Advertisement

Long-Distance Signaling of Iron Deficiency in Plants

  • Yusuke Enomoto
  • Fumiyuki Goto
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 19)

Abstract

Iron is an essential nutrient used for many physiological reactions in a whole plant body. A large amount of iron exists in the Earth’s crust, but plants cannot uptake iron from roots efficiently because of the low iron solubility. The uptake and translocation of iron from roots to shoots are strictly controlled in order to maintain homeostasis of cytosol. It has been suggested that long-distance signaling from shoots to roots is involved in the regulation mechanisms of iron uptake. The identification of genes related to iron uptake was made possible because of the rapid development of molecular biology since the 1990s.

In this chapter, we describe the history of the discovery of the iron uptake genes and their regulation factors, and explain the interaction of these factors. Furthermore, we show some models of long-distance signaling which consistently explain the relationship between the phenotype of some mutants and the gene functions involved in iron uptake.

Keywords

Iron Nicotianamine Transporter Long-distance signal Iron deficiency 

Notes

Acknowledgment

We thank David Johnson for critical reading. We thank Springer for permission to use figures shown in Figs. 1 and 6.

References

  1. Arnaud N, Ravet K, Borlotti A, Touraine B, Boucherez J, Fizames C, Briat JF, Cellier F, Gaymard F (2007) The IRE/IRP1-cytosolic aconitase iron regulatory switch does not operate in plants. Biochem J 405:523–531PubMedCrossRefGoogle Scholar
  2. Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 281:32395–32402PubMedCrossRefGoogle Scholar
  3. Bienfait HF (1989) Prevention of stress in iron metabolism of plants. Acta Bot Neerl 38:105–129Google Scholar
  4. Brumbarova T, Bauer P (2005) Iron-mediated control of the basic helix-loop-helix protein FER, a regulator of uptake in tomato. Plant Physiol 137:1018–1026PubMedCrossRefGoogle Scholar
  5. Bughio N, Yamaguchi H, Nishizawa NK, Nakanishi H, Mori S (2002) Cloning an iron-regulated metal transporter from rice. J Exp Bot 53:1677–1682PubMedCrossRefGoogle Scholar
  6. Cassin G, Mari S, Curie C, Briat JF, Czernic P (2009) Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine. J Exp Bot 60:1249–1259PubMedCrossRefGoogle Scholar
  7. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Pant Physiol 154:810–819CrossRefGoogle Scholar
  8. Clemens S (2001) Molecular mechanism of plant metal tolerance and homeostasis. Planta 212:475–486PubMedCrossRefGoogle Scholar
  9. Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 12:3400–3412Google Scholar
  10. Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357PubMedCrossRefGoogle Scholar
  11. Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110PubMedCrossRefGoogle Scholar
  12. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033PubMedCrossRefGoogle Scholar
  13. Curie C, Briat JF (2003) Iron transport and signaling in plants. Plant Biol 54:183–206CrossRefGoogle Scholar
  14. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755PubMedCrossRefGoogle Scholar
  15. DiDonato RJ Jr, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine–metal complexes. Plant J 39:403–414PubMedCrossRefGoogle Scholar
  16. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205PubMedCrossRefGoogle Scholar
  17. Enomoto Y, Hodoshima H, Shimada H, Shoji K, Yoshihara T, Goto F (2007) Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta 227:81–89PubMedCrossRefGoogle Scholar
  18. Enomoto Y, Hashida S, Shoji K, Shimada H, Yoshihara T, Goto F (2009) Expressions of iron uptake genes in roots are affected by long-distance signals both in non-graminaceous and in graminaceous plants. In: IPNC XVI paper:1209Google Scholar
  19. Giehl RF, Lima JE, von Wirén N (2012) Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24:33–49PubMedCrossRefGoogle Scholar
  20. Green LS, Rogers EE (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiol 136:2523–2531PubMedCrossRefGoogle Scholar
  21. Grusak MA, Pezeshgi S (1996) Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol 110:329–334PubMedGoogle Scholar
  22. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613PubMedCrossRefGoogle Scholar
  23. Herbik A, Giritch A, Horstmann C, Becker R, Balzer HJ, Baumlein H, Stephan UW (1996) Iron and copper nutrition-dependent changes in protein expression in a tomato wild type and the nicotianamine-free mutant chloronerva. Plant Physiol 111:533–540PubMedCrossRefGoogle Scholar
  24. Hodoshima H, Enomoto Y, Shoji K, Shimada H, Goto F, Yoshihara T (2007) Differential regulation of cadmium-inducible expression of iron-deficiency-responsive genes in tobacco and barley. Physiol Plant 129:622–634CrossRefGoogle Scholar
  25. Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346PubMedCrossRefGoogle Scholar
  26. Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc Natl Acad Sci USA 104:7373–7378PubMedCrossRefGoogle Scholar
  27. Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577:528–534PubMedCrossRefGoogle Scholar
  28. Kakei Y, Ishimaru Y, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK (2012) OsYSL16 plays a role in the allocation of iron. Plant Mol Biol 79:583–594PubMedCrossRefGoogle Scholar
  29. Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271PubMedCrossRefGoogle Scholar
  30. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152PubMedCrossRefGoogle Scholar
  31. Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK (2003a) Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants. Plant J 36:780–793PubMedCrossRefGoogle Scholar
  32. Kobayashi T, Yoshihara T, Jiang T, Goto F, Nakanishi H, Mori S, Nishizawa NK (2003b) Combined deficiency of iron and other divalent cations mitigates the symptoms of iron deficiency in tobacco plants. Physiol Plant 119:400–408CrossRefGoogle Scholar
  33. Kobayashi T, Ogo Y, Itai RN, Nakanishi H, Takahashi M, Mori S, Nishizawa NK (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc Natl Acad Sci USA 104:19150–19155PubMedCrossRefGoogle Scholar
  34. Kobayashi T, Itai RN, Aung MS, Senoura T, Nakanishi H, Nishizawa NK (2012) The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. Plant J 69:81–91PubMedCrossRefGoogle Scholar
  35. Landsberg EC (1984) Regulation of iron-stress-response by whole-plant activity. J Plant Nutr 7:609–621CrossRefGoogle Scholar
  36. Lawson DM, Treffry A, Artymiuk PJ, Harrison PM, Yewdall SJ, Luzzago A, Cesareni G, Levi S, Arosio P (1989) Identification of the ferroxidase centre in ferritin. FEBS Lett 254:207–210PubMedCrossRefGoogle Scholar
  37. Le Jean M, Schikora A, Mari S, Briat JF, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J 44:769–782PubMedCrossRefGoogle Scholar
  38. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800PubMedCrossRefGoogle Scholar
  39. Li L, Cheng X, Ling HQ (2004) Isolation and characterization of Fe(III)-chelate reductase gene LeFRO1 in tomato. Plant Mol Biol 54:125–136PubMedCrossRefGoogle Scholar
  40. Ling HQ, Koch G, Baumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96:7098–7103PubMedCrossRefGoogle Scholar
  41. Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99:13938–13943PubMedCrossRefGoogle Scholar
  42. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22:2219–2236PubMedCrossRefGoogle Scholar
  43. Lynch SR (2011) Why nutritional iron deficiency persists as a worldwide problem. J Nutr 141:763S–768SPubMedCrossRefGoogle Scholar
  44. Maas FM, van de Wetering DA, van Beusichem ML, Bienfait HF (1988) Characterization of phloem iron and its possible role in the regulation of Fe-efficiency reactions. Plant Physiol 87:167–171PubMedCrossRefGoogle Scholar
  45. Mori S (1999) Iron acquisition by plants. Curr Opin Plant Biol 2:250–253PubMedCrossRefGoogle Scholar
  46. Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S (2000) Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Mol Biol 44:199–207PubMedCrossRefGoogle Scholar
  47. Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kikuchi S, Mori S, Nishizawa NK (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore Fe-deficient barley roots. Plant J 30:83–94PubMedCrossRefGoogle Scholar
  48. Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442PubMedCrossRefGoogle Scholar
  49. Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454PubMedCrossRefGoogle Scholar
  50. Ogo Y, Itai RN, Nakanishi H, Inoue H, Kobayashi T, Suzuki M, Takahashi M, Mori S, Nishizawa NK (2006) Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J Exp Bot 57:2867–2878PubMedCrossRefGoogle Scholar
  51. Ogo Y, Nakanishi Itai R, Nakanishi H, Kobayashi T, Takahashi M, Mori S, Nishizawa NK (2007) The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions. Plant J 51:366–377PubMedCrossRefGoogle Scholar
  52. Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Fe homeostasis in plant cells: does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration? Planta 213:967–976PubMedCrossRefGoogle Scholar
  53. Rellán-Álvarez R, Giner-Martínez-Sierra J, Orduna J, Orera I, Rodríguez-Castrillón JA, García-Alonso JI, Abadía J, Alvarez-Fernández A (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102PubMedCrossRefGoogle Scholar
  54. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697PubMedCrossRefGoogle Scholar
  55. Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799PubMedCrossRefGoogle Scholar
  56. Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180PubMedCrossRefGoogle Scholar
  57. Schaaf G, Schikora A, Haberle J, Vert G, Ludewig U, Briat JF, Curie C, von Wiren N (2005) A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774PubMedCrossRefGoogle Scholar
  58. Schikora A, Schmidt W (2001) Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiol 125:1679–1687PubMedCrossRefGoogle Scholar
  59. Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193PubMedCrossRefGoogle Scholar
  60. Schmidt W, Steinbach S (2000) Sensing iron—a whole plant approach. Ann Bot 86:589–593CrossRefGoogle Scholar
  61. Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118PubMedCrossRefGoogle Scholar
  62. Schuler M, Rellán-Álvarez R, Fink-Straube C, Abadía J, Bauer P (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in arabidopsis. Plant Cell 24:2380–2400PubMedCrossRefGoogle Scholar
  63. Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2007) The arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601PubMedCrossRefGoogle Scholar
  64. Staiger D (2002) Chemical strategies for iron acquisition in plants. Angew Chem Int Ed 41:2259–2264CrossRefGoogle Scholar
  65. Takagi S, Nomoto K, Takemoto T (1984) Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J Plant Nutr 7:469–477CrossRefGoogle Scholar
  66. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280PubMedCrossRefGoogle Scholar
  67. Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030–1043PubMedCrossRefGoogle Scholar
  68. Vasconcelos M, Musetti V, Li CM, Datta SK, Grusak MA (2004) Functional analysis of transgenic rice (Oryza sativa L.) transformed with an Arabidopsis thaliana ferric reductase (AtFRO2). Soil Sci Plant Nutr 50:1151–1157CrossRefGoogle Scholar
  69. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233PubMedCrossRefGoogle Scholar
  70. Vert GA, Briat JF, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804PubMedCrossRefGoogle Scholar
  71. von Wiren N, Khodr H, Hider RC (2000) Hydroxylated phytosiderophore species possess an enhanced chelate stability and affinity for iron(III). Plant Physiol 124:1149–1158CrossRefGoogle Scholar
  72. Wang HY, Klatte M, Jakoby M, Bäumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226:897–908PubMedCrossRefGoogle Scholar
  73. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147:1181–1191PubMedCrossRefGoogle Scholar
  74. Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94PubMedCrossRefGoogle Scholar
  75. White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080PubMedCrossRefGoogle Scholar
  76. Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol 46:1505–1514PubMedCrossRefGoogle Scholar
  77. Wu T, Zhang HT, Wang Y, Jia WS, Xu XF, Zhang XZ, Han ZH (2012) Induction of root Fe(III) reductase activity and proton extrusion by iron deficiency is mediated by auxin-based systemic signalling in Malus xiaojinensis. J Exp Bot 63:859–870PubMedCrossRefGoogle Scholar
  78. Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844PubMedCrossRefGoogle Scholar
  79. Yoshihara T, Kobayashi T, Goto F, Masuda T, Higuchi K, Nakanishi H, Nishizawa NK, Mori S (2003) Regulation of the iron-deficiency responsive gene, ids2, of barley in tobacco. Plant Biotechnol 20:33–41CrossRefGoogle Scholar
  80. Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F (2006) Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep 25:365–373PubMedCrossRefGoogle Scholar
  81. Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15:613–621PubMedCrossRefGoogle Scholar
  82. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Hiroo Gakuen Junior & Senior High SchoolTokyoJapan
  2. 2.Biotechnology SectorCentral Research Institute of Electric Power Industry (CRIEPI)Abiko-shiJapan

Personalised recommendations