Rice Tolerance to Iron-Deficient and Iron-Toxic Soil Conditions elucidate Mechanisms and Implications

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Pradip Kumar Saini¹ , Kushal Sachan² , Surekha S³ , Asif Islam⁴ , Nageshwar⁵

¹Acharya Narendra Deva University of Agriculture and Technology, Kumarganj, Ayodhya (Uttar Pradesh, India.

²Department of Soil Science and Agricultural Chemistry, C. S. Azad University of Agriculture and Technology Kanpur U.P -208002, India.

³Department of Crop Physiology, College of Sericulture, Chintamani UAS, GKVK, Bangalore- Karnataka, India.

⁴School of Agricultural Biotechnology, Punjab Agricultural University, Ferozepur Rd, Ludhiana, Punjab 141027, India.

⁵Department of Genetics and Plant Breeding, CSAUA&T Kanpur, Uttar Pradesh 208002, India.

Corresponding Author Email: pradipnduat@gmail.com

DOI : https://doi.org/10.51470/JPB.2022.1.2.14

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Introduction

Iron (Fe) is an essential micronutrient for plant growth and development, playing a crucial role in various physiological processes, including photosynthesis, respiration, and nitrogen fixation. However, the availability of iron in the soil can vary widely, leading to either deficiency or toxicity, both of which can severely limit plant productivity and yield. Iron deficiency is a common nutritional disorder affecting crops grown in calcareous and alkaline soils, while iron toxicity occurs in waterlogged or acidic soils with excessive iron concentrations. Understanding the mechanisms underlying plant tolerance to these contrasting soil conditions is essential for improving crop resilience and ensuring sustainable agricultural production [1]. The ability of plants to tolerate and adapt to fluctuating iron availability in soil is essential for agricultural sustainability and food security. Understanding the mechanisms underlying plant responses to iron deficiency and toxicity is imperative for developing resilient crop cultivars and optimizing agronomic practices. This review aims to elucidate the physiological, biochemical, and molecular mechanisms that govern plant tolerance to iron-deficient and iron-toxic soil conditions. By unraveling these intricate processes, we can identify targets for crop improvement and devise strategies for sustainable soil management in diverse agroecosystems.

Physiological and Morphological Adaptations

Plants have evolved various physiological and morphological adaptations to cope with iron deficiency and toxicity. In iron-deficient soils, plants exhibit enhanced root growth and branching to increase the exploration of soil volume and access to iron resources. Additionally, the secretion of organic acids and proton extrusion from roots facilitates the solubilization and mobilization of iron in the rhizosphere. Conversely, under iron-toxic conditions, plants may develop aerenchyma to enhance oxygen diffusion in waterlogged soils and limit the uptake of excess iron ions [2].

Plants exhibit a range of physiological and morphological adaptations to cope with iron-deficient and iron-toxic soil conditions. Under iron deficiency, plants often enhance root growth and branching to increase soil exploration and access to iron resources. This involves the proliferation of lateral roots and increased root surface area for nutrient uptake. Additionally, plants secrete organic acids into the rhizosphere, promoting the solubilization and mobilization of iron in the soil. Proton extrusion from root cells creates acidic conditions, further facilitating iron uptake. Conversely, in iron-toxic soils, plants may develop aerenchyma, which aids in oxygen diffusion in waterlogged environments. This adaptation helps mitigate the effects of reduced oxygen availability and limits the uptake of excess iron ions, which can be harmful. Plants tightly regulate ion homeostasis to prevent the accumulation of toxic levels of iron. They employ specialized uptake mechanisms, including ferric chelate reductases and iron-regulated transporters, to facilitate the efficient uptake and transport of iron ions. Furthermore, plants utilize various iron transporters and chelators to facilitate internal iron transport and distribution. Vacuolar sequestration of excess iron ions serves as a detoxification mechanism, enabling plants to mitigate the adverse effects of iron toxicity. Under iron deficiency, plants undergo metabolic adjustments to optimize iron utilization and allocate resources to essential physiological processes. These adjustments include the reprogramming of metabolic pathways involved in chlorophyll biosynthesis, photosynthesis, and energy metabolism. In response to iron toxicity, plants activate antioxidant defense mechanisms to mitigate oxidative stress caused by reactive oxygen species accumulation. Enzymatic antioxidants such as superoxide dismutase and catalase play crucial roles in scavenging reactive oxygen species and protecting cellular components from oxidative damage [3]. Overall, the intricate interplay between physiological and morphological adaptations enables plants to withstand the challenges posed by iron-deficient and iron-toxic soil conditions, ensuring optimal growth and productivity in diverse environmental settings.

Iron Uptake and Transport Systems

At the molecular level, plants have developed sophisticated mechanisms for iron uptake and transport to maintain iron homeostasis under varying soil conditions. Key components of the iron uptake system include the ferric chelate reductase (FRO) and iron-regulated transporter (IRT) families, which mediate the reduction of ferric iron and its subsequent uptake by root cells. Additionally, various iron transporters and chelators, such as mugineic acid family phytosiderophores (MAs), play crucial roles in the internal transport and distribution of iron within the plant. Iron uptake and transport systems in plants are sophisticated mechanisms essential for maintaining iron homeostasis and ensuring optimal growth and development [4]. These systems involve a series of molecular processes that enable plants to acquire iron from the soil and transport it to various tissues and organs. Key components of iron uptake and transport systems include ferric chelate reductases (FROs), iron-regulated transporters (IRTs), and various iron transporters and chelators. Ferric chelate reductases (FROs) are integral membrane proteins located in the root epidermis and are responsible for reducing ferric iron (Fe^3+) to ferrous iron (Fe^2+), which is more soluble and readily available for uptake by plant roots. This reduction process is essential for enhancing the uptake of ferric iron, particularly under conditions of low iron availability in the soil.

Iron-regulated transporters (IRTs) are another crucial component of the plant iron uptake system. These transporters are responsible for the uptake of ferrous iron from the soil into the root cells. They play a central role in facilitating the transport of iron across the plasma membrane of root cells, allowing for efficient iron uptake under both iron-deficient and iron-sufficient conditions. In addition to FROs and IRTs, plants utilize various iron transporters and chelators to facilitate the internal transport and distribution of iron within different cellular compartments. For example, the mugineic acid family phytosiderophores (MAs) are small organic molecules synthesized and secreted by the roots of graminaceous plants under iron-deficient conditions. These phytosiderophores chelate ferric iron in the soil, forming soluble iron complexes that are subsequently taken up by specific transporters in the root cells. Once inside the plant, iron is transported to various tissues and organs through a complex network of transport proteins and chelators. This internal transport system ensures the efficient distribution of iron to essential metabolic processes, such as chlorophyll biosynthesis, photosynthesis, and respiration. Vacuolar sequestration of excess iron ions serves as a detoxification mechanism, allowing plants to maintain iron homeostasis and prevent the accumulation of toxic levels of iron within the cell. Overall, the coordinated action of ferric chelate reductases, iron-regulated transporters, and various iron transporters and chelators enables plants to acquire, transport, and utilize iron efficiently, thereby ensuring optimal growth and development in diverse environmental conditions [5-6]. Understanding the molecular mechanisms underlying plant iron uptake and transport systems is crucial for improving crop resilience to iron deficiency and toxicity and enhancing agricultural productivity.

Antioxidant Defense Mechanisms

Both iron deficiency and toxicity can induce oxidative stress in plants due to the production of reactive oxygen species (ROS). To counteract oxidative damage, plants employ antioxidant defense mechanisms, including enzymatic antioxidants such as superoxide dismutase (SOD), catalase (CAT), and peroxidases, as well as non-enzymatic antioxidants like ascorbate and glutathione. These antioxidants scavenge ROS and protect cellular components from oxidative damage, thereby enhancing plant tolerance to iron stress. Antioxidant defense mechanisms are crucial for plants to combat oxidative stress induced by various environmental factors, including iron deficiency and iron toxicity. These mechanisms involve a complex interplay of enzymes and non-enzymatic antioxidants that collectively neutralize reactive oxygen species (ROS) and prevent oxidative damage to cellular components. Enzymatic antioxidants such as superoxide dismutase (SOD), catalase (CAT), and peroxidases play key roles in ROS scavenging. SOD catalyzes the dismutation of superoxide radicals, while CAT decomposes hydrogen peroxide into water and oxygen. Peroxidases help reduce hydrogen peroxide and other organic peroxides using reducing agents like ascorbate and glutathione. Non-enzymatic antioxidants, including ascorbate (Vitamin C), glutathione (GSH), and carotenoids, directly scavenge ROS and participate in redox reactions to maintain cellular redox balance. Ascorbate and glutathione regenerate other antioxidants and act as substrates for peroxidases, contributing to ROS detoxification [7].

Under oxidative stress, plants induce the expression of antioxidant enzyme genes through the action of transcription factors such as AP2/ERF, MYB, and NAC. This induction enhances the production of antioxidant enzymes and ROS-scavenging proteins, bolstering the plant’s defense against oxidative damage. Iron deficiency and iron toxicity can both trigger oxidative stress by promoting ROS generation. Antioxidant defense mechanisms help mitigate the effects of oxidative stress by scavenging ROS and protecting cellular components from damage. By maintaining redox homeostasis, plants can enhance their tolerance to iron stress and sustain normal physiological processes even under adverse conditions. Understanding the regulation and function of antioxidant systems in plants is essential for developing strategies to enhance crop tolerance to iron stress and improve agricultural productivity in diverse environments [8]. By harnessing the power of antioxidant defense mechanisms, plants can better cope with environmental challenges and thrive in dynamic ecosystems.

Signaling Pathways

Plant responses to iron deficiency and toxicity are regulated by complex signaling networks involving various hormones, transcription factors, and signaling molecules. Ethylene, auxin, and cytokinins have been implicated in the regulation of root morphogenesis and iron uptake under low iron conditions, while jasmonic acid and salicylic acid mediate defense responses to iron toxicity. Moreover, iron deficiency responses (IDRs) and iron deficiency-induced transcription factors (FITs) play pivotal roles in orchestrating the expression of genes involved in iron acquisition and homeostasis. Signaling pathways play a pivotal role in regulating plant responses to iron deficiency and iron toxicity, orchestrating adaptive mechanisms at the molecular, cellular, and physiological levels. These pathways involve a complex network of signaling molecules, transcription factors, and hormonal regulators that coordinate plant growth and development in response to fluctuating iron availability in the soil [9].

1. Hormonal Regulation:

   Hormones such as ethylene, auxins, cytokinins, jasmonic acid (JA), and salicylic acid (SA) are key regulators of plant responses to iron stress. Ethylene and auxins modulate root morphogenesis and iron uptake under low iron conditions, promoting the development of lateral roots and enhancing iron acquisition efficiency. Cytokinins influence root architecture and nutrient allocation, affecting plant tolerance to iron stress. JA and SA regulate defense responses to iron toxicity, activating antioxidant defense mechanisms and detoxification pathways to mitigate oxidative stress [10].

2. Iron Deficiency Responses (IDRs):

   Plants activate a set of physiological and biochemical responses collectively known as iron deficiency responses (IDRs) to cope with iron deficiency stress. IDRs include alterations in root architecture, increased expression of iron uptake genes, and enhanced secretion of iron-chelating compounds such as phytosiderophores and organic acids. Transcription factors such as the iron deficiency-induced transcription factors (FITs) regulate the expression of genes involved in iron acquisition and homeostasis, coordinating plant responses to low iron availability [11].

3. Signaling Molecules and Transcriptional Regulation:

   Signaling molecules such as reactive oxygen species (ROS), nitric oxide (NO), and calcium ions (Ca^2+) act as secondary messengers in iron signaling pathways, transmitting signals from the extracellular environment to the nucleus. These signaling molecules modulate the activity of transcription factors involved in the regulation of iron-responsive genes, fine-tuning gene expression in response to changes in iron availability. Transcriptional regulators such as bHLH transcription factors (e.g., FIT, IAA-LEUCINE RESISTANT3) and MYB transcription factors (e.g., MYB72) play critical roles in mediating iron responses and coordinating downstream gene expression programs [12].

4. Cross-Talk with Other Stress Signaling Pathways:

   Iron signaling pathways interact with other stress signaling pathways, enabling plants to integrate responses to multiple environmental stresses. Crosstalk between iron, drought, salinity, and pathogen defense signaling pathways allows plants to prioritize resource allocation and optimize stress tolerance strategies. For example, the activation of JA and SA signaling pathways in response to iron toxicity may enhance plant resistance to biotic stresses while mitigating the effects of iron-induced oxidative stress. Understanding the intricate signaling pathways involved in plant responses to iron deficiency and iron toxicity is essential for developing strategies to enhance crop tolerance to iron stress and improve agricultural productivity in iron-limiting soils. By deciphering the molecular mechanisms underlying iron signaling, researchers can identify targets for crop improvement and develop resilient cultivars capable of thriving in diverse environmental conditions [13].

Implications for Crop Improvement:

Elucidating the mechanisms underlying plant tolerance to iron-deficient and iron-toxic soils has significant implications for crop breeding and management strategies. By harnessing molecular breeding techniques and genomic resources, breeders can develop cultivars with enhanced tolerance to iron stress, thereby improving crop productivity and resilience in diverse agroecosystems. Furthermore, agronomic practices such as soil amendment, crop rotation, and water management can mitigate the adverse effects of iron stress on plant growth and yield, contributing to sustainable agricultural intensification. Understanding the physiological, biochemical, and molecular mechanisms underlying plant tolerance to iron-deficient and iron-toxic soil conditions has significant implications for crop improvement strategies aimed at enhancing productivity and sustainability in agricultural systems [14].

1. Breeding for Iron Stress Tolerance:

   Insights into the genetic basis of plant tolerance to iron stress provide opportunities for breeding cultivars with enhanced resilience to iron-deficient and iron-toxic soils. By utilizing genomic resources, molecular markers, and high-throughput phenotyping techniques, breeders can identify and introgress beneficial alleles associated with iron stress tolerance into elite crop germplasm. This approach facilitates the development of improved cultivars with enhanced nutrient uptake efficiency, root architecture, and metabolic resilience under iron stress conditions [15].

2. Trait-Based Selection and Marker-Assisted Breeding:

   Trait-based selection and marker-assisted breeding strategies enable breeders to target specific traits associated with iron stress tolerance, such as root morphology, iron uptake efficiency, and antioxidant capacity. By employing genomic selection methods and quantitative trait loci (QTL) analysis, breeders can expedite the development of superior cultivars with improved performance under iron stress. The integration of genomic information and phenotypic data allows for the identification of genomic regions and candidate genes associated with iron stress tolerance, facilitating the selection of elite breeding lines with desirable traits [16].

3. Genetic Engineering and Transgenic Approaches:

   Genetic engineering and transgenic approaches offer novel opportunities for enhancing crop tolerance to iron stress by modulating key genes and pathways involved in iron uptake, transport, and homeostasis. Genetic manipulation of iron transporters, transcription factors, and antioxidant enzymes can enhance plant resilience to iron-deficient and iron-toxic conditions, improving nutrient acquisition efficiency and stress tolerance. Engineered crops with enhanced iron stress tolerance traits can contribute to sustainable agriculture by reducing yield losses and improving nutrient-use efficiency in challenging environments [7].

4. Precision Agriculture and Soil Management Practices:

   Precision agriculture techniques, including soil amendment, nutrient management, and agronomic practices, can help mitigate the adverse effects of iron stress on crop productivity. Soil amendments such as iron chelates, organic fertilizers, and pH adjustments can improve iron availability and uptake in iron-deficient soils, while drainage systems and water management practices can alleviate iron toxicity in waterlogged soils. Integrated nutrient management strategies, including crop rotation, cover cropping, and organic amendments, promote soil health and fertility, reducing the impact of iron stress on crop performance [3].

5. Multi-omics Approaches and Systems Biology:

   Multi-omics approaches, including genomics, transcriptomics, proteomics, and metabolomics, provide comprehensive insights into the molecular mechanisms underlying plant responses to iron stress. Integration of multi-omics data through systems biology approaches enables the elucidation of complex gene regulatory networks and metabolic pathways involved in iron stress tolerance. Systems biology frameworks facilitate the identification of key genes, proteins, and metabolites associated with iron stress responses, informing targeted intervention strategies for crop improvement and stress resilience, leveraging advances in genetics, genomics, and biotechnology offers promising avenues for enhancing crop tolerance to iron-deficient and iron-toxic soil conditions. By integrating knowledge of plant physiology, molecular biology, and agronomy, researchers and breeders can develop resilient crop cultivars capable of thriving in diverse agroecosystems, contributing to global food security and sustainability efforts [5].

Conclusion:

In conclusion, understanding the physiological, biochemical, and molecular mechanisms underlying plant tolerance to iron-deficient and iron-toxic soil conditions is critical for enhancing crop resilience and sustainability. By unraveling the intricate interplay between plants and soil iron availability, researchers can devise innovative strategies for crop improvement and soil management, ensuring food security and environmental stewardship in the face of global challenges, unraveling the intricate mechanisms underlying plant tolerance to iron-deficient and iron-toxic soil conditions holds immense significance for agricultural sustainability and food security. Iron stress poses significant challenges to crop productivity, limiting plant growth, and yield in diverse agroecosystems worldwide. However, understanding the physiological, biochemical, and molecular responses of plants to iron stress provides valuable insights into strategies for crop improvement and soil management.

From physiological and morphological adaptations to sophisticated iron uptake and transport systems, plants have evolved intricate mechanisms to cope with fluctuating iron availability in the soil. Root architecture modifications, iron uptake mechanisms, antioxidant defense systems, and signaling pathways play crucial roles in enabling plants to withstand iron stress and maintain optimal growth and productivity. The implications of unraveling these mechanisms extend beyond basic research to practical applications in crop breeding, genetic engineering, and agronomic practices. Breeders can harness genomic tools and molecular breeding techniques to develop cultivars with enhanced tolerance to iron stress, thereby increasing resilience and productivity in iron-limited environments. Precision agriculture and soil management practices further complement these efforts by optimizing nutrient availability and mitigating the adverse effects of iron stress on crop performance. Furthermore, multi-omics approaches and systems biology frameworks offer holistic insights into the complex interplay between genes, proteins, and metabolites underlying plant responses to iron stress. By integrating multi-omics data and computational modeling, researchers can identify key regulators and metabolic pathways associated with iron stress tolerance, paving the way for targeted intervention strategies and precision breeding programs. In essence, elucidating the mechanisms of plant tolerance to iron stress represents a crucial step towards sustainable agriculture and environmental stewardship. By leveraging scientific advances and interdisciplinary collaborations, we can develop resilient crop cultivars, improve soil fertility, and enhance agricultural productivity in iron-challenged environments. Ultimately, the collective efforts of researchers, breeders, and farmers are essential for addressing global challenges and ensuring food security for future generations.

Conflict of Interest Statement:

The authors declare no conflict of interest.

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