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Iron uptake and metabolism in the rhizobia/legume symbioses

  • Chapter
Iron Nutrition and Interactions in Plants

Part of the book series: Developments in Plant and Soil Sciences ((DPSS,volume 43))

Abstract

Iron-containing proteins figure prominently in the nitrogen-fixing symbioses between bacteria of the genera Azorhizobium, Bradyrhizobium and Rhizobium and their respective plant hosts. Although iron is abundant in the soil, the acquisition of iron is problematic due to its low solubility at biological pH under aerobic conditions. The study of iron acquisition as it pertains to these economically important symbioses is directed at answering three questions: 1) how do rhizobial cells acquire iron as free-living microorganisms where they must compete for this nutrient with other soil inhabitants 2) how do the plant hosts acquire enough iron for the symbiosis and 3) how do rhizobia acquire iron as symbionts? Production and /or utilization of ferric-specific ligands (siderophores) has now been documented in the laboratory for a number of rhizobial species, but there is limited information on whether production and /or untilization occurs either in the soil or in planta. Studies with rhizobial mutants which can no longer produce and /or utilize siderophores should address whether siderophores contribute to functional symbioses. In addition, the ability to produce and /or utilize siderophores may affect the outcome of both interstrain and interspecific competition in the rhizosphere and in bulk soil. Some progress has been made at documenting the effects of iron deficiency on nodule development. Studies are also underway to determine whether, in addition to its central structural role, iron may also play a regulatory role in the symbioses. This review is an attempt to give an overview of the field, and hopefully will stimulate further research on the iron nutrition of these symbioses which account for such a significant proportion of the world’s biologically fixed nitrogen.

Rhizobia will be used to refer collectively to the genera Azorhizobiun, Bradyrhizobium and Rhizobium throughout this article.

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References

  • Ames-Gottfred N P, Christie B R and Jordan D C 1989 Use of the chrome azurol S agar plate technique to differentiate strains and field isolates of Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 55, 707–710.

    PubMed  CAS  Google Scholar 

  • Appanna V D 1988 A comparative study of exopolysac-charide synthesis in Rhizobium meliloti JJ-1 exposed to aluminum and iron. Microbios 55, 33–39.

    CAS  Google Scholar 

  • Bagg A and Neilands J B 1987 Molecular mechanisms of regulation of siderophore-mediated iron assimilation. Microbiol. Rev. 51, 509–518.

    PubMed  CAS  Google Scholar 

  • Bergersen F J 1963 Iron in the developing soybean nodule. Aust. J. Biol. Sci. 16, 916–19.

    CAS  Google Scholar 

  • Bosch I, Meidl E J, Hoult M, Plessner O and Guerinot M L 1988 Iron uptake and metabolism in the Bradyrhizobium / soybean symbiosis. In Nitrogen Fixation: Hundred Years After. Eds. H. Bothe, F J deBruijn and W E Newton, p. 652. Gustav Fischer, New York.

    Google Scholar 

  • Braun V, Hantke K, Eick-Helmerick K, Köster W, PreBler U, Sauer M, Schäffer S, Schöffler H, Staudenmaier H and Zimmermann L 1987 Iron transport systems in Escherichia coli. In Iron Transport in Microbes, Plants and Animals. Eds. G Winkelmann, D van der Helm and J B Neilands. pp 35–51. VCH Publishers, New York, NY.

    Google Scholar 

  • Brown J C and Chaney R L 1971 Effect of iron on the transport of citrate into the xylem of soybeans and tomatoes. Plant Physiol. 47, 836–840.

    Article  PubMed  CAS  Google Scholar 

  • Buyer J S, Sikora L J and Chaney R L 1989 A new growth medium for the study of siderophore-mediated interactions. Biol. Fertil. Soil 8, 97–101.

    Article  Google Scholar 

  • Carrillo-Castaneda G and Peralta J R V 1988 Siderophorelike activities in Rhizobium phaseoli. J. Plant Nutr. 11, 935–944.

    Article  Google Scholar 

  • Chaney R L, Brown J C and Tiffin L O 1972 Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol. 50, 208–213.

    Article  PubMed  CAS  Google Scholar 

  • Crichton R R, Ponce-Ortiz Y, Koch M H J, Parfait R and Stuhrmann H B 1978. Isolation and characterizaiton of phytoferritin from pea (Pisum sativum) and lentil (Lens esculenta). Biochem J. 171, 349–256.

    PubMed  CAS  Google Scholar 

  • Crowley D E, Reid C P P and Szaniszlo P J 1987 Microbial siderophores as iron sources for plants. In Iron Transport In Microbes, Plants and Animals. Eds. G Winkelmann, D van der Helm and J B Neilands. pp 375–386. VCH Publishers, New York, NY.

    Google Scholar 

  • Dart P J 1977 Infection and development of leguminous nodules. In A Treatise on Dinitrogen Fixation. Eds. R W F Hardy and W S Silver, pp 367–472. John Wiley and Sons, New York.

    Google Scholar 

  • deLorenzo V, Wee S, Herrero M and Neilands J B 1987 Operator sequences of the aerobactin Operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J. Bacteriol. 169, 2624–2630.

    CAS  Google Scholar 

  • Djordjevic M A, Gabriel D W and Rolfe B G 1987 Rhizobium — the refined parasite of legumes. Annu. Rev. Phytopathol. 25, 145–168.

    Article  Google Scholar 

  • Enard C, Diolez A and Expert D 1988 Systemic virulence of Erwinia chrysanthemi 3937 requires a functional iron assimilation system. J. Bacteriol. 170, 2419–2426.

    PubMed  CAS  Google Scholar 

  • Ferrala N F, Champlin A K, and Fekete F A 1986 Morphological differences in the capsular polysaccharide of nitrogen-fixing Azotobacter chroococcum B-8 as a function of iron and molybdenum starvation. FEMS Microbiol. Lett. 33, 137–142.

    Article  CAS  Google Scholar 

  • Fischer H M, Alvarez-Morales and Hennecke H 1986 The pleiotropic nature of symbiotic regulatory mutants: Bradyrhizobium japonium nifA gene is involved in control of nif gene expression and formation of determinate symbiosis. Mol. Gen. Genet. 209, 621–626.

    Article  Google Scholar 

  • Fischer H M, Bruderer T and Hennecke H 1988 Essential and non-essential domains in the Bradyrhizobium japonicum NifA protein: Identification of indispensable cysteine residues potentially involved in redox and/or metal binding. Nucleic Acids Res. 16, 2207–2224.

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmann J and Wollum A G II 1989a In vitro growth responses of Bradyrhizobium japonicum to soybean rhizosphere bacteria. Soil Biol. Biochem. 21, 131–135.

    Article  Google Scholar 

  • Fuhrmann J and Wollum A G II 1989b Nodulation competition among Bradyrhizobium japonicum strains as influenced by rhizophere bacteria and iron availability. Biol. Fertil. Soils 7, 108–112.

    Article  Google Scholar 

  • Gardner W K, Barber D A and Parbery D G 1983 The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil 70, 107–124.

    Article  CAS  Google Scholar 

  • Gill P R and Neilands J B 1989 Cloning of a genomic region required for a high affinity iron uptake system in Rhizobium meliloti 1021. Mol. Microbiol. 3, 1183–1189.

    Article  PubMed  CAS  Google Scholar 

  • Gill P R, Barton L L, Scoble M D and Neilands J B 1990 A high affinity iron transport system of Rhizobium meliloti may be required for efficient nitrogen fixation in planta. Plant and Soil 130, 211–217.

    Article  Google Scholar 

  • Griggs D W and Konisky J 1989 Mechanism for ironregulated transcription of the Escherichia coli cir gene: Metal-dependent binding of Fur protein to the promoters. J. Bacteriol. 171, 1048–1054.

    PubMed  CAS  Google Scholar 

  • Guerinot M L and Chelm B K 1986 Bacterial Δ-aminolevulinic acid synthase activity is not essential for leghemoglobin formation in the soybean/Bradyrhizobium japonicum symbiosis. Proc. Natl. Acad. Sci. USA 83, 1837–1841.

    Article  PubMed  CAS  Google Scholar 

  • Guerinot M L, Meidl E J and Plessner O 1990 Citrate as a siderophore in Bradyrhizobium japonicum. J. Bacteriol. 172, 3298–3303.

    PubMed  CAS  Google Scholar 

  • Hantke K 1982 Negative control of iron uptake systems in Escherichia coli. FEMS Microbiol. Lett. 15, 83–86.

    Article  CAS  Google Scholar 

  • Henderson N, Austin S and Dixon R A 1989 Role of metal ions in negative regulation of nitrogen fixation by the nifL gene product from Klebsiella pneumoniae. Mol. Gen. Genet. 216, 484–491.

    Article  CAS  Google Scholar 

  • John T R and Nadler K D 1983 Characterization of a Rhizobium leguminosarum mutant strain deficient in heme biosynthesis. Plant Physiol. 72S, 109.

    Google Scholar 

  • Jurkevitch E, Hadar Y and Chen Y 1988 Involvement of bacterial siderophores in the remedy of lime-induced chlorosis in peanut. Soil Sci. Soc. Am. J. 52, 1032–1037.

    Article  CAS  Google Scholar 

  • Ko M P, Huang P-Y, Huang J-S and Barker K R 1987 The occurrence of phytoferritin and its relationship to effectiveness of soybean nodules. Plant Physiol. 83, 299–305.

    Article  PubMed  CAS  Google Scholar 

  • Laudenbach D E and Straus N A 1988 Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J. Bacteriol. 170, 508–5026.

    Google Scholar 

  • Leong J 1986 Siderophores: Their biochemistry and possible role in the biocontrol of plant pathogens. Annu. Rev. Phytopathol. 24, 187–209.

    Article  CAS  Google Scholar 

  • Leong S A, Williams P H and Ditta G S 1985 Analysis of the 5’ regulatory region of the gene for Δ-aminolevulinic acid synthetase of Rhizobium meliloti. Nucleic Acid Res. 13, 5965–5976.

    Article  PubMed  CAS  Google Scholar 

  • McClung C R, Somerville J E, Guerinot M L and Chelm B K 1987 Structure of the Bradyrhizobium japonicum gene hem A encoding 5-aminolevulinic acid synthase. Gene 54, 133–139.

    Article  PubMed  CAS  Google Scholar 

  • Miller J F, Mekalanos J J and Falkow S 1989 Coordinate regulation and sensory transduction in the control of bacterial virulence. Science 243, 916–922.

    Article  PubMed  CAS  Google Scholar 

  • Modi M, Shah K S and Modi V V 1985 Isolation and characterisation of catechol-like siderophore from cowpea Rhizobium RA-1. Arch. Microbiol. 141, 156–158.

    Article  CAS  Google Scholar 

  • Moshiri F, Stults L, Novak P and Maier R J 1983. Nif -Hup- mutants of Rhizobium japonicum. J. Bacteriol. 155, 926–929.

    PubMed  CAS  Google Scholar 

  • Nadler K D, Johnston A W B, Chen J-W and John T R 1990 A Rhizobium leguminosarum mutant defective in symbiotic iron acquisition. J. Bacteriol. 172, 670–677.

    PubMed  CAS  Google Scholar 

  • Nambiar P T C and Sivaramakrishnan S 1987 Detection and assay of siderophores in cowpea rhizobia (Bradyrhizobium) using radioactive Fe (59Fe). Lett. Appl. Microbiol. 4, 37–40.

    Article  CAS  Google Scholar 

  • Neilands J B and Leong S A 1986 Siderophores in relation to plant growth and disease. Annu. Rev. Plant Physiol. 37: 187–208.

    Article  CAS  Google Scholar 

  • Neilands J B 1989 Siderophore systems of bacteria and fungi. In Metal Ions and Bacteria. Eds. T J Beveridge and R J Doyle, pp 141–163. John Wiley and Sons, New York.

    Google Scholar 

  • Noel K D, Stacey G, Tandon S R, Silver L E and Brill W J 1982 Rhizobium japonicum mutants defective in symbiotic nitrogen fixation. J. Bacteriol. 152, 485–494.

    PubMed  CAS  Google Scholar 

  • O’Hara G W, Dilworth M J, Boonkerd N and Parkpian P 1988a Iron-deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp. New Phytol. 108, 51–57.

    Article  Google Scholar 

  • O’Hara G W, Hartzook A, Bell R W and Loneragan J F 1988b Response to Bradyrhizobium strain of peanut cultivars grown under iron stress. J. Plant Nutr. 11, 843–852.

    Article  Google Scholar 

  • Patel H N, Chakraborty R N and Desai S B 1988 Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol. Lett. 56, 131–134.

    Article  CAS  Google Scholar 

  • Payne S M 1988 Iron and virulence in the family enterobac-teriaceae. CRC Microbiol. Rev. 16, 81–111.

    Article  CAS  Google Scholar 

  • Poole K and Braun V 1988 Iron regulation of Serratia marcescens hemolysin gene expresison. Infect. Immun. 56, 2967–2971.

    PubMed  CAS  Google Scholar 

  • Reigh G and O’Connell M 1988 Siderophore production is strain specific in Rhizobium. In Nitrogen Fixation: Hundred Years After. Eds. H Bothe, F J deBruijn and W E Newton, p. 826. Gustav Fischer, New York.

    Google Scholar 

  • Redinbaugh M G and Campbell W H 1983 Reduction of ferric citrate catalyzed by NADH: nitrate reductase. Biochem. Biophys. Res. Commun. 114, 1182–1188.

    Article  PubMed  CAS  Google Scholar 

  • Rioux C R, Jordan D C and Rattray J B M 1986a Iron requirement of Rhizobium legwninosarum and secretion of anthranilic acid during growth on an iron-deficient medium. Arch. Biochem. Biophys. 248, 175–182.

    Article  PubMed  CAS  Google Scholar 

  • Rioux C R, Jordan D C and Rattray J B M 1986b Anthranilate-promoted iron uptake in Rhizobium leguminosarum. Arch. Biochem. Biophys. 248, 183–189.

    Article  PubMed  CAS  Google Scholar 

  • Römheld V 1987 Different strategies for iron acquisition in higher plants. Physiol. Plant. 70, 231–234.

    Article  Google Scholar 

  • Roessler P G and Nadler K D 1982 Effects of iron deficiency on heme biosynthesis in Rhizobium japonicum. J. Bacteriol. 149, 1021–1026.

    PubMed  CAS  Google Scholar 

  • Salinas P C, Tolmasky M E and Crosa J H 1989 Regulation of the iron uptake system in Vibrio anguillarum: Evidence for a cooperative effect between two transcriptional activators. Proc. Natl. Acad. Sci. USA 86, 3529–3533.

    Article  PubMed  CAS  Google Scholar 

  • Schwyn B and Neilands J B 1987a Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47–56.

    Article  PubMed  CAS  Google Scholar 

  • Schwyn B and Neilands K B 1987b Siderophores from agronomically important species of the Rhizobiaceae. Comments Agric. Food Chem. 1, 95–114.

    CAS  Google Scholar 

  • Skorupska A, Choma A, Derylo M and Lorkiewicz Z 1988 Siderophore containing 2,3-dihydroxybenzoic acid and threonine formed by Rhizobium trifolii. Acta Biochim. Pol. 35, 119–130.

    PubMed  CAS  Google Scholar 

  • Skorupska A, Derylo M and Lorkiewicz Z 1989 Siderophore production and utilization by Rhizobium trifolii. Biol. Metals 2, 45–49.

    Article  CAS  Google Scholar 

  • Smith M J and Neilands J B 1984 Rhizobactin, a siderophore from Rhizobium meliloti. J. Plant Nutr. 7, 449–458.

    Article  CAS  Google Scholar 

  • Smith M J and Neilands J B 1987 Rhizobactin, a structurally novel siderophore biochemically related to the opines. In Molecular Strategies For Crop Protection. Eds. C J Arntzen and C Ryan, pp 157–168. Alan R. Liss, Inc., New York.

    Google Scholar 

  • Smith M J, Shoolery J N, Schwyn B, Holden I and Neilands J B 1985 Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. J. Am. Chem. Soc. 107, 1739–1743.

    Article  CAS  Google Scholar 

  • Spiro S, Roberts R E and Guest J R 1989 FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expresison. Mol. Microbiol. 3, 601–608.

    Article  PubMed  CAS  Google Scholar 

  • Soerensen K U, Terry R E, Jolley V D, Brown J C and Vargas M E 1988 The interaction of iron-stress response and root nodules in iron efficient and inefficient soybeans. J. Plant Nutr. 1, 853–862.

    Article  Google Scholar 

  • Soerensen K U, Terry R E, Jolley V D and Brown J C 1989 Iron-stress response of inoculated and non-inoculated roots of an iron inefficient soybean cultivar in a split-root system. J. Plant Nutr. 12, 437–447.

    Article  CAS  Google Scholar 

  • Stoebner J A and Payne S M 1988 Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect. Immun. 56, 2891–2895.

    PubMed  CAS  Google Scholar 

  • Terry R E, Hartzook A, Jolley V D and Brown J C 1988 Interactions of iron nutrition and symbiotic nitrogen fixation in peanuts. J Plant Nutr. 11, 811–820.

    Article  CAS  Google Scholar 

  • Tiffin L O 1970 Translocation of iron citrate and phosphorus in xylem exudate of soybean. Plant Physiol. 45, 280–283.

    Article  PubMed  CAS  Google Scholar 

  • Trageser M and Unden G 1989 Role of cysteine residues and of metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration in Escherichia coli. Mol. Microbiol. 3, 593–599.

    Article  PubMed  CAS  Google Scholar 

  • Udvardi M K, Price G D, Gresshoff P M and Day D A 1988 A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett. 231, 36–40.

    Article  CAS  Google Scholar 

  • Van der Mark F and Van der Briel W 1985 Purification and partial characterization of ferritin from normal and ironloaded leaves of Phaseolus vulgaris. Plant Sci. 39, 55–60.

    Article  Google Scholar 

  • Verma D P S and Long S 1983 The molecular biology of Rhizobium-legume symbiosis. Int. Rev. Cytol. Suppl. 14, 211–245.

    CAS  Google Scholar 

  • Verma D P S, Kazazian V, Zogbi V and Bal A K 1978 Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules. J. Cell Biol. 78, 919–936.

    Article  PubMed  CAS  Google Scholar 

  • Winkelmann G 1979 Surface polymers and hydroxy acids: A model of iron supply in sideramine-free fungi. Arch. Microbiol. 121, 43–51.

    Article  CAS  Google Scholar 

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  1. Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

    M. L. Guerinot

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  1. Department of Soil and Water Sciences, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Y. Chen

  2. Department of Plant Pathology and Microbiology, Faculty of Agriculture, The Hebrew Universtiy of Jerusalem, Rehovot, 76100, Israel

    Y. Hadar

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Guerinot, M.L. (1991). Iron uptake and metabolism in the rhizobia/legume symbioses. In: Chen, Y., Hadar, Y. (eds) Iron Nutrition and Interactions in Plants. Developments in Plant and Soil Sciences, vol 43. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-3294-7_29

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  • DOI: https://doi.org/10.1007/978-94-011-3294-7_29

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