1932

Abstract

Iron is an essential nutrient for most life on Earth because it functions as a crucial redox catalyst in many cellular processes. However, when present in excess iron can lead to the formation of harmful hydroxyl radicals. Hence, the cellular iron balance must be tightly controlled. Perturbation of iron homeostasis is a major strategy in host-pathogen interactions. Plants use iron-withholding strategies to reduce pathogen virulence or to locally increase iron levels to activate a toxic oxidative burst. Some plant pathogens counteract such defenses by secreting iron-scavenging siderophores that promote iron uptake and alleviate iron-regulated host immune responses. Mutualistic root microbiota can also influence plant disease via iron. They compete for iron with soil-borne pathogens or induce a systemic resistance that shares early signaling components with the root iron-uptake machinery. This review describes the progress in our understanding of the role of iron homeostasis in both pathogenic and beneficial plant-microbe interactions.

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2017-08-04
2024-04-19
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Literature Cited

  1. Ahmed E, Holmstrom SJ. 1.  2014. Siderophores in environmental research: roles and applications. Microb. Biotechnol. 7:196–208 [Google Scholar]
  2. Albarouki E, Schafferer L, Ye FH, von Wiren N, Haas H. 2.  et al. 2014. Biotrophy-specific downregulation of siderophore biosynthesis in Colletotrichum graminicola is required for modulation of immune responses of maize. Mol. Microbiol. 92:338–55 [Google Scholar]
  3. Aznar A, Chen NWG, Rigault M, Riache N, Joseph D. 3.  et al. 2014. Scavenging iron: a novel mechanism of plant immunity activation by microbial siderophores. Plant Physiol 164:2167–83 [Google Scholar]
  4. Aznar A, Chen NWG, Thomine S, Dellagi A. 4.  2015. Immunity to plant pathogens and iron homeostasis. Plant Sci 240:90–97 [Google Scholar]
  5. Aznar A, Patrit O, Berger A, Dellagi A. 5.  2015. Alterations of iron distribution in Arabidopsis tissues infected by Dickeya dadantii. . Mol. Plant Pathol. 16:521–28 [Google Scholar]
  6. Barash I, Zion R, Krikun J, Nachmias A. 6.  1988. Effect of iron status on Verticillium wilt disease and on in vitro production of siderophores by Verticillium dahliae. . J. Plant Nutr. 11:893–905 [Google Scholar]
  7. Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C. 7.  et al. 2011. Monoubiquitin-dependent endocytosis of the IRON-REGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants. PNAS 108:E450–58 [Google Scholar]
  8. Bashir K, Nishizawa NK. 8.  2006. Deoxymugineic acid synthase. Plant Signal. Behav. 1:290–92 [Google Scholar]
  9. Berendsen RL, Van Verk MC, Stringlis IA, Zamioudis C, Tommassen J. 9.  et al. 2015. Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genom 16:539 [Google Scholar]
  10. Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J. 10.  et al. 2010. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann. Bot. 105:811–22 [Google Scholar]
  11. Carvalhais LC, Dennis PG, Badri DV, Tyson GW, Vivanco JM, Schenk PM. 11.  2013. Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLOS ONE 8:e56457 [Google Scholar]
  12. Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wiren N. 12.  2011. Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J. Plant Nutr. Soil Sci. 174:3–11 [Google Scholar]
  13. Cassat JE, Skaar EP. 13.  2013. Iron in infection and immunity. Cell Host Microbe 13:509–19 [Google Scholar]
  14. Chapelle E, Mendes R, Bakker PAHM, Raaijmakers JM. 14.  2016. Fungal invasion of the rhizosphere microbiome. ISME J 10:265–68 [Google Scholar]
  15. Chen LM, Dick WA, Streeter JG, Hoitink HAJ. 15.  1998. Fe chelates from compost microorganisms improve Fe nutrition of soybean and oat. Plant Soil 200:139–47 [Google Scholar]
  16. Colangelo EP, Guerinot ML. 16.  2004. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–12 [Google Scholar]
  17. Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML. 17.  2003. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–10 [Google Scholar]
  18. Cornelis P. 18.  2010. Iron uptake and metabolism in pseudomonads. Appl. Microbiol. Biotechnol. 86:1637–45 [Google Scholar]
  19. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat J-F. 19.  2000. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. 347:749–55 [Google Scholar]
  20. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat J-F, Walker EL. 20.  2001. Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake. Nature 409:346–49 [Google Scholar]
  21. Darbani B, Briat JF, Holm PB, Husted S, Noeparvar S, Borg S. 21.  2013. Dissecting plant iron homeostasis under short and long-term iron fluctuations. Biotechnol. Adv. 31:1292–307 [Google Scholar]
  22. Deák M, Horváth GV, Davletova S, Török K, Sass L. 22.  et al. 1999. Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat. Biotechnol. 17:192–96 [Google Scholar]
  23. Dellagi A, Brisset M, Paulin J, Expert D. 23.  1998. Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol. Plant-Microbe Interact. 11:734–42 [Google Scholar]
  24. Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y. 24.  et al. 2005. Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J. 43:262–72 [Google Scholar]
  25. Dellagi A, Segond D, Rigault M, Fagard M, Simon C. 25.  et al. 2009. Microbial siderophores exert a subtle role in Arabidopsis during infection by manipulating the immune response and the iron status. Plant Physiol 150:1687–96 [Google Scholar]
  26. De Vleesschauwer D, Djavaheri M, Bakker PAHM, Höfte M. 26.  2008. Pseudomonas fluorescens WCS374r–induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid–repressible multifaceted defense response. Plant Physiol. 148:1996–2012 [Google Scholar]
  27. DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL. 27.  2004. Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J. 39:403–14 [Google Scholar]
  28. Dinneny JR, Long TA, Wang JY, Jung JW, Mace D. 28.  et al. 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320:942–45 [Google Scholar]
  29. Dixon RA. 29.  2001. Natural products and plant disease resistance. Nature 411:843–47 [Google Scholar]
  30. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 30.  2010. MYB transcription factors in Arabidopsis. . Trends Plant Sci. 15:573–81 [Google Scholar]
  31. Duijff B, De Kogel W, Bakker PAHM, Schippers B. 31.  1994. Influence of pseudobactin 358 on the iron nutrition of barley. Soil Biol. Biochem. 26:1681–88 [Google Scholar]
  32. Dutton MV, Evans CS. 32.  1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 42:881–95 [Google Scholar]
  33. Eichhorn H, Lessing F, Winterberg B, Schirawski J, Kämper J. 33.  et al. 2006. A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. . Plant Cell 18:3332–45 [Google Scholar]
  34. Eide D, Broderius M, Fett J, Guerinot ML. 34.  1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. PNAS 93:5624–28 [Google Scholar]
  35. El Oirdi M, Trapani A, Bouarab K. 35.  2010. The nature of tobacco resistance against Botrytis cinerea depends on the infection structures of the pathogen. Environ. Microbiol. 12:239–53 [Google Scholar]
  36. Escolar L, Pérez-Martín J, De Lorenzo V. 36.  1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223–29 [Google Scholar]
  37. Expert D, Enard C, Masclaux C. 37.  1996. The role of iron in plant host-pathogen interactions. Trends Microbiol 4:232–37 [Google Scholar]
  38. Fenton H. 38.  1894. Oxidation of tartaric acid in presence of iron. J. Chem. Soc. Trans. 65:899–910 [Google Scholar]
  39. Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G. 39.  et al. 2014. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–67 [Google Scholar]
  40. Fourcroy P, Tissot N, Gaymard F, Briat JF, Dubos C. 40.  2016. Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe2+ transport system. Mol. Plant 9:485–88 [Google Scholar]
  41. Franza T, Expert D. 41.  2013. Role of iron homeostasis in the virulence of phytopathogenic bacteria: an “à la carte” menu. Mol. Plant Pathol. 14:429–38 [Google Scholar]
  42. Franza T, Mahé B, Expert D. 42.  2005. Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55:261–75 [Google Scholar]
  43. Ganz T, Nemeth E. 43.  2015. Iron homeostasis in host defence and inflammation. Nat. Rev. Immunol. 15:500–10 [Google Scholar]
  44. García MJ, Lucena C, Romera FJ, Alcántara E, Pérez-Vicente R. 44.  2010. Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. . J. Exp. Bot. 61:3885–99 [Google Scholar]
  45. Giehl FH, Lima JE, Von Wiren N. 45.  2012. Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24:33–49 [Google Scholar]
  46. Guerinot ML, Ying Y. 46.  1994. Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–20 [Google Scholar]
  47. Haas H, Eisendle M, Turgeon BG. 47.  2008. Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46:149–87 [Google Scholar]
  48. Haber F, Weiss J. 48.  1934. The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. Lond. Ser. A 147:332–51 [Google Scholar]
  49. Hacquard S, Kracher B, Hiruma K, Münch PC, Garrido-Oter R. 49.  et al. 2016. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun. 7:11362 [Google Scholar]
  50. Haney CH, Samuel BS, Bush J, Ausubel FM. 50.  2015. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat. Plants 1:15051 [Google Scholar]
  51. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 51.  2004. Trichoderma species—opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43–56 [Google Scholar]
  52. Hider RC, Kong X. 52.  2010. Chemistry and biology of siderophores. Nat. Product Rep. 27:637 [Google Scholar]
  53. Hindt MN, Guerinot ML. 53.  2012. Getting a sense for signals: regulation of the plant iron deficiency response. Biochim. Biophys. Acta 1823:1521–30 [Google Scholar]
  54. Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S. 54.  et al. 2016. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–74 [Google Scholar]
  55. Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y. 55.  et al. 2009. Rice OsYSL15 is an iron-regulated iron(III)–deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J. Biol. Chem. 284:3470–79 [Google Scholar]
  56. Ipcho S, Sundelin T, Erbs G, Kistler HC, Newman M-A, Olsson S. 56.  2016. Fungal innate immunity induced by bacterial microbe-associated molecular patterns (MAMPs). Genes Genomes Genet 6:1585–95 [Google Scholar]
  57. Ivanov R, Brumbarova T, Bauer P. 57.  2012. Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Mol. Plant 5:27–42 [Google Scholar]
  58. Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P. 58.  2004. FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. . FEBS Lett. 577:528–34 [Google Scholar]
  59. Jin CW, Chen WW, Meng ZB, Zheng SJ. 59.  2008. Iron deficiency–induced increase of root branching contributes to the enhanced root ferric chelate reductase activity. J. Integr. Plant Biol. 50:1557–62 [Google Scholar]
  60. Jin CW, Li GX, Yu XH, Zheng SJ. 60.  2010. Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Ann. Bot. 105:835–41 [Google Scholar]
  61. Kai K, Shimizu B, Mizutani M, Watanabe K, Sakata K. 61.  2006. Accumulation of coumarins in Arabidopsis thaliana. . Phytochemistry 67:379–86 [Google Scholar]
  62. Kieu NP, Aznar A, Segond D, Rigault M, Simond-Côte E. 62.  et al. 2012. Iron deficiency affects plant defence responses and confers resistance to Dickeya dadantii and Botrytis cinerea. . Mol. Plant Pathol. 13:816–27 [Google Scholar]
  63. Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R. 63.  et al. 2009. The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–71 [Google Scholar]
  64. Kloepper JW, Leong J, Teintze M, Schroth MN. 64.  1980. Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr. Microbiol. 4:317–20 [Google Scholar]
  65. Kobayashi T, Nishizawa NK. 65.  2012. Iron uptake, translocation, and regulation in higher plants. Annu. Rev. Plant Biol. 63:131–52 [Google Scholar]
  66. Koen E, Besson-Bard A, Duc C, Astier J, Gravot A. 66.  et al. 2013. Arabidopsis thaliana nicotianamine synthase 4 is required for proper response to iron deficiency and to cadmium exposure. Plant Sci 209:1–11 [Google Scholar]
  67. Kontoghiorghes GJ, Kolnagou A, Skiada A, Petrikkos G. 67.  2010. The role of iron and chelators on infections in iron overload and non iron loaded conditions: prospects for the design of new antimicrobial therapies. Hemoglobin 34:227–39 [Google Scholar]
  68. Krikun J, Frank ZR. 68.  1975. Effect of sequestrene on the reaction to Verticillium dahliae of peanuts growing in calcareous loess soil. Phytoparasitica 3:77–78 [Google Scholar]
  69. Lakshmanan V, Kitto SL, Caplan JL, Hsueh Y-H, Kearns DB. 69.  et al. 2012. Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. . Plant Physiol. 160:1642–61 [Google Scholar]
  70. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML. 70.  2002. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. . PNAS 99:7072–77 [Google Scholar]
  71. Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C. 71.  et al. 2005. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–51 [Google Scholar]
  72. Lareen A, Burton F, Schäfer P. 72.  2016. Plant root-microbe communication in shaping root microbiomes. Plant Mol. Biol. 90:575–87 [Google Scholar]
  73. Laulhere JP, Briat JF. 73.  1993. Iron release and uptake by plant ferritin: effects of pH, reduction and chelation. Biochem. J. 290:693–99 [Google Scholar]
  74. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J. 74.  et al. 2015. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–64 [Google Scholar]
  75. Leeman M, den Ouden FM, Van Pelt JA, Dirkx FPM, Steijl H. 75.  et al. 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. . Phytopathology 86:149–55 [Google Scholar]
  76. Lemanceau P, Alabouvette C, Couteaudier Y. 76.  1988. Studies on the disease suppressiveness of soils. XIV. Modification of the receptivity level of a suppressive and a conducive soil to fusarium-wilt in response to the supply of iron or of glucose. Agronomie 8:155–62 [Google Scholar]
  77. Lemanceau P, Expert D, Gaymard F, Bakker P, Briat J-F. 77.  2009. Role of iron in plant-microbe interactions. Adv. Bot. Res. 51:491–549 [Google Scholar]
  78. Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y. 78.  2007. Targeted alterations in iron homeostasis underlie plant defense responses. J. Cell Sci. 120:596–605 [Google Scholar]
  79. Liu J, Osbourn A, Ma P. 79.  2015. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8:689–708 [Google Scholar]
  80. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN. 80.  2010. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22:2219–36 [Google Scholar]
  81. Loper JE, Buyer JS. 81.  1991. Siderophores in microbial interactions on plant surfaces. Mol. Plant-Microbe Interact. 4:5–13 [Google Scholar]
  82. López-Berges MS, Capilla J, Turrà D, Schafferer L, Matthijs S. 82.  et al. 2012. HapX-mediated iron homeostasis is essential for rhizosphere competence and virulence of the soilborne pathogen Fusarium oxysporum. Plant Cell 24:3805–22 [Google Scholar]
  83. Lugtenberg B, Kamilova F. 83.  2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–56 [Google Scholar]
  84. Luo Y, Han Z, Chin SM, Linn S. 84.  1994. Three chemically distinct types of oxidants formed by iron-mediated Fenton reactions in the presence of DNA. PNAS 91:12438–42 [Google Scholar]
  85. Macur RE, Mathre DE, Olsen RA. 85.  1991. Interactions between iron nutrition and Verticillium wilt resistance in tomato. Plant Soil 134:281–86 [Google Scholar]
  86. Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ. 86.  et al. 2016. Recognizing plant defense priming. Trends Plant Sci 21:818–22 [Google Scholar]
  87. Maurer F, Müller S, Bauer P. 87.  2011. Suppression of Fe deficiency gene expression by jasmonate. Plant Physiol. Biochem. 49:530–36 [Google Scholar]
  88. Mei B, Buddet AD, Leong SA. 88.  1993. sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. PNAS 90:903–7 [Google Scholar]
  89. Meiser J, Lingam S, Bauer P. 89.  2011. Posttranslational regulation of the iron deficiency basic helix-loop-helix transcription factor FIT is affected by iron and nitric oxide. Plant Physiol 157:2154–66 [Google Scholar]
  90. Meziane H, Van der Sluis I, Van Loon LC, Höfte M, Bakker PAHM. 90.  2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177–85 [Google Scholar]
  91. Miethke M, Marahiel MA. 91.  2007. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71:413–51 [Google Scholar]
  92. Morant AV, Jorgensen K, Jorgensen C, Paquette SM, Sanchez-Perez R. 92.  et al. 2008. β-Glucosidases as detonators of plant chemical defense. Phytochemistry 69:1795–813 [Google Scholar]
  93. Nouet C, Motte P, Hanikenne M. 93.  2011. Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16:395–404 [Google Scholar]
  94. Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y. 94.  et al. 2011. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286:5446–54 [Google Scholar]
  95. Ohata T, Kanazawa K, Mihashi S, Kishi-Nishizawa N, Fushiya S. 95.  et al. 1993. Biosynthetic pathway of phytosiderophores in iron-deficient graminaceous plants. Soil Sci. Plant Nutr. 39:745–49 [Google Scholar]
  96. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H. 96.  et al. 2006. NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836–53 [Google Scholar]
  97. Ong ST, Ho JZS, Ho B, Ding JL. 97.  2006. Iron-withholding strategy in innate immunity. Immunobiology 211:295–314 [Google Scholar]
  98. Palmer CM, Guerinot ML. 98.  2009. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat. Chem. Biol. 5:333–40 [Google Scholar]
  99. Palmer CM, Hindt MN, Schmidt H, Clemens S, Guerinot ML. 99.  2013. MYB10 and MYB72 are required for growth under iron-limiting conditions. PLOS Genet. 9:e1003953 [Google Scholar]
  100. Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C. 100.  et al. 2004. Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol. Plant. 122:465–77 [Google Scholar]
  101. Pieterse CMJ, De Jonge R, Berendsen RL. 101.  2016. The soil-borne supremacy. Trends Plant Sci 21:171–73 [Google Scholar]
  102. Pieterse CMJ, Van der Does, Zamioudis C, Leon-Reyes A, Van Wees SCM. 102.  2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489–521 [Google Scholar]
  103. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R. 103.  et al. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–80 [Google Scholar]
  104. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. 104.  2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347–75 [Google Scholar]
  105. Pozo MJ, Van der Ent S, Van Loon L, Pieterse CMJ. 105.  2008. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria‐induced systemic resistance in Arabidopsis thaliana. . New Phytol. 180:511–23 [Google Scholar]
  106. Radzki W, Gutierrez Mañero FJ, Algar E, Lucas García JA, García-Villaraco A, Ramos Solano B. 106.  2013. Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek 104:321–30 [Google Scholar]
  107. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 107.  1999. A ferric-chelate reductase for iron uptake from soils. Nature 397:694–97 [Google Scholar]
  108. Rodríguez-Celma J, Lin WD, Fu GM, Abadía J, Lopez-Millán AF, Schmidt W. 108.  2013. Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. . Plant Physiol. 162:1473–85 [Google Scholar]
  109. Romera FJ, Alcántara E, De La Guardia MD. 109.  1999. Ethylene production by Fe-deficient roots and its involvement in the regulation of Fe-deficiency stress responses by Strategy I plants. Ann. Bot. 83:51–55 [Google Scholar]
  110. Romera FJ, García MJ, Alcántara E, Pérez-Vicente R. 110.  2011. Latest findings about the interplay of auxin, ethylene and nitric oxide in the regulation of Fe deficiency responses by Strategy I plants. Plant Signal. Behav. 6:167–70 [Google Scholar]
  111. Römheld V. 111.  1987. Different strategies for iron acquisition in higher plants. Physiol. Plant. 70:231–34 [Google Scholar]
  112. Rudrappa T, Czymmek KJ, Paré PW, Bais HP. 112.  2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–56 [Google Scholar]
  113. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW. 113.  2004. Bacterial volatiles induce systemic resistance in Arabidopsis. . Plant Physiol. 134:1017–26 [Google Scholar]
  114. Santi S, Schmidt W. 114.  2009. Dissecting iron deficiency–induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–84 [Google Scholar]
  115. Schagerlöf U, Wilson G, Hebert H, Al-Karadaghi S, Hägerhäll C. 115.  2006. Transmembrane topology of FRO2, a ferric chelate reductase from Arabidopsis thaliana. . Plant Mol. Biol. 62:215–21 [Google Scholar]
  116. Schippers B, Bakker AW, Bakker PAHM. 116.  1987. Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Annu. Rev. Phytopathol. 25:339–58 [Google Scholar]
  117. Schmid NB, Giehl RF, Döll S, Mock H-P, Strehmel N. 117.  et al. 2014. Feruloyl-CoA 6′-hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. . Plant Physiol. 164:160–72 [Google Scholar]
  118. Schmidt H, Gunther C, Weber M, Sporlein C, Loscher S. 118.  et al. 2014. Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLOS ONE 9:e102444 [Google Scholar]
  119. Schmidt W. 119.  1999. Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141:1–26 [Google Scholar]
  120. Segarra G, Van der Ent S, Trillas I, Pieterse CMJ. 120.  2009. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11:90–96 [Google Scholar]
  121. Segond D, Dellagi A, Lanquar V, Rigault M, Patrit O. 121.  et al. 2009. NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J. 58:195–207 [Google Scholar]
  122. Séguéla M, Briat JF, Vert G, Curie C. 122.  2008. Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth‐dependent pathway. Plant J 55:289–300 [Google Scholar]
  123. Selote D, Samira R, Matthiadis A, Gillikin JW, Long TA. 123.  2015. Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol 167:273–86 [Google Scholar]
  124. Shen C, Yang Y, Liu K, Zhang L, Guo H. 124.  et al. 2016. Involvement of endogenous salicylic acid in iron-deficiency responses in Arabidopsis. . J. Exp. Bot. 67:4179–93 [Google Scholar]
  125. Shimizu B, Fujimori A, Miyagawa H, Ueno T, Watanabe K, Ogawa K. 125.  2000. Resistance against Fusarium wilt induced by non-pathogenic Fusarium. Ipomoea tricolor. J. Pestic. Sci. 25:365–72 [Google Scholar]
  126. Sivitz A, Grinvalds C, Barberon M, Curie C, Vert G. 126.  2011. Proteasome-mediated turnover of the transcriptional activator FIT is required for plant iron-deficiency responses. Plant J 66:1044–52 [Google Scholar]
  127. Sivitz AB, Hermand V, Curie C, Vert G. 127.  2012. Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLOS ONE 7:e44843 [Google Scholar]
  128. Skaar EP. 128.  2010. The battle for iron between bacterial pathogens and their vertebrate hosts. PLOS Pathog 6:e1000949 [Google Scholar]
  129. Sun H, Wang L, Zhang B, Ma J, Hettenhausen C. 129.  et al. 2014. Scopoletin is a phytoalexin against Alternaria alternata in wild tobacco dependent on jasmonate signalling. J. Exp. Bot. 65:4305–15 [Google Scholar]
  130. Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 130.  2010. The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J. Bacteriol. 192:117–26 [Google Scholar]
  131. Theil EC. 131.  1987. Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu. Rev. Biochem. 56:289–315 [Google Scholar]
  132. Trapet P, Avoscan L, Klinguer A, Pateyron S, Citerne S. 132.  et al. 2016. The Pseudomonas fluorescens siderophore pyoverdine weakens. Arabidopsis thaliana defense in favor of growth in iron-deficient conditions. Plant Physiol. 171:675–93 [Google Scholar]
  133. Troxell B, Hassan HM. 133.  2013. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front. Cell. Infect. Microbiol. 3:59 [Google Scholar]
  134. Van de Mortel JE, De Vos RCH, Dekkers E, Pineda A, Guillod L. 134.  et al. 2012. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160:2173–88 [Google Scholar]
  135. Van der Ent S, Van Wees SCM, Pieterse CMJ. 135.  2009. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–88 [Google Scholar]
  136. Van der Ent S, Verhagen BW, Van Doorn R, Bakker D, Verlaan MG. 136.  et al. 2008. MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol. 146:1293–304 [Google Scholar]
  137. Vansuyt G, Robin A, Briat JF, Curie C, Lemanceau P. 137.  2007. Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. . Mol. Plant-Microbe Interact. 20:441–47 [Google Scholar]
  138. Verbon EH, Liberman LM. 138.  2016. Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci 21:218–29 [Google Scholar]
  139. Verhagen BW, Glazebrook J, Zhu T, Chang HS, van Loon LC, Pieterse CM. 139.  2004. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895–908 [Google Scholar]
  140. Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML. 140.  et al. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–33 [Google Scholar]
  141. Vert GA, Briat JF, Curie C. 141.  2003. Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804 [Google Scholar]
  142. Vogt T. 142.  2010. Phenylpropanoid biosynthesis. Mol. Plant 3:2–20 [Google Scholar]
  143. Walker EL, Connolly EL. 143.  2008. Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Curr. Opin. Plant Biol. 11:530–35 [Google Scholar]
  144. Wang N, Cui Y, Liu Y, Fan H, Du J. 144.  et al. 2013. Requirement and functional redundancy of lb subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. . Mol. Plant 6:503–13 [Google Scholar]
  145. Weinberg ED, Weinberg GA. 145.  1995. The role of iron in infection. Curr. Opin. Infect. Dis. 8:164–69 [Google Scholar]
  146. Weller D, Raaijmakers JM, McSpadden Gardener B, Thomashow L. 146.  2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309–48 [Google Scholar]
  147. Wild M, Davière J-M, Regnault T, Sakvarelidze-Achard L, Carrera E. 147.  et al. 2016. Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses. Dev. Cell 37:190–200 [Google Scholar]
  148. Yang CH, Crowley DE. 148.  2000. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl. Environ. Microbiol. 66:345–51 [Google Scholar]
  149. Ye F, Albarouki E, Lingam B, Deising HB, von Wirén N. 149.  2014. An adequate Fe nutritional status of maize suppresses infection and biotrophic growth of Colletotrichum graminicola. . Physiol. Plant. 151:280–92 [Google Scholar]
  150. Yehuda Z, Shenker M, Hadar Y, Chen YN. 150.  2000. Remedy of chlorosis induced by iron deficiency in plants with the fungal siderophore rhizoferrin. J. Plant Nutr. 23:1991–2006 [Google Scholar]
  151. Yuan Y, Wu H, Wang N, Li J, Zhao W. 151.  et al. 2008. FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. . Cell Res. 18:385–97 [Google Scholar]
  152. Yuan YX, Zhang J, Wang DW, Ling HQ. 152.  2005. AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in Strategy I plants. Cell Res. 15:613–21 [Google Scholar]
  153. Zamioudis C, Hanson J, Pieterse CMJ. 153.  2014. β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol 204:368–79 [Google Scholar]
  154. Zamioudis C, Korteland J, Van Pelt JA, Van Hamersveld M, Dombrowski N. 154.  et al. 2015. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J. 84:309–22 [Google Scholar]
  155. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ. 155.  2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–18 [Google Scholar]
  156. Zhang HM, Sun Y, Xie XT, Kim MS, Dowd SE, Pare PW. 156.  2009. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–77 [Google Scholar]
  157. Zhou C, Guo J, Zhu L, Xiao X, Xie Y. 157.  et al. 2016. Paenibacillus polymyxa BFKC01 enhances plant iron absorption via improved root systems and activated iron acquisition mechanisms. Plant Physiol. Biochem. 105:162–73 [Google Scholar]
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