seeds are sown directly, coating seeds with oxidants, such as calcium peroxide (at 50100% of the seed’s weight), can enhance germination and seedling growth by boosting oxygen availability. Postpone planting until the peak levels of Fe have subsided. Opt for intermittent irrigation instead of continuous flooding on poorly drained soils with high levels of iron and organic matter. Perform dry tillage after harvesting rice to enhance iron oxidation during the fallow period, helping to minimize iron accumulation during the next flooding phase (Dobermann and Fairhurst, 2000). One effective strategy to lessen the negative effects of Fe toxicity on rice output and photosynthesis is the use of Si (Dos Santos et al., 2020).

A major problem impacting rice production is iron toxicity, especially in regions where soil iron concentrations are high. This is because the ferrous ion (Fe²⁺) is more soluble in anaerobic settings, like rice fields that are submerged. This causes oxidative stress, which hinders the growth and development of plants. Reduced output and symptoms like leaf bronzing emphasize how urgently this agricultural issue needs to be resolved. Many techniques are used to reduce iron toxicity and improve rice tolerance, including as providing organic matter, managing water levels, applying particular potassium fertilizers and creating rice cultivars that are resistant to iron toxicity. The identification of brassinosteroids and quantitative trait loci (QTLs) can also improve resistance to iron toxicity. To create sustainable management strategies that incorporate chemical and biological interventions, more study is required and biotechnology advancements can produce cultivars with improved tolerance features. A comprehensive understanding of iron toxicity and its management is crucial for sustainable farming methods. 

The authors say that there is no conflict of interest.