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Iron homeostasis and plant immune responses: Recent insights and translational implications

2020; Elsevier BV; Volume: 295; Issue: 39 Linguagem: Inglês

10.1074/jbc.rev120.010856

1083-351X

John H. Herlihy, Terri A. Long, John M. McDowell,

Plant responses to water stress

Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency–related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification. Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency–related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification. Iron (Fe) is an essential micronutrient for all living organisms, including plants and their associated microbes (1Camprubi E. Jordan S.F. Vasiliadou R. Lane N. Iron catalysis at the origin of life.IUBMB Life. 2017; 69 (28470848): 373-38110.1002/iub.1632Crossref PubMed Scopus (39) Google Scholar). Iron readily donates and accepts electrons, as it can exist in multiple oxidation states, particularly its ferric (Fe3+) and ferrous forms (Fe2+). Therefore, iron cofactors such as heme and Fe-sulfur clusters function in all primary metabolic processes, including respiration, DNA synthesis and repair, and cell proliferation and differentiation (1Camprubi E. Jordan S.F. Vasiliadou R. Lane N. Iron catalysis at the origin of life.IUBMB Life. 2017; 69 (28470848): 373-38110.1002/iub.1632Crossref PubMed Scopus (39) Google Scholar). In plants, iron is also essential for chlorophyll and hormone synthesis and photosynthesis. Despite iron's essentiality, iron overload can cause damage in any organism. This is because iron's potent electron chemistry also makes it dangerous when it is in physiological excess. Iron acts as a catalyst with hydrogen peroxide through the Fenton reaction (Table 1), producing more dangerous reactive oxygen species (ROS), including the highly reactive hydroxide ion (2Winterbourn C.C. Toxicity of iron and hydrogen peroxide: the Fenton reaction.Toxicol. Lett. 1995; 82-83 (8597169): 969-97410.1016/0378-4274(95)03532-XCrossref PubMed Scopus (675) Google Scholar). These potent oxidizers damage lipids, proteins, and nucleic acids (3Becana M. Moran J. Iturbe-Ormaetxe I. Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection.Plant Soil. 1998; 201: 137-14710.1023/A:1004375732137Crossref Scopus (203) Google Scholar, 4Pinto S.D S. Souza A.E.D. Oliva M.A. Pereira E.G. Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron.Sci. Agric. 2016; 73: 217-22610.1590/0103-9016-2015-0288Crossref Scopus (24) Google Scholar). When the damage becomes too severe, the cell cannot be saved and undergoes programmed cell death (5Tsai T.-M. Huang H.-J. Effects of iron excess on cell viability and mitogen-activated protein kinase activation in rice roots.Physiol. Plant. 2006; 127: 583-59210.1111/j.1399-3054.2006.00696.xCrossref Scopus (18) Google Scholar). Thus, balance of iron levels is imperative for all organisms. Accordingly, plants tightly regulate iron uptake, localization, transport, and storage. Exciting recent progress has been achieved in understanding how plants acquire and transport biologically active iron from the soil and respond to iron-deficient environments (6Samira R. Stallmann A. Massenburg L.N. Long T.A. Ironing out the issues: integrated approaches to understanding iron homeostasis in plants.Plant Sci. 2013; 210 (23849132): 250-25910.1016/j.plantsci.2013.06.004Crossref PubMed Scopus (0) Google Scholar, 7Kobayashi T. Nozoye T. Nishizawa N.K. Iron transport and its regulation in plants.Free Radic. Biol. Med. 2019; 133 (30385345): 11-2010.1016/j.freeradbiomed.2018.10.439Crossref PubMed Scopus (43) Google Scholar).Table 1GlossaryFenton reaction—A catalytic process by which free iron converts hydrogen peroxide to the biologically dangerous hydroxide radical.Pathogen-associated molecular pattern (PAMP)—Conserved epitopes of plant-pathogenic microbes that are recognized by plants to initiate an immune response.Pattern-triggered immunity (PTI)—A plant immune response triggered by receptor-mediated perception of PAMPs, typified by production of ROS, cell wall reinforcement, and transcriptional reprogramming.Pathogen effector—Proteinaceous virulence factor secreted by plant pathogens into host tissues or cells to disrupt immune functioning and accommodate pathogen growth and reproduction.Effector-triggered immunity (ETI)—A potent plant immune response triggered by perception of intracellular pathogen effectors or their activity; typified by programmed cell death called hypersensitive response (HR) to limit pathogen spread.Biotrophic pathogen—A plant pathogen that subsists on living host tissue during its entire life cycle.Necrotrophic pathogen—A plant pathogen that secretes virulence factors to kill host tissues and facilitate its feeding or reproduction.Hemibiotrophic pathogen—A plant pathogen that employs a biotrophic lifestyle at the start of infection but transitions to a necrotroph to complete its life cycle.Strategy I iron uptake—Mechanism for plant iron acquisition that relies on rhizosphere acidification and iron reduction, followed by direct import of ferrous iron; utilized by all non-Poaceae (nongrass) plants.Strategy II iron uptake—Mechanism for plant iron acquisition employed by the Poaceae (grasses); involves secretion of iron-binding phytosiderophores into the rhizosphere followed by uptake of the iron-siderophore complex.Nutritional immunity—A process, first described in mammals, by which a host organism restricts availability of nutrients following infection to starve a pathogen.Ferroptosis—Programmed cell death marked by accumulation of iron and loss of antioxidant protections, culminating in a runaway Fenton reaction and lipid peroxidation.Biofortification—Breeding or genetic engineering efforts designed to improve the nutritional content of edible plant tissues. Open table in a new tab Along with the challenge of maintaining nutrient homeostasis, plants also must cope with a wide variety of pathogens and pests. Plants have evolved robust mechanisms for perception of detrimental microbes, which in turn trigger physiological responses to impede infection (8Cook D.E. Mesarich C.H. Thomma B.P. Understanding plant immunity as a surveillance system to detect invasion.Annu. Rev. Phytopathol. 2015; 53 (26047564): 541-56310.1146/annurev-phyto-080614-120114Crossref PubMed Scopus (217) Google Scholar). Recent progress on iron homeostasis has been paralleled by progress in the molecular plant-microbe interaction field on understanding plant pathogen surveillance proteins, immune system signaling, and suppression of immunity by pathogen virulence proteins. These foci have provided huge payoffs in understanding how plants and microbes interact at the molecular level (9Michelmore R. Coaker G. Bart R. Beattie G. Bent A. Bruce T. Cameron D. Dangl J. Dinesh-Kumar S. Edwards R. Eves-van den Akker S. Gassmann W. Greenberg J.T. Hanley-Bowdoin L. Harrison R.J. et al.Foundational and translational research opportunities to improve plant health.Mol. Plant Microbe Interact. 2017; 30 (28398839): 515-51610.1094/MPMI-01-17-0010-CRCrossref PubMed Scopus (12) Google Scholar). The impact of iron on plant-pathogen interactions has been acknowledged for a considerable span of time but has received limited attention; indeed, iron homeostasis and plant immunity are typically studied in isolation from each other. One goal of this review is to highlight recent studies that connect iron and plant-pathogen interactions. We also discuss the implications of iron-immunity cross-talk on efforts to breed iron-fortified crops. We begin with primers on the regulatory networks that mediate plant immunity and plant iron homeostasis. Plant immune responses are activated when the plant detects signals that are diagnostic of pathogen invasion. For example, plants recognize a variety of pathogen-associated molecular patterns (PAMPs), initiating pattern-triggered immunity (PTI; Fig. 1C) (10Katagiri F. Tsuda K. Understanding the plant immune system.Mol. Plant Microbe Interact. 2010; 23 (20653410): 1531-153610.1094/MPMI-04-10-0099Crossref PubMed Scopus (136) Google Scholar). PAMPs are epitopes such as bacterial flagellin or fungal and oomycete cell wall components. Such epitopes are often evolutionarily conserved, allowing for detection of groups of pathogens (e.g. multiple species) that share the epitope (11Boller T. He S.Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens.Science. 2009; 324 (19423812): 742-74410.1126/science.1171647Crossref PubMed Scopus (582) Google Scholar). PAMPs can be detected in the apoplast by cell-surface receptors (12Gust A.A. Felix G. Receptor like proteins associate with sobir1-type of adaptors to form bimolecular receptor kinases.Curr. Opin. Plant Biol. 2014; 21 (25064074): 104-11110.1016/j.pbi.2014.07.007Crossref PubMed Scopus (0) Google Scholar). Such recognition initiates cytoplasmic protein kinase cascades, Ca2+ influx, and rapid production of ROS (13Macho A.P. Zipfel C. Plant PRRs and the activation of innate immune signaling.Mol. Cell. 2014; 54 (24766890): 263-27210.1016/j.molcel.2014.03.028Abstract Full Text Full Text PDF PubMed Scopus (438) Google Scholar). As discussed below, iron plays a key role in ROS generation. ROS and hormone signals interact with each other to stimulate diverse molecular and cellular responses that strengthen plant cells against pathogen attack (14Karapetyan S. Dong X. Redox and the circadian clock in plant immunity: a balancing act.Free Radic. Biol. Med. 2018; 119 (29274381): 56-6110.1016/j.freeradbiomed.2017.12.024Crossref PubMed Scopus (24) Google Scholar). PAMP perception leads to reprogramming of thousands of genes, including genes for antimicrobial proteins (e.g. iron-sequestering defensins discussed below) and secondary metabolites with antimicrobial activity (13Macho A.P. Zipfel C. Plant PRRs and the activation of innate immune signaling.Mol. Cell. 2014; 54 (24766890): 263-27210.1016/j.molcel.2014.03.028Abstract Full Text Full Text PDF PubMed Scopus (438) Google Scholar). At the cellular level, pathogens often require access to individual cells or host vasculature; thus, the plant produces callose to reinforce cell walls against hydrolases and pathogen secretion systems (15Luna E. Pastor V. Robert J. Flors V. Mauch-Mani B. Ton J. Callose deposition: a multifaceted plant defense response.Mol. Plant Microbe Interact. 2011; 24 (20955078): 183-19310.1094/MPMI-07-10-0149Crossref PubMed Scopus (374) Google Scholar). All microbial pathogens produce PAMPs and are therefore vulnerable to PTI. Accordingly, pathogen success depends on evasion of detection and/or suppression of PTI signaling (16Nobori T. Mine A. Tsuda K. Molecular networks in plant-pathogen holobiont.FEBS Lett. 2018; 592 (29714033): 1937-195310.1002/1873-3468.13071Crossref PubMed Scopus (10) Google Scholar). Many pathogens disguise themselves by secreting proteins to bind PAMPs, thereby obscuring recognition, leading to PTI (17Sánchez-Vallet A. Saleem-Batcha R. Kombrink A. Hansen G. Valkenburg D.-J. Thomma B.P. Mesters J.R. Fungal effector ECP6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization.eLife. 2013; 2 (23840930): e0079010.7554/eLife.00790Crossref PubMed Scopus (141) Google Scholar). In a second strategy to interfere with activation of host immunity, pathogens secrete virulence proteins called effectors to inhibit critical regulatory components of host immune signaling (18Toruño T.Y. Stergiopoulos I. Coaker G. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners.Annu. Rev. Phytopathol. 2016; 54 (27359369): 419-44110.1146/annurev-phyto-080615-100204Crossref PubMed Google Scholar). Effectors from bacteria, fungi, and oomycetes have been shown to target similar hubs in the host immune signaling network (19Mukhtar M.S. Carvunis A.R. Dreze M. Epple P. Steinbrenner J. Moore J. Tasan M. Galli M. Hao T. Nishimura M.T. Pevzner S.J. Donovan S.E. Ghamsari L. Santhanam B. Romero V. et al.Independently evolved virulence effectors converge onto hubs in a plant immune system network.Science. 2011; 333 (21798943): 596-60110.1126/science.1203659Crossref PubMed Scopus (511) Google Scholar). The action of these effectors results in an attenuated immune response called effector-triggered susceptibility (20Chisholm S.T. Coaker G. Day B. Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response.Cell. 2006; 124 (16497589): 803-81410.1016/j.cell.2006.02.008Abstract Full Text Full Text PDF PubMed Scopus (1797) Google Scholar). To counter the threat of effector-triggered susceptibility, plants have evolved resistance proteins (R proteins) to detect pathogen effectors and initiate effector-triggered immunity (ETI; Fig. 1D) (21Kourelis J. van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.Plant Cell. 2018; 30 (29382771): 285-29910.1105/tpc.17.00579Crossref PubMed Scopus (173) Google Scholar). Some R proteins bind directly to the cognate effector, similar to direct binding of PAMP ligands by pattern recognition receptors. However, it is more common for R proteins to indirectly detect effectors by “guarding” immune hubs that effectors target (21Kourelis J. van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.Plant Cell. 2018; 30 (29382771): 285-29910.1105/tpc.17.00579Crossref PubMed Scopus (173) Google Scholar). By perceiving the virulence activities of effectors (e.g. proteolytic degradation of an immune signaling protein) rather than the effectors themselves, a single R protein can protect the plant from multiple pathogens that have converged to target the same protein complex (22Van Der Biezen E.A. Jones J.D. Plant disease-resistance proteins and the gene-for-gene concept.Trends Biochem. Sci. 1998; 23 (9868361): 454-45610.1016/S0968-0004(98)01311-5Abstract Full Text Full Text PDF PubMed Scopus (561) Google Scholar). ETI and PTI activate many of the same signaling pathways and defense responses. However, ETI is typically faster, its signaling is more resistant to pathogen interference, and the downstream responses are stronger than in PTI (10Katagiri F. Tsuda K. Understanding the plant immune system.Mol. Plant Microbe Interact. 2010; 23 (20653410): 1531-153610.1094/MPMI-04-10-0099Crossref PubMed Scopus (136) Google Scholar). Moreover, ETI is often distinguished from PTI by activation of programmed cell death at the site of infection, referred to as the hypersensitive response (HR). A recent study describes a novel role for iron in activation of ETI and will be discussed below (23Dangol S. Chen Y. Hwang B.K. Jwa N.-S. Iron-and reactive oxygen species-dependent ferroptotic cell death in rice-Magnaporthe oryzae interactions.Plant Cell. 2019; 31 (30563847): 189-20910.1105/tpc.18.00535Crossref PubMed Scopus (0) Google Scholar). Plant pathogens typically follow one of three lifestyles: biotrophic, hemibiotrophic, or necrotrophic (Fig. 1C). Biotrophic pathogens can only extract nutrients from living host cells (24McDowell J.M. Genomes of obligate plant pathogens reveal adaptations for obligate parasitism.Proc. Natl. Acad. Sci. U. S. A. 2011; 108 (21576481): 8921-892210.1073/pnas.1105802108Crossref PubMed Scopus (0) Google Scholar). Such pathogens are able to suppress host immunity, extract nutrients, and complete their life cycle without killing host cells. Contrastingly, necrotrophic pathogens kill host cells with toxins and complete their life cycle by feeding from dead or dying plant tissue (25Mengiste T. Plant immunity to necrotrophs.Annu. Rev. Phytopathol. 2012; 50 (22726121): 267-29410.1146/annurev-phyto-081211-172955Crossref PubMed Scopus (285) Google Scholar). Hemibiotrophic pathogens begin the infection cycle with an extended period of biotrophy before triggering a necrotrophic program. Plants deploy different immune responses against pathogens with these contrasting lifestyles, and plant hormones play key roles in coordinating the immune responses that are most efficient against pathogens with these contrasting lifestyles (26Spoel S.H. Dong X. Making sense of hormone crosstalk during plant immune responses.Cell Host Microbe. 2008; 3 (18541211): 348-35110.1016/j.chom.2008.05.009Abstract Full Text Full Text PDF PubMed Scopus (351) Google Scholar). For example, the phenolic phytohormone salicylic acid (SA) is typically produced in response to biotrophic pathogens and activates the hypersensitive response (27Mukhtar M.S. McCormack M.E. Argueso C.T. Pajerowska-Mukhtar K.M. Pathogen tactics to manipulate plant cell death.Curr. Biol. 2016; 26 (27404256): R608-R61910.1016/j.cub.2016.02.051Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 28Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.Annu. Rev. Phytopathol. 2005; 43 (16078883): 205-22710.1146/annurev.phyto.43.040204.135923Crossref PubMed Scopus (2511) Google Scholar). Contrastingly, immune responses against necrotrophs and herbivores do not involve cell death and are activated by the phytohormones jasmonic acid (JA) and ethylene (ET) (25Mengiste T. Plant immunity to necrotrophs.Annu. Rev. Phytopathol. 2012; 50 (22726121): 267-29410.1146/annurev-phyto-081211-172955Crossref PubMed Scopus (285) Google Scholar). The SA and JA/ET pathways antagonize each other to tailor the response to the invading pathogen, so that the plant utilizes its resources most efficiently (Fig. 1C) (26Spoel S.H. Dong X. Making sense of hormone crosstalk during plant immune responses.Cell Host Microbe. 2008; 3 (18541211): 348-35110.1016/j.chom.2008.05.009Abstract Full Text Full Text PDF PubMed Scopus (351) Google Scholar, 29Hillmer R.A. Tsuda K. Rallapalli G. Asai S. Truman W. Papke M.D. Sakakibara H. Jones J.D.G. Myers C.L. Katagiri F. The highly buffered Arabidopsis immune signaling network conceals the functions of its components.PLoS Genet. 2017; 13 (28472137): e100663910.1371/journal.pgen.1006639Crossref PubMed Scopus (54) Google Scholar). As a general rule, biotrophs are more vulnerable to ETI than are necrotrophs. This is because biotrophs depend on living plant cells for nutrients, whereas necrotrophs purposefully trigger host cell death. Indeed, some necrotrophs activate ETI as a virulence strategy (30Lorang J. Necrotrophic exploitation and subversion of plant defense: a lifestyle or just a phase, and implications in breeding resistance.Phytopathology. 2019; 109 (30451636): 332-34610.1094/PHYTO-09-18-0334-IACrossref PubMed Scopus (10) Google Scholar). These differing pathogen lifestyles hold important implications for predicting whether crop biofortification could impact disease resistance and will be discussed below. 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Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake.Nature. 2001; 409 (11201743): 346-34910.1038/35053080Crossref PubMed Scopus (0) Google Scholar). Strategy I plants also utilize small iron-binding compounds for acquisition, especially the phenolic coumarins (43Tsai H.-H. Schmidt W. Mobilization of iron by plant-borne coumarins.Trends Plant Sci. 2017; 22 (28385337): 538-54810.1016/j.tplants.2017.03.008Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar). The regulatory pathways that control activation of Strategy I uptake genes have been studied intensively and have been reviewed (44Gao F. Robe K. Gaymard F. Izquierdo E. Dubos C. The transcriptional control of iron homeostasis in plants: a tale of bHLH transcription factors?.Front. Plant Sci. 2019; 10 (30713541): 610.3389/fpls.2019.00006Crossref PubMed Scopus (47) Google Scholar). In the following paragraphs, we summarize pathways with connections to immune signaling or potential roles in iron biofortification. Basic helix-loop-helix (bHLH) transcription factors (TFs) play a key role in regulating iron homeostasis, characterized by heterodimerization between different clades of the bHLH superfamily. Activation of the Strategy I iron uptake response in the outer cells of the root is primarily regulated by the bHLH TF Fe deficiency–induced transcription factor (FIT) (45Bauer P. Ling H.-Q. Guerinot M.L. FIT, the ER-like iron deficiency induced transcription factor in Arabidopsis.Plant Physiol. Biochem. 2007; 45 (17466530): 260-26110.1016/j.plaphy.2007.03.006Crossref PubMed Scopus (0) Google Scholar). FIT heterodimerizes with clade Ib bHLHs, which facilitate FIT stability upon iron deficiency (46Cui Y. Chen C.-L. Cui M. Zhou W.-J. Wu H.-L. Ling H.-Q. Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis.Mol. Plant. 2018; 11 (29960107): 1166-118310.1016/j.molp.2018.06.005Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar). FIT then promotes transcription of iron mobilization genes, including ferric reduction oxidase 2 (FRO2), which encodes a protein for reduction of ferric iron in the rhizosphere, and iron-regulated transporter 1 (IRT1), which encodes a transporter that delivers reduced ferrous iron into the root epidermis (45Bauer P. Ling H.-Q. Guerinot M.L. FIT, the ER-like iron deficiency induced transcription factor in Arabidopsis.Plant Physiol. Biochem. 2007; 45 (17466530): 260-26110.1016/j.plaphy.2007.03.006Crossref PubMed Scopus (0) Google Scholar, 47Connolly E.L. Campbell N.H. Grotz N. Prichard C.L. Guerinot M.L. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control.Plant Physiol. 2003; 133 (14526117): 1102-111010.1104/pp.103.025122Crossref PubMed Scopus (282) Google Scholar) (Fig. 1A). Monocots utilize the Strategy II iron uptake mechanism, which occurs through extrusion of mugineic acid family phytosiderophores, such as deoxymugineic acid, via the transporter of mugineic acid 2 (TOM2) (48Nozoye T. Nagasaka S. Kobayashi T. Sato Y. Uozumi N. Nakanishi H. Nishizawa N.K. The phytosiderophore efflux transporter TOM2 is involved in metal transport in rice.J. Biol. Chem. 2015; 290 (26432636): 27688-2769910.1074/jbc.M114.635193Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar). Ferric-mugineic acid family phy-tosiderophore chelates are subsequently transported into the root via YSL transporters and reduced for utilization after uptake. Moreover, the response of rice and other monocots to iron deficiency differs from that of maize by utilizing aspects of both Strategy I and II for iron uptake (49Wairich A. de Oliveira B.H.N. Arend E.B. Duarte G.L. Ponte L.R. Sperotto