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Molnár, Z.; Solomon, W.; Mutum, L.; Janda, T. Mechanisms of Fe Deficiency in the Rhizosphere. Encyclopedia. Available online: https://encyclopedia.pub/entry/44325 (accessed on 20 November 2024).
Molnár Z, Solomon W, Mutum L, Janda T. Mechanisms of Fe Deficiency in the Rhizosphere. Encyclopedia. Available at: https://encyclopedia.pub/entry/44325. Accessed November 20, 2024.
Molnár, Zoltán, Wogene Solomon, Lamnganbi Mutum, Tibor Janda. "Mechanisms of Fe Deficiency in the Rhizosphere" Encyclopedia, https://encyclopedia.pub/entry/44325 (accessed November 20, 2024).
Molnár, Z., Solomon, W., Mutum, L., & Janda, T. (2023, May 15). Mechanisms of Fe Deficiency in the Rhizosphere. In Encyclopedia. https://encyclopedia.pub/entry/44325
Molnár, Zoltán, et al. "Mechanisms of Fe Deficiency in the Rhizosphere." Encyclopedia. Web. 15 May, 2023.
Mechanisms of Fe Deficiency in the Rhizosphere
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This entry is adapted from the peer-reviewed paper 10.3390/plants12101945

One of the most significant constraints on agricultural productivity is the low availability of iron (Fe) in soil, which is directly related to biological, physical, and chemical activities in the rhizosphere. The rhizosphere has a high iron requirement due to plant absorption and microorganism density. Plant roots and microbes in the rhizosphere play a significant role in promoting plant iron (Fe) uptake, which impacts plant development and physiology by influencing nutritional, biochemical, and soil components. The concentration of iron accessible to these live organisms in most cultivated soil is quite low due to its solubility being limited by stable oxyhydroxide, hydroxide, and oxides. The dissolution and solubility rates of iron are also significantly affected by soil pH, microbial population, organic matter content, redox processes, and particle size of the soil. In Fe-limiting situations, plants and soil microbes have used active strategies such as acidification, chelation, and reduction, which have an important role to play in enhancing soil iron availability to plants. In response to iron deficiency, plant and soil organisms produce organic (carbohydrates, amino acids, organic acids, phytosiderophores, microbial siderophores, and phenolics) and inorganic (protons) chemicals in the rhizosphere to improve the solubility of poorly accessible Fe pools. The investigation of iron-mediated associations among plants and microorganisms influences plant development and health, providing a distinctive prospect to further our understanding of rhizosphere ecology and iron dynamics.

rhizosphere iron deficiency iron acquisition microorganisms

1. Introduction

Iron (Fe), the fourth most abundant and necessary micronutrient for the growth of plants and other organisms, is insoluble in neutral and alkaline soils, making it unavailable to plants. Fe is considered a vital element in the plant system for controlling life-sustaining processes, such as respiration, nitrogen fixation, photosynthesis, assimilation, the synthesis and repair of nucleotides, metal homeostasis, hormonal regulation, and chlorophyll production due to its redox-active nature under biological circumstances [1][2][3][4][5]. Fe can exist in two different oxidation states (Fe2+ and Fe3+), and it can switch between them by receiving and giving away electrons. In crucial metabolic pathways, such as respiration and photosynthesis, which are needed for plants to make energy, iron plays a key role in enzyme reactions requiring electron transfer [2][6].
Although total Fe is a highly plentiful element in the soil, its accessibility to plants is generally quite low [7]. Thus, insufficiency of iron is one of the most significant limiting variables that influences crop yields, the quality of food, and human nutrition. Inadequate iron absorption results in interveinal chlorosis, stunted growth, reduced nutritional value, and diminished plant yield. Iron deficiency-induced anemia, one of the world’s most common nutritional disorders, requires adequate iron levels in food crops [8]. According to reports, one third of the world’s farmed lands suffer from Fe deficiency, resulting in a considerable annual drop in agricultural productivity, especially in calcareous soils [9][10].
Fe deficiency causes major changes in a plant’s physiology and metabolism, slowing plant growth, impacting nutritional quality, and lowering yield [11], which, in turn, affect the health of people through the food chain, especially those with diets high in plant-based foods.
Plants must boost soil iron’s mobility to overcome its limited availability. In response to Fe deficiency, plants have evolved sophisticated systems to maintain cellular Fe homeostasis by modifying their physiology, morphology, metabolism, and gene expression to enhance Fe availability [12][13]. Basically, these methods involve: (i) acidification, which is facilitated by the secretion of organic acids or protons; (ii) chelation of Fe3+ by ligands, which may include siderophores that have an extremely strong affinity for Fe3+; and (iii) the reduction of Fe3+ to Fe2+ through the action of reductases and reducing substances [14][15][16].
Most of the physical, chemical, and biological activities in soil are linked to the geochemistry of iron (Fe) [17] and, consequently, to how much iron is available to the microorganisms and plants that grow in the soil. Iron is mostly found in the rhizosphere as Fe3+, which is inaccessible to plants. The rhizosphere is a thin, dynamic zone with substantial abiotic and biotic interactions between soil microorganisms and plant roots [18]. Plant metabolism strongly influences the rhizospheric environment through the release of 5–21% of photosynthetic material by root exudates [19]. Rhizosphere activities and the rhizosphere’s impact on plants are mostly controlled by the release of a complex combination of low and high molecular weight compounds from roots, such as carbohydrates, amino acids, organic acids, protons, phytosiderophores, enzymes, and phenolics [20]. Several microorganisms that interact with plants release siderophores in response to an iron deficiency [21]. These substances can modify the physical, biological, and chemical properties of the soil near the roots.

2. Dynamics of Iron in the Rhizosphere

2.1. Status of Fe in the Rhizosphere and Soil

The rhizosphere is the active zone across a plant root that is home to a diverse population of microorganisms and is impacted by the chemicals produced by plant roots. Rhizosphere processes are the communications between plant roots–soil–microbes that occur and alter continually, impacting things such as nutrient solubility, their movement through the soil, and plant absorption. These systems’ primary driving force seems to be tied to processes of root exudation (Figure 1). Root exudates are organic and inorganic chemicals released by plant roots. They include high and low molecular weight substances, such as carbohydrates, proteins, amino acids, organic acids, protons, polypeptides, enzymes, and hormones, in the rhizospheric soil environment [22][23]. Rhizosphere priming effect occurs when plant roots release recently formed photosynthates into the rhizosphere, which speeds up the breakdown of organic materials by saprotrophic soil bacteria and increases plant nutrient availability [24]. Increased root exudates in the soil improve microbial biomass and soil fertility levels. The dynamics of Fe in the rhizosphere can also be affected by organic compounds generated by the degradation of soil organic matter. These soil microorganisms are essential for the nutrient transformation in the soil and crop plant nutrition absorption. Plants may affect soil qualities by modifying the composition of root exudates, allowing them to adapt and survive under severe environments.
Plants 12 01945 g001 550
Figure 1. Mechanisms that alter the availability of iron in the rhizosphere. Plants and microbes can improve the bioavailability of iron via (a) acidification—secretion of protons and organic acids, (b) chelation—excretion of complexing molecules with varying affinities for Fe (siderophores, phytosiderophores, carboxylic acids, and phenolics), and (c) reduction—release of substances with reducing characteristics or development of a membrane-bound reductase activity.
Iron is one of the most plentiful elements in the soil, but after it is weathered, Fe(III) and Fe(II) ions can be released through dissolution and oxidation/reduction. However, when hydroxyl ions (OH-) are present, it almost always forms Fe hydroxides and oxides, which have very poor solubility [14]. The dissolution and solubility rates of pedogenic iron oxides (oxides, oxyhydroxides, and hydroxides) play an important role in regulating iron accessibility. The dissolution and solubility rates of iron soil oxides are also significantly affected by pH, microbial population, organic matter content, redox processes, and particle size of the soil [7][14][15][25][26]. Soil pH is the most important of these parameters since it can decrease Fe availability by as much as 95% for every unit increase in soil pH above neutral [27]. When the pH is lowered, the ferric iron is released from its bond with the oxide, making it easier for the roots of plants to absorb it [28]. Fe is transformed to an insoluble Fe–hydroxyl compound in salty, calcareous, alkaline, and sodic soils, which prevents the element from being taken up by plant roots [25]. Soil organic matter level and its breakdown rate affect Fe accessibility because of the formation of excess bicarbonates and phosphates, which hinder the uptake of Fe [4][29].
One of the most significant constraints on agricultural productivity is the low accessibility of iron (Fe) in the soil, which is directly linked to the biological, physical, and chemical activities taking place in the rhizosphere due to the interactions between the soil, microorganisms, and plants [20]. It is widely known that plant roots can alter the pH of the rhizosphere by releasing protons through the H-ATPase enzyme in epidermal cells [30]. This can also occur during Fe deficiency; thus, the plant’s impact on pH can result in the exudation of inorganic metals through the plant roots. Iron deficiency causes soil organisms to emit organic (carbohydrates, amino acids, organic acids, phytosiderophores, phenolics, siderophores, and enzymes) and inorganic (protons) chemicals to improve the solubility of inaccessible Fe pools [20]. Soil pH can be lowered by the plant’s secretion of low molecular weight organic acids [30]. Thus, in order for microorganisms to survive and flourish, the rhizosphere is a geographically and temporally uneven habitat with quick changes in potentially harsh conditions, such as cycles of water stress and anaerobiosis.
It has been extensively documented that metal complexation by humic substances derived from various sources improves plant iron nutrition. The chelation of Fe3+ by the organic ligands that comprise the dissolved organic matter has a substantial effect on the solubility of soil iron as well. Reported by [31], more than 95% of the Fe in soil solution is probably complexed or chelated. Depending on the molecular size of humic substances (HS) and solubility, the presence of humified fractions of organic matter in soil sediments and solutions might help provide a reservoir of Fe for plants that exhale metal ligands and supply Fe–HS complexes that are directly utilizable by plant Fe absorption processes [32]. In addition to having iron-chelating qualities, which help enhance iron bioavailability, humic substances also exhibit redox-reactive properties [33].

2.2. Iron Interaction with Plant and Rhizospheric Microorganisms

In the rhizosphere, iron competition is important for microbial and plant–microbe interactions. Competition for Fe occurs among microbes and plants, regarding which has the competitive edge due to their capacity to break down plant-derived chelators and their closeness to the surface of the root. However, plants might avoid direct competition with microbes because the amount and type of exudates they release into the rhizosphere change over time and space [34]. Plant to plant interactions, as well as microbial interactions in non-sterile growth circumstances, can modify the iron status of plants. It is well known that the microorganisms in the soil have a substantial impact on the iron nutrition of plants. The iron content of plants can be significantly increased by intercropping grain and legumes [35]. The intercropping of wheat and chickpeas raised the Fe content in wheat seeds [36], whereas the intercropping of maize and peanuts improved the Fe nutrition of peanuts in a calcareous soil [37]. So, researchers might postulate that the rhizosphere microbes are responsible for the higher iron absorption with intercropped plants.
Rhizosphere microbes live in an environment where plant activity has a substantial effect on the accessibility of nutrients. In the rhizosphere, a wide variety of biotic interactions take place that might influence the composition and diversity of the microbial population in the soil near the roots. These species’ uptake of iron results in complicated interactions, ranging from mutualism to competition [38]. The organization of the microbial community is typically influenced more by biotic interactions in the rhizosphere than by abiotic factors, which are more common in the bulk soil. By excreting rhizodeposits into the rhizosphere, plants provide a fertile and dynamic environment for the microbial populations. The content of iron in solution is further reduced by the iron absorption of these microbes and the host plant. As a result, there is high competition among rhizosphere microbes for iron, encouraging those with the most effective iron absorption strategy [38].

2.3. Impact of Plants and Microorganisms on the Iron Status

Plants and microorganisms play important roles in the cycling and availability of iron in the environment. Plant-associated microbes may promote plant development and affect crop output and quality by mobilizing and transporting nutrients [39]. It has been proven that soil microbes play a significant role in promoting plant iron (Fe) absorption in Fe-limiting situations [40][41]. Plant roots and rhizospheric microorganisms release substances such as organic acids, proteins, phenolics, phytosiderophores, and siderophores, which can promote the solubilization of low-availability iron in the soil [14][20][42].
A research report showed that in Chinese cabbage leaves and stalks the concentration of soluble protein, soluble sugar, and vitamin C was significantly decreased under Fe-deficiency stress conditions, whereas the content of cellulose and nitrate was increased [43]. The same study found that Fe-deficiency stress significantly lowered net photosynthetic rate and nitrate reductase activity in the leaves. Iron shortage in the rhizosphere resulted in a 40% rise in root biomass as well as elevated levels of citrate, malate, and phenols in root exudates [44]. The increase in root biomass and elevated levels of these compounds in the root exudates in response to iron deficiency are part of the plant’s adaptive response to this micronutrient limitation.
In Fe-limiting situations, plants and soil microorganisms have used active strategies to enhance soil iron availability, which plays a key role in promoting iron absorption. In the rhizosphere, iron oxides are more easily soluble and dissolvable due to processes such as acidification, chelation, and reduction (Figure 1).

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Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Zoltán Molnár
,
Wogene Solomon
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Lamnganbi Mutum
,
Tibor Janda
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Update Date: 16 May 2023
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