Advertisement

Plant and Soil

, Volume 165, Issue 2, pp 261–274 | Cite as

Strategies of plants for acquisition of iron

  • H. Marschner
  • V. Römheld
Article

Abstract

Two different types of root response to Fe deficiency (strategies) have been identified in species of the Plant Kingdom. In Strategy I which occurs in all plant species except grasses, a plasma membrane-bound reductase is induced with enhanced net excretion of protons. Often the release of reductants/chelators is also higher. In Strategy II which is confined to grasses, there is an increase in the biosynthesis and secretion of phytosiderophores which form chelates with FeIII. Uptake of FeIII phytosiderophores is mediated by a specific transporter in the plasma membrane of root cells of grasses. From results based mainly on long-term studies under non-axenic conditions this classification into two strategies has been questioned, and the utilization of Fe from microbial siderophores has been considered as an alternative strategy particularly in grasses. Possible reasons for controversial results are discussed in some detail. The numerous effects of microorganisms in non-axenic cultures, and the as yet inadequate characterization of the so-called standard (basic) reductase present major limitations to understanding different mechanisms of Fe acquisition. In comparison with the progress made in identifying the cellular mechanisms of root responses in Strategy I and Strategy II plants, our understanding is poor concerning the processes taking place in the apoplasm of root rhizodermal cells and of the role of low-molecular-weight root exudates and siderophores in Fe acquisition of plants growing in soils of differing Fe availability.

Key words

iron phytosiderophores root apoplasm root exudates siderophores standard reductase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alcàntara E and De LaGuardia M L 1991 Variability of sunflower inbred lines to iron deficiency stress. Plant and Soil 130, 93–96.CrossRefGoogle Scholar
  2. Askerlund P and Larsson C 1991 Transmembrane electron transport in plasma membrane vesicles loaded with an NADH-generating system or ascorbate. Plant Physiol. 96, 1178–1184.Google Scholar
  3. Bacic A, Harris P J and Stone B A 1988 Structure and function of plant cell walls. In The Biochemistry of Plants, Vol. 14. Carbohydrates. Ed. J Preiss. pp 297–358. Academic Press, San Diego, New York.Google Scholar
  4. Bar-Ness E, Chen Y, Hadar Y, Marschner H and Römheld V 1991 Siderophores of Pseudomonas putida as an iron source for dicot and monocot plants. In Iron Nutrition and Interactions in Plants. Eds. Y Chen and Y Hadar. pp 271–281. Kluwer Acad. Publishers, Dordrecht.Google Scholar
  5. Bar-Ness E, Hadar Y, Chen Y, Römheld V and Marschner H 1992a Short-term effects of rhizosphere microorganisms on Fe uptake from microbial siderophores by maize and oat. Plant Physiol. 100, 451–456.Google Scholar
  6. Bar-Ness E, Hadar Y, Chen Y, Shanzer A and Libman A 1992b Iron uptake by plants from microbial siderophores. A study with 7-nitrobenz-2 oxa-1,3-diazole-desferrioxamine as fluorescent ferrioxamine B analog. Plant Physiol. 99, 1329–1335.Google Scholar
  7. Bavaresco L, Fregoni M and Fraschini P 1991 Investigations on iron uptake and reduction by excised roots of different grapevine rootstocks and a V. vinifera cultivar. Plant and Soil 130, 109–113.CrossRefGoogle Scholar
  8. Bavaresco L, Fregoni M and Fugher C 1994 Effect of some biological methods to improve Fe-efficiency in grafted grapevine. Proc. 7th. Intern. Symp. on Iron Nutrition and Interactions in Plants. Ed. J Abadia. Kluwer Academic Publishers, Dordrecht.Google Scholar
  9. Bienfait H F 1985 Regulated redox processes at the plasmalemma of plant root cells and their function in iron uptake. J. Bioenerg. and Biomemb. 17, 73–83.CrossRefGoogle Scholar
  10. Bienfait F 1988 Prevention of stress in iron metabolism of plants. Acta Bot. Neerl. 38, 105–129.Google Scholar
  11. Bienfait F and Lüttge U 1988 On the function of two systems that can transfer electrons across the plasma membrane. Plant Physiol. Biochem. 26, 665–671.Google Scholar
  12. Brown J C and Jolley V D 1989 Plant metabolic responses to iron-deficiency stress. BioScience 39, 546–551.Google Scholar
  13. Brown J C, Jolley V D and Lytle C M 1991 Comparative evaluation of iron solubilizing substances (phytosiderophores) released by oats and corn: Iron-efficient and iron-inefficient plants. Plant and Soil 130: 157–163.CrossRefGoogle Scholar
  14. Brüggemann W and Moog P R 1989 NADH-dependent Fe3+ EDTA and oxygen reduction by plasma membrane vesicles from barley roots. Physiol. Plant. 75, 245–254.Google Scholar
  15. Brüggemann W, Moog P R, Nakagawa H, Janiesch P and Kuiper P J C 1991 Plasma membrane-bound NADH: Fe3+-EDTA reductase and iron deficiency in tomato (Lycopersicum esculentum). Is there a Turbo reductase? Physiol. Plant. 79, 339–346.CrossRefGoogle Scholar
  16. Buckhout T J, Bell P F, Luster D G and Chaney R L 1989 Iron-stress induced redox activity in tomato (Lycopersicum esculentum Mill.) is localized on the plasma membrane. Plant Physiol. 90, 151–156.Google Scholar
  17. Cakmak I, van deWetering D A M, Marschner H and Bienfait H F 1987 Involvement of superoxide radical in extracellular ferric reduction by iron-deficient bean roots. Plant Physiol. 85, 310–314.Google Scholar
  18. Chaney R L and Bell P F 1987 Complexity of iron nutrition: Lessons for plant-soil interaction research. J. Plant Nutr. 10, 963–994.Google Scholar
  19. Chaney R L, Chen Y, Green C E, Holden M J, Bell P F, Luster D G and Angle J S 1992 Root hairs on chlorotic tomatoes are an effect of chlorosis rather than part of the adaptive Fe-stress-response. J. Plant Nutr. 15, 1857–1875.Google Scholar
  20. Clark R B, Römheld V and Marschner H 1988 Iron uptake and phytosiderophore release by roots of sorghum genotypes. J. Plant Nutr. 11, 663–676.Google Scholar
  21. Cress W A, Johnson G V and Barton L L 1986 The role of endomycorrhizal fungi in iron uptake by Hilaria jamesii. J. Plant Nutr. 9, 547–556.Google Scholar
  22. Crowley D E, Wang Y C, Reid C P P and Szaniszlo P J 1991 Mechanisms of iron acquisition from siderophores by microorganisms and plants. Plant and Soil 130, 179–198.CrossRefGoogle Scholar
  23. Crowley D E, Römheld V, Marschner H and Szaniszlo P J 1992 Root-microbial effects on plant iron uptake from siderophores and phytosiderophores. Plant and Soil 142, 1–7.Google Scholar
  24. Crowley D E, Reid C P P and Szaniszlo P J 1988 Utilization of microbial siderophores in iron acquisition by oat. Plant Physiol. 87, 680–685.Google Scholar
  25. Drechsel H, Metzger J, Freund S, Jung G, Boelaert J R and Winkelmann G 1991 Rhizoferrin—a novel siderophore from the fungus Rhizopus microsporus var. rhizopodiformis. Biol. Metals 4, 238–243.CrossRefGoogle Scholar
  26. Evans P T and Malmberg R L 1989 Do polyamines have roles in plant development? Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 235–269.Google Scholar
  27. Federico R, Cona A, Angelini R, Schinia M E and Giartosio A 1990 Characterization of maize polyamine oxidase. Phytochemistry 29, 2411–2414.CrossRefPubMedGoogle Scholar
  28. Fleming A L, Chaney R L and Coulombe B A 1984 Bicarbonate inhibits Fe-stress response and Fe uptake-translocation of chlorosis-susceptible soybean cultivars. J. Plant Nutr. 7, 699–714.Google Scholar
  29. Ganmore-Neumann R, Bar-Yosef B, Shanzer A and Libman J 1992 Enhanced iron (Fe) uptake by synthetic siderophores in corn roots. J. Plant Nutr. 15, 1027–1037.Google Scholar
  30. Gries D and Runge M 1992 The ecological significance of iron mobilization in wild grasses. J. Plant Nutr. 15, 1727–1737.Google Scholar
  31. Hartmann A 1988 Ecophysiological aspects of growth and nitrogen fixation in Azospirillum sp. Plant and Soil 110, 225–238.Google Scholar
  32. Haselwandter K, Dobernigg B, Beck W, Jung G, Cansier A and Winkelmann A 1992 Isolation and identification of hydroxamate siderophores of ericoid mycorrhizal fungi. Biol. Metals 5, 51–56.Google Scholar
  33. Holden M J, Luster D G, Chaney R L, Buckhout T J and Robinson C J 1991 Fe3+ chelate reductase activity of plasma membranes isolated from tomato (Lycopersicon esculentum Mill.) roots. Comparison of enzymes from Fe-deficient and Fe-sufficient roots. Plant Physiol. 97, 537–544.Google Scholar
  34. Holden M J, Luster D G, Chaney R L and Buckhout T J 1992 Enzymology of ferric chelate reduction at the root plasma membrane. J. Plant Nutr. 15, 1667–1678.Google Scholar
  35. Hopkins B G, Jolley V D and Brown J C 1992 Plant utilization of iron solubilized by oat phytosiderophore. J. Plant Nutr. 15, 1599–1612.Google Scholar
  36. Inskeep W P and Bloom P R 1986 Effect of soil moisture on soil pCO2, soil solution bicarbonate, and iron chlorosis in soybeans. Soil Sci. Soc. Am. J. 50, 946–952.Google Scholar
  37. Inskeep W P and Bloom P R 1987 Soil chemical factors associated with soybean chlorosis in Calciaquolls of Western Minnesota. Agron. J. 79, 779–786.Google Scholar
  38. Jolley V D and Brown J C 1987 Soybean response to iron-deficiency stress as related to iron supply in the growth medium. J. Plant Nutr. 10, 637–651.Google Scholar
  39. Jolley V D, Fairbanks D J, Stevens W B, Terry R E and Orf J H 1992 Root iron-reduction capacity for genotypic evaluation of iron efficiency in soybean. J. Plant Nutr. 15, 1679–1690.Google Scholar
  40. Jurkevitch E, Hadar Y and Chen Y 1986 The remedy of lime-induced chlorosis in peanuts by Pseudomonas sp. siderophores. J. Plant Nutr. 9, 535–545.Google Scholar
  41. 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.Google Scholar
  42. Kawai S, Takagi S and Sato Y 1988 Mugineic acid-family phytosiderophores in root-secretions of barley, corn and sorghum varieties. J. Plant Nutr. 11, 633–642.Google Scholar
  43. Loeppert R H and Hallmark C T 1985 Indigenous soil properties influencing the availability of iron in calcareous soils. Soil Sci. Soc. Am. J. 49, 597–603.Google Scholar
  44. Loomis W D and Durst R W 1991 Boron and cell walls. Curr. Top. Plant Biochem. Physiol. 10, 149–178.Google Scholar
  45. Lytle C M and Jolley V D 1991 Iron deficiency stress response of various C-3 and C-4 grain crop genotypes: Strategy II mechanism evaluated. J. Plant Nutr. 14, 341–362.Google Scholar
  46. Lytle C M, Jolley V D and Brown J C 1991 Iron-efficient and iron-inefficient oats and corn respond differently to iron-deficiency stress. Plant and Soil 130, 165–172.CrossRefGoogle Scholar
  47. Manthey J A, McCoy D L and Crowley D E 1993 Chelation effects on the iron reduction and uptake by low-iron stress tolerant and non-tolerant citrus rootstocks. J. Plant Nutr. 16, 881–893.Google Scholar
  48. Marschner H 1991 Symposium summary and future research areas. In Iron Nutrition and Interactions in Plants. Eds. Y Chen and Y Hadar. pp 365–372. Kluwer Academic Publishers, Dordrecht.Google Scholar
  49. Marschner H, Römheld V and Kissel M 1986 Different strategies in higher plants in mobilization and uptake of iron. J. Plant Nutr. 9, 695–713.Google Scholar
  50. Marschner H, Treeby M and Römheld V 1989 Role of root-induced changes in the rhizosphere for iron acquisition in higher plants. Z. Pflanzenernaehr. Bodenkd. 152, 197–204.Google Scholar
  51. McCray J M and Matocha J E 1992 Effect of soil water levels on solution bicarbonate, chlorosis and growth of sorghum. J. Plant Nutr. 15, 1877–1890.Google Scholar
  52. Mori S and Nishizawa N 1989 Identification of barley chromosome No. 4, possible encoder of genes of mugineic acid synthesis from 2′-deoxymugineic acid using wheat-barley addition lines. Plant Cell Physiol. 30, 1057–1061.Google Scholar
  53. Mori S, Nishizawa N, Hayashi H, Chino M, Yoshimura E and Ishihara J 1991 Why are young rice plants highly susceptible to iron deficiency? Plant and Soil 130, 143–156.CrossRefGoogle Scholar
  54. Morris D R, Loeppert R H and Moore T J 1990 Indigenous soil factors influencing iron chlorosis of soybean in calcareous soils. Soil Sci. Soc. Am. J. 54, 1329–1336.Google Scholar
  55. Nelson S D 1992 Response of several wildland shrubs and forbs of arid regions to iron-deficiency stress. J. Plant Nutr. 15, 2015–2023.Google Scholar
  56. Nelson M, Cooper C R, Crowley D E, Reid C P P and Szaniszlo P J 1988 An Escherichia coli bioassay of individual siderophores in soil. J. Plant Nutr. 11, 915–924.Google Scholar
  57. Nishizawa N and Mori S 1987 The particular vesicle appearing in the barley root cells and its relation to mugineic acid secretion. J. Plant Nutr. 10, 1013–1020.Google Scholar
  58. Okumura N, Nishizawa N K, Umehara Y and Mori S 1991 An iron deficiency-specific cDNA from barley roots having two homologous cysteine-rich MT domains. Plant Mol. Biol. 17, 531–533.CrossRefPubMedGoogle Scholar
  59. Onyezili F N and Ross J D 1993 Iron deficiency stress responses of five graminaceous monocots. J. Plant Nutr. 16, 953–974.Google Scholar
  60. Römheld V and Kramer D 1983 Relationship between proton efflux and rhizodermal transfer cells induced by iron deficiency. Z. Pflanzenphysiol. 113, 73–83.Google Scholar
  61. Römheld V 1987 Existence of two different strategies for the acquisition of iron in higher plants. In Iron Transport in Microbes, Plant and Animals. Eds. G Winkelmann, D Van der Helm and J B Neilands. pp 353–374. VCH Verlag Weinheim, FRG.Google Scholar
  62. Römheld V 1991 The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: An ecological approach. Plant and Soil 130, 127–134.CrossRefGoogle Scholar
  63. Römheld V and Kramer D 1983 Relationship between proton efflux and rhizodermal transfer cells induced by iron deficiency. Z. Pflanzenphysiol. 113, 73–83.Google Scholar
  64. Römheld V and Marschner H 1986 Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175–180.Google Scholar
  65. Römheld V and Marschner H 1990 Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores. Plant and Soil 123, 147–153.CrossRefGoogle Scholar
  66. Romera F J, Alcantara E and de laGuardia M D 1992 Effects of bicarbonate, phosphate and high pH on the reducing capacity of Fe-deficient sunflower and cucumber plants. J. Plant Nutr. 15, 1519–1530.Google Scholar
  67. Shaw G, Leake J R, Baker A J M and Read D J 1990 The biology of mycorrhiza in the Ericaceae. XVII. The role of mycorrhizal infection in the regulation of iron uptake by ericaceous plants. New Phytol. 115, 251–258.Google Scholar
  68. Shenker M, Oliver I, Helmann M, Hadar Y and Chen Y 1992 Utilization by tomatoes of iron mediated by a siderophore produced by Rhizopus arrhizus. J. Plant Nutr. 15, 2173–2182.Google Scholar
  69. Singh K, Chino M, Nishizawa N K, Goto S, Nakanishi T, Takagi S and Mori S 1992 Iron extraction efficacy of plant borne mugineic acid family phytosiderophores in Indian calcareous soils. J. Plant Nutr. 15, 1625–1645.Google Scholar
  70. Siqueira J O, Nair M G, Hammerschmidt R and Safir G R 1991 Significance of phenolic compounds in plant-soil-microbial systems. Crit. Rev. Plant Sci. 10, 63–121.Google Scholar
  71. Shojima S, Nishizawa N K, Fushiya S, Nozoe S, Kumashiro, Nagata T, Ohata T and Mori S 1989 Biosynthesis of nicotianamine in the suspension-cultured cells of tobacco (Nicotiana megalosiphon). Biol. Metals 2, 142–145.CrossRefGoogle Scholar
  72. Schmidt W 1993 Iron stress-induced redox reactions in bean roots. Physiol. Plant. 89, 448–452.CrossRefGoogle Scholar
  73. Scholz G, Becker R, Pich A and Stephan U W 1992 Nicotianamine — a common constituent of Strategy I and II of iron acquisition by plants: a review. J. Plant Nutr. 15, 1647–1665.Google Scholar
  74. Takagi S, Kamei S and Ming-HoYu 1988 Efficiency of iron extraction from soil by mugineic acid family phytosiderophores. J. Plant Nutr. 11, 643–651.Google Scholar
  75. Takagi S, Nomoto K and Takemoto T 1984 Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J. Plant Nutr. 7, 469–477.Google Scholar
  76. Treeby M and Uren N 1993 Iron deficiency stress response amongst citrus rootstocks. Z. Pflanzenernaehr. Bodenkd. 156, 8581.Google Scholar
  77. Treeby M, Marschner H and Römheld V 1989 Mobilization of iron and other micronutrients from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant and Soil 114, 217–226.Google Scholar
  78. Watanabe S, Matsumoto S and Wada H 1990 Microbial decomposition of mugineic acids — a new aspect of relation between plant and microorganisms. In Transactions 14th Intern. Congr. Soil Science, Kyoto, Vol. III, pp 272–273.Google Scholar
  79. Winkelmann G 1992 Structures and functions of fungal siderophores containing hydroxamate and complexane type iron binding ligands. Mycol. Res. 96, 529–534.Google Scholar
  80. Wirén Nvon, Römheld V, Morel J L, Guckert A and Marschner H 1993 Influence of microorganisms on iron acquisition in maize. Soil Biol. Biochem. 25, 371–376.CrossRefGoogle Scholar
  81. Zhang F, Römheld V and Marschner H 1991 Role of the root apoplasm for iron acquisition by wheat plants. Plant Physiol. 97, 1302–1305.Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • H. Marschner
    • 1
  • V. Römheld
    • 1
  1. 1.Institut für Pflanzenernährung (330)Universität HohenheimStuttgartGermany

Personalised recommendations