The Potential of Siderophores in Biological Control in Plant Diseases

The Potential of Siderophores in Biological Control in Plant Diseases

Published: 2025.01.09

Received: 2024.09.25

Accepted: 2025.01.06

Gurudatt M. Hegde

Professor

Department of Plant Pathology, University of Agricultural Sciences, India

Premchand U

Subject Mater Specialist

ICAR-KVK, Indi (Vijayapura II), University of Agricultural Sciences, Dharwad, Karnataka, India

Raghavendra Mesta

Professor

Plant Pathology, University of Horticultural Sciences, Bagalkot, Karnataka, India

DOI: https://doi.org/10.56669/HGRS2291

ABSTRACT

Siderophores, the secondary metabolites produced by various microorganisms such as fungi and bacteria, are pivotal in enhancing plant growth and controlling plant diseases, particularly under iron-deficient conditions. These small organic molecules, capable of chelating ferric iron (Fe³⁺), convert it into the more soluble and bioavailable ferrous form (Fe²⁺), facilitating essential physiological processes in plants, including chlorophyll synthesis and oxidation-reduction reactions. This improved iron uptake significantly enhances crop quality and yield. Siderophores are classified based on their functional groups into hydroxamates, catecholates, and carboxylates, and can be produced in artificial iron-restricted media. Notably, siderophores like Pyoverdine from Pseudomonas spp., and those produced by fungi such as Trichoderma asperellum and Streptomyces spp., have demonstrated significant plant growth-promoting effects in various crops, including sugarcane, ryegrass, and cucumber. Beyond promoting plant growth, siderophores act as potent biocontrol agents by competing with phytopathogens for iron, thus inhibiting their growth and reducing their pathogenicity. This biocontrol efficacy operates through mechanisms such as nutrient competition, antibiosis, niche exclusion, and interference with pathogen signaling. Siderophore-producing bacteria like Pseudomonas putida and Bacillus subtilis have shown effectiveness in controlling harmful microorganisms such as Fusarium oxysporum and Sclerotium rolfsii, supporting sustainable agricultural practices by reducing reliance on synthetic agrochemicals. However, the effectiveness of siderophore-based biocontrol strategies can be influenced by environmental factors, the specific affinity of siderophores for iron, and the pathogen’s siderophore receptors. Phenotypic plasticity among bacteria and the dynamics of siderophore production are also critical factors affecting their success. Despite these challenges, the potential of siderophores in sustainable agriculture is substantial. Continued research and field trials are crucial to optimize their application, enabling the development of eco-friendly agricultural practices that enhance crop yields and reduce dependency on synthetic chemicals, contributing to global food security.

Keywords: Siderophores, Biocontrol, Ferric Iron (Fe³⁺), Ferrous Iron (Fe²⁺), Agriculture, Plant Growth-Promoting Bacteria, Biosynthesis, Iron Chelation

INTRODUCTION

Iron is one of the most abundant elements in the Earth's crust (Gamit and Tank, 2014 and Huber, 2005). It is a vital element for nearly all living microorganisms, playing a crucial role in various metabolic pathways essential for growth and development, including the catalysis of electron transfer systems. Additionally, hundreds of metabolic enzymes contain iron as cofactors, such as heme groups or Fe-S clusters (Miethke and Marahiel, 2007). As a transition metal, iron exists in two oxidation states: ferric (Fe³⁺) and ferrous (Fe²⁺), both of which are key players in oxidation-reduction reactions (Taylor and Konhauser, 2005). In its ferrous state (Fe²⁺), iron is highly soluble, with a solubility of up to 100 mM at pH 7. However, Fe³⁺, which is crucial for the growth and development of microorganisms, is only soluble to a concentration of 10⁻⁹ M at biological pH (Petsko, 1985).

At neutral pH and under aerobic conditions, iron oxidizes to form insoluble oxyhydroxide polymers (Paul and Dubey, 2015), making it less accessible to microorganisms. Iron is an essential element in photosynthesis, as it is a component of photosystem I, the cytochrome b6f complex, and photosystem II, with Fe ions playing a role in chlorophyll synthesis (Miethke and Marahiel, 2007). Iron is also required for the regulation of vitamins, amino acids, porphyrins, nitrogen fixation, oxygen transport, methanogenesis, respiration, including the citric acid cycle, oxidative phosphorylation, nucleic acid synthesis, and many biosynthetic processes in microorganisms. Although iron is abundant in soils, it often exists in an insoluble form. Fe deficiency in plants is a major economic issue that seriously impacts the quality and yield of crops (Briat et al., 2015). To survive in iron-depleted environments, many microbes have developed various strategies for iron scavenging, with siderophore production being one of the primary mechanisms (Ganz and Nemeth, 2015; Briat et al., 2015; Ahmed and Holmström, 2014).

Siderophores are iron-chelating molecules that sequester and solubilize the available ferric form of iron from various habitats (Nagoba and Vedpathak, 2011). The term "siderophore," derived from the Greek words ‘sideros,’ meaning ‘iron,’ and ‘phores,’ meaning ‘bearer,’ was coined by Lankford in 1973 to mean "iron carrier" (Ishimaru and Loper, 1973). Siderophores are low-molecular-weight molecules, typically ranging from 400 to 1,500 Da, which are excreted by various microorganisms, such as fungi, bacteria, and some plants, under conditions of iron starvation. Recently, a few mammalian siderophores have also been reported by Devireddy et al. (2010). Both Gram-positive and Gram-negative bacteria produce siderophores under iron stress conditions (Tian et al., 2009; Saharan and Nehra, 2009). Most aerobic and facultative anaerobic bacteria are reported to produce at least one type of siderophore (Neilands, 1995; Hider and Kong, 2010). Recent reports indicate that more than 500 different siderophores have been identified from selected microorganisms, with 270 of these being well-characterized (Boukhalfa, 2003).

A variety of bacteria referred to as plant-growth-promoting bacteria (PGPB) can colonize the rhizosphere and promoting Fe uptake by plants (Rahimi et al., 2020; Nwachukwu et al., 2024). These microorganisms can produce Fe ions under iron-deficient conditions. The PGPB of interest synthesize and release siderophores under appropriate conditions, thereby increasing and regulating Fe bioavailability (Raymond et al., 2003). Siderophores are low-molecular-weight compounds (500-1,500 Da) with a high affinity for Fe(III) (Kf > 1,030). The affinity of siderophores for Fe is so high that they can remove Fe from the molecules of Fe-binding proteins, such as ferritin, transferrin, and lactoferrin (Li et al., 2016; Ratledge and Dover, 2000). Thus, the main function of siderophores is to convert Fe bound to proteins or water-soluble compounds into a form accessible to microorganisms (Dertz et al., 2006). Siderophore-producing PGPB promote plant growth and improve host plant nutrition (Campestre et al., 2016), but there are other benefits of PGPB for plants. For example, they can solubilize phosphates (Timofeeva et al., 2019) and fix atmospheric nitrogen (Pankievicz et al., 2021). Given that both mineral phosphate and mineral (inorganic) nitrogen are required for siderophore synthesis, consortia of such PGPB are regarded as potential microbial-fertilizers. Other PGPB may affect crop growth by reducing the impact of soil-borne plant pathogens through the production of antimicrobial compounds and extracellular enzymes (Latha et al., 2009). Siderophore-producing microbes generate numerous Fe-chelating compounds (Alam, 2014), thereby accelerating the physiological and biochemical processes of plants under unfavorable conditions (Sultana et al., 2021; Hofmann et al., 2021). Adding both Fe(III) and siderophores to the soil enhances plant growth compared to adding Fe(III) alone, as evidenced by the increase in plant weight (De Serrano, 2017). In recent years, research has focused on novel agro-ecological approaches aimed at agro-biodiversity management (Castiglione et al., 2021). Plant biostimulants are next-generation products with significant potential for sustainable agriculture. Microbial-based biostimulants, composed of beneficial microorganisms, enhance plant growth, nutrient uptake, and stress resilience. Recent advancements focus on selecting microorganisms with targeted growth-promoting activities to improve nutrient assimilation under conditions of low availability. Furthermore, plant growth-promoting bacteria (PGPB) isolated from salinized and desertified regions are being explored for their potential to mitigate environmental stresses (Castiglione et al., 2021).

This review examines the role of siderophore-producing PGPB (Plant Growth-Promoting Bacteria), classifies the various types of siderophores produced by bacteria and fungi that hold promise for agriculture based on their physicochemical properties, and describes the biosynthesis, acquisition in bacterial cells, and release of Fe from the Fe–siderophore complex in plants. Additionally, the review discusses methods for detecting, producing, and extracting siderophores and siderophore-producing bacteria, as well as their applications in agriculture.

PHYSICO-CHEMICAL NATURE OF SIDEROPHORE

Siderophores produced by microorganisms vary in their physical and chemical structures. Based on their involvement in ferric ion coordination, siderophores can be classified into hydroxamates, such as desferrioxamine; catecholates, such as enterobactin; and carboxylates, such as achromobactin. Additionally, certain siderophores are of a mixed type, classified based on their structural features, functional groups, and types of ligands (Crowley, 2006; Meneely, 2007; Arora and Verma, 2017; Timofeeva et al., 2022).

Hydroxymate siderophore

Hydroxamate siderophores, produced by both fungi and bacteria, represent one of the most ubiquitous categories of siderophores found in nature and are well studied. Fusarium spp. produce fusigen, Trichoderma spp. produce coprogens, Pseudomonas fluorescens secretes ferribactin and pseudobactin, Pseudomonas putida produces pyoverdine, and Bacillus subtilis secretes bacillibactin (Hofte, 1993; Winkelmann, 1997; Maurer et al., 1968; Zahner et al., 1963; Diekmann and Zahner, 1967; Sayer and Emery, 1968; Neilands, 1973; Bagmare et al., 2019; Kalyan et al., 2022).

Initially, hydroxamate-type siderophores were detected using Neilands' spectrophotometric assay (McCormack et al., 2003; Saha et al., 2015). Later, different assays were developed, such as electrospray ionization mass spectrometry (ESI-MS) (Neilands, 1981), modified overlaid Chrome Azurol S (O-CAS) (Perez-Miranda, 2007), and Csaky’s assay (Pal and Gokarn, 2010), which show strong absorption between 425 nm and 500 nm. Hydroxamate siderophores have three hydroxamate groups, which can be arranged in a linear (e.g., desferrioxamine B) or cyclic (e.g., vicibactin) structure (Soares, 2022). These groups consist of C(C=O)N-(OH)R, where R is an amino acid or a derivative like lysine or ornithine, typically present in acylated and formylated hydroxylamines (Miethke and Marahiel, 2007; Shanmugaiah et al., 2015). Each hydroxamate group provides two oxygen atoms that form a bidentate ligand with iron, enabling the formation of a hexadentate octahedral complex with Fe³⁺ (Ali and Vidhale, 2013). Ustilago sphaerogena produces ferrichrome, Neisseria gonorrhoeae produces small quantities of gonobactin, and Neisseria meningitidis produces nocobactin.

Catecholate (Phenolates) siderophore

This class of siderophore, also known as phenol-catecholate, is the second most common type of siderophore and is primarily produced by bacteria such as Escherichia coli, Salmonella typhimurium, and Bacillus subtilis, which produce enterochelin and bacillibactin, respectively (Dertz et al., 2006; Shanmugaiah et al., 2015; Khasheii et al., 2021). This class is also exclusively produced by fungi belonging to the order Mucorales. Phenol-catecholate siderophores contain a cyclic trimer of 2,3-mono- or dihydroxybenzoyl-L-serine acid groups, each of which provides two oxygen atoms, resulting in a hexadentate structure that chelates iron with remarkable affinity for Fe(III) (Meneely, 2007; Soares, 2022). The hexadentate structure forms an octahedral complex with iron. This group is derived from salicylate or dihydroxybenzoic acid. Enterochelin has a high iron-binding affinity, whereas pyochelin has a relatively weak affinity. Studies have shown that certain bacteria, such as Erwinia carotovora, can produce catecholate siderophores alone, while others, such as fluorescent pseudomonads, produce mixed siderophores (Leong and Neilands, 1982). Catecholate siderophores can be detected by various assays, including the Neilands spectrophotometric assay (McCormack et al., 2003), high-performance liquid chromatography (HPLC) with diode-array detection (DAD), electrospray ionization mass spectrometry (ESI-MS) (Fiedler et al., 2001), and the O-CAS assay (Perez-Miranda et al., 2007). Catecholate-type siderophores form a wine-colored complex with ferric chloride, which absorbs maximally at 495 nm (Ali and Vidhale, 2013).

Carboxylate siderophore

It is produced by a few bacteria and fungi, including Rhizobium species, which produce siderophores such as Rhizobactin (from Rhizobium meliloti) and Rhizoferrin (from Rhizopus microsporus), and Staphylococcus species, which produce Staphyloferrin A (Drechsel et al., 1995; Berenguer et al., 2019; Ghosh et al., 2020). The Rhizobium meliloti strain DM4 is known for producing Rhizobactin, which is one of the best-characterized siderophores of this type (Smith and Neilands, 1984). Staphyloferrin A, a highly hydrophilic carboxylate-type siderophore, is produced by Staphylococcus hyicus DSW 20459 (Meiwes et al., 1990). Under acidic pH, these groups of siderophores are more active in chelating iron than catecholate and hydroxamate groups, making them more prevalent in microorganisms dwelling in acidic environments (Khasheii et al., 2021). They have carboxyl and hydroxyl groups as donor groups for iron bonding (Shanmugaiah et al., 2015). The formation of these siderophores involves the binding of two amide bonds between the terminal carboxylic groups of two molecules of citric acid and either 1,4-diaminobutane or D-ornithine (Soares, 2022). These siderophores can be detected by spectrophotometric tests, with absorption maxima between 190 and 280 nm (Shenker et al., 1992), and by the O-CAS assay (Perez-Miranda, 2007).

Mixed types and pyoverdine

In addition to the previously mentioned categories, some siderophores contain multiple Fe-chelating groups and are classified as mixed-type siderophores. Among these, certain fluorescent strains of Pseudomonas produce siderophores known as pyoverdines (Budzikiewicz et al., 1993; Budzikiewicz et al., 1997). These pyoverdines are characterized by the presence of a quinoline chromophore, a peptide, and a dicarboxylic acid (or its corresponding amide) attached to the chromophore. While the peptide sequence remains consistent within the same bacterial strain, it can vary across different strains and species (Ringel and Brüser, 2018). There are mainly three types of pyoverdines—pyoverdine, pyoverdine 0, and pyoverdine A (also known as ferribactin)—that have been isolated from Pseudomonas fluorescens (Philson et al., 1982). Other species within the Pseudomonas genus, such as Pseudomonas syringae and Pseudomonas aureofaciens, are also known to produce pyoverdine-type siderophores (Bultreys et al., 2001; Beiderbeck et al., 1999). The first siderophore isolated from Azotobacter vinelandii was azotobactin (Bulen et al., 1962), a pyoverdine-type siderophore, whose structure was determined using nuclear magnetic resonance (NMR) (Schaffner et al., 1996). The chromophore in pyoverdines exhibits unique optical properties, with specific absorption and fluorescence peaks at 380 nm and 500 nm, respectively (Yoneyama et al., 2011).

Additionally, Yersinia pestis produces the siderophore yersiniabactin, which contains phenolate, thiazole, oxazoline, and carboxylate groups involved in iron binding. Bacteria like Rhodococcus (which produces rhodobactin) and Paracoccus denitrificans (which produces parabactin) are examples of organisms that synthesize siderophores containing both catecholate and hydroxamate groups. The structures of pseudobactin and pseudobactin A, distinguished by their quinoline derivatives, have been described in Pseudomonas B10 (Teintze et al., 1981). Moreover, Pseudomonas fluorescens produces various other siderophores, including enantio-pyochelin (Youard et al., 2007), quinolobactin (Mossialos et al., 2000), ornicorrugatin, and pseudomonins (Matthijs et al., 2008). Interestingly, Pantoea eucalypti M91 is capable of producing pyoverdine-like and pyochelin-like siderophores in alkaline media (Campestre et al., 2016).

Pyoverdine, produced by various Pseudomonas species, is also reported to have direct antifungal properties, contributing to the suppression of pathogen development by increasing competition for iron. Generally, fungal siderophores have a lower affinity for Fe(III) compared to bacterial siderophores (Sharma and Johri, 2003). For instance, the siderophore produced by P. fluorescens WCS374r (Psb374) is crucial for inducing resistance in rice against Magnaporthe oryzae. When rice was inoculated with a mutant WCS374r strain deficient in pseudobactin and then infected with M. oryzae, no suppression of disease was observed, highlighting the importance of siderophores in plant defense mechanisms (Aznar and Dellagi, 2015). Pyoverdines are believed to be involved in the biological control of phytopathogenic microorganisms in the rhizosphere, as they are known to form stable complexes with soil Fe, making this essential element unavailable for consumption by harmful rhizosphere microorganisms (Ambrosi et al., 2000).

SIDEROPHORE DETECTION, PRODUCTION AND EXTRACTION

Various methods have been developed for detecting siderophores produced by bacteria or fungi during growth in liquid or solid cultures. Among these, the most universally applicable method for all types of siderophores is the Chrome Azurol S (CAS) assay. Other methods, such as the hexadecyl trimethyl ammonium bromide (HDTMA) assay (Schwyn and Neilands, 1987), the succinate medium assay (Meyer and Abdallah, 1978), and the Page and Trigerström (1988) method for extracting crystals of crude siderophores, are more specific to particular types of siderophores. Therefore, these methods are often used as a follow-up to the CAS assay to indicate the specific type of siderophore produced.

Chrome Azurol S (CAS) assay

The Chrome Azurol S (CAS) method, developed by Schwyn and Neilands (1987) and modified by Alexander and Zuberer (1991), is a non-specific assay for detecting all siderophore types and low molecular weight organic acids. In the CAS assay, siderophores remove Fe from the CAS complex, causing a color change from blue to orange, which can be measured colorimetrically. This method may underestimate siderophore levels if residual Fe is present. The CAS solution is prepared by combining a ferric solution with CAS and CTAB, stabilized with a MES buffer. The filtered culture supernatant is mixed with the CAS solution and incubated, after which absorbance at 630 nm is measured to estimate siderophore production. The method has been used successfully for detecting siderophores in organisms like Piriformospora indica and Pythium spp.

Hexadecyl trimethyl ammonium bromide (HDTMA) assay

The Hexadecyl Trimethyl Ammonium Bromide (HDTMA) assay is used for detecting and quantifying siderophores, which are iron-chelating molecules produced by microorganisms. This assay leverages the ability of siderophores to bind iron, displacing the HDTMA from its iron complex, and causing a visible color change that can be measured spectrophotometrically. The HDTMA assay begins with the preparation of an iron-HDTMA complex by mixing a ferric solution (FeCl₃) with HDTMA, resulting in a stable, colored complex. Microorganisms suspected of producing siderophores are cultured, and the supernatant the liquid portion obtained after removing cells is collected following incubation. When the culture supernatant is mixed with the iron-HDTMA complex, the presence of siderophores leads to the chelation of iron, displacing the HDTMA, and causing the solution's color to shift. The degree of this color change is proportional to the concentration of siderophores in the sample, which can be quantified by measuring the absorbance at a specific wavelength. The assay's sensitivity allows for the detection of even low levels of siderophores, making it particularly effective for catecholate-type siderophores, although it can be adapted for others. The absorbance readings from the assay are compared against a standard curve generated using known concentrations of a siderophore, such as desferrioxamine, to quantify the siderophores present in the sample. While the HDTMA assay offers high sensitivity and quantitative results, it has some limitations. The presence of other substances in the culture medium may interfere with the assay, potentially leading to false positives or negatives. Additionally, while the assay is effective, it may not distinguish between different types of siderophores without further steps.

Succinate medium assay

The succinate medium assay detects and measures siderophore production by microorganisms. Siderophores are iron-chelating compounds produced to sequester iron, which is essential for microbial growth. This assay uses a succinate medium that is iron-deficient to stimulate siderophore production. In the procedure, the succinate medium is prepared with succinic acid and essential nutrients but with very low iron. After inoculating and incubating microorganisms in this medium, siderophores are detected using methods like the Chrome Azurol S (CAS) assay, which shows a color change from blue to orange, or spectrophotometry to measure absorbance. The assay is advantageous due to its selectivity for siderophore production and compatibility with various microorganisms. However, it may require additional tests to identify specific siderophore types and can be affected by trace iron contamination. Overall, it is a valuable tool for studying siderophore production.

APPLICATION OF SIDEROPHORE IN THE FIELD OF AGRICULTURE

Plant growth promoter

Iron is a micronutrient, which plays a major role in plant biosynthesis. It is required in chlorophyll synthesis, oxidation-reduction reaction and many physiological processes of a plant (Briant et al. 1995). The siderophore produced by a microorganism which will help in enhancing plant growth by increasing the iron uptake by plants. This leads to significant increases in quality and quantity of crop production which ultimately results in higher food production. Siderophore act as a plant growth promoter by make the Fe³⁺ form of iron to Fe²⁺ which is an available form that leads to easy uptake of Iron by a plant for their growth (Masalha et al. 2000,16). The commonly known plant growth-producing siderophore is Pyoverdine siderophore produced by Pseudomonas spp. (Kloepper et al. 1980; Gamalero and Glick 2011). In sugarcane and ryegrass, the siderophore produced by E. coli from the endo-rhizosphere which thus helps in enhancing plant growth (Gangwar and Kaur 2009). Rungin et al. (2019) showed that the siderophore formed by endophytic Streptomyces spp. isolated from roots of Thai jasmine rice plant induced the plant growth, and thus increased root, shoot biomass and length of the plant. Qi and Zhao (2013) found that the siderophore of Trichoderma asperellum has a potential role in cucumber growth. The plant growth promoting activity of the fungi by producing siderophore is found in Trichoderma asperellum, T. harzianum, Aspergillus niger, Penicillium citrinum, E. coli, and Streptomyces spp. (Yadav et al. 2011).

The symbiotic relationship between ecto-mycorrhiza and plant growth is facilitated by siderophores, which supply iron to the plant's roots (Van Scholl et al., 2008). Plants secrete phenolic exudates that enhance the solubility of insoluble ions, improving iron uptake by plants through their siderophore-secreting microbes (Jin et al., 2010).

Siderophores as biocontrol agents in agriculture

Siderophores, high-affinity iron-chelating compounds produced by microorganisms under iron-limiting conditions, play a crucial role in biocontrol against various phytopathogens (Table 1). The increasing interest in biocontrol agents (BCAs) is driven by the need for eco-friendly alternatives to synthetic agrochemicals, which face restrictions due to their toxicity and potential carcinogenic effects (Agrios, 2005 and Anonymous, 2018). Additionally, the growing resistance of phytopathogens to conventional fungicides and bactericides has heightened the demand for novel biocontrol strategies, including the exploitation of siderophores.

Table 1. Overview of siderophore-producing bacteria and fungi

Sl. No.	Siderophore	Organism	Reference
Bacteria
	2-Deoxystreptamine	Bacillus subtilis	Chandwani et al., 2023
	2,3-dihydroxybenzoic acid	Azospirillum brasilense; Azotobacter vinelandii	Corbin and Bulen et al., 1969; Bachhawat and Ghosh, 1987; Cornish and Page, 1995
	3,5-DHB-threonine	Azospirillum lipoferum	Shah et al., 1992
	3,5-DHB-lysine	Azospirillum lipoferum	Shah et al., 1992
	Amphotericin B	Brevibacillus brevis GZDF3	Sheng et al., 2020
	Aminochelin	Azotobacter vinelandii	Corbin and Bulen et al., 1969; Bachhawat and Ghosh, 1987; Cornish and Page, 1995
	Amychelin	Amycolatopsis spp. AA4	Seyedsayamdost et al., 2011.
	Anguibactin	Vibrio anguillarum 775(pJM1); Acinetobacter baumannii ATCC 19606	Actis et al., 1986; Tolmasky et al., 1988; Jalal et al., 1989; Chen et al., 1994; Chen et al., 1996; Dorsey et al., 2004; Sandy et al., 2010; Lemos et al., 2010; Naka et al., 2013; Balado et al., 2018
	Azotobactin	Azotobacter vinelandii	Bulen et al., 1962; Knosp et al., 1984; Demange et al., 1988; Huyer and Page,1988; Page et al., 1991; Budzikiewicz et al., 1992; Cornish and Page, 1998; Palanché et al., 2004; Wichard et al., 2009; Yoneyama et al., 2011; Rosa-Núñez et al., 2023
	Azotochelin	Azotobacter vinelandii	Duhme et al., 1998; Cornish and Page, 1998
	Amphibactin	Vibrio neptunius	Galvis et al., 2021
	Cepabactine	Burkholderia cepacia	Azelvandre, 1993
	Chrysobactin	Erwinia chrysanthemi	Persmark et al., 1989; Franza et al., 1991; Persmark et al., 1992; Persmark and Neilands, 1992; Tomisic et al., 2008; Sandy and Butler, 2011
	Cupriachelin	Cupriaviolus necator H16	Wang et al., 2014
	Deoxyvasicinone	Bacillus subtilis	Chandwani et al., 2023
	Desferrioxamine B andE Desferrioxamine G, B and E	Streptomyces viridosporus; Streptomyces griseus; Streptomyces pilosus; Streptomyces ambofaciens; Streptomyces coelicolor; Streptomyces lividans; Streptomyces spp.; Streptomyces aureofaciens	Imbert et al., 1995; Béchet and Blondeau, 1998; Shimon et al., 1998; Challis and Ravel, 2000; Challis and Hopwood, 2003. Yamanaka et al., 2005; Baroma-Gomez et al. 2006; Schneider et al., 2007; Kodani et al., 2011; Roberts et al., 2012; Sidebottom et al., 2013
	Erythrobactin	Saccharopolyspora erythraea SGT2	Oliveira et al., 2006
	Ferribactin	P. fluresence	Hohlneicher et al., 1995
	Ferricoelichelin	Streptomyces ambofaciens	Galet et al., 2015
	Ferrioxamine	Streptomyces ambofaciens	Galet et al., 2015
	Fumitremorgin C	Bacillus subtilis	Chandwani et al., 2023
	Gingerone A	Bacillus subtilis	Chandwani et al., 2023
	Heptapeptide GE23077	Actinomadura spp. DSMZ13491	Mazzei et al., 2012
	Heterobactin	Rhodo coccus and Nocardia	Lee et al., 2012
	JBIR-16 P	Nocardia tenerifensis NBRC101015JBIR-16	Mukai et al., 2009
	Metabolome	S. tropica CNB-440	Ejje et al., 2013
	Miserotoxin	Bacillus subtilis	Chandwani et al., 2023
	Nocardamine	Citricoccus spp. KMM3890	Kalinovskaya et al., 2011
	Nocardimicins A, B, C, D, E, F	Nocardia spp. TP-A0674	Ikeda et al., 2005
	Ornibactine	Burkholderia cepacia	Tabacchioni et al., 1995
	Oxachelin	Streptomyces spp. GW9/1258	Sontag et al., 2006
	Pipercide	Bacillus subtilis	Chandwani et al., 2023
	Pipernonaline,	Bacillus subtilis	Chandwani et al., 2023
	Pseudobactine	Pseudomonas putida B10	Andriollo et al., 1992; Ambrosi et al., 2000
	Protochelin	Azotobacter vinelandii	Cornish and Page, 1995
	Piscibactin	Vibrio anguillarum; Vibrio ordalii; Vibrio neptunius	Balado et al., 2018; Ruiz et al., 2019; Galvis et al., 2021
	Peucechelin	Streptomyces peucetius	Kodani et al., 2015; Magar et al., 2024
	Pyroverdin	Pseudomonas aeruginosa; P. chlororaphis; P. florescens	Cox and Adams, 1985; Boukhalfa et al., 2006; Ghssein and Ezzeddine, 2022
	Pyoverdin	Pseudomonas fluorescens	Geisen et al., 1992
	pyochelin	Pseudomonas aeruginosa; Pseudomonas putida	Liu and Shokrani, 1978; Sriyosachati and Cox, 1986; Ankenbauer et al., 1988; Ó Cuív et al., 2004; Brandel et al., 2012; Cunrath et al., 2020; Ghssein and Ezzeddine, 2022
	pseudopaline	Pseudomonas aeruginosa	Ghssein and Ezzeddine, 2022
	Rhizobactin	Rhizobium meliloti; Sinorhizobium meliloti	Smith and Neilands, 1984; Reigh, 1991; Persmark et al., 1993; Smith et al., 1995; Barton et al., 1996; Lynch et al., 2001; Ó Cuív et al., 2004; Fadeev et al., 2005
	Schizokien	Bacillus magaterium; Ralstonia solanacearum; Rhizobium leguminosarum IARI 917	Bhatt and Denny, 2004; Storey et al., 2006; Santos, 2012
	Staphyloferrin A	Staphylococcus hyicus	Konetschny‐Rapp et al., 1990; Meiwes et al., 1990; Beasley et al., 2009; Cooper, 2011; Beasley et al., 2011; Milner et al., 2013
	Staphyloferrin B	Ralstonia metallidurans; Staphylococcus aureus; Ralstonia metallidurans; Ralstonia solanacearum; Staphylococci spp.; Bacillus megaterium; Staphylococcus aureus	Haag et al., 1994; Bhatt and Denny, 2004; Grigg et al., 2010; Beasley et al., 2011
	Spirilobactin	Azospirillum brasilense	Bachhawat and Ghosh, 1987
	Tsukubachelin B	Streptomyces spp. TM-74	Kodani et al., 2013
	Vanchrobactin	Vibrio spp.	Balado et al., 2009; Sandy et al., 2010; Lemos et al., 2010
	vicibactin	Rhizobium leguminosarum bv. viciae	Dilworth et al., 1998
	Vibrioferrin	Azotobacter vinelandii	Baars et al., 2016
Fungi
	Cis-Fusarinine,	Fusarium spp.	Jalal et al., 1986; Johnson, 2008; Holinsworth and Martin, 2009; Fatima et al., 2017; Jalal and van der Helm, 2017
	Corpgen, Corpgen B	Altenaria spp.; Curvularia spp.; Fusarium spp.; Stmphyllium spp.; Trichoderma spp.; Leptosphaerulina spp.; Laccaria laccat; Laccaria bicolor	Haselwandter et al., 2013
	Dimerum Acid	Cylindrocarpon spp.; Fusarium spp.; Stmphyllium spp.; Verticillium dahliae	Harrington and Neilands, 1982; Manulis et al., 1987; Dori et al., 1990; Hördt et al., 2000
	Ferrichrome, Ferrichrome C	Aspergillus spp.; Histoplasma spp.; Hymenoscyphus spp.; Oidiodendron spp.; Penicillium spp.; Pseudomonas spp.; Saccharomyces spp.; Trichophyton spp.; Microsporum spp.	Dayan et al., 1993; Yun et al., 2000; Heymann et al., 2000; Heymann et al., 2002; Hannauer et al., 2010; Aguiar et al., 2021
	Ferricrocin	Aspergillus spp.; Altenaria spp.; Curvularia spp.; Histoplasma spp.; Hymenoscyphus spp.; Laccaria laccata Laccaria bicolor; Microsporum spp.; Oidiodendron spp.; Penicillium spp. Trichoderma spp.; Trichophyton spp.	Eisendle et al., 2006; Wallner et al., 2009; Kajula et al., 2010; Haselwandter et al., 2013; Oide et al., 2015; Mukherjee et al., 2018; Happacher et al., 2023
	Ferrirhodin	Botrytis spp.; Fusarium spp.; Penicillium spp.	Jalal et al., 1985; Kieu et al., 2012; Munawar et al., 2013
	Ferrirubin	Aspergillus spp.; Paecilomyces spp.; Penicillium spp.	Will et al., 2024
	Fusarinine B & C	Fusarium spp.; Gibberella spp.; Nectria spp.; Trichoderma spp.	Hördt et al., 2000; Zhai et al., 2015; Lu et al., 2019;Aguiar et al., 2022
	Malonichrome,	Fusarium spp.	Oide et al., 2015
	N-Dimethylcoprogen	Altenaria spp.; Fusarium spp.	Jalal et al., 1988
	Neocoprogen I, II	Altenaria spp.; Curvularia spp.; Cylindrocarpon spp.; Onygena spp.	Hossain et al., 1987
	Neocoprogenii	Altenaria spp.; Curvularia spp.	Anke et al., 1991
	Palmitoylcoprogen	Trichoderma spp.	Anke et al., 1991
	Triacetylfusarinine C	Laccaria laccata; Laccaria bicolor	Heymann et al., 1999; Haas et al., 2003; Haselwandter et al., 2013; Aguiar et al., 2022; Azel et al., 2023

Mechanisms of biocontrol by siderophores

Siderophores contribute to biocontrol through several mechanisms, including nutrient competition, antibiosis, niche exclusion, and interference with pathogen cell signaling (May et al., 1997; Duffy and Defago, 1999). Iron acquisition via siderophores occurs at the microbial cell surface and involves receptor-mediated, energy-dependent transport systems (Stintzi et al., 2000; Sigel and Sigel, 1998; Wandersman, 2004). Under iron-deficient conditions, bacteria not only produce siderophores but also upregulate receptor molecules in their outer membranes to facilitate iron uptake. Siderophores form iron complexes that are transported into cells through specific receptors such as FepA and FecA, and via the ABC transporter system (Boos and Eppler, 2001). The internalized iron is released into the cytoplasm, often through the action of the TonB protein complex, which may involve hydrolysis of the siderophore or reduction of Fe³⁺ to Fe²⁺ by NAD(P)H-linked mechanisms. This process ensures that iron is sequestered from competing microorganisms, inhibiting their growth and pathogenicity. In Escherichia coli, for example, ferric-siderophore complexes are internalized and hydrolyzed by esterase (encoded by the fes gene), releasing ferrous iron that is unavailable to non-producing strains. This restricts the growth of pathogenic bacteria and fungi in the rhizosphere, enhancing the competitive advantage of siderophore-producing microorganisms (Loper and Buyer, 1991).

Siderophores in plant growth promotion and disease resistance

Siderophores such as pyoverdine and pyochelin, produced by Plant Growth-Promoting Rhizobacteria (PGPR), play a dual role in enhancing plant growth and suppressing phytopathogens by limiting the availability of iron in the rhizosphere (Hofte et al., 1992). While many siderophores demonstrate efficacy in vitro, their performance in field conditions varies due to environmental factors, leading to the registration of only a limited number of biocontrol agents for agricultural use (Anonymous, 2019).

In agricultural practices, inoculation of soil with siderophore-producing bacteria like Pseudomonas putida has been shown to enhance plant growth and yield through the production of siderophores, HCN, proteases, antimicrobials, and phosphate-solubilizing enzymes (Kloepper et al., 1980; Chaiharn et al., 2008). Additionally, hydroxamate-type siderophores are crucial in immobilizing heavy metals in the soil, thus preventing toxicity and maintaining soil fertility (McGrath et al., 1995).

Siderophore-mediated inhibition of phytopathogens

Several studies have demonstrated the ability of siderophore-producing bacteria and fungi to inhibit the growth of harmful microorganisms (Table 2). For instance, siderophores inhibit various phytopathogenic fungi, including Phytophthora parasitica, Pythium ultimum, Fusarium oxysporum, and Sclerotinia sclerotiorum (Seuk et al., 1988; Hamdan et al., 1991; Buysens et al., 1996; McLoughlin et al., 1992). The significance of siderophore production in biocontrol was first highlighted by Kloepper et al. (1980), who demonstrated its role in controlling Erwinia carotovora through fluorescent pseudomonads. Subsequent studies confirmed the correlation between siderophore synthesis and the inhibition of F. oxysporum chlamydospore germination (Elad and Baker, 1985 and Sneh et al., 1984). Moreover, mutants deficient in siderophore production exhibit reduced biocontrol efficacy (Keel et al., 1989; Loper and Buyer, 1991).

Siderophores can affect microbial communities by inhibiting competing microorganisms, as observed in the competition between Pseudomonas aeruginosa and Burkholderia cepacia for iron, where P. aeruginosa's superior pyoverdine conferred a competitive advantage (Leinweber et al., 2018).

Table 2. Commonly using Siderophore producing organisms against phytopathogens

Sl. No.	Phyto-Pathogen	Siderophore producing organism
1	Erwinia carotovora	Pseudomonas aeruginosa; P. putida; P. fluorescens
2	Erwinia amylovora	P. fluorescens; Bacillus subtilis
3	Fusarium oxysporum	Pseudomonas spp.; Bacillus subtilis
4	Gaeumannomyces graminis	Pseudomonads spp.
5	Ralstonia solanacearum	P. alcaligenes; P. Putida; P. fluorescens; Bacillus subtilis; B. megaterium
6	Xanthomonas oryzae	P. putida; P. fluorescens, lysobacter spp.
7	Clavibacter michiganensis	P. putida; P. fluorescens
8	Xanthomonas campestris pv. malvacearum	Trichoderma harzianum; P. fluorescens; Bacillus subtilis
9	Xanthomonas axonopodis pv. vignaeradiatae	P. aeruginosa; Bacillus subtilis

Factors influencing biocontrol efficacy

The effectiveness of siderophore-producing bacteria as biocontrol agents depends on several factors, including the quantity and affinity of siderophores for ferric ions, the iron-binding properties of the pathogen's siderophores, phenotypic plasticity, and temporal dynamics of siderophore production (Kramer et al., 2020). Phenotypic plasticity allows bacteria to adjust their iron uptake pathways in response to competition, as seen in the rapid upregulation of pyoverdine production by P. aeruginosa under low iron conditions (Perraud et al., 2020).

The success of PGPR as biocontrol agents also hinges on the compatibility of their siderophores with the pathogen's receptors, which can determine whether the pathogen is effectively outcompeted for iron (Gu et al., 2020). Additionally, siderophores can induce systemic resistance (ISR) in plants, providing a broad-spectrum defense against diseases, as demonstrated in Pseudomonas fluorescens WCS374r's induction of ISR in rice against Magnaporthe oryzae (De Vleesschauwer et al., 2008).

Siderophores in overcoming drug resistance and enhancing crop yield

Siderophores have also been explored for their potential to overcome membrane-associated drug resistance by facilitating drug transport into cells through siderophore-drug conjugates (Ribeiro and Simoes, 2019). The biocontrol potential of siderophore-producing bacteria has been demonstrated in various crops, with notable examples including Bacillus subtilis against Fusarium oxysporum and Macrophomina phaseolina in chickpea (Patil et al., 2014), and Pseudomonas fluorescens against Sclerotium rolfsii and F. oxysporum in pepper (Xianmei et al., 2011).

The use of siderophore-producing microorganisms as biocontrol agents offers a promising strategy for sustainable agriculture. Their ability to suppress phytopathogens, promote plant growth, and enhance crop yield, while reducing reliance on synthetic chemicals, underscores their importance in modern agricultural practices. However, achieving consistent biocontrol efficacy requires a comprehensive understanding of ecological interactions and the factors influencing siderophore production and iron acquisition. Continued research and field trials are essential to optimize the application of siderophore-producing BCAs in diverse agricultural environments.

CONCLUSION

Siderophores have been extensively studied and established as effective biocontrol agents, significantly influencing both plant growth regulation and disease management. Their role in facilitating iron uptake is crucial, enhancing plant health and productivity by converting Fe³⁺ (ferric ion) to Fe²⁺ (ferrous ion) which is more readily absorbed by plants. This process not only supports essential physiological functions but also contributes to increased crop yields. In terms of disease management, siderophores play a pivotal role by sequestering iron and thereby limiting its availability to pathogens. This mechanism of iron chelation disrupts the growth of various phytopathogens, including both fungi and bacteria, through nutrient competition, antibiosis, and niche exclusion. Beneficial microorganisms such as Pseudomonas spp. and Trichoderma spp. demonstrate substantial potential in reducing disease incidence and boosting plant resistance. However, the practical application of siderophore-based biocontrol is challenged by variability in performance due to factors such as environmental conditions, cropping seasons, and climatic variations. This variability highlights the necessity for further research to identify and characterize novel siderophores, explore their biosynthesis, and understand their specific functions across different habitats. Advancements in research are needed to address these challenges and optimize the use of siderophore-producing biocontrol agents. By refining these strategies and understanding the intricate interactions between siderophores, plants, and pathogens, we can enhance the efficacy of biological control methods and achieve more consistent and sustainable outcomes in agricultural practices.

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