Next Article in Journal
Oleanolic Acid Dimers with Potential Application in Medicine—Design, Synthesis, Physico-Chemical Characteristics, Cytotoxic and Antioxidant Activity
Next Article in Special Issue
Unraveling the lncRNA-miRNA-mRNA Regulatory Network Involved in Poplar Coma Development through High-Throughput Sequencing
Previous Article in Journal
Molecular Mechanisms of Plant Responses to Copper: From Deficiency to Excess
Previous Article in Special Issue
Genome-Wide Identification and Characterization of Lignin Synthesis Genes in Maize
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 25
Issue 13
10.3390/ijms25136992
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Phosphorus-Iron Nexus: Decoding the Nutrients Interaction in Soil and Plant

by
Xingqi Yang
,
Chang Liu
,
Cuiyue Liang
,
Tianqi Wang
* and
Jiang Tian
Root Biology Center, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(13), 6992; https://doi.org/10.3390/ijms25136992
Submission received: 13 June 2024 / Revised: 25 June 2024 / Accepted: 25 June 2024 / Published: 26 June 2024
(This article belongs to the Collection Advances in Molecular Plant Sciences)
Browse Figures
Versions Notes

Abstract

:
Phosphorus (P) and iron (Fe) are two essential mineral nutrients in plant growth. It is widely observed that interactions of P and Fe could influence their availability in soils and affect their homeostasis in plants, which has received significant attention in recent years. This review presents a summary of latest advances in the activation of insoluble Fe-P complexes by soil properties, microorganisms, and plants. Furthermore, we elucidate the physiological and molecular mechanisms underlying how plants adapt to Fe-P interactions. This review also discusses the current limitations and presents potential avenues for promoting sustainable agriculture through the optimization of P and Fe utilization efficiency in crops.

1. Introduction

Phosphorus (P) is one of the essential mineral nutrients for plant growth and plays a critical role in the formation of organic molecules essential for plant development, including DNA, RNA, ATP and phospholipids [1]. However, agricultural production often faces problems such as suboptimal P fertilizer use efficiency and reduced soil P effectiveness, which result in plant P deficiency [2]. As a crucial micronutrient for plants, iron (Fe) is vital for the synthesis of proteins involved in photosynthesis and respiration [3]. Although Fe is the most abundant metal element in soil, its bioavailability is often low, making Fe deficiency a common occurrence in plants [4]. There is a complex interplay between Fe and P in both soil and plant, with profound effects on soil properties and plant growth [5,6]. For example, in acidic conditions, Fe is easily bounded with phosphate (Pi) to form Fe-P complex, reducing availability of both Pi and Fe in soils [7]. In plants, interaction of P and Fe influence vary of biological processes, such as Fe accumulation in apoplast inhibits primary root elongation of Arabidopsis thaliana under P deficiency [8], suggesting that the Fe-P interaction in plants contributes to regulate strategies of plant adaptation to nutrients deficient environments. Therefore, elucidating the mechanisms and identifying the modulating factors of the P-Fe nexus within both soil and plant systems is pivotal for advancing understanding of soil nutrient cycling and enhancing the efficiency of plant nutrient utilization.
In this review, we summarized recent breakthroughs in the interplay of P and Fe, particularly focusing on the regulation of soil properties and microorganism on Fe-P complexes formation in soil, as well discussed the intricate modulation of Fe-P interaction on network of root morphology and physiological functions in plants. Our works intend to clarify mechanisms associated with Fe-deficient and P-deficient disorders for devising strategies conducive to sustainable agriculture.

2. P-Fe Interactions in Soil

In most soils, Fe oxide is the principal Fe form, and the biogeochemical cycling of Fe based on the redox transformation between Fe+2 and Fe+3. Due to its redox-sensitive property, Fe often chemically reacts with Pi, then forms insoluble Fe-P complex via ligand exchange and surface precipitation, especially in acidic soil where Fe is more active (Figure 1) [9,10]. The surface of Fe-P complexes is then coated with a hydrated Fe oxide layer, culminating in the creation of a sealed state, further decreases bioavailability of P and Fe [11]. In addition, the inositol bounded with Pi groups on surface could be attracted to Fe oxides with positively charged colloidal surface and forming Fe-inositol-P complexes, which is firmly preserved in soil due to its stability and the resistance to phytase hydrolysis [12]. Hence, the fixation of Pi by Fe diminishes both Fe and Pi availability in soil and decelerates their biogeochemical cycling.

2.1. The Influences of Soil Properties on P-Fe Interactions

The forms and interaction of Pi and Fe could be regulated by physicochemical properties of soil, including soil pH, redox potential (Eh) and humic substances. Particularly, in acidic conditions, Fe oxides in soil might be the primary P-adsorbing phases [13,14]. Elevating soil pH appropriately could enhance P desorption via decreasing adsorption sites and increasing the electrostatic repulsion between clays and Pi [10,15]. The combination of P and Fe caused by low pH has become a global problem to be solved [16,17]. Especially in acidic soil in southern China, the low availability of soil Pi leads to excess P fertilizer application in farmland, which, however, causes P surplus and exacerbate soil quality deterioration [18]. The overaccumulation of P in soil, in turn, result in a reduction in the effectiveness of Fe [19]. Hence, promoting sustainable agricultural development in acidic soil requires augmenting soil P availability, especially promoting the desorption of insoluble Fe-P.
The variabilities of Eh in soils could fluctuate the biogeochemical cycling of P and Fe [20]. First, soil Eh controls the form and bioavailability of Fe [20]. The reduction condition in soil is enhanced with a decrease in the soil Eh, which induces the transformation of Fe3+ to Fe2+ and the dissolution of Fe oxides, ultimately resulting in the release of adsorbed or coprecipitated P from the Fe-P complex [21]. Conversely, elevated Eh values result in the oxidation of Fe2+ into Fe3+, thus facilitate the formation of Fe-P complex [22]. Additionally, in reduction layer of soil, Fe3+-oxyhydroxides can be reductively dissolved. The radial O2 loss (ROL), oxygen (O2) leakage by plant roots when adapting to low-O2 conditions, could drive soluble Fe2+ toward the root surface, which is then spontaneously oxidized and forms Fe plaques consisting of Fe hydroxides, including ferrihydrite, goethite, and siderite [23]. Fe plaques are primarily observed in proximity to mature roots, which have a negative impact on P supply to plants due to their surface chemical activity and high specific surface area [24]. It is noteworthy that the quantity of Fe plaques determines their role as an inhibitor or reservoir for soil P. Although the Fe plaque-P co-precipitates have the potential to limit the effectiveness of P, moderate Fe plaque-P may also serve as a safe haven for P, which may be dissolved and released as available Pi and Fe by secondary metabolites released by plants and microorganisms [7].
The humic substances act to retard the formation of the Fe-P complex via binding cations and the sites of precipitation and crystallization, thereby increase the solubility of P in soils [25,26]. P can be absorbed by humic-Fe complexes to form ternary humic-Fe-P complexes, which exhibit a maximum P sorption that is significantly higher than that of Fe oxides [27]. And the connection between humic substances and P primarily bases on Fe bridges in a labile form which may be easily desorbed [28]. Moreover, humic-Fe complexes exhibit a dissolution of organic P in soil, as evidenced by their higher absorption capacity for phytate compared to Fe-oxides [29]. Collectively, humic-Fe-P complexes constitute a significant pool of soil P for utilization by plants.

2.2. The P-Fe Interaction in Soil Affected by Microorganisms

Microorganisms are pervasive in soil, exerting a pivotal influence on mineral nutrient cycling within ecosystems and functioning as intermediaries in the communication between plants and soil [30]. P and Fe are essential mineral nutrients for microbial growth. To activate insoluble Fe-P complexes in the environment, microorganisms enhance the availability of P and Fe via the release of secondary metabolites, including organic acids, siderophores, and redox substances (Figure 1 and Table 1) [31,32].
In P-limited and Fe-limited soils, the accumulation of microorganism with organic acids secreting capacity has been observed (Table 1) [33,34,35,36]. The secretion of organic acids by microorganisms facilitates the reductive dissolution of Fe minerals, prevents the aggregation of Fe oxide crystals, results in liberation of P and Fe from Fe-P complexes [34]. Oxalic acid, citric acid and gluconic acid are the primary organic acids released in response to Pi and Fe starvation [10,35,36]. Beneficial microorganisms, such as arbuscular mycorrhizal fungi (AMF), have been shown to liberate inorganic P [37] and organic P [38] bound to Fe oxides via the release of significant amounts of organic acids [39], thereby supply sufficient P and Fe for plants [40,41,42,43]. However, a contrasting opinion demonstrates that organic acid could barely solubilize the Fe-P complex due to the high pKsp and low dissolution rates of the Fe-P complex [44,45]. Consequently, certain microorganisms may activate Fe-P complexes via distinct mechanisms, such as chelating and reducing, rather than releasing organic acids [46,47].
Siderophores, a class of secondary metabolites secreted by microorganisms under Fe deficient conditions, exhibit a high capacity for efficiently activating and chelating Fe [44,48,49]. It is noteworthy that the secretion of siderophores by microorganisms is not only induced by low-Fe conditions but also influenced by low-P conditions [50]. The abilities of microorganisms to release P and produce siderophores are consistently distinguished in numerous studies. In fact, in acidic soils with high amounts of Fe-P complexes, the release of insoluble Fe by siderophore concurrently enhances the bioavailability of P (Table 1) [31,51,52,53]. The dissolution of Fe-P complexes via siderophore could be traced back to a study from 40 years ago, in which two siderophores (i.e., desferrioxamine-B, desferriferrichrome) were demonstrated to facilitate the diffusion of Fe and P in low-pH soil [54]. This reinstated P-solubilization from Fe-organic P complexes by siderophore had also been identified in recent work [55]. Furthermore, a Streptomyces sp. CoT10 exhibited a high solubility for FePO4, which was directly mediated by its siderophores, thereby enhanced P accumulation in plants [56]. Collectively, siderophore-secreting microorganisms represent a crucial pathway for the promotion of Fe and P solubilization and availability in acidic soils.
Some microorganisms are capable of secreting reductive substances to reduce Fe3+ into Fe2+, thus inhibits the formation of Fe oxides and averts Fe-P fixation (Table 1) [57]. Phenazine, a secretion of microorganisms with reducibility, is found to be highly exudated under low-P conditions [58] and mediates specific chemical reactions leading to the dissolution of Fe oxides in soil [59,60]. A recent study has been demonstrated that phenazine secreted from Pseudomonas could enhance the bioavailability of P in sediment consisting of Fe oxide-P complexes [61]. In P-limited condition, the production of phenazine in Pseudomonas might be positively regulated by phoB, a cytoplasmic response regulator that responds to P starvation [61,62]. Further investigation is required to determine the influence of other reductive substances, such as flavins, on the activation of insoluble Fe-P complexes. It is notable that certain microorganisms possess their own reducing or oxidizing abilities, which are mediated by electron transport and transfer or oxidases and reductases. These progresses facilitate the conversion of Fe2+ and Fe3+ into each other and regulate the combination of Fe oxides colloids and PO43− [63,64,65,66]. Modulating the ratio of oxidizing bacteria to reducing bacteria is also a crucial aspect in enhancing the effectiveness of Fe and P in soil. In addition, the secretion of phytase represents another pathway by which microorganisms activate insoluble Fe-P complexes in soil [67]. Overall, microorganisms play a multifaceted role in the liberation of unavailable Fe-P complexes in soils, thereby contribute significantly to the biogeochemical cycling of Fe and P.
Table 1. Mechanisms of microorganisms in activating insoluble Fe and P in soil.
Table 1. Mechanisms of microorganisms in activating insoluble Fe and P in soil.
MechanismFunctionBacteria or SubstanceReferences
Release organic acids In acidic environment, secrete oxalic acid in response to insoluble P, such as goethite (P-Fe oxides)Aspergillus niger[10,36]
Low-P soil promotes P-solubilizing bacteria accumulation and organic acids secretionP-solubilizing bacteria[33]
Release citric acid to adapt to acidic environmentAspergillus niger[35]
Dissolve P from goethite via secreting low-molecular-weight organic acids, enhance P content of Solanum lycopersicumRhizophagus irregularis[39]
Siderophore
secretion		Solubilization of P from Fe-phosphates at acid pHdesferrioxamine-B and desferriferrichrome[54]
Solubilize P from Fe-phytate complexesSiderophore-secreting bacteria[55]
Activate insoluble Fe-P complexes in rhizosphere, enhance P and Fe in Camellia oleiferaStreptomyces sp. CoT10[56]
Redox abilityRelease P from Fe-rich sludge via reducing Fe3+ to Fe2+Fe-reducing bacteria[57]
Release phenazine-1-carboxamide to promote Fe reduction and dissolve Fe (hydr)oxidesPseudomonas chlororaphis[59]
Phenazines reductively dissolve ferrihydrite and hematite the reaction rate is increases as the pH decreasesPyocyanin, phenazine-1-carboxylate, phenazine-1-carboxamide and 1-hydroxyphenazine[60]
Release phenazine to reduce Fe3+ to Fe2+, solubilize P from phosphate hydrous ferric oxides and marine sedimentsPseudomonas aeruginosa[61]
Increase Fe-P in sediment and oxidizing Fe2+ to Fe3+Fe-oxidizing bacteria [65]

3. Interactions of P-Fe in Plants

In responding to P or Fe deficiencies, plant employ multiple physiological and molecular mechanisms, including elevating nutrient uptake efficiency via modulating root morphology and liberating insoluble nutrients by release of exudates [68]. Intricate interactions between P and Fe are also exhibited within plant, especially in regulating root growth, metabolism of exudates and hormone, as well maintaining nutrients homeostasis [69,70,71].

3.1. Fe uptake Process Influenced by P

Plants have evolved two strategies for Fe uptake [72]. In strategy I, plants reduce soil Fe3+ to Fe2+ via the FERRIC REDUCTASE OXIDASE (FRO) [73] and subsequently take up Fe2+ into the roots via the IRON-REGULATED TRANSPORTER1 (IRT1) [74]. Additionally, under low Fe stress, strategy I plants can secrete compounds with redox activity, such as coumarins, to increase Fe availability in the soil [75,76]. In strategy II, plants could secrete mugineic acids (MAs) family phytosiderophore to chelate Fe in the soil, then the MA-Fe complexes are transported into the roots via the YELLOW STRIPE (YS) or YELLOW STRIPE LIKE (YSL) transporters [77,78].
Interestingly, under Fe-limited conditions, low-P promote Fe accumulation in plant roots [79,80,81]. Meanwhile, it is found that increasing external P concentration inhibits Fe uptake and translocation [82,83], exacerbating chlorosis induced by low-Fe [84,85]. In addition, in P-deficient condition, Fe content was not reduced in irt1 mutants compared to wild type, suggesting that Fe uptake under P deficiency might be independent of IRT1 function [86]. In rice (Oryza sativa L.), the expression of genes involved in Fe uptake has been shown to be suppressed under P deficiency [87]. Conversely, the upregulation of VACUOLAR IRON TRANSPORTER (VIT) by P deficiency resulted in Fe accumulation in root vacuoles and cell walls [88], suggesting that the negative regulation of genes involved in Fe uptake may be feedback for Fe accumulation in P-deficient plants [79,88]. Although Fe deficiency also leads to P accumulation in plants [89], P deficiency is considered to have a more pronounced effect on Fe homeostasis than Fe deficiency on P homeostasis [80].

3.2. The Fe-Mediated Root Development Response to Low-P

In plants, roots serve as the primary organ for nutrient uptake. In response to P deficiency, plants modify root morphology, including reducing primary root (PR) elongation and increasing root hair density [90]. The maintenance of Fe homeostasis plays a pivotal role in the response to P deficiency (Figure 1). Reduction of Fe concentration alleviates the inhibition of PR elongation induced by P deficiency [91,92,93,94]. Conversely, excessive Fe supplementation exacerbated the growth inhibition of PR under P-deficiency [95,96]. The growth limitation of PR induced by low-P is primarily attributed to the deposition and valence state of Fe in the apoplast of stem cell niche and cortical cells in elongation zone [97,98,99,100].
LOW PHOSPHATE ROOT 1 (LPR1) protein is considered to be a Fe-dependent P sensor that is a multicopper oxidase (Figure 2). It catalyzes the oxidation of Fe2+ to Fe3+ in the extracellular space, which is critical for Fe transport and homeostasis in plants [101,102]. LPR1 controls root development in P-deficient plants by modulating the accumulation of Fe in apoplast (apo-Fe) in the meristematic and elongation zones of the PR [96,98,103]. The aggregation of apo-Fe resulted in the formation of reactive oxygen species (ROS) and the deposition of callose, which promoted cell wall stiffening in the elongation zone [97,98]. This, in turn, led to the closure of plasmodesmata (PD), obstruction of intercellular transport pathways and inhibition of root cell proliferation, ultimately suppressed PR elongation [96,97,104]. Several processes have been reported to regulate or co-work with LPR1 under low-P conditions (Figure 2). PHOSPHATE DEFICIENCY RESPONSE 2 (PDR2), encoded a single P5-type ATPase protein and expressed in endoplastic reticulum, restrained the activity of LPR1, and LPR1-PDR2 module was vital for deposition of Fe and callose in apoplast under low-P conditions [92,96]. The bZIP family transcription factor ELONGATED HYPOCOTYL5 (HY5) activated LPR1 expression in Arabidopsis roots under P deficiency, resulting in the accumulation of apo-Fe [105]. In addition, HISTONE DEACETYLASE COMPLEX1 (HDC1) might interact with HISTONE DEACETYLASE 6 (HDA6) and be recruited to the LPR1 locus via a chromatin remodeler BRAHMA (BRM), thus suppressed LPR1 transcription. Consequently, BRM, HDC1, and HDA6 negatively regulate the suppression of PR growth under low-P conditions [106,107].
Malate is a vital component in the regulation of apo-Fe in roots under Pi starvation conditions. Under low Pi conditions, the presence of Fe induced the accumulation of SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) in the nucleus, which thereby activated the expression of ALUMINUM-ACTIVATED MALATE TRANSPORTER 1 (ALMT1) and elevated internal malate concentration [97,98,108]. Following oxidizing by LPR1, Fe3+ could form complexes with malate and suppress the reduction to Fe2+, thereby limiting Fe uptake by cells, further facilitating Fe deposition in the apoplast (Figure 2) [91,97,98]. In Arabidopsis, several pathways have been identified to regulate the STOP1-ALMT1 module under P-deficient conditions (Figure 2). As upstream proteins of STOP1, ALUMINUM SENSITIVE 3 (ALS3) interacted with SENSITIVE TO ALUMINUM RHIZOTOXICITY 1 (STAR1) to form an ABC transporter complex on the tonoplast membrane, which inhibited the accumulation of STOP1 protein in the nucleus, thus decreased the malate level [100,108,109]. SIZ1, a SUMO E3 ligase, negatively modulated STOP1 signaling to regulate Fe accumulation and hydroxyl radical production under P deficiency [110,111]. Additionally, the transcription factor WRKY33 promoted the accumulation of Fe3+ in root tips by modulating ALMT1 expression, thus inhibited PR growth under low-P conditions [112].
Recently, the homeostasis of Fe, particularly Fe reduction in the apoplast, has attracted increasing attention (Figure 2). CYTOSOLIC ROOT REDUCTION (CRR) is a membrane protein that catalyzes the conversion of Fe3+ to Fe2+. Under low-P conditions, the crr mutant increased apo-Fe in the root meristem and shortened PR length compared to the wild type. Conversely, overexpression of CRR reduced apo-Fe deposition and alleviated the suppression of PR growth [8]. HYPERSENSITIVE TO LOW P1 (HYP1), a metalloreductase, is found to be upregulated in the proximal zone of the root apical meristem under P deficiency, which regulated Fe-dependent PR growth [113]. In addition, PHOSPHATE-DEFICIENCY SENSITIVE1 (PDE1) encoded a hydroxyphenylpyruvate reductase, which was downregulated in response to P deficiency, concurrently enhancing Fe accumulation in the PR [114]. Collectively, the modulation of the oxidizing and reducing processes of apo-Fe represents a crucial pathway for regulating PR growth under P starvation.
It is notable that the Fe translocation could mitigate the accumulation of apo-Fe under low-P conditions. In contrast to Arabidopsis, the PR of rice is lengthened in P deficiency. This may be related to the upregulation of VIT, which leads to the sequestration of Fe into vacuoles (Figure 2) [88]. Nevertheless, further investigation is required to ascertain whether other plants exhibit the similar capacity for self-regulation, enabling themself to reduce Fe accumulation under P-deficiency. Furthermore, in response to prolonged P deficiency, root meristems were engaged in cell differentiation to prevent the accumulation of excess Fe and callose in apoplast. This process is mediated by CLAVATA3/ENDOSPERM SURROUNDING REGION 14 (CLE14). In P deficiency, Fe accumulation in the root meristem led to the expression of CLE14 in the proximal meristematic region. The receptors CLAVATA2 (CLV2) and CLV2/PEP1 RECEPTOR 2 (PEPR2) were capable of sensing CLE14, which in turn triggered differentiation in the root meristem to prevent long-term damage of PR induced by low-P [115].
Root hair (RH) serve to enhance the surface area of root, thereby facilitate the acquisition of nutrients. The promotion of RH development represents a strategy employed by plants to adapt to low-P environments, which also necessitates the maintenance of Fe homeostasis [6]. In Arabidopsis under P deficiency, the formation of RH was contingent upon an optimal Fe concentration, both excessive and deficient Fe supplementation impeded RH development [116]. PHOSPHATE RESPONSE (PHR), the core transcription factor of the P starvation response, regulated Fe-mediated RH development in low-P conditions. This was primarily accomplished by directly regulating expression of Fe-homeostasis related gene FERRITIN1 (FER1), which facilitated the removal of excess Fe [117,118]. Furthermore, alterations in Fe concentrations under low-P condition influenced vesicle trafficking, which in turn affects PIN-FORMED 2 (PIN2) recycling, further promoted auxin transport to affect PHR1 expression, ultimately facilitated RH growth [6]. HEMERYTHRIN MOTIF-CONTAINING REALLY INTERESTING NEW GENE AND ZINC FINGER PROTEINS (HRZs), a potential Fe sensor, was downregulated in low-Fe condition and triggered the degradation of the PHR2 protein [119], suggested that HRZs interacts with PHR2 to coordinate P and Fe homeostasis in rice.

3.3. The Exudates Metabolism Response to Fe-P Interaction

In response to nutrient stress, plants secrete secondary metabolites internally to modulate the process of nutrient deficiency, and externally to activate insoluble nutrients in the rhizosphere [120]. Similar to microorganisms, organic acids are vital secondary metabolites secreted by plants under P or Fe deficiency [121,122]. In Fe-deficient conditions, the exudation of malate and citrate is elevated by low-P, and the exogenous application of malate and citrate effectively alleviates Fe and P deficiencies [85]. After secreting into the rhizosphere, organic acids mobilize Fe and P under acidic conditions via chelation with Fe and competing for adsorption sites of Pi [123,124,125,126]. Among organic acids from root exudates, citrate exhibits the greatest capacity for activating soil P, followed by oxalate, malate, acetic acid, and succinic acid [127,128]. In both Fe-limited and P-limited condition, malate and citrate are secreted in abundance into the rhizosphere [129,130], suggesting that these two organic acids may be crucial root exudates for activating insoluble Fe-P in the soil.
The redox substances secreted by plants of strategy I are crucial in regulating the availability of P in the soil. For example, coumarins from root exudates are not only induced by Fe deficiency but also upregulated by P deficiency. In the rhizosphere, coumarins facilitate the reduction of Fe3+ to release P from Fe-P complexes [131,132], which also contributes to Fe accumulation induced by Pi starvation [80]. The secretion of coumarins is orchestrated by the MYB63 transcription factor through the PHOSPHATE DEFICIENCY RESPONSE9 (PDR9) pathway under Fe and P combined deficient conditions [133]. However, recent studies have demonstrated that low-P is conversely found to downregulate the secretion of several kinds of coumarins under Fe-limited conditions [134,135]. These discrepancies in coumarin secretion induced by low-P may be related to the distinct types of coumarins having varying degrees of efficiency in activating soil Fe and P, as well as in their metabolism within plants. This is evidenced by the upregulation of esculin, esculetin and scopoletin, but downregulation of dihydroxyscopoletin under P deficiency [132]. In addition to coumarins, flavonoids secreted by lupin roots have been shown to mobilize insoluble Fe-P [136]. Although multiple redox-active root exudates have been validated for regulating plant Fe nutrition [75,76,137,138,139], further investigation is required to determine whether they can activate P by releasing Fe.
The phytosiderophore secreted by strategy II plants under low-Fe conditions is regulated by external P levels. In Fe-limited environments, low-P enhances early growth and Fe accumulation in the shoot of barley, but suppresses the release of mugineic acids [140]. The inhibition in phytosiderophore secretion may be associated with alleviating Fe-deficient chlorosis. Nevertheless, the role of phytosiderophore in activating insoluble Fe-P complexes in the rhizosphere, and the direct influence of P levels on the biosynthesis as well as secretion pathways of phytosiderophore remains inadequately supported by evidence.
The community and function of microorganisms in the rhizosphere can be reshaped by root exudates, which act as nutrients and energy sources [141]. Recruited beneficial bacteria have been demonstrated to modulate the P-Fe interaction in plants. A strain of Pseudomonas putida enhanced expression of two Pi starvation-induced genes and inhibited PR growth by accumulating Fe in the roots of Arabidopsis [142]. Furthermore, P. putida was observed to alleviate chlorosis in fit1 and irt1-1 mutants, and suppress the expression levels of IRT1 in the wild-type plants [142]. These evidences suggests that P. putida may regulate the utilization of P via modulating P signaling in plants, but influence Fe uptake through special mechanism, such as siderophore secretion. Although plants occupy advantageous positions in activating insoluble Fe-P in soil compared to rhizobacteria [143], elucidating the modulatory mechanisms of microbial composition by root exudates and plant growth by beneficial bacteria could provide new insights into the efficient utilization of nutrients mediated by microbe-plant interactions in the rhizosphere. It is also crucial to acknowledge that endogenous secretions also exert regulatory effects on endophytic microorganisms, which may subsequently influence the responses to Fe and P deficiencies, including apo-Fe accumulation, P and Fe signal transduction. This represents a significant avenue for future research.

3.4. The Fe-Influenced Hormone Metabolism Response to Low-P

The metabolism of hormones is vital for plants in response to nutrient deficiencies [144,145]. In adaption to low-P and low-Fe environments, the metabolisms of primary hormones are significantly regulated in plant, including auxins, gibberellins, ethylene, and brassinosteroids. For instance, Fe deficiency suppresses gibberellin in roots, resulting in the accumulation of DELLA growth-inhibitory factors in the meristematic and elongation zones, thereby inhibiting the elongation of the PR [146]. Although a similar process has also been observed in P-deficient plants [147], further investigation is required to demonstrate whether gibberellin metabolism is related to P-Fe interaction in plants. Fe and P deficiencies also regulate the metabolisms of ethylene and auxins. In low-Fe conditions, ethylene and auxins synergistically inhibit root elongation [148,149,150]. In Arabidopsis roots, enhanced ethylene signaling promotes auxin synthesis in the root tips, which is associated with the PR development under low-P conditions [151], suggesting that ethylene and auxin interaction might participate in responses mediated by apo-Fe in P deficiency.
The functions of brassinosteroids (BR) have attracted considerable attention in recent years, mainly due to its capacity to alleviate the adverse effects of biotic and abiotic stresses on plants [152,153]. Furthermore, BR is involved in regulating the responses of plants to low-Fe and low-P conditions. BRASSINAZOLE RESISTANT 1 (BZR1), a key transcription factor in the BR signaling pathway, controls Fe accumulation in the root elongation zone by suppressing LPR1 expression, thus prevents PR inhibition in P deficiency (Figure 2). Conversely, under low-Fe conditions, activation of BR signaling may lead to cell wall relaxation, promoting cell elongation and root growth [99]. A suppressor of BR signaling, BRI1 KINASE INHIBITOR 1 (BKI1), is downregulated by low-Fe and upregulated by low-P to modulate root development [99]. In addition, BR interacts with ethylene to regulate plant responses to Fe deficiency. 24-epibrassinolide (EBR), a member of the BR family, has been observed to increase the activity of the FRO via the inhibition of ethylene production in high-Fe seedlings, while reduce its activity in low-Fe seedlings [154], whether this process is related to external P levels requires further investigation.

3.5. The Photosynthesis Affected by Fe-P Interaction

Fe and P are essential components of photosynthetic enzymes, and are vital for chlorophyll synthesis. Deficiencies in either Fe or P severely impede photosynthesis [155]. The inhibition of photosynthesis induced by Fe-deficiency is dependent on the P status. Under high-P conditions, plants are more prone to exhibit Fe-deficiency chlorosis and genes related to chloroplast synthesis and photosynthesis are downregulated, whereas the chlorosis is mitigated by reducing the P level [156]. In P starvation, Fe is one of the most accumulated metals in chloroplasts, and genes related to Fe homeostasis, including NICOTIANAMINE SYNTHASE 3 (NAS3) and FER1, are upregulated in Arabidopsis [79,157], implying that Fe distribution is essential for the photosynthetic response to low-P conditions. In Arabidopsis, PHOSPHATE CO-TRANSPORTER 4;4 (PHT4;4), encodes an ascorbate transporter in chloroplasts, interacted with a transcription factor bZIP58, resulted in an alleviation in the decline of photosynthesis induced by low-Fe and low-P deficiency [158]. Under Fe deficiency, P deprivation led to an upregulation of bZIP58 expression, thereby enhanced the transcription levels of nucleus-encoded photosynthetic genes. Concurrently, bZIP58 promoted the synthesis of ascorbate (AsA) via induction of VITAMINC4 (VTC4) expression, then increased ascorbic acid in the chloroplast mediated by PHT4;4. AsA prevented the accumulation of ROS, which in turn maintained the expression of bZIP58 and its downstream photosynthetic genes [158].

4. Perspectives

In the past few decades, the Fe-P interactions in plants and soil have been extensively studied, yet the comprehensive effects of this interaction in conjunction with plants and soil remain to be elucidated. In order to explore the Fe-P interaction in soil, root, and leaf, a multi-dimensional interactome could be constructed, including genomics, transcriptomics, proteomics, metabolomics and microbiomics. In addition, the endophyte has been demonstrated to enhance the utilization efficiency of nutrients in plants. It would be of interest to determine whether the endophyte could influence the homeostasis and signaling of Fe and P in plants, particularly with regard to regulating apo-Fe status in roots under low-P conditions. Furthermore, given the intricate relationship between P and Fe in plants and soil, it is important to develop and apply P and Fe fertilizers in a manner that is appropriate for the specific conditions. The application of beneficial microorganisms and functional substances, derived from the soil-plant interaction process, to the dissolution of insoluble Fe-P complexes could be a significant pathway to the synergistic achievement of efficient Fe and P in acidic soil.

Author Contributions

T.W., J.T. and C.L. (Cuiyue Liang) conceived the idea; T.W., X.Y. and C.L. (Chang Liu) summarized publications and wrote the manuscript; J.T. and C.L. (Cuiyue Liang) reviewed the manuscript and provided input. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Open Competition Program of Ten Major Directions of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province (2022SDZG07), National Natural Science Foundation of China (32302662, 32172658, and 32172659), the Natural Science Foundation of Guangdong Province (2021A1515010826), the STIC Grant (SGDX20210823103535007), Key Areas Research and Development Programs of Guangdong Province (2022B0202060005).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

There is no new data in this work.

Acknowledgments

The figures were created with BioRender.com.

Conflicts of Interest

The authors declare that there is no conflict of interests regarding the publication of this manuscript.

References

  1. Lambers, H. Phosphorus acquisition and utilization in plants. Annu. Rev. Plant Biol. 2022, 73, 17–42. [Google Scholar] [CrossRef] [PubMed]
  2. Paz-Ares, J.; Puga, M.I.; Rojas-Triana, M.; Martinez-Hevia, I.; Diaz, S.; Poza-Carrión, C.; Miñambres, M.; Leyva, A. Plant adaptation to low phosphorus availability: Core signaling, crosstalks, and applied implications. Mol. Plant 2022, 15, 104–124. [Google Scholar] [CrossRef] [PubMed]
  3. Ning, X.Y.; Lin, M.F.; Huang, G.H.; Mao, J.P.; Gao, Z.; Wang, X.L. Research progress on iron absorption, transport, and molecular regulation strategy in plants. Front. Plant Sci. 2023, 14, 1190768. [Google Scholar] [CrossRef] [PubMed]
  4. Riaz, N.; Guerinot, M.L. All together now: Regulation of the iron deficiency response. J. Exp. Bot. 2021, 72, 2045–2055. [Google Scholar] [CrossRef] [PubMed]
  5. Wang, C.Q.; Thielemann, L.; Dippold, M.A.; Guggenberger, G.; Kuzyakov, Y.; Banfield, C.C.; Ge, T.; Guenther, S.; Bork, P.; Horn, M.A.; et al. Can the reductive dissolution of ferric iron in paddy soils compensate phosphorus limitation of rice plants and microorganisms? Soil Biol. Biochem. 2022, 168, 108653. [Google Scholar] [CrossRef]
  6. Xue, C.W.; Li, W.F.; Shen, R.F.; Lan, P. Impacts of iron on phosphate starvation-induced root hair growth in Arabidopsis. Plant Cell Environ. 2023, 46, 215–238. [Google Scholar] [CrossRef] [PubMed]
  7. Martinengo, S.; Santoro, V.; Schiavon, M.; Celi, L.; Martin, M.; Said-Pullicino, D. The influence of phosphorus availability on rice root traits driving iron plaque formation and dissolution, and implications for phosphorus uptake. Plant Soil 2024, 494, 603–616. [Google Scholar] [CrossRef]
  8. Clúa, J.; Montpetit, J.; Jimenez-Sandoval, P.; Naumann, C.; Santiago, J.; Poirier, Y. A CYBDOM protein impacts iron homeostasis and primary root growth under phosphate deficiency in Arabidopsis. Nat. Commun. 2024, 15, 423. [Google Scholar] [CrossRef]
  9. Li, S.J.; Lin, Z.G.; Liu, M.; Jiang, F.Z.; Chen, J.; Yang, X.J.; Wang, S.X. Effect of ferric chloride on phosphorus immobilization and speciation in Dianchi Lake sediments. Ecotoxicol. Environ. Saf. 2020, 197, 110637. [Google Scholar] [CrossRef]
  10. Su, M.; Meng, L.Z.; Zhao, L.; Tang, Y.K.; Qiu, J.J.; Tian, D.; Li, Z. Phosphorus deficiency in soils with red color: Insights from the interactions between minerals and microorganisms. Geoderma 2021, 404, 115311. [Google Scholar] [CrossRef]
  11. Memon, M. Role of Fe-Oxides for Predicting Phosphorus Sorption in Calcareous Soils; KIT Scientific Publishing: Karlsruhe, Germany, 2008. [Google Scholar]
  12. Celi, L.; Prati, M.; Magnacca, G.; Santoro, V.; Martin, M. Role of crystalline iron oxides on stabilization of inositol phosphates in soil. Geoderma 2020, 374, 114442. [Google Scholar] [CrossRef]
  13. Antelo, J.; Fiol, S.; Pérez, C.; Mariño, S.; Arce, F.; Gondar, D.; López, R. Analysis of phosphate adsorption onto ferrihydrite using the CD-MUSIC model. J. Colloid Interface Sci. 2010, 347, 112–119. [Google Scholar] [CrossRef] [PubMed]
  14. Devau, N.; Hinsinger, P.; Le Cadre, E.; Colomb, B.; Gérard, F. Fertilization and pH effects on processes and mechanisms controlling dissolved inorganic phosphorus in soils. Geochim. Cosmochim. Acta 2011, 75, 2980–2996. [Google Scholar] [CrossRef]
  15. Penn, C.J.; Camberato, J.J. A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 2019, 9, 120. [Google Scholar] [CrossRef]
  16. Sattari, S.Z.; Bouwman, A.F.; Giller, K.E.; van Ittersum, M.K. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc. Natl. Acad. Sci. USA 2012, 109, 6348–6353. [Google Scholar] [CrossRef] [PubMed]
  17. Withers, P.J.A.; Hodgkinson, R.A.; Rollett, A.; Dyer, C.; Dils, R.; Collins, A.L.; Bilsborrow, P.E.; Bailey, G.; Sylvester-Bradley, R. Reducing soil phosphorus fertility brings potential long-term environmental gains: A UK analysis. Environ. Res. Lett. 2017, 12, 063001. [Google Scholar] [CrossRef]
  18. Islam, M.; Siddique, K.H.; Padhye, L.P.; Pang, J.; Solaiman, Z.M.; Hou, D.; Srinivasarao, C.; Zhang, T.; Chandana, P.; Venu, N.; et al. A critical review of soil phosphorus dynamics and biogeochemical processes for unlocking soil phosphorus reserves. Adv. Agron. 2024, 185, 153–249. [Google Scholar]
  19. Fink, J.R.; Inda, A.V.; Tiecher, T.; Barrón, V. Iron oxides and organic matter on soil phosphorus availability. Cienc. Agrotecnol. 2016, 40, 369–379. [Google Scholar] [CrossRef]
  20. Husson, O. Redox potential (Eh) and pH as drivers of soil/plant/microorganism systems: A transdisciplinary overview pointing to integrative opportunities for agronomy. Plant Soil 2013, 362, 389–417. [Google Scholar] [CrossRef]
  21. Henderson, R.; Kabengi, N.; Mantripragada, N.; Cabrera, M.; Hassan, S.; Thompson, A. Anoxia-induced release of colloid-and nanoparticle-bound phosphorus in grassland soils. Environ. Sci. Technol. 2012, 46, 11727–11734. [Google Scholar] [CrossRef]
  22. Chiriţă, P.; Schlegel, M.L. Reaction of FeS with Fe (III)-bearing acidic solutions. Chem. Geol. 2012, 334, 131–138. [Google Scholar] [CrossRef]
  23. Limmer, M.A.; Evans, A.E.; Seyfferth, A.L. A new method to capture the spatial and temporal heterogeneity of aquatic plant iron root plaque in situ. Environ. Sci. Technol. 2021, 55, 912–918. [Google Scholar] [CrossRef] [PubMed]
  24. Li, C.; Ma, X.; Wang, Y.; Sun, Q.; Chen, M.S.; Zhang, C.S.; Ding, S.M.; Dai, Z.H. Root-mediated acidification, phosphatase activity and the phosphorus-cycling microbial community enhance phosphorus mobilization in the rhizosphere of wetland plants. Water Res. 2024, 255, 121548. [Google Scholar] [CrossRef] [PubMed]
  25. Fu, Z.Y.; Wu, F.F.; Song, K.; Lin, Y.; Bai, Y.C.; Zhu, Y.R.; Giesy, J.P. Competitive interaction between soil-derived humic acid and phosphate on goethite. Appl. Geochem. 2013, 36, 125–131. [Google Scholar] [CrossRef]
  26. Sundman, A.; Karlsson, T.; Sjöberg, S.; Persson, P. Impact of iron-organic matter complexes on aqueous phosphate concentrations. Chem. Geol. 2016, 426, 109–117. [Google Scholar] [CrossRef]
  27. Gerke, J. Humic (organic matter)-Al(Fe)-phosphate complexes: An underestimated phosphate form in soils and source of plant available phosphate. Soil Sci. 2010, 175, 417–425. [Google Scholar] [CrossRef]
  28. Gerke, J. Review Article: The effect of humic substances on phosphate and iron acquisition by higher plants: Qualitative and quantitative aspects. J. Plant Nutr. Soil Sci. 2021, 184, 329–338. [Google Scholar] [CrossRef]
  29. Gerke, J. Phytate (inositol hexakisphosphate) in soil and phosphate acquisition from inositol phosphates by higher plants. A review. Plants 2015, 4, 253–266. [Google Scholar] [CrossRef]
  30. Jansson, J.K.; McClure, R.; Egbert, R.G. Soil microbiome engineering for sustainability in a changing environment. Nat. Biotechnol. 2023, 41, 1716–1728. [Google Scholar] [CrossRef]
  31. Rawat, P.; Das, S.; Shankhdhar, D.; Shankhdhar, S.C. Phosphate-solubilizing microorganisms: Mechanism and their role in phosphate solubilization and uptake. J. Soil Sci. Plant Nutr. 2021, 21, 49–68. [Google Scholar] [CrossRef]
  32. Koza, N.A.; Adedayo, A.A.; Babalola, O.O.; Kappo, A.P. Microorganisms in plant growth and development: Roles in abiotic stress tolerance and secondary metabolites secretion. Microorganisms 2022, 10, 1528. [Google Scholar] [CrossRef] [PubMed]
  33. Mimmo, T.; Del Buono, D.; Terzano, R.; Tomasi, N.; Vigani, G.; Crecchio, C.; Pinton, R.; Zocchi, G.; Cesco, S. Rhizospheric organic compounds in the soil-microorganism-plant system: Their role in iron availability. Eur. J. Soil Sci. 2014, 65, 629–642. [Google Scholar] [CrossRef]
  34. Li, F.Y.; Koopal, L.; Tan, W.F. Roles of different types of oxalate surface complexes in dissolution process of ferrihydrite aggregates. Sci. Rep. 2018, 8, 2060. [Google Scholar] [CrossRef] [PubMed]
  35. Li, Z.; Bai, T.S.; Dai, L.T.; Wang, F.W.; Tao, J.J.; Meng, S.T.; Hu, Y.X.; Wang, S.M.; Hu, S.J. A study of organic acid production in contrasts between two phosphate solubilizing fungi: Penicillium oxalicum and Aspergillus niger. Sci. Rep. 2016, 6, 25313. [Google Scholar] [CrossRef] [PubMed]
  36. Zhang, L.; Song, X.W.; Shao, X.Q.; Wu, Y.L.; Zhang, X.Y.; Wang, S.M.; Pan, J.J.; Hu, S.J.; Li, Z. Lead immobilization assisted by fungal decomposition of organophosphate under various pH values. Sci. Rep. 2019, 9, 13353. [Google Scholar] [CrossRef] [PubMed]
  37. Genre, A.; Lanfranco, L.; Perotto, S.; Bonfante, P. Unique and common traits in mycorrhizal symbioses. Nat. Rev. Microbiol. 2020, 18, 649–660. [Google Scholar] [CrossRef] [PubMed]
  38. Andrino, A.; Boy, J.; Mikutta, R.; Sauheitl, L.; Guggenberger, G. Carbon investment required for the mobilization of inorganic and organic phosphorus bound to goethite by an arbuscular mycorrhiza (Solanum lycopersicum x Rhizophagus irregularis). Front. Environ. Sci. 2019, 7, 26. [Google Scholar] [CrossRef]
  39. Andrino, A.; Guggenberger, G.; Kernchen, S.; Mikutta, R.; Sauheitl, L.; Boy, J. Production of organic acids by arbuscular mycorrhizal fungi and their contribution in the mobilization of phosphorus bound to iron oxide. Front. Plant Sci. 2021, 12, 661842. [Google Scholar] [CrossRef] [PubMed]
  40. Martino, E.; Perotto, S. Mineral transformations by mycorrhizal fungi. Geomicrobiol. J. 2010, 27, 609–623. [Google Scholar] [CrossRef]
  41. Clarholm, M.; Skyllberg, U.; Rosling, A. Organic acid induced release of nutrients from metal-stabilized soil organic matter-the unbutton model. Soil Biol. Biochem. 2015, 84, 168–176. [Google Scholar] [CrossRef]
  42. Fan, X.X.; Chang, W.; Feng, F.J.; Song, F.Q. Responses of photosynthesis-related parameters and chloroplast ultrastructure to atrazine in alfalfa (Medicago sativa L.) inoculated with arbuscular mycorrhizal fungi. Ecotoxicol. Environ. Saf. 2018, 166, 102–108. [Google Scholar] [CrossRef] [PubMed]
  43. Kabir, A.H.; Debnath, T.; Das, U.; Prity, S.A.; Haque, A.; Rahman, M.M.; Parvez, M.S. Arbuscular mycorrhizal fungi alleviate Fe-deficiency symptoms in sunflower by increasing iron uptake and its availability along with antioxidant defense. Plant Physiol. Biochem. 2020, 150, 254–262. [Google Scholar] [CrossRef] [PubMed]
  44. Marschner, P.; Crowley, D.; Rengel, Z. Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis-model and research methods. Soil Biol. Biochem. 2011, 43, 883–894. [Google Scholar] [CrossRef]
  45. Tian, J.; Ge, F.; Zhang, D.; Deng, S.; Liu, X. Roles of phosphate solubilizing microorganisms from managing soil phosphorus deficiency to mediating biogeochemical P cycle. Biology 2021, 10, 158. [Google Scholar] [CrossRef] [PubMed]
  46. Hamdali, H.; Moursalou, K.; Tchangbedji, G.; Ouhdouch, Y.; Hafidi, M. Isolation and characterization of rock phosphate solubilizing actinobacteria from a Togolese phosphate mine. Afr. J. Biotechnol. 2012, 11, 312. [Google Scholar] [CrossRef]
  47. Han, L.C.; Wang, X.; Li, B.G.; Shen, G.F.; Tao, S.; Fu, B.; Han, Y.M.; Li, W.; Long, S.X.; Peng, S.Y.; et al. Enhanced Fe-bound phosphate availability by the combined use of Mg-modified biochar and phosphate-solubilizing bacteria. J. Environ. Chem. Eng. 2022, 10, 107232. [Google Scholar] [CrossRef]
  48. Gu, S.H.; Wei, Z.; Shao, Z.Y.; Friman, V.P.; Cao, K.H.; Yang, T.J.; Kramer, J.; Wang, X.F.; Li, M.; Mei, X.L.; et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat. Microbiol. 2020, 5, 1002–1010. [Google Scholar] [CrossRef] [PubMed]
  49. Wang, N.Q.; Wang, T.Q.; Chen, Y.; Wang, M.; Lu, Q.F.; Wang, K.G.; Dou, Z.C.; Chi, Z.G.; Qiu, W.; Dai, J.; et al. Microbiome convergence enables siderophore-secreting-rhizobacteria to improve iron nutrition and yield of peanut intercropped with maize. Nat. Commun. 2024, 15, 839. [Google Scholar] [CrossRef] [PubMed]
  50. Elena, M.; de Villegas, D. Microbial Siderophores; Varma, A., Chincholkar, S.B., Eds.; Springer: Berlin/Heidelberg, Germany, 2007; pp. 219–231. [Google Scholar]
  51. Jones, D.L.; Oburger, E. Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling; Bünemann, E., Oberson, A., Frossard, E., Eds.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 169–198. [Google Scholar]
  52. Vindeirinho, J.M.; Soares, H.M.V.M.; Soares, E.V. Modulation of siderophore production by Pseudomonas fluorescens through the manipulation of the culture medium composition. Appl. Biochem. Biotechnol. 2021, 193, 607–618. [Google Scholar] [CrossRef]
  53. Silva, L.I.d.; Pereira, M.C.; Carvalho, A.M.X.d.; Buttrós, V.H.; Pasqual, M.; Dória, J. Phosphorus-solubilizing microorganisms: A key to sustainable agriculture. Agriculture 2023, 13, 462. [Google Scholar] [CrossRef]
  54. Reid, R.K.; Reid, C.P.P.; Szaniszlo, P.J. Effects of synthetic and microbially produced chelates on the diffusion of iron and phosphorus to a simulated root in soil. Biol. Fert. Soils 1985, 1, 45–52. [Google Scholar] [CrossRef]
  55. Wang, S.; Walker, R.; Schicklberger, M.; Nico, P.S.; Fox, P.M.; Karaoz, U.; Chakraborty, R.; Brodie, E.L. Microbial phosphorus mobilization strategies across a natural nutrient limitation gradient and evidence for linkage with iron solubilization traits. Front. Microbiol. 2021, 12, 572212. [Google Scholar] [CrossRef] [PubMed]
  56. Cui, K.P.; Xu, T.; Chen, J.W.; Yang, H.Y.; Liu, X.M.; Zhuo, R.; Peng, Y.H.; Tang, W.; Wang, R.; Chen, L.S.; et al. Siderophores, a potential phosphate solubilizer from the endophyte Streptomyces sp. CoT10, improved phosphorus mobilization for host plant growth and rhizosphere modulation. J. Clean. Prod. 2022, 367, 133110. [Google Scholar] [CrossRef]
  57. Li, R.H.; Wang, W.J.; Zhao, R.X.; Zhang, J.Y.; Sun, L.; Li, X.Y.; Li, B. New insights into the microbial-driven metal reductive dissolution for enhanced phosphorus release from iron-rich sludge. J. Clean. Prod. 2023, 392, 136290. [Google Scholar] [CrossRef]
  58. Dar, D.; Thomashow, L.S.; Weller, D.M.; Newman, D.K. Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes. eLife 2020, 9, e59726. [Google Scholar] [CrossRef] [PubMed]
  59. Hernandez, M.E.; Kappler, A.; Newman, D.K. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 2004, 70, 921–928. [Google Scholar] [CrossRef] [PubMed]
  60. Wang, Y.; Newman, D.K. Redox reactions of phenazine antibiotics with ferric(hydr)oxides and molecular oxygen. Environ. Sci. Technol. 2008, 42, 2380–2386. [Google Scholar] [CrossRef] [PubMed]
  61. McRose, D.L.; Newman, D.K. Redox-active antibiotics enhance phosphorus bioavailability. Science 2021, 371, 1033–1037. [Google Scholar] [CrossRef]
  62. Jensen, V.; Löns, D.; Zaoui, C.; Bredenbruch, F.; Meissner, A.; Dieterich, G.; Münch, R.; Häussler, S. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and-independent pathways. J. Bacteriol. 2006, 188, 8601–8606. [Google Scholar] [CrossRef]
  63. Smolders, E.; Baetens, E.; Verbeeck, M.; Nawara, S.; Diels, J.; Verdievel, M.; Peeters, B.; De Cooman, W.; Baken, S. Internal loading and redox cycling of sediment iron explain reactive phosphorus concentrations in lowland rivers. Environ. Sci. Technol. 2017, 51, 2584–2592. [Google Scholar] [CrossRef]
  64. Liu, X.; Ye, Y.; Xiao, K.; Rensing, C.; Zhou, S.G. Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments. Mol. Microbiol. 2020, 113, 783–793. [Google Scholar] [CrossRef] [PubMed]
  65. Wang, J.J.; Gao, M.M.; Yang, Y.J.; Lu, S.P.; Wang, G.L.; Qian, X.Q. Interactions of Vallisneria natans and iron-oxidizing bacteria enhance iron-bound phosphorus formation in eutrophic lake sediments. Microorganisms 2022, 10, 413. [Google Scholar] [CrossRef] [PubMed]
  66. Dong, H.L.; Zeng, Q.; Sheng, Y.Z.; Chen, C.M.; Yu, G.G.; Kappler, A. Coupled iron cycling and organic matter transformation across redox interfaces. Nat. Rev. Earth Environ. 2023, 4, 659–673. [Google Scholar] [CrossRef]
  67. Wang, F.; Zhang, L.; Zhou, J.C.; Rengel, Z.; George, T.S.; Feng, G. Exploring the secrets of hyphosphere of arbuscular mycorrhizal fungi: Processes and ecological functions. Plant Soil 2022, 481, 1–22. [Google Scholar] [CrossRef]
  68. Chen, L.; Liao, H. Engineering crop nutrient efficiency for sustainable agriculture. J. Integr. Plant Biol. 2017, 59, 710–735. [Google Scholar] [CrossRef] [PubMed]
  69. Bouain, N.; Korte, A.; Satbhai, S.B.; Nam, H.I.; Rhee, S.Y.; Busch, W.; Rouached, H. Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation. PLoS Genet. 2019, 15, e1008392. [Google Scholar] [CrossRef] [PubMed]
  70. García, M.J.; Lucena, C.; Romera, F.J. Ethylene and nitric oxide involvement in the regulation of Fe and P deficiency responses in dicotyledonous plants. Int. J. Mol. Sci. 2021, 22, 4904. [Google Scholar] [CrossRef]
  71. Puga, M.I.; Poza-Carrión, C.; Martinez-Hevia, I.; Perez-Liens, L.; Paz-Ares, J. Recent advances in research on phosphate starvation signaling in plants. J. Plant Res. 2024, 137, 315–330. [Google Scholar] [CrossRef]
  72. Marschner, H.; Römheld, V. Strategies of plants for acquisition of iron. Plant Soil 1994, 165, 261–274. [Google Scholar] [CrossRef]
  73. Robinson, N.J.; Procter, C.M.; Connolly, E.L.; Guerinot, M.L. A ferric-chelate reductase for iron uptake from soils. Nature 1999, 397, 694–697. [Google Scholar] [CrossRef]
  74. Vert, G.g.; Grotz, N.; Dédaldéchamp, F.; Gaymard, F.d.r.; Guerinot, M.L.; Briat, J.F.o.; Curie, C. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 2002, 14, 1223–1233. [Google Scholar] [CrossRef] [PubMed]
  75. Robe, K.; Izquierdo, E.; Vignols, F.; Rouached, H.; Dubos, C. The coumarins: Secondary metabolites playing a primary role in plant nutrition and health. Trends Plant Sci. 2021, 26, 248–259. [Google Scholar] [CrossRef] [PubMed]
  76. Paffrath, V.; Tandron Moya, Y.A.; Weber, G.; von Wirén, N.; Giehl, R.F.H. A major role of coumarin-dependent ferric iron reduction in strategy I-type iron acquisition in Arabidopsis. Plant Cell 2024, 36, 642–664. [Google Scholar] [CrossRef] [PubMed]
  77. Suzuki, M.; Urabe, A.; Sasaki, S.; Tsugawa, R.; Nishio, S.; Mukaiyama, H.; Murata, Y.; Masuda, H.; Aung, M.S.; Mera, A.; et al. Development of a mugineic acid family phytosiderophore analog as an iron fertilizer. Nat. Commun. 2021, 12, 1558. [Google Scholar] [CrossRef] [PubMed]
  78. Yoneyama, T. Iron delivery to the growing leaves associated with leaf chlorosis in mugineic acid family phytosiderophores-generating graminaceous crops. Soil Sci. Plant Nutr. 2021, 67, 415–426. [Google Scholar] [CrossRef]
  79. Misson, J.; Raghothama, K.G.; Jain, A.; Jouhet, J.; Block, M.A.; Bligny, R.; Ortet, P.; Creff, A.; Somerville, S.; Rolland, N.; et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. USA 2005, 102, 11934–11939. [Google Scholar] [CrossRef] [PubMed]
  80. Li, W.F.; Lan, P. Genome-wide analysis of overlapping genes regulated by iron deficiency and phosphate starvation reveals new interactions in Arabidopsis roots. BMC Res. Notes 2015, 8, 555. [Google Scholar] [CrossRef] [PubMed]
  81. Hoehenwarter, W.; Mönchgesang, S.; Neumann, S.; Majovsky, P.; Abel, S.; Müller, J. Comparative expression profiling reveals a role of the root apoplast in local phosphate response. BMC Plant Biol. 2016, 16, 106. [Google Scholar] [CrossRef] [PubMed]
  82. Elliott, G.C.; Läuchli, A. Phosphorus efficiency and phosphate-iron interaction in maize. Agron. J. 1985, 77, 399–403. [Google Scholar] [CrossRef]
  83. Romera, F.J.; Alcántara, E.; de la Guardia, M.D. Effects of bicarbonate, phosphate and high pH on the reducing capacity of Fe-deficient sunflower and cucumber plants. J. Plant Nutr. 1992, 15, 1519–1530. [Google Scholar] [CrossRef]
  84. Sánchez-Rodríguez, A.R.; del Campillo, M.C.; Torrent, J. The severity of iron chlorosis in sensitive plants is related to soil phosphorus levels. J. Sci. Food Agric. 2014, 94, 2766–2773. [Google Scholar] [CrossRef] [PubMed]
  85. Zhang, J.C.; Wang, X.N.; Sun, W.; Wang, X.F.; Tong, X.S.; Ji, X.L.; An, J.P.; Zhao, Q.; You, C.X.; Hao, Y.J. Phosphate regulates malate/citrate-mediated iron uptake and transport in apple. Plant Sci. 2020, 297, 110526. [Google Scholar] [CrossRef] [PubMed]
  86. Tsai, H.H.; Schmidt, W. One way. Or another? Iron uptake in plants. New Phytol. 2017, 214, 500–505. [Google Scholar] [CrossRef] [PubMed]
  87. Zheng, L.Q.; Huang, F.L.; Narsai, R.; Wu, J.J.; Giraud, E.; He, F.; Cheng, L.J.; Wang, F.; Wu, P.; Whelan, J.; et al. Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 2009, 151, 262–274. [Google Scholar] [CrossRef]
  88. Ding, Y.; Wang, Z.G.; Ren, M.L.; Zhang, P.; Li, Z.N.; Chen, S.; Ge, C.L.; Wang, Y.L. Iron and callose homeostatic regulation in rice roots under low phosphorus. BMC Plant Biol. 2018, 18, 326. [Google Scholar] [CrossRef] [PubMed]
  89. Zanin, L.; Venuti, S.; Zamboni, A.; Varanini, Z.; Tomasi, N.; Pinton, R. Transcriptional and physiological analyses of Fe deficiency response in maize reveal the presence of Strategy I components and Fe/P interactions. BMC Genom. 2017, 18, 154. [Google Scholar] [CrossRef] [PubMed]
  90. Liu, D. Root developmental responses to phosphorus nutrition. J. Integr. Plant Biol. 2021, 63, 1065–1090. [Google Scholar] [CrossRef] [PubMed]
  91. Svistoonoff, S.; Creff, A.; Reymond, M.; Sigoillot-Claude, C.; Ricaud, L.; Blanchet, A.; Nussaume, L.; Desnos, T. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 2007, 39, 792–796. [Google Scholar] [CrossRef]
  92. Ticconi, C.A.; Lucero, R.D.; Sakhonwasee, S.; Adamson, A.W.; Creff, A.; Nussaume, L.; Desnos, T.; Abel, S. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl. Acad. Sci. USA 2009, 106, 14174–14179. [Google Scholar] [CrossRef]
  93. Péret, B.; Desnos, T.; Jost, R.; Kanno, S.; Berkowitz, O.; Nussaume, L. Root architecture responses: In search of phosphate. Plant Physiol. 2014, 166, 1713–1723. [Google Scholar] [CrossRef]
  94. Liu, X.X.; Zhu, X.F.; Xue, D.W.; Zheng, S.J.; Jin, C.W. Beyond iron-storage pool: Functions of plant apoplastic iron during stress. Trends Plant Sci. 2023, 28, 941–954. [Google Scholar] [CrossRef] [PubMed]
  95. Ward, J.T.; Lahner, B.; Yakubova, E.; Salt, D.E.; Raghothama, K.G. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol. 2008, 147, 1181–1191. [Google Scholar] [CrossRef]
  96. Müller, J.; Toev, T.; Heisters, M.; Teller, J.; Moore, K.L.; Hause, G.; Dinesh, D.C.; Bürstenbinder, K.; Abel, S. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev. Cell 2015, 33, 216–230. [Google Scholar] [CrossRef] [PubMed]
  97. Balzergue, C.; Dartevelle, T.; Godon, C.; Laugier, E.; Meisrimler, C.; Teulon, J.-M.; Creff, A.; Bissler, M.; Brouchoud, C.; Hagège, A.; et al. Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat. Commun. 2017, 8, 15300. [Google Scholar] [CrossRef] [PubMed]
  98. Mora-Macías, J.; Ojeda-Rivera, J.O.; Gutiérrez-Alanís, D.; Yong-Villalobos, L.; Oropeza-Aburto, A.; Raya-González, J.; Jiménez-Domínguez, G.; Chávez-Calvillo, G.; Rellán-Álvarez, R.; Herrera-Estrella, L. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc. Natl. Acad. Sci. USA 2017, 114, E3563–E3572. [Google Scholar] [CrossRef] [PubMed]
  99. Singh, A.P.; Fridman, Y.; Holland, N.; Ackerman-Lavert, M.; Zananiri, R.; Jaillais, Y.; Henn, A.; Savaldi-Goldstein, S. Interdependent nutrient availability and steroid hormone signals facilitate root growth plasticity. Dev. Cell 2018, 46, 59–72.e54. [Google Scholar] [CrossRef] [PubMed]
  100. Wang, X.Y.; Wang, Z.; Zheng, Z.; Dong, J.; Song, L.; Sui, L.Q.; Nussaume, L.; Desnos, T.; Liu, D. Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency. Plant Physiol. 2019, 179, 300–316. [Google Scholar] [CrossRef]
  101. Xu, Z.R.; Cai, M.L.; Yang, Y.; You, T.T.; Ma, J.F.; Wang, P.; Zhao, F.J. The ferroxidases LPR1 and LPR2 control iron translocation in the xylem of Arabidopsis plants. Mol. Plant 2022, 15, 1962–1975. [Google Scholar] [CrossRef] [PubMed]
  102. Zhu, Q.Y.; Wang, Y.; Liu, X.X.; Ye, J.Y.; Zhou, M.; Jing, X.T.; Du, W.X.; Hu, W.J.; He, C.; Zhu, Y.X.; et al. The ferroxidases are critical for Fe(II) oxidation in xylem to ensure a healthy Fe allocation in Arabidopsis thaliana. Front. Plant Sci. 2022, 13, 958984. [Google Scholar] [CrossRef]
  103. Naumann, C.; Heisters, M.; Brandt, W.; Janitza, P.; Alfs, C.; Tang, N.; Toto Nienguesso, A.; Ziegler, J.; Imre, R.; Mechtler, K.; et al. Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development. Curr. Biol. 2022, 32, 2189–2205.e2186. [Google Scholar] [CrossRef]
  104. Gutiérrez-Alanís, D.; Ojeda-Rivera, J.O.; Yong-Villalobos, L.; Cárdenas-Torres, L.; Herrera-Estrella, L. Adaptation to phosphate scarcity: Tips from Arabidopsis roots. Trends Plant Sci. 2018, 23, 721–730. [Google Scholar] [CrossRef] [PubMed]
  105. Gao, Y.Q.; Bu, L.H.; Han, M.L.; Wang, Y.L.; Li, Z.Y.; Liu, H.T.; Chao, D.Y. Long-distance blue light signalling regulates phosphate deficiency-induced primary root growth inhibition. Mol. Plant 2021, 14, 1539–1553. [Google Scholar] [CrossRef] [PubMed]
  106. Xu, J.M.; Wang, Z.Q.; Wang, J.Y.; Li, P.F.; Jin, J.F.; Chen, W.W.; Fan, W.; Kochian, L.V.; Zheng, S.J.; Yang, J.L. Low phosphate represses histone deacetylase complex1 to regulate root system architecture remodeling in Arabidopsis. New Phytol. 2020, 225, 1732–1745. [Google Scholar] [CrossRef]
  107. Li, T.; Zhang, R.Y.; Satheesh, V.; Wang, P.; Ma, G.J.; Guo, J.F.; An, G.Y.; Lei, M.G. The chromatin remodeler BRAHMA recruits HISTONE DEACETYLASE6 to regulate root growth inhibition in response to phosphate starvation in Arabidopsis. J. Integr. Plant Biol. 2022, 64, 2314–2326. [Google Scholar] [CrossRef] [PubMed]
  108. Godon, C.; Mercier, C.; Wang, X.Y.; David, P.; Richaud, P.; Nussaume, L.; Liu, D.; Desnos, T. Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells. Plant J. 2019, 99, 937–949. [Google Scholar] [CrossRef] [PubMed]
  109. Dong, J.S.; Piñeros, M.A.; Li, X.X.; Yang, H.B.; Liu, Y.; Murphy, A.S.; Kochian, L.V.; Liu, D. An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots. Mol. Plant 2017, 10, 244–259. [Google Scholar] [CrossRef] [PubMed]
  110. Mercier, C.; Roux, B.; Have, M.; Le Poder, L.; Duong, N.; David, P.; Leonhardt, N.; Blanchard, L.; Naumann, C.; Abel, S.; et al. Root responses to aluminium and iron stresses require the SIZ1 SUMO ligase to modulate the STOP1 transcription factor. Plant J. 2021, 108, 1507–1521. [Google Scholar] [CrossRef] [PubMed]
  111. Zheng, Z.; Liu, D. SIZ1 regulates phosphate deficiency-induced inhibition of primary root growth of Arabidopsis by modulating Fe accumulation and ROS production in its roots. Plant Signal. Behav. 2021, 16, 1946921. [Google Scholar] [CrossRef] [PubMed]
  112. Shen, N.; Hou, S.F.; Tu, G.Q.; Lan, W.Z.; Jing, Y.P. Transcription factor WRKY33 mediates the phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in Arabidopsis roots. Int. J. Mol. Sci. 2021, 22, 9275. [Google Scholar] [CrossRef]
  113. Maniero, R.A.; Picco, C.; Hartmann, A.; Engelberger, F.; Gradogna, A.; Scholz-Starke, J.; Melzer, M.; Künze, G.; Carpaneto, A.; von Wirén, N.; et al. Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency. Nat. Commun. 2024, 15, 422. [Google Scholar] [CrossRef]
  114. Wang, L.Y.; Qian, J.; Li, M.; Zheng, H.; Yang, X.; Zheng, M.; Hsu, Y.F. Arabidopsis PDE1 confers phosphate-deficiency tolerance in primary root growth. Plant Cell Rep. 2023, 43, 8. [Google Scholar] [CrossRef] [PubMed]
  115. Gutiérrez-Alanís, D.; Yong-Villalobos, L.; Jimenez-Sandoval, P.; Alatorre-Cobos, F.; Oropeza-Aburto, A.; Mora-Macías, J.; Sánchez-Rodríguez, F.; Cruz-Ramírez, A.; Herrera-Estrella, L. Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev. Cell 2017, 41, 555–570.e553. [Google Scholar] [CrossRef] [PubMed]
  116. Mueller, M. Arabidopsis Root Hair Development in Adaptation to Iron and Phosphate Supply; Mathematisch-Naturwissenschaftliche Fakultät I; Humboldt-Universität zu Berlin: Berlin, Germany, 2007. [Google Scholar]
  117. Bournier, M.; Tissot, N.; Mari, S.; Boucherez, J.; Lacombe, E.; Briat, J.F.; Gaymard, F. Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. J. Biol. Chem. 2013, 288, 22670–22680. [Google Scholar] [CrossRef] [PubMed]
  118. Briat, J.F.; Rouached, H.; Tissot, N.; Gaymard, F.; Dubos, C. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: Potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front. Plant Sci. 2015, 6, 129608. [Google Scholar] [CrossRef] [PubMed]
  119. Guo, M.N.; Ruan, W.Y.; Zhang, Y.B.; Zhang, Y.X.; Wang, X.Q.; Guo, Z.H.; Wang, L.; Zhou, T.; Paz-Ares, J.; Yi, K.K. A reciprocal inhibitory module for Pi and iron signaling. Mol. Plant 2022, 15, 138–150. [Google Scholar] [CrossRef] [PubMed]
  120. Chai, Y.N.; Schachtman, D.P. Root exudates impact plant performance under abiotic stress. Trends Plant Sci. 2022, 27, 80–91. [Google Scholar] [CrossRef] [PubMed]
  121. Chen, Z.C.; Liao, H. Organic acid anions: An effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils. J. Genet. Genom. 2016, 43, 631–638. [Google Scholar] [CrossRef] [PubMed]
  122. Panchal, P.; Miller, A.J.; Giri, J. Organic acids: Versatile stress-response roles in plants. J. Exp. Bot. 2021, 72, 4038–4052. [Google Scholar] [CrossRef] [PubMed]
  123. Jones, D.L.; Darah, P.R.; Kochian, L.V. Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 1996, 180, 57–66. [Google Scholar] [CrossRef]
  124. Hamada, Y.Z.; Carlson, B.; Dangberg, J. Interaction of malate and lactate with chromium (III) and iron (III) in aqueous solutions. Synth. React. Inorg. Met.-Org. Chem. 2005, 35, 515–522. [Google Scholar] [CrossRef]
  125. Deiana, S.; Palma, A.; Premoli, A.; Senette, C. Possible role of the polyuronic components in accumulation and mobilization of iron and phosphate at the soil-root interface. Plant Physiol. Biochem. 2007, 45, 341–349. [Google Scholar] [CrossRef] [PubMed]
  126. Gerke, J. The acquisition of phosphate by higher plants: Effect of carboxylate release by the roots. A critical review. J. Plant Nutr. Soil Sci. 2015, 178, 351–364. [Google Scholar] [CrossRef]
  127. Dong, D.F.; Peng, X.X.; Yan, X.L. Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiol. Plant. 2004, 122, 190–199. [Google Scholar] [CrossRef]
  128. Hernández, G.; Ramírez, M.; Valdés-López, O.; Tesfaye, M.; Graham, M.A.; Czechowski, T.; Schlereth, A.; Wandrey, M.; Erban, A.; Cheung, F.; et al. Phosphorus stress in common bean: Root transcript and metabolic responses. Plant Physiol. 2007, 144, 752–767. [Google Scholar] [CrossRef] [PubMed]
  129. Ryan, P.; Delhaize, E.; Jones, D. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Biol. 2001, 52, 527–560. [Google Scholar] [CrossRef] [PubMed]
  130. Valentinuzzi, F.; Pii, Y.; Vigani, G.; Lehmann, M.; Cesco, S.; Mimmo, T. Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria × ananassa. J. Exp. Bot. 2015, 66, 6483–6495. [Google Scholar] [CrossRef] [PubMed]
  131. Schmid, N.B.; Giehl, R.F.H.; Döll, S.; Mock, H.P.; Strehmel, N.; Scheel, D.; Kong, X.; Hider, R.C.; von Wirén, N. Feruloyl-CoA 6′-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol. 2013, 164, 160–172. [Google Scholar] [CrossRef] [PubMed]
  132. Ziegler, J.; Schmidt, S.; Chutia, R.; Müller, J.; Böttcher, C.; Strehmel, N.; Scheel, D.; Abel, S. Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J. Exp. Bot. 2015, 67, 1421–1432. [Google Scholar] [CrossRef]
  133. DeLoose, M.; Cho, H.; Bouain, N.; Choi, I.; Prom-U-Thai, C.; Shahzad, Z.; Zheng, L.; Rouached, H. PDR9 allelic variation and MYB63 modulate nutrient-dependent coumarin homeostasis in Arabidopsis. Plant J. 2024, 117, 1716–1727. [Google Scholar] [CrossRef]
  134. Chutia, R.; Abel, S.; Ziegler, J. Iron and phosphate deficiency regulators concertedly control coumarin profiles in Arabidopsis thaliana roots during iron, phosphate, and combined deficiencies. Front. Plant Sci. 2019, 10, 113. [Google Scholar] [CrossRef]
  135. Chutia, R.; Scharfenberg, S.; Neumann, S.; Abel, S.; Ziegler, J. Modulation of phosphate deficiency-induced metabolic changes by iron availability in Arabidopsis thaliana. Int. J. Mol. Sci. 2021, 22, 7609. [Google Scholar] [CrossRef] [PubMed]
  136. Tomasi, N.; Weisskopf, L.; Renella, G.; Landi, L.; Pinton, R.; Varanini, Z.; Nannipieri, P.; Torrent, J.; Martinoia, E.; Cesco, S. Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol. Biochem. 2008, 40, 1971–1974. [Google Scholar] [CrossRef]
  137. Chen, Y.T.; Wang, Y.; Yeh, K.C. Role of root exudates in metal acquisition and tolerance. Curr. Opin. Plant Biol. 2017, 39, 66–72. [Google Scholar] [CrossRef]
  138. Rajniak, J.; Giehl, R.F.H.; Chang, E.; Murgia, I.; von Wirén, N.; Sattely, E.S. Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nat. Chem. Biol. 2018, 14, 442–450. [Google Scholar] [CrossRef]
  139. Todorov, L.T.; Kostova, I.P. Coumarin-transition metal complexes with biological activity: Current trends and perspectives. Front. Chem. 2024, 12, 1342772. [Google Scholar] [CrossRef]
  140. Ladouceur, A.; Tozawa, S.; Alam, S.; Kamei, S.; Kawai, S. Effect of low phosphorus and iron-deficient conditions on phytosiderophore release and mineral nutrition in barley. Soil Sci. Plant Nutr. 2006, 52, 203–210. [Google Scholar] [CrossRef]
  141. McRose, D.L.; Li, J.Y.; Newman, D.K. The chemical ecology of coumarins and phenazines affects iron acquisition by pseudomonads. Proc. Natl. Acad. Sci. USA 2023, 120, e2217951120. [Google Scholar] [CrossRef]
  142. Esparza-Reynoso, S.; Ayala-Rodríguez, J.Á.; López-Bucio, J. Pseudomonas putida configures Arabidopsis root architecture through modulating the sensing systems for phosphate and iron acquisition. Plant Sci. 2024, 342, 112028. [Google Scholar] [CrossRef] [PubMed]
  143. Wang, C.; Dippold, M.A.; Guggenberger, G.; Kuzyakov, Y.; Guenther, S.; Dorodnikov, M. The wetter the better? Preferences in plant-microbial competition for phosphorus sources in rice cultivation under contrasting irrigation. Soil Biol. Biochem. 2024, 191, 109339. [Google Scholar] [CrossRef]
  144. Jia, Z.T.; Giehl, R.F.; von Wirén, N. Nutrient-hormone relations: Driving root plasticity in plants. Mol. Plant 2022, 15, 86–103. [Google Scholar] [CrossRef]
  145. Waadt, R.; Seller, C.A.; Hsu, P.-K.; Takahashi, Y.; Munemasa, S.; Schroeder, J.I. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 2022, 23, 680–694. [Google Scholar] [CrossRef] [PubMed]
  146. Wild, M.; Davière, J.M.; Regnault, T.; Sakvarelidze-Achard, L.; Carrera, E.; Lopez Diaz, I.; Cayrel, A.; Dubeaux, G.; Vert, G.; Achard, P. Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses. Dev. Cell 2016, 37, 190–200. [Google Scholar] [CrossRef] [PubMed]
  147. Jiang, C.F.; Gao, X.H.; Liao, L.L.; Harberd, N.P.; Fu, X.D. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol. 2007, 145, 1460–1470. [Google Scholar] [CrossRef] [PubMed]
  148. Curie, C.; Mari, S. New routes for plant iron mining. New Phytol. 2017, 214, 521–525. [Google Scholar] [CrossRef] [PubMed]
  149. Celletti, S.; Pii, Y.; Valentinuzzi, F.; Tiziani, R.; Fontanella, M.C.; Beone, G.M.; Mimmo, T.; Cesco, S.; Astolfi, S. Physiological responses to Fe deficiency in split-root tomato plants: Possible roles of auxin and ethylene? Agronomy 2020, 10, 1000. [Google Scholar] [CrossRef]
  150. Zhang, H.Y.; Yang, Y.M.; Sun, C.Y.; Liu, X.Q.; Lv, L.L.; Hu, Z.B.; Yu, D.Y.; Zhang, D. Up-regulating GmETO1 improves phosphorus uptake and use efficiency by promoting root growth in soybean. Plant Cell Environ. 2020, 43, 2080–2094. [Google Scholar] [CrossRef] [PubMed]
  151. Yu, H.L.; Luo, N.; Sun, L.C.; Liu, D. HPS4/SABRE regulates plant responses to phosphate starvation through antagonistic interaction with ethylene signalling. J. Exp. Bot. 2012, 63, 4527–4538. [Google Scholar] [CrossRef]
  152. Nolan, T.M.; Vukašinović, N.; Liu, D.R.; Russinova, E.; Yin, Y.H. Brassinosteroids: Multidimensional regulators of plant growth, development, and stress responses. Plant Cell 2020, 32, 295–318. [Google Scholar] [CrossRef]
  153. Li, S.M.; Zheng, H.X.; Lin, L.; Wang, F.; Sui, N. Roles of brassinosteroids in plant growth and abiotic stress response. Plant Growth Regul. 2021, 93, 29–38. [Google Scholar] [CrossRef]
  154. Wang, B.L.; Li, Y.; Zhang, W.H. Brassinosteroids are involved in response of cucumber (Cucumis sativus) to iron deficiency. Ann. Bot. 2012, 110, 681–688. [Google Scholar] [CrossRef]
  155. Therby-Vale, R.; Lacombe, B.; Rhee, S.Y.; Nussaume, L.; Rouached, H. Mineral nutrient signaling controls photosynthesis: Focus on iron deficiency-induced chlorosis. Trends Plant Sci. 2022, 27, 502–509. [Google Scholar] [CrossRef]
  156. Saenchai, C.; Bouain, N.; Kisko, M.; Prom-u-thai, C.; Doumas, P.; Rouached, H. The involvement of OsPHO1;1 in the regulation of iron transport through integration of phosphate and zinc deficiency signaling. Front. Plant Sci. 2016, 7, 396. [Google Scholar] [CrossRef]
  157. Hirsch, J.; Marin, E.; Floriani, M.; Chiarenza, S.; Richaud, P.; Nussaume, L.; Thibaud, M.C. Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 2006, 88, 1767–1771. [Google Scholar] [CrossRef]
  158. Nam, H.I.; Shahzad, Z.; Dorone, Y.; Clowez, S.; Zhao, K.; Bouain, N.; Lay-Pruitt, K.S.; Cho, H.; Rhee, S.Y.; Rouached, H. Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling. Nat. Commun. 2021, 12, 7211. [Google Scholar] [CrossRef]
Ijms 25 06992 g001
Figure 1. Schematic overview of the Fe-P interactions in plants and soils. 1. Fe and P are essential nutrients for plants, and their interactions participate in various biological processes in plants and soils. Fe is readily bounded to P and forms insoluble Fe-P complexes, thereby reducing the availability of Fe and P in acidic soil. 2. In the rhizosphere, microorganisms have been demonstrated to activate Fe-P complexes via secreting organic acids, siderophores, and redox substances (phenazine) into soil. 3. Furthermore, in response to Fe-P deficiencies, plants also release organic acids and redox substances (coumarins) to enhance the bioavailability of Fe and P. The interaction between microorganisms and root exudates may be crucial in promoting Fe-P activation. 4. In addition, the interaction of P and Fe exhibits intricate regulation in root morphology, hormone metabolism, and photosynthesis in plants. The mechanisms of Fe-P interaction in plants and soils have the potential to promote sustainable agriculture by enhancing P and Fe utilization efficiency in plants.
Figure 1. Schematic overview of the Fe-P interactions in plants and soils. 1. Fe and P are essential nutrients for plants, and their interactions participate in various biological processes in plants and soils. Fe is readily bounded to P and forms insoluble Fe-P complexes, thereby reducing the availability of Fe and P in acidic soil. 2. In the rhizosphere, microorganisms have been demonstrated to activate Fe-P complexes via secreting organic acids, siderophores, and redox substances (phenazine) into soil. 3. Furthermore, in response to Fe-P deficiencies, plants also release organic acids and redox substances (coumarins) to enhance the bioavailability of Fe and P. The interaction between microorganisms and root exudates may be crucial in promoting Fe-P activation. 4. In addition, the interaction of P and Fe exhibits intricate regulation in root morphology, hormone metabolism, and photosynthesis in plants. The mechanisms of Fe-P interaction in plants and soils have the potential to promote sustainable agriculture by enhancing P and Fe utilization efficiency in plants.
Ijms 25 06992 g001
Ijms 25 06992 g002
Figure 2. The network of Fe in the apoplast modulates primary root growth under P starvation. In P deficiency, Fe is accumulated in the apoplast of stem cell niche and elongation zone cortical cells (yellow part of root on the left side of diagram). The accumulation of Fe triggers the production of reactive oxygen species (ROS), which induces cell wall stiffening and callose deposition, thereby suppresses primary root elongation. This process necessitates the participation of LPR1 in the oxidation of Fe2+ and the involvement of CRR, HYP1, and PDE1 in the reduction of Fe3+. BZR1 and the BRM-mediated recruitment of the HDC1-HDA6 complex to the LPR1 loci both repress LPR1 transcription, while HY5 elevates the expression of LPR1. PDR2 negatively regulates the accumulation of apo-Fe under low-P conditions by restricting the actions of LPR1. The secretion of malate into the apoplast via the ALMT1 could chelate Fe3+ and thus promote Fe accumulation. STOP1 and WRKY33 increase ALMT1 transcription under low-P conditions. SIZ1 downregulated the signaling of STOP1. The accumulation of STOP1 protein is inhibited by ALS3-STAR1 modules. It is possible that apo-Fe may be stored in the vacuole via VIT, but further confirmation is required to determine whether this pathway is present in all plants.
Figure 2. The network of Fe in the apoplast modulates primary root growth under P starvation. In P deficiency, Fe is accumulated in the apoplast of stem cell niche and elongation zone cortical cells (yellow part of root on the left side of diagram). The accumulation of Fe triggers the production of reactive oxygen species (ROS), which induces cell wall stiffening and callose deposition, thereby suppresses primary root elongation. This process necessitates the participation of LPR1 in the oxidation of Fe2+ and the involvement of CRR, HYP1, and PDE1 in the reduction of Fe3+. BZR1 and the BRM-mediated recruitment of the HDC1-HDA6 complex to the LPR1 loci both repress LPR1 transcription, while HY5 elevates the expression of LPR1. PDR2 negatively regulates the accumulation of apo-Fe under low-P conditions by restricting the actions of LPR1. The secretion of malate into the apoplast via the ALMT1 could chelate Fe3+ and thus promote Fe accumulation. STOP1 and WRKY33 increase ALMT1 transcription under low-P conditions. SIZ1 downregulated the signaling of STOP1. The accumulation of STOP1 protein is inhibited by ALS3-STAR1 modules. It is possible that apo-Fe may be stored in the vacuole via VIT, but further confirmation is required to determine whether this pathway is present in all plants.
Ijms 25 06992 g002
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yang, X.; Liu, C.; Liang, C.; Wang, T.; Tian, J. The Phosphorus-Iron Nexus: Decoding the Nutrients Interaction in Soil and Plant. Int. J. Mol. Sci. 2024, 25, 6992. https://doi.org/10.3390/ijms25136992

AMA Style

Yang X, Liu C, Liang C, Wang T, Tian J. The Phosphorus-Iron Nexus: Decoding the Nutrients Interaction in Soil and Plant. International Journal of Molecular Sciences. 2024; 25(13):6992. https://doi.org/10.3390/ijms25136992

Chicago/Turabian Style

Yang, Xingqi, Chang Liu, Cuiyue Liang, Tianqi Wang, and Jiang Tian. 2024. "The Phosphorus-Iron Nexus: Decoding the Nutrients Interaction in Soil and Plant" International Journal of Molecular Sciences 25, no. 13: 6992. https://doi.org/10.3390/ijms25136992

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop