Skip to main content

Advertisement

Springer Nature Link
Log in

Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Iron is an essential element for plants and microbes. However, in most cultivated soils, the concentration of iron available for these living organisms is very low because its solubility is controlled by stable hydroxides, oxyhydroxides and oxides. In the rhizosphere, there is a high demand of iron because of the iron uptake by plants, and microorganisms which density and activity are promoted by the release of root exudates. Plants and microbes have evolved active strategies of iron uptake. Iron incorporation by these organisms lead to complex interactions ranging from competition to mutualism. These complex interactions are under the control of physico-chemical properties of the soils in which they occur, and reciprocally iron uptake strategies of plants and microbes impact these soil properties. These iron-mediated interactions between soils, plants and microbes impact the plant growth and health and their analysis, together with that of the resulting iron dynamics, is of a major agronomic interest. Analysis of the complex interactions soils, plants and microbes represent also a unique opportunity to progress in our knowledge of the rhizosphere ecology. This progression requires merging complementary expertises and study strategies in soil science, plant biology and microbiology. This review provides information on (i) iron status in soil and rhizosphere, iron uptake by plants and microbes, and on (ii) the corresponding study strategies. Finally, illustrations of how integration of these approaches allows gaining knowledge in the complex interactions occurring in the rhizosphere are given.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Bakker PAHM, Lamers JG, Bakker AW, Marugg JD, Weisbeek PJ, Schippers B (1986) The role of siderophores in potato tuber yield increase by Pseudomonas putida in a short rotation of potato. Neth J Plant Pathol 92:249–256. doi:10.1007/BF01977588

    Google Scholar 

  • Bakker PAHM, Bakker AW, Marugg JD, Weisbeek PJ, Schippers B (1987) Bioassay for studying the role of siderophores in potato growth stimulation by Pseudomonas spp. in short potato rotations. Soil Biol Biochem 4:443–449. doi:10.1016/0038-0717(87)90036-8

    Google Scholar 

  • 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 281:32395–32402. doi:10.1074/jbc.M604133200

    PubMed  CAS  Google Scholar 

  • Bauer P, Thiel T, Klatte M, Bereczky Z, Brumbarova T, Hell R, Grosse I (2004) Analysis of sequence, map position, and gene expression reveals conserved essential genes for iron uptake in Arabidopsis and tomato. Plant Physiol 136:4169–4183. doi:10.1104/pp.104.047233

    PubMed  CAS  Google Scholar 

  • Becker JO, Cook RJ (1988) Role of siderophores in suppression of Pythium species and production of increased-growth response of wheat by fluorescent pseudomonads. Phytopathology 78:778–782. doi:10.1094/Phyto-78-778

    CAS  Google Scholar 

  • Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P (2003) Differential regulation of Nramp and irt metal transporter genes in wild type and iron uptake mutants of tomato. J Biol Chem 278:24697–24704. doi:10.1074/jbc.M301365200

    PubMed  CAS  Google Scholar 

  • Blume H-P, Bruemmer GW, Schwertmann U, Horn R, Koegel-Knabner I, Stahr K, Auerswald K, Beyer L, Hartmann A, Litz N, Scheinost A, Stanjek H et al (2002) Shaffer/Schachtschabel/Lehrbuch der Bodenkunde, 15th edn. Heidelberg, Spektrum Akademischer Verlag

    Google Scholar 

  • Borggaard OK (1988) Phase identification by selective dissolution techniques. In: Stucki JW, Goodman BA, Schwertmann U (eds) Iron in soils and clay minerals. D Reidel, Dordrecht, pp 83–97

    Google Scholar 

  • Bossier P, Höfte M, Verstraete W (1988) Ecological significance of siderophores in soil. Adv Microb Ecol 10:384–414

    Google Scholar 

  • Bossis E, Lemanceau P, Latour X, Gardan L (2000) Taxonomy of Pseudomonas fluorescens and Pseudomonas putida: current status and need for revision. Agronomie 20:51–63. doi:10.1051/agro:2000112

    Google Scholar 

  • Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339. doi:10.1023/A:1020218608266

    PubMed  CAS  Google Scholar 

  • Briat JF, Gaymard F (2007) Iron nutrition and interactions in plants—Preface. Plant Physiol Biochem 45:259. doi:10.1016/j.plaphy.2007.03.005

    CAS  Google Scholar 

  • Brown AL, Yamaguchi S, Leal-Diaz J (1965) Evidence for translocation of iron in plants. Plant Physiol 40:35–38. doi:10.1104/pp.40.1.35

    PubMed  CAS  Google Scholar 

  • Brumbarova T, Bauer P (2005) Iron-mediated control of the basic helix-loop-helix protein FER, a regulator of iron uptake in tomato. Plant Physiol 137:1018–1026. doi:10.1104/pp. 104.054270

    PubMed  CAS  Google Scholar 

  • Budzikiewicz H (1997) Siderophores of fluorescent pseudomonads. Z Naturforsch 52c:713–720

    Google Scholar 

  • Budzikiewicz H (2004) Siderophores of the Pseudomonadaceae sensu stricto (fluorescent and non fluorescent Pseudomonas spp.). In: Herz W, Falk H, Kirby GW (eds) Progress in the chemistry of organic natural products. Vienna, Springer, pp 81–237

    Google Scholar 

  • Buyer JS, Sikora LJ, Kratzke MG (1990) Monoclonal antibodies to ferric pseudobactin, the siderophore of plant growth-promoting Pseudomonas putida B10. Appl Environ Microbiol 56:419–424

    PubMed  CAS  Google Scholar 

  • Buysens S, Heungens K, Poppe J, Höfte M (1996) Involvement of pyochelin and pyoverdin in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 62:865–871

    PubMed  CAS  Google Scholar 

  • Carrasco N, Kretzschmar R, Pesch ML, Kraemer SM (2008) Effects of anionic surfactants on ligand-promoted dissolution of iron and aluminum hydroxides. J Colloid Interface Sci 321:279–287. doi:10.1016/j.jcis.2008.02.011

    PubMed  CAS  Google Scholar 

  • Chaney RL, Brown JC, Tiffin LO (1972) Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol 50:208–213. doi:10.1104/pp.50.2.208

    PubMed  CAS  Google Scholar 

  • Chao TT, Zhou L (1983) Extraction techniques for selective dissolution of amorphous iron-oxides from soils and sediments. Soil Sci Soc Am J 47:225–232

    CAS  Google Scholar 

  • Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072. doi:10.1104/pp.116.3.1063

    PubMed  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412. doi:10.1105/tpc.104.024315

    PubMed  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330. doi:10.1016/j.pbi.2006.03.015

    PubMed  CAS  Google Scholar 

  • 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 14:1347–1357. doi:10.1105/tpc.001263

    PubMed  CAS  Google Scholar 

  • 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 133:1102–1110. doi:10.1104/pp.103.025122

    PubMed  CAS  Google Scholar 

  • Cornelis P, Matthijs S (2007) Pseudomonas siderophores and their biological significance. In: Varma A, Chincholkar S (eds) Microbial siderophores. Springer-Verlag, Berlin Heildeberg, pp 193–203

    Google Scholar 

  • Cornelis P, Hohnadel D, Meyer JM (1989) Evidence for different pyoverdine-mediated iron uptake systems among Pseudomonas aeruginosa strains. Infect Immun 57:3491–3497

    PubMed  CAS  Google Scholar 

  • Cornelis P, Baysse C, Matthijs S (2008) Iron uptake in Pseudomonas. In: Cornelis P (ed) Pseudomonas, genomics and molecular biology. Caister Academic, Norfolk, pp 213–235

    Google Scholar 

  • Cornell RM, Schwertmann U (2003) The iron oxides, 2nd edn. Wiley–VCH, Weinheim

    Google Scholar 

  • Crowley DE, Gries D (1994) Modelling of iron availability in the plant rhizosphere. In: Manthey JA, Crowley DE, Luster DG (eds) Biochemistry of metal micronutrients in the rhizosphere. CRC, Boca Raton, Florida, pp 199–220

    Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349. doi:10.1038/35053080

    PubMed  CAS  Google Scholar 

  • Darrah PR (1991) Models of the rhizosphere. I. Microbial population dynamics around a root releasing soluble and insoluble carbon. Plant Soil 133:187–199. doi:10.1007/BF00009191

    CAS  Google Scholar 

  • De Boer M, Bom P, Kindt F, Keurentjes JJB, Von der Sluis I, Van Loon LC, Bakker PAHM (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93:626–632. doi:10.1094/PHYTO.2003.93.5.626

    PubMed  Google Scholar 

  • De Santiago A, Diaz I, del Campillo MD, Torrent J, Delgado A (2008) Predicting the incidence of iron deficiency chlorosis from hydroxylamine-extractable iron in soil. Soil Sci Soc Am J 72:1493–1499. doi:10.2136/sssaj2007.0366

    Google Scholar 

  • Di Donato RJ, LA Jr R, 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 39:403–414. doi:10.1111/j.1365-313X.2004.02128.x

    Google Scholar 

  • Drechsel H, Jung J (1998) Peptide siderophores. J Pept Sci 4:147–181. doi:10.1002/(SICI) 1099-1387(199805) 4:3<147::AID-PSC136>3.0.CO;2-C

    PubMed  CAS  Google Scholar 

  • Duijff BJ, Meijer JW, Bakker PAHM, Schippers B (1993) Siderophore-mediated competition for iron and induced resistance in the suppression of Fusarium wilt of carnation by fluorescent Pseudomonas spp. Neth J Plant Pathol 99:277–289. doi:10.1007/BF01974309

    CAS  Google Scholar 

  • Duijff BJ, Bakker PAHM, Schippers B (1994a) Suppression of Fusarium wilt of carnation by Pseudomonas putida WCS358 at different levels of disease incidence and iron availability. Biocontrol Sci Technol 4:279–288. doi:10.1080/09583159409355336

    Google Scholar 

  • Duijff BJ, De Kogel WJ, Bakker PAHM, Schippers B (1994b) Influence of pseudobactin 358 on the iron nutrition of barley. Soil Biol Biochem 26:1681–1994. doi:10.1016/0038-0717(94) 90321-2

    CAS  Google Scholar 

  • Duijff BJ, Recorbet G, Bakker PAHM, Loper JE, Lemanceau P (1999) Microbial antagonism at the root level is involved in the suppression of Fusarium wilt by the combination of nonpathogenic Fusarium oxysporum Fo47 and Pseudomonas putida WCS358. Phytopathology 89:1073–1079. doi:10.1094/PHYTO.1999.89.11.1073

    PubMed  CAS  Google Scholar 

  • Eckhardt U, Marques AM, Buckhout TJ (2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol Biol 45:437–448. doi:10.1023/A:1010620012803

    PubMed  CAS  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628. doi:10.1073/pnas.93.11.5624

    PubMed  CAS  Google Scholar 

  • Elad Y, Baker R (1985) The role of competition for iron and carbon in suppression of chlamydospore germination of Fusarium spp. by Pseudomonas spp. Phytopathology 75:1053–1059. doi:10.1094/Phyto-75-1053

    CAS  Google Scholar 

  • Emery T (1965) Isolation, characterization, and properties of fusarinine, a hydroxamic derivative of ornithine. Biochem 4:1410–1417. doi:10.1021/bi00883a028

    CAS  Google Scholar 

  • Eng BH, Guerinot ML, Eide D, Saier MH (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166:1–7. doi:10.1007/s002329900442

    PubMed  CAS  Google Scholar 

  • Faraldo-Gomez JD, Sansom MS (2003) Acquisition of siderophores in Gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116. doi:10.1038/nrm1015

    PubMed  CAS  Google Scholar 

  • Gamalero E, Martinotti MG, Trotta A, Lemanceau P, Berta G (2002) Morphogenetic modifications induced by Pseudomonas fluorescens A6RI and Glomus mosseae BEG12 in the root system of tomato differ according to the plant growth conditions. New Phytol 155:293–300. doi:10.1046/j.1469-8137.2002.00460.x

    Google Scholar 

  • Geels FP, Schmidt EDL, Schippers B (1985) The use of 8-hydroxyquinoline for the isolation and prequantification of plant growth-stimulating rhizosphere pseudomonads. Biol Fertil Soils 1:167–173. doi:10.1007/BF00257633

    CAS  Google Scholar 

  • Gendre D, Czernic P, Conejero G, Pianelli K, Briat JF, Lebrun M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J 49:1–15. doi:10.1111/j.1365-313X.2006.02937.x

    PubMed  CAS  Google Scholar 

  • Ghysels B, Min Dieu BT, Beatson SA, Pirnay JP, Oschner UA, Vasil ML, Cornelis P (2004) FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. Microbiology 150:1671–1680. doi:10.1099/mic.0.27035-0

    PubMed  CAS  Google Scholar 

  • Gleyzes C, Tellier S, Astruc M (2002) Fractionation studies of trace elements in contaminated soils and sediments: a review of sequential extraction procedures. Trends Analyt Chem 21:451–467. doi:10.1016/S0165-9936(02) 00603-9

    CAS  Google Scholar 

  • Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743–772. doi:10.1146/annurev.mi.48.100194.003523

    PubMed  CAS  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta-Biomembr 1465:190–198. doi:10.1016/S0005-2736(00)00138-3

    CAS  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820

    PubMed  CAS  Google Scholar 

  • Hanesch M, Stanjek H, Petersen N (2006) Thermomagnetic measurements of soil iron minerals: the role of organic carbon. Geophys J Int 165:53–61. doi:10.1111/j.1365-246X.2006.02933.x

    CAS  Google Scholar 

  • Hantke K (1981) Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182:288–292. doi:10.1007/BF00269672

    PubMed  CAS  Google Scholar 

  • Harmsen J (2007) Measuring bioavailability: From a scientific approach to standard methods. J Environ Qual 36:1420–1428. doi:10.2134/jeq2006.0492

    PubMed  CAS  Google Scholar 

  • Harmsen J, Rulkens W, Eijsackers H (2005) Bioavailability, concept for understanding or tool for predicting? Land Contam Reclam 13:161–171

    Google Scholar 

  • Henriques R, Jásik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C (2002) Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol Biol 50:587–597. doi:10.1023/A:1019942200164

    PubMed  CAS  Google Scholar 

  • Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, Stephan UW, Baumlein H (1999) Isolation, characterization and cDNA cloning of nicotianamine synthase from barley—A key enzyme for iron homeostasis in plants. Eur J Biochem 265:231–239. doi:10.1046/j.1432-1327.1999.00717.x

    PubMed  CAS  Google Scholar 

  • Heron G, Crouzet C, Bourg ACM, Christensen TH (1994) Speciation of Fe(II) and Fe(III) in contaminated aquifer sediments using chemical extraction techniques. Environ Sci Technol 28:1698–1705. doi:10.1021/es00058a023

    CAS  Google Scholar 

  • Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471–479. doi:10.1104/pp.119.2.471

    PubMed  CAS  Google Scholar 

  • Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, Mori S (2001) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J 25:159–167. doi:10.1046/j.1365-313x.2001.00951.x

    PubMed  CAS  Google Scholar 

  • Höfte M, Bakker PAHM (2007) Competition for iron and induced systemic resistance by siderophores of plant growth promoting rhizobacteria. In: Varma A, Chincholkar S (eds) Microbial siderophores. Springer-Verlag, Berlin Heildeberg, pp 121–133

    Google Scholar 

  • Hohnadel D, Meyer JM (1988) Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol 170:4865–4873

    PubMed  CAS  Google Scholar 

  • Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2003) Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J 36:366–381. doi:10.1046/j.1365-313X.2003.01878.x

    PubMed  CAS  Google Scholar 

  • 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 45:335–346. doi:10.1111/j.1365-313X.2005.02624.x

    PubMed  CAS  Google Scholar 

  • Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) From the cover: mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc Natl Acad Sci USA 104:7373–7378. doi:10.1073/pnas.0610555104

    PubMed  CAS  Google Scholar 

  • 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 577:528–534. doi:10.1016/j.febslet.2004.10.062

    PubMed  CAS  Google Scholar 

  • Jurkevitch E, Hadar Y, Chen Y, Chino M, Mori S (1993) Indirect utilization of the phytosiderophore mugineic acid as an iron source to rhizosphere fluorescent Pseudomonas. Biometals 6:119–123. doi:10.1007/BF00140113

    PubMed  CAS  Google Scholar 

  • Kiczka M, Wiederhold JG, Kraemer SM, Bourdon B, Kretzschmar R (2007) The impact of Fe isotope fractionation by plants on the isotopic signature of soils. Geochim Cosmochim Acta 71:A482

    Google Scholar 

  • Kikkeri R, Traboulsi H, Humbert N, Gumienna-Kontecka E, Arad-Yellin R, Melman G, Elhabiri M, Albrecht-Gary AM, Shanzer A (2007) Toward iron sensors: bioinspired tripods based on fluorescent phenol-oxazoline coordination sites. Inorg Chem 46:2485–2497. doi:10.1021/ic061952u

    PubMed  CAS  Google Scholar 

  • Kilz S, Lenz C, Fuchs R, Budzikiewicz H (1999) A fast screening method for the identification of siderophores from fluorescent Pseudomonas spp. by liquid chromatography/electrospray mass spectrometry. J Mass Spectrom 34:281–290. doi:10.1002/(SICI)1096-9888(199904)34:4<281::AID-JMS750>3.0.CO;2-M

    PubMed  CAS  Google Scholar 

  • Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280. doi:10.1016/j.febslet.2007.04.043

    PubMed  CAS  Google Scholar 

  • Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298. doi:10.1126/science.1132563

    PubMed  CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320. doi:10.1007/BF02602840

    CAS  Google Scholar 

  • Kobayashi T, Nakanishi H, Takahashi M, Kawasaki S, Nishizawa NK, Mori S (2001) In vivo evidence that Ids3 from Hordeum vulgare encodes a dioxygenase that converts 2′-deoxymugineic acid to mugineic acid in transgenic rice. Planta 212:864–871. doi:10.1007/s004250000453

    PubMed  CAS  Google Scholar 

  • 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 104:19150–19155. doi:10.1073/pnas.0707010104

    PubMed  CAS  Google Scholar 

  • Koedam N, Wittouck E, Gaballa A, Gillis A, Höfte M, Cornellis P (1994) Detection and differentiation of microbial siderophores by isolelectric focusing and chrome azurol S overlay. Biometals 7:287–291. doi:10.1007/BF00144123

    PubMed  CAS  Google Scholar 

  • Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424. doi:10.1111/j.1365-313X.2004.02146.x

    PubMed  CAS  Google Scholar 

  • Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18. doi:10.1007/s00027-003-0690-5

    CAS  Google Scholar 

  • Kraemer SM, Cheah SF, Zapf R, Xu JD, Raymond KN, Sposito G (1999) Effect of hydroxamate siderophores on Fe release and Pb(II) adsorption by goethite. Geochim Cosmochim Acta 63:3003–3008. doi:10.1016/S0016-7037(99)00227-6

    CAS  Google Scholar 

  • Kraemer SM, Crowley D, Kretzschmar R (2006) Geochemical aspects of phytosiderophore-promoted iron acquisition by plants. Adv Agron 91:1–46. doi:10.1016/S0065-2113(06) 91001-3

    CAS  Google Scholar 

  • Labanowski J, Monna F, Bermond A, Cambier P, Fernandez C, Lamy I, van Oort F (2008) Kinetic extractions to assess mobilization of Zn, Pb, Cu, and Cd in a metal-contaminated soil: EDTA vs. citrate. Environ Pollut 3:693–701. doi:10.1016/j.envpol.2007.06.054

    Google Scholar 

  • La Force MJ, Fendorf S (2000) Solid-phase iron characterization during common selective sequential extractions. Soil Sci Soc Am J 64:1608–1615

    Google Scholar 

  • Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schroeder A, Kramer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051. doi:10.1038/sj.emboj.7600864

    PubMed  CAS  Google Scholar 

  • Lehto NH, Davisn W, Zhang H, Tych W (2006) Analysis of micro-nutrient behaviour in the rhizosphere using a DGT parameterised dynamic plant uptake model. Plant Soil 282:227–238. doi:10.1007/s11104-005-5848-6

    CAS  Google Scholar 

  • 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 44:769–782. doi:10.1111/j.1365-313X.2005.02569.x

    PubMed  Google Scholar 

  • Leeman M, Den Ouden FM, Van Pelt JA, Dirkx FPM, Steijl H, Bakker PAHM, Schippers B (1996) Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149–155. doi:10.1094/Phyto-86-149

    CAS  Google Scholar 

  • Lemanceau P, Alabouvette C, Meyer JM (1986) Production of fusarinine and iron assimilation by pathogenic and non-pathogenic Fusarium. In: Swinburne TR (ed) Iron, siderophores and plant diseases. Plenum, New York and London, pp 251–259

    Google Scholar 

  • Lemanceau P, Alabouvette C, Couteaudier Y (1988a) Recherches sur la résistance des sols aux maladies. XIV. Modification du niveau de réceptivité d’un sol résistant et d’un sol sensible aux fusarioses vasculaires en réponse à des apports de fer ou de glucose. Agronomie 8:155–162. doi:10.1051/agro:19880209

    Google Scholar 

  • Lemanceau P, Samson R, Alabouvette C (1988b) Recherches sur la résistance des sols aux maladies. XV. Comparaison des populations de Pseudomonas fluorescents dans un sol résistant et un sol sensible aux fusarioses vasculaires. Agronomie 8:243–249. doi:10.1051/agro:19880310

    Google Scholar 

  • Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C, Schippers B (1992) Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Appl Environ Microbiol 58:2978–2982

    PubMed  CAS  Google Scholar 

  • Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C, Schippers B (1993) Antagonistic effect of nonpathogenic Fusarium oxysporum Fo47 and pseudobactin 358 upon pathogenic Fusarium oxysporum f. sp. dianthi. Appl Environ Microbiol 59:74–82

    PubMed  CAS  Google Scholar 

  • Lemanceau P, Robin A, Mazurier S, Vansuyt G (2007) Implication of pyoverdines in the interactions of fluorescent pseudomonads with soil microflora and plant in the rhizosphere. In: Varma A, Chincholkar SB (eds) Microbial siderophores. Soil biology, vol. 12. Springer-Verlag, Berlin Heidelberg, pp 165–192

    Google Scholar 

  • Li L, Cheng X, Ling HQ (2004) Isolation and characterization of Fe(III)-chelate reductase gene LeFRO1 in tomato. Plant Mol Biol 54:125–136. doi:10.1023/B:PLAN.0000028790.75090.ab

    PubMed  Google Scholar 

  • Lindsay WL (1979) Chemical equilibria in soils. Wiley, Chuchester

    Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428

    CAS  Google Scholar 

  • 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 99:13938–13943. doi:10.1073/pnas.212448699

    PubMed  CAS  Google Scholar 

  • Loper JE (1988) Role of fluorescent siderophore production in biological control of Pythium ultimum by a Pseudomonas fluorescens strain. Phytopathology 78:166–172. doi:10.1094/Phyto-78-166

    CAS  Google Scholar 

  • Loper JE, Buyer JS (1991) Siderophores in microbial interactions on plant surfaces. Mol Plant Microbe Interact 4:5–13

    CAS  Google Scholar 

  • Loper JE, Lindow SE (1994) A biological sensor for iron available to bacteria in their habitats on plant surfaces. Appl Environ Microbiol 60:1934–1941

    PubMed  CAS  Google Scholar 

  • Loper JE, Henkels MD (1997) Availability of iron to Pseudomonas fluorescens in rhizopshere and bulk soil evaluated with an ice nucleation reporter gene. Appl Environ Microbiol 63:99–105

    PubMed  CAS  Google Scholar 

  • Loper JE, Lindow SE (1997) Reporter gene systems useful in evaluating in situ gene expression by soil-and plant-associated bacteria. In: Hurst CJ (ed) Manual of environmental microbiology. America Society for Microbiology, Washington, pp 482–492

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  • Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274. doi:10.1007/BF00008069

    CAS  Google Scholar 

  • Marschner P, Crowley DE (1997) Iron stress and pyoverdin production by a fluorescent pseudomonad in the rhizosphere of white lupine (Lupinus albus L.) and barley (Hordeum vulgare L.). Appl Environ Microbiol 63:227–281

    Google Scholar 

  • Marschner P, Crowley DE (1998) Phytosiderophores decrease iron stress and pyoverdine production of Pseudomonas fluorescens Pf-5 (pvd-inaZ). Soil Biol Biochem 30:1275–1280. doi:10.1016/S0038-0717(98)00039-X

    CAS  Google Scholar 

  • Marschner H, Römheld V, Kissel M (1987) Localization of phytosiderophore release and iron uptake along intact barley roots. Physiol Plant 71:157–162. doi:10.1111/j.1399-3054.1987.tb02861.x

    CAS  Google Scholar 

  • Maurhofer M, Hase C, Meuwly P, Metraux JP, Défago G (1994) Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 84:139–146. doi:10.1094/Phyto-84-139

    CAS  Google Scholar 

  • Meyer JM, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physico-chemical properties. J Gen Microbiol 107:319–328

    CAS  Google Scholar 

  • Meyer JM, Hallé F, Hohnadel D, Lemanceau P, Ratefiarivelo H (1987) Siderophores of Pseudomonas—Biological properties. In: Winkelmann G, Van der Helm D, Neilands JB (eds) Iron transport in microbes, plants and animals. VCH, Weinheim, pp 189–205

    Google Scholar 

  • Meyer JM, Stintzi A, De Vos D, Cornelis P, Tappe R, Taraz K, Budzikiewicz H (1997) Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143:35–43

    PubMed  CAS  Google Scholar 

  • Meyer JM, Geoffroy VA, Baida N, Gardan L, Izard D, Lemanceau P, Achouak W, Palleroni NJ (2002) Siderophore typing, a powerful tool for the taxonomy of fluorescent and non-fluorescent Pseudomonas. Appl Environ Microbiol 68:2745–2453. doi:10.1128/AEM.68.6.2745-2753.2002

    PubMed  CAS  Google Scholar 

  • Meyer JM, Gruffaz C, Raharinosy V, Bezverbnaya I, Schäfer M, Budzikiewicz H (2008) Siderotyping of fluorescent Pseudomonas: molecular mass determination by mass spectrometry as a powerful pyoverdine siderotyping method. Biometals 21:259–271. doi:10.1007/s10534-007-9115-6

    PubMed  CAS  Google Scholar 

  • Mirleau P, Delorme S, Philippot L, Meyer JM, Mazurier S, Lemanceau P (2000) Fitness in soil and rhizosphere of Pseudomonas fluorescens C7R12 compared with a C7R12 mutant affected in pyoverdine synthesis and uptake. FEMS Microbiol Ecol 34:35–44. doi:10.1111/j.1574-6941.2000.tb00752.x

    PubMed  CAS  Google Scholar 

  • Mirleau P, Philippot L, Corberand T, Lemanceau P (2001) Involvement of nitrate reductase and pyoverdine in competitiveness of Pseudomonas fluorescens strain C7R12 in soil. Appl Environ Microbiol 67:2627–2635. doi:10.1128/AEM.67.6.2627-2635.2001

    PubMed  CAS  Google Scholar 

  • Misaghi IJ, Stowell LJ, Grogan RG, Spearman LC (1982) Fungistatic activity of water-soluble fluorescent pigments of fluorescent pseudomonads. Phytopathology 72:33–36. doi:10.1094/Phyto-72-33

    CAS  Google Scholar 

  • Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK (2003) Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiol 132:1989–1997. doi:10.1104/pp.102.019869

    PubMed  CAS  Google Scholar 

  • Mori S, Nishizawa NK (1987) Methionine as a dominant precursor of phytosiderophores in Gramineae plants. Plant Cell Physiol 28:1081–1092

    CAS  Google Scholar 

  • Mossialos D, Amoutzias GD (2007) Siderophores in fluorescent pseudomonads: new tricks from an old dog. Future Microbiol 2:387–395. doi:10.2217/17460913.2.4.387

    PubMed  CAS  Google Scholar 

  • Mossialos D, Ochsner U, Baysse C, Chablain P, Pirnay JP, Koedam N, Budzikiewicz H, Fernandez DU, Schafer M, Ravel J, Cornelis P (2002) Identification of new, conserved, nonribosomal peptide synthetases from fluorescent pseudomonads involved in the biosynthesis of the siderophore pyoverdine. Mol Microbiol 45:1673–1685. doi:10.1046/j.1365-2958.2002.03120.x

    PubMed  CAS  Google Scholar 

  • 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 44:199–207. doi:10.1023/A:1006491521586

    PubMed  CAS  Google Scholar 

  • 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 secretion in Fe- deficient barley roots. Plant J 30:83–94. doi:10.1046/j.1365-313X.2002.01270.x

    PubMed  CAS  Google Scholar 

  • Neilands JB (1981) Iron absorption and transport in microorganisms. Annu Rev Nutr 1:27–46. doi:10.1146/annurev.nu.01.070181.000331

    PubMed  CAS  Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396. doi:10.1051/agro:2003011

    CAS  Google Scholar 

  • Nozoye T, Inoue H, Takahashi M, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2007) The expression of iron homeostasis-related genes during rice germination. Plant Mol Biol 64:35–47. doi:10.1007/s11103-007-9132-4

    PubMed  CAS  Google Scholar 

  • 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 57:2867–2878. doi:10.1093/jxb/erl054

    PubMed  CAS  Google Scholar 

  • Ogo Y, Itai RN, 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 51:366–377. doi:10.1111/j.1365-313X.2007.03149.x

    PubMed  CAS  Google Scholar 

  • Ogo Y, Kobayashi T, Nakanishi IR, Nakanishi H, Kakei Y, Takahashi M, Toki S, Mori S, Nishizawa NK (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. 283:13407–13417

  • Palanche T, Marmolle F, Abdallah MA, Shanzer A, Albrecht-Gary AM (1999) Fluorescent siderophore-based chemosensors: iron(III) quantitative determinations. J Biol Inorg Chem 4:188–198. doi:10.1007/s007750050304

    PubMed  CAS  Google Scholar 

  • Parfitt RL, Childs CW (1988) Estimation of forms of Fe and Al—a review and analysis of contrasting soils by dissolution and Mössbauer methods. Aust J Soil Res 26:121–144. doi:10.1071/SR9880121

    CAS  Google Scholar 

  • Poole K (2004) Pseudomonas. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. American Society of Microbiology Press, Washington, pp 293–310

    Google Scholar 

  • Powell PE, Cline GR, Reid CPP, Szaniszlo PJ (1980) Occurrence of hydroxamate siderophore iron chelators in soils. Nature 287:833–834. doi:10.1038/287833a0

    CAS  Google Scholar 

  • Raaijmakers JM, Van der Sluis L, Koster M, Bakker PAHM, Weisbeek PJ, Schippers B (1995) Utilisation of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can J Microbiol 41:126–135

    CAS  Google Scholar 

  • Reichard PU, Kraemer SM, Frazier SW, Kretzschmar R (2005) Goethite dissolution in the presence of phytosiderophores: Rates, mechanisms, and the synergistic effect of oxalate. Plant Soil 276:115–132. doi:10.1007/s11104-005-3504-9

    CAS  Google Scholar 

  • Reichard PU, Kretzschmar R, Kraemer SM (2007a) Rate laws of steady-state and non-steady-state ligand-controlled dissolution of goethite. Colloids Surf A Physicochem Eng Asp 306:22–28. doi:10.1016/j.colsurfa.2007.03.001

    CAS  Google Scholar 

  • Reichard PU, Kretzschmar R, Kraemer SM (2007b) Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim Cosmochim Acta 71:5635–5650. doi:10.1016/j.gca.2006.12.022

    CAS  Google Scholar 

  • Reichman SM, Parker DR (2007) Probing the effect of light and temperature on diurnal rhythms of phytosiderophore release in wheat. New Phytol 174:101–108. doi:10.1111/j.1469-8137.2007.01990.x

    PubMed  CAS  Google Scholar 

  • Reyes I, Torrent J (1997) Citrate-ascorbate as a highly selective extractant for poorly crystalline iron oxides. Soil Sci Soc Am J 61:1647–1654

    CAS  Google Scholar 

  • Robin A, Vansuyt G, Corberand T, Briat JF, Lemanceau P (2006a) The soil type affects both the differential accumulation of iron between wild type and ferritin over-expressor tobacco plants and the sensitivity of their rhizosphere bacterioflora to iron stress. Plant Soil 283:73–81. doi:10.1007/s11104-005-9437-5

    CAS  Google Scholar 

  • Robin A, Mougel C, Siblot S, Vansuyt G, Mazurier S, Lemanceau P (2006b) Effect of ferritin over-expression in tobacco on the structure of bacterial and pseudomonad communities associated with the roots. FEMS Microbiol Ecol 58:492–502. doi:10.1111/j.1574-6941.2006.00174.x

    PubMed  CAS  Google Scholar 

  • Robin A, Mazurier S, Mougel C, Vansuyt G, Corberand T, Meyer JM, Lemanceau P (2007) Diversity of root-associated fluorescent pseudomonads as affected by ferritin over-expression in tobacco. Environ Microbiol 9:1724–1737. doi:10.1111/j.1462-2920.2007.01290.x

    PubMed  CAS  Google Scholar 

  • Robin A, Vansuyt G, Hinsinger P, Meyer JM, Briat JF, Lemanceau P (2008) Iron dynamics in the rhizosphere: consequences for plant health and nutrition. Adv Agron 99:183–225. doi:10.1016/S0065-2113(08)00404-5

    CAS  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697. doi:10.1038/17800

    PubMed  CAS  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180. doi:10.1104/pp.80.1.175

    PubMed  Google Scholar 

  • Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H(+)-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant Physiol Biochem 43:287–292. doi:10.1016/j.plaphy.2005.02.007

    PubMed  CAS  Google Scholar 

  • Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, Von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096. doi:10.1074/jbc.M311799200

    PubMed  CAS  Google Scholar 

  • Schaaf G, Schikora A, Häberle J, Vert G, Ludewig U, Briat JF, Curie C, Von Wirén N (2005) A putative function of the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774. doi:10.1093/pcp/pci081

    PubMed  CAS  Google Scholar 

  • Schagerlöf U, Wilson G, Hebert H, Al-Karadaghi S, Hägerhäll C (2006) Transmembrane topology of FRO2, a ferric chelate reductase from Arabidopsis thaliana. Plant Mol Biol 62:215–221. doi:10.1007/s11103-006-9015-0

    PubMed  Google Scholar 

  • Scheinost AC, Schwertmann U (1999) Color identification of iron oxides and hydroxysulfates: Use and limitations. Soil Sci Soc Am J 63:1463–1471

    CAS  Google Scholar 

  • Scher FM, Baker R (1980) Mechanism of biological control in a Fusarium-suppressive soil. Phytopathology 70:412–417. doi:10.1094/Phyto-70-412

    Google Scholar 

  • Scher FM, Baker R (1982) Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72:1567–1573. doi:10.1094/Phyto-72-1567

    CAS  Google Scholar 

  • Schwertmann U (1964) Differenzierung der eisenoxide des bodens durch extraktion mit ammoniumoxalat-lösung. Z Pflanzenernaehr Bodenkd 105:194–202. doi:10.1002/jpln.3591050303

    CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 106:47–56. doi:10.1016/0003-2697(87) 90612-9

    Google Scholar 

  • Shojima S, Nishizawa NK, Mori S (1989) Establishment of a cell free system for the biosynthesis of nicotianamine. Plant Cell Physiol 30:673–677

    CAS  Google Scholar 

  • Simeoni LA, Lindsay WL, Baker R (1987) Critical iron level associated with biological control of Fusarium wilt. Phytopathology 77:1057–1061. doi:10.1094/Phyto-77-1057

    CAS  Google Scholar 

  • Sneh B, Dupler M, Elad Y, Baker R (1984) Chlamydospore germination of Fusarium oxysporum f.sp. cucumerinum as affected by fluorescent and lytic bacteria from a Fusarium-suppressive soil. Phytopathology 74:1115–1124. doi:10.1094/Phyto-74-1115

    Google Scholar 

  • Soltanpour PN, Schwab AP (1977) A new soil test for simultaneous extraction of macro- and micro-nutrients in alkaline soils. Commun Soil Sci Plant Anal 8:195–207. doi:10.1080/00103627709366714

    CAS  Google Scholar 

  • Steinberg C, Edel-Hermann V, Alabouvette C, Lemanceau P (2007) Soil suppressiveness to plant diseases. In: Van Elsas D, Jansson JK, Trevors JT (eds) Modern Soil Microbiology, 2nd edn. CRC, Taylor & Francis Group, London, pp 455–477

    Google Scholar 

  • Stintzi A, Evans K, Meyer JM, Poole K (1998) Quorum sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine synthesis. FEMS Microbiol Lett 166:341–345. doi:10.1111/j.1574-6968.1998.tb13910.x

    PubMed  CAS  Google Scholar 

  • Sugiura Y, Tanaka H, Mino Y, Ishida T, Ota N, Nomoto K, Yosioka H, Takemoto T (1981) Structure, properties, and transport mechanism of iron(III) complex of mugineic acid, a possible phytosiderophore. J Am Chem Soc 103:6979–6982. doi:10.1021/ja00413a043

    CAS  Google Scholar 

  • Takagi SI (1976) Naturally occurring iron–chelating compounds in oat–root and rice–root washings.1. Activity measurement and preliminary characterization. Soil Sci Plant Nutr 22:423–433

    CAS  Google Scholar 

  • Takagi SI, Nomoto K, Takemoto T (1984) Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J Plant Nutr 7:469–477. doi:10.1080/01904168409363213

    CAS  Google Scholar 

  • Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469. doi:10.1038/88143

    PubMed  CAS  Google Scholar 

  • Taylor SR (1964) Abundance of chemical elements in the continental crust—A new table. Geochim Cosmochim Acta 28:1273–1285. doi:10.1016/0016-7037(64) 90129-2

    CAS  Google Scholar 

  • Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851. doi:10.1021/ac50043a017

    CAS  Google Scholar 

  • Vansuyt G, Robin A, Briat JF, Curie C, Lemanceau P (2007) Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol Plant Microbe Interact 4:441–447. doi:10.1094/MPMI-20-4-0441

    Google Scholar 

  • Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589–599. doi:10.1046/j.1365-313X.2002.01381.x

    PubMed  CAS  Google Scholar 

  • 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 14:1223–1233. doi:10.1105/tpc.001388

    PubMed  CAS  Google Scholar 

  • 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 132:796–804. doi:10.1104/pp.102.016089

    PubMed  CAS  Google Scholar 

  • Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30. doi:10.1016/j.tim.2006.11.004

    PubMed  CAS  Google Scholar 

  • Van Wuytswinkel O, Vansuyt G, Grignon N, Fourcroy P, Briat JF (1999) Iron homeostasis alteration in transgenic tobacco overexpressing ferritin. Plant J 17:93–97. doi:10.1046/j.1365-313X.1999.00349.x

    PubMed  Google Scholar 

  • Von Wirén N, Römheld V, Morel JL, Guckert A, Marschner H (1993) Influence of microorganisms on iron acquisition in maize. Soil Biol Biochem 25:371–376. doi:10.1016/0038-0717(93) 90136-Y

    Google Scholar 

  • Von Wirén N, Mori S, Marschner H, Römheld V (1994) Iron inefficiency in maize mutant ys1 (Zea mays L. cv Yellow-Stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol 106:71–77

    Google Scholar 

  • Von Wirén N, Römheld V, Shioiri T, Marschner H (1995) Competition between micro-organisms and roots of barley and sorghum for iron accumulated in the root apoplasm. New Phytol 130:511–521. doi:10.1111/j.1469-8137.1995.tb04328.x

    Google Scholar 

  • Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94. doi:10.1104/pp.010829

    PubMed  CAS  Google Scholar 

  • Whiteley M, Kimberely ML, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13604–13609. doi:10.1073/pnas.96.24.13904

    Google Scholar 

  • Wiederhold JG, Teutsch N, Kraemer SM, Halliday AN, Kretzschmar R (2007a) Iron isotope fractionation in oxic soils by mineral weathering and podzolization. Geochim Cosmochim Acta 71:5821–5833. doi:10.1016/j.gca.2007.07.023

    CAS  Google Scholar 

  • Wiederhold JG, Teutsch N, Kraemer SM, Halliday AN, Kretzschmar R (2007b) Iron isotope fractionation during pedogenesis in redoximorphic soils. Soil Sci Soc Am J 71:1840–1850. doi:10.2136/sssaj2006.0379

    CAS  Google Scholar 

  • Winkelmann G (1991) Handbook of microbial iron chelate. CRC, Bocca Raton, Florida

    Google Scholar 

  • Winkelmann G (2001) Siderophore transport in fungi. In: Winkelmann G (ed) Microbial transport systems. Wiley-VCH, Weinheim, pp 463–480

    Google Scholar 

  • Winkelmann G (2002) Microbial siderophore-mediated transport. Biochem Soc Trans 30:691–696. doi:10.1042/BST0300691

    PubMed  CAS  Google Scholar 

  • Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392. doi:10.1007/s10534-006-9076-1

    PubMed  CAS  Google Scholar 

  • Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 87:345–351. doi:10.1128/AEM.66.1.345-351.2000

    Google Scholar 

  • Yehuda Z, Shenker M, Römheld V, Marschner H, Hadar Y, Chen Y (1996) The role of ligand exchange in the uptake of iron from microbial siderophores by gramineous plants. Plant Physiol 112:1273–1280

    PubMed  CAS  Google Scholar 

  • 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 10:835–844. doi:10.1046/j.1365-313X.1996.10050835.x

    PubMed  CAS  Google Scholar 

  • 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 15:613–621. doi:10.1038/sj.cr.7290331

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. INRA, Université de Bourgogne, UMR1229 ‘Microbiologie du Sol et de l’Environnement’, CMSE, 17 rue Sully, BV 86510, 21034, Dijon cedex, France

    Philippe Lemanceau

  2. Institute for Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany

    Petra Bauer

  3. University of Vienna, Department of Environmental Geosciences, Althanstraße 14, 1090, Vienna, Austria

    Stephan Kraemer

  4. CNRS, Université Montpellier II, SupAgro, INRA, UMR5004 ‘Biochimie et Physiologie Moléculaire des Plantes’, Place Pierre Viala, 34060, Montpellier cedex I, France

    Jean-François Briat

Authors
  1. Philippe Lemanceau
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Petra Bauer
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Stephan Kraemer
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Jean-François Briat
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Philippe Lemanceau.

Additional information

Responsible Editor: Philippe Hinsinger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lemanceau, P., Bauer, P., Kraemer, S. et al. Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes. Plant Soil 321, 513–535 (2009). https://doi.org/10.1007/s11104-009-0039-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0039-5

Keywords