Plant and Soil

, Volume 329, Issue 1–2, pp 1–25 | Cite as

Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition

  • Stefano CescoEmail author
  • Guenter Neumann
  • Nicola Tomasi
  • Roberto Pinton
  • Laure Weisskopf
Marschner Review


Plants release a multitude of organic compounds into the rhizosphere, some of which are flavonoids. These products of secondary metabolism are mainly studied for their antioxidant properties and for their role in the establishment of rhizobium-legume symbiosis; however, it has been recently demonstrated that flavonoids can also affect nutrient availability through soil chemical changes. This review will give an overview of the types and amounts of flavonoids released by roots of different plant species, as well as summarize the available knowledge on root exudation mechanisms. Subsequently, factors influencing their release will be reported, and the methodological approaches used in the literature will be critically described. Finally, the direct contribution of plant-borne flavonoids on the nitrogen, phosphorous and iron availability into the rhizosphere will be discussed.


Nutrient availability Nitrogen Phosphorous Iron Root exudates Transmembrane transport 



We would like to thank Dr. Kirsty Agnoli for English corrections and Prof. Hans Lambers (University of Western Australia) for his critical revision of the manuscript which also greatly benefited from the detailed and constructive criticisms of four anonymous reviewers. Research was supported by grant from Italian M.U.R.S.T.


  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Amann C, Amberger A (1988) Verringerung der Phosphatsorption durch Zusatz organischer Verbindungen zu Böden in Abhängigkeit vom pH Wert. Z Pflanzenernahr Bodenkd 151:41–46CrossRefGoogle Scholar
  3. Armero J, Requejo R, Jorrin J, Lopez-Valbuena R, Tena M (2001) Release of phytoalexins and related isoflavonoids from intact chickpea seedlings elicited with reduced glutathione at root level. Plant Physiol Biochem 39:785–795CrossRefGoogle Scholar
  4. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  5. Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008a) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179:209–223PubMedCrossRefGoogle Scholar
  6. Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Pena C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz F, Vivanco JM (2008b) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146:762–771PubMedCrossRefGoogle Scholar
  7. Bécard G, Douds D, Pfeffer P (1992) Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825PubMedGoogle Scholar
  8. Bécard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW (1995) Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbioses. Mol Plant Microbe Interact 8:252–258Google Scholar
  9. Bienfait HF (1985) Regulated redox processes at the plasmalemma of plant root cells and their function in iron uptake. J Bioenerg Biomembranes 17:73–83CrossRefGoogle Scholar
  10. Bienfait HF, Van den Briel W, Mesland-Mul NT (1985) Free space iron pools in roots: generation and mobilization. Plant Physiol 78:596–600PubMedCrossRefGoogle Scholar
  11. Bolanos-Vásquez MC, Werner D (1997) Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv phaseoli on nod gene-inducing flavonoids in root extracts of Phaseolus vulgaris. Mol Plant Microbe Interact 10:339–346CrossRefGoogle Scholar
  12. Bors W, Heller W, Michel C, Saran M (1990) Flavonoids as antioxidants: determination of radical-scavenging efficiencies. Methods Enzymol 186:343–355PubMedCrossRefGoogle Scholar
  13. Brown MH, Paulsen IT, Skurray RA (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:393–401CrossRefGoogle Scholar
  14. Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant-Microb Interact 13:693–698CrossRefGoogle Scholar
  15. Cakmak I, Marschner H (1988) Increase in membrane permeability and exudation in roots of zinc deficient plants. J Plant Physiol 132:356–361Google Scholar
  16. Chang C, Suzuki A, Kumai S, Tamura S (1969) Chemical studies on “clover sickness.” II. Biological functions of isoflavonoids and their related compounds. Agric Biol Chem 33:398–408Google Scholar
  17. Chobot V, Huber C, Trettenhahn G, Hadacek F (2009) (±)-catechin: chemical weapon, antioxidant, or stress regulator? J Chem Ecol 35:980–996PubMedCrossRefGoogle Scholar
  18. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365PubMedCrossRefGoogle Scholar
  19. Cornell RM, Schwertmann U (2003) The iron oxides, 2nd edn. Wiley-VCH, WeinheimGoogle Scholar
  20. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) An iron-regulated maize gene involved in high affinity [FeIII] transport. Nature 409:346–349PubMedCrossRefGoogle Scholar
  21. D’Arcy-Lameta (1986) Study of soybean and lentil root exudates. II. Identification of some polyphenolic compounds, relation with plantlet physiology. Plant Soil 92:113–123CrossRefGoogle Scholar
  22. Deiana S, Pilo MI, Premoli A, Senette C, Solinas V, Gessa G (2003) Interaction of oxidation products from caffeic acid with Fe(III) and Fe(II). J Plant Nutr 26:1909–1926CrossRefGoogle Scholar
  23. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Lett 581:2255–2262PubMedCrossRefGoogle Scholar
  24. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200Google Scholar
  25. Dinkelaker B, Hengeler C, Neumann G, Eltrop L, Marschner H (1997) Root exudates and mobilization of nutrients. In: Rennenberg H, Eschrich W, Ziegler H (eds) Trees—contributions to modern tree physiology. Backhuys, Leiden, pp 441–452Google Scholar
  26. Eckhardt NA (2006) The role of flavonoids in root nodule development and auxin transport in Medicago truncatula. Plant Cell 18:1539–1540CrossRefGoogle Scholar
  27. El Hajji H, Nkhili E, Tomao V, Dangles O (2006) Interactions of quercitin with iron and copper ions: complexation and autoxidation. Free Radic Res 40:303–320PubMedCrossRefGoogle Scholar
  28. El-Baz FK, Mohamed AA, Aboul-Enein AM, Salama ZA (2004) Alteration in root exudates level during Fe-deficiency in two cucumber cultivars. Int J Agric Biol 6:45–48Google Scholar
  29. Engels C, Neumann G, Gahoonia T, George E, Schenk M (2000) Assessment of the ability of roots for nutrient acquisition. In: Smit AL, Bengough AG, Engels C, Van Noordwijk M, Pellerin S, Van de Geijn SC (eds) Root methods. A handbook. Springer, Heidelberg, pp 403–459Google Scholar
  30. Frangne N, Eggmann T, Koblischke C, Weissenbock G, Martinoia E, Klein M (2002) Flavone glucoside uptake into barley mesophyll and arabidopsis cell culture vacuoles. Energization occurs by H+-antiport and ATP-binding cassette-type mechanisms. Plant Physiol 128:726–733PubMedCrossRefGoogle Scholar
  31. Gagnon H, Ibrahim RK (1997) Effects of various elicitors on the accumulation and secretion of isoflavonoids in white lupin. Phytochemistry 44:1463–1467CrossRefGoogle Scholar
  32. Gagnon H, Seguin J, Ernst Bleichert E, Tahara S, Ibrahim RK (1992) Biosynthesis of white lupin isoflavonoids from [U-14C]L-phenylalanine and their release into the culture medium. Plant Physiol 100:76–79PubMedCrossRefGoogle Scholar
  33. Gardner WK, Parbery DG, Barber DA (1982) The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil/root interface. Plant Soil 68:19–32CrossRefGoogle Scholar
  34. Gardner WK, Parbery DG, Barber DA (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 Soil 70:107–124CrossRefGoogle Scholar
  35. Gerke J, Römer W, Jungk A (1994) The excretion of citric and malic acid by proteoid roots of Lupinus albus L., effects on soil solution concentrations of phosphate, iron, and aluminium in the proteoid rhizosphere in samples of an Oxisol and a Luvisol. Z Pflanzenernahr Bodenkd 155:339–343CrossRefGoogle Scholar
  36. Gerke J, Beißner L, Römer W (2000a) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. J Plant Nutr Soil Sci 163:207–212CrossRefGoogle Scholar
  37. Gerke J, Römer W, Beißner L (2000b) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. II. The importance of soil and plant parameters for uptake of mobilized P. J Plant Nutr Soil Sci 163:213–219CrossRefGoogle Scholar
  38. Gollany HT, Schumacher TE, Rue RR, Liu SY (1993) A carbon dioxide microelectrode for in situ pCO2 measurement. Microchem J 48:42–49CrossRefGoogle Scholar
  39. Gomez C, Terrier N, Torregrosa L, Gomez C, Vialet S, Fournier-Level A, Verries C, Souquet JM, Mazauric JP, Klein M, Cheynier V, Ageorges A (2009) Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol 150:402–415PubMedCrossRefGoogle Scholar
  40. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826PubMedCrossRefGoogle Scholar
  41. Graham TL (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603PubMedCrossRefGoogle Scholar
  42. Guerinot ML, Ying Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820PubMedGoogle Scholar
  43. Haase S, Neumann G, Kania A, Kuzyakov Y, Römheld V, Kandeler E (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221CrossRefGoogle Scholar
  44. Hagström J, James WM, Skene KR (2001) A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil 232:81–90CrossRefGoogle Scholar
  45. Hartley A, Barger N, Belnap J, Okin GS (2007) Dryland Ecosystems. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Springer-Verlag, Berlin, pp 271–308CrossRefGoogle Scholar
  46. Hiltner L (1904) Uber neuere erfahrungen und problem auf dem gebeit der bodenbakteriologie und unter besonderer berucksichtigung der grundungung und brache. Arb Deutsche Landwirsch Ges 98:59–78Google Scholar
  47. Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origin of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59CrossRefGoogle Scholar
  48. Hofmann A, Wittenmayer L, Arnold G, Schieber A, Merbach W (2009) Root exudation of phloridzin by apple seedlings (Malus x domestica Borkh.) with symptoms of apple replant disease. J Appl Bot Food Quality 82:193–198Google Scholar
  49. Hughes M, Donnelly C, Crozier A, Wheeler CT (1999) Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Can J Bot 77:1311–1315CrossRefGoogle Scholar
  50. Hungria M, Joseph CM, Phillips DA (1991) Rhizobium-nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris). Plant Physiol 97:759–764PubMedCrossRefGoogle Scholar
  51. Isobe K, Tateishi A, Nomura K, Inoue H, Tsuboki Y (2001) Flavonoids in the extract and exudate of the roots of leguminous crops. Plant Prod Sci 4:278–279CrossRefGoogle Scholar
  52. Iwashina T (2003) Flavonoid function and activity to other plants and microorganisms. Bol Sci Space 17:24–44CrossRefGoogle Scholar
  53. Jasinski M, Ducos E, Martinoia E, Boutry M (2003) The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177PubMedCrossRefGoogle Scholar
  54. Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144:278–285PubMedCrossRefGoogle Scholar
  55. Kalinova J, Vrchotova N, Triska J (2007) Exudation of allelopathic substances in buckwheat (Fagopyrum esculentum Moench). J Agric Food Chem 55:6453–6459PubMedCrossRefGoogle Scholar
  56. Kape R, Parniske M, Brandt S, Werner D (1992a) Isoliquiritigenin, a strong nod gene-inducing and glyceollin resistance-inducing flavonoid from soybean root exudates. Appl Environ Microbiol 58:1705–1710PubMedGoogle Scholar
  57. Kape R, Wex K, Parniske M, Görge E, Wetzel A, Werner D (1992b) Legume root metabolites and VA-mycorrhiza development. J Plant Physiol 141:54–60Google Scholar
  58. Kidd PS, Llugany M, Poschenrieder C, Gunsé B, Barceló J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352PubMedCrossRefGoogle Scholar
  59. Klein M, Martinoia E, Hoffmann-Thoma G, Weissenbock G (2000) A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J 21:289–304PubMedCrossRefGoogle Scholar
  60. Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580:1112–1122PubMedCrossRefGoogle Scholar
  61. Kneer R, Poulev AA, Olesinski A, Raskin I (1999) Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L. J Exp Bot 50:1553–1559CrossRefGoogle Scholar
  62. Kraemer SM, Crowley DE, Kretzschmar R (2006) Geochemical aspects of phytosiderophores-promoted iron acquisition by plants. Adv Agron 91:1–46CrossRefGoogle Scholar
  63. Lane GA, Biggs D, Sutherland ORW, Skipp RA (1987) Isoflavonoids as feeding deterrents and antifungal components from root of Lupinus angustifolius. J Chem Ecol 13:771–783CrossRefGoogle Scholar
  64. Larose G, Chênevert R, Moutoglis P, Gagné S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339CrossRefGoogle Scholar
  65. Leon-Barrios M, Dakora FD, Joseph CM, Phillips DA (1993) Isolation of rhizobium meliloti nod gene inducers from alfalfa rhizosphere soil. Appl Environ Microbiol 59:636–639PubMedGoogle Scholar
  66. Lindsay WL (1979) Chemical equilibria in soils. Wiley, ChuchesterGoogle Scholar
  67. Lindsay WL (1991) Inorganic equilibria affecting micronutrients in soils. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture. Soil Science Society of America Inc, Madison, pp 89–112Google Scholar
  68. Loper JE, Buyer JS (1991) Siderophores in microbial interactions on plant surphases. Mol Plant Microbe Interact 4:5–13Google Scholar
  69. Loyola-Vargas VM, Broeckling CD, Badri D, Vivanco JM (2007) Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta 225:301–310PubMedCrossRefGoogle Scholar
  70. Lu Y, Irani NG, Grotewold E (2005) Covalent attachment of the plant natural product naringenin to small glass and ceramic beads. BMC Chem Biol 5:3–12PubMedCrossRefGoogle Scholar
  71. Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit Rev Plant Sci 24:267–281CrossRefGoogle Scholar
  72. Malinowski DP, Alloush GA, Belesky DP (1998) Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 205:1–12CrossRefGoogle Scholar
  73. Malinowski DP, Zuo H, Belesky DP, Alloush GA (2004) Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. fungal endophytes. Plant Soil 267:1–12CrossRefGoogle Scholar
  74. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038PubMedCrossRefGoogle Scholar
  75. Marschner H (1988) Mechanism of manganese acquisition by roots from soils. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer Academic, Dordrecht, pp 191–204Google Scholar
  76. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  77. Martin FM, Perotto S, Bonfante P (2001) In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 263–296Google Scholar
  78. Masaoka Y, Kojima M, Sugihara S, Yoshihara T, Koshino M, Ichihara A (1993) Dissolution of ferric phosphate by alfalfa (Medicago sativa L.) root exudates. Plant Soil 155(156):75–78CrossRefGoogle Scholar
  79. Massonneau A, Langlade N, Leon S, Smutny J, Vogt E, Neumann G, Martinoia E (2001) Metabolic changes associated with cluster root development in white lupin (Lupinus albus L.): relationship between organic acid excretion, sucrose metabolism and energy status. Planta 213:534–542PubMedCrossRefGoogle Scholar
  80. Maxwell CA, Phillips DA (1990) Concurrent synthesis and release of nod-gene-inducing flavonoids from alfalfa roots. Plant Physiol 93:1552–1558PubMedCrossRefGoogle Scholar
  81. Mira L, Fernandez MT, Santos M, Rocha R, Florencio MH, Jennings KR (2002) Interactions of flavonoids with iron and copper ions: a mechanism for their antioxidant activity. Free Radic Res 36:1199–1208PubMedCrossRefGoogle Scholar
  82. Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153PubMedCrossRefGoogle Scholar
  83. Neumann G (2006) Collection of root exudates and rhizosphere soil solution from soil-grown plants. In: Luster J, Finlay R (eds) Handbook of methods used in rhizosphere research. Swiss Federal Research Institute WSL, Birmensdorf, pp 317–318Google Scholar
  84. Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167PubMedCrossRefGoogle Scholar
  85. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. CRC, Boca Raton, pp 23–72Google Scholar
  86. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorous deficiency during proteoid root development in white lupin. Planta 208:373–382CrossRefGoogle Scholar
  87. Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot 85:909–920CrossRefGoogle Scholar
  88. Neumann G, George TS, Plassard C (2009) Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant Soil 321:431–456CrossRefGoogle Scholar
  89. Olsen RA, Bennett JH, Blume D, Brown JC (1981) Chemical aspects of the Fe stress response mechanism in tomatoes. J Plant Nutr 3:905–921CrossRefGoogle Scholar
  90. Pandya S, Iyer P, Gaitonde V, Parekh T, Desai A (1999) Chemotaxis of rhizobium SP.S2 towards Cajanus cajan root exudate and its major components. Curr Microbiol 38:205–209PubMedCrossRefGoogle Scholar
  91. Perry LG, Alford ER, Horiuchi J, Paschke MW, Vivanco JM (2007) Chemical signals in the rhizosphere: root-root and root-microbe communication. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC, Boca Raton, pp 297–330Google Scholar
  92. Pislewska M, Bednarek P, Stobiecki M, Wojtaszek P (2002) Cell wall-associated isoflavonoids and ss-glucosidase activity in Lupinus albus plants responding to environmental stimuli. Plant Cell Environ 25:29–40CrossRefGoogle Scholar
  93. Plaxton WC (1998) Metabolic aspects of phosphate starvation in plants. In: Lynch JP, Deikman L (eds) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes. Am Soc Plant Physiol, pp 229–238Google Scholar
  94. Pueppke SG, Bolanos-Vasquez MC, Werner D, Bec-Ferte MP, Prome JC, Krishnan HB (1998) Release of flavonoids by the soybean cultivars McCall and Peking and their perception as signals by the nitrogen-fixing symbiont Sinorhizobium fredii. Plant Physiol 117:599–608PubMedCrossRefGoogle Scholar
  95. Rao AS (1990) Root flavonoids. Bot Rev 56:1–84CrossRefGoogle Scholar
  96. Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in rhizobium. Nature 323:632–635CrossRefGoogle Scholar
  97. 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 276:115–132CrossRefGoogle Scholar
  98. Rengel Z, Gutteridge R, Hirsch P, Hornby D (1996) Plant genotype, micronutrient fertilization and take-all colonization influence bacterial populations in the rhizosphere of wheat. Plant Soil 183:269–277CrossRefGoogle Scholar
  99. 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 99:183–225CrossRefGoogle Scholar
  100. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697PubMedCrossRefGoogle Scholar
  101. Römheld V, Marschner H (1986) Mobilization of iron in the rhizosphere of different plant species. Adv Plant Nutr 2:155–204Google Scholar
  102. Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193PubMedCrossRefGoogle Scholar
  103. Schmidt PE, Broughton WJ, Werner D (1994) Nod factors of Bradyrhizobium japonicum and I NGR234 induce flavonoid accumulation in soybean root exudate. Mol Plant Microbe Interact 7:384–390Google Scholar
  104. Schwab AP, Lindsay WL (1989) A computer simulation of Fe(III) and Fe(II) complexation in nutrient solution. II. Exp Soil Sci Am J 53:34–38CrossRefGoogle Scholar
  105. Smit AL, Bengough AG, Engels C, Van Noordwijk M, Pellerin S, Van de Geijn SC (2000) Root methods. A handbook. Springer, HeidelbergGoogle Scholar
  106. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, New YorkGoogle Scholar
  107. Steele HL, Werner D, Cooper JE (1999) Flavonoids in seed and root exudates of Lotus pedunculatus and their biotransformation by Mesorhizobium loti. Physiol Plant 107:251–258CrossRefGoogle Scholar
  108. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306PubMedCrossRefGoogle Scholar
  109. Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-Rhizobium symbiosis. Plant Physiol 144:2000–2008PubMedCrossRefGoogle Scholar
  110. Suominen L, Luukkainen R, Roos C, Lindstrom K (2003) Activation of the nodA promoter by the nodD genes of Rhizobium galegae induced by synthetic flavonoids or Galega orientalis root exudate. FEMS Microbiol Lett 219:225–232PubMedCrossRefGoogle Scholar
  111. Susin S, Abadia J, Sàanchez-Beyes JA, Peleato ML, Abadia A, Gelpi E, Abadia J (1993) Riboflavin 3′- and 5′ sulphate, two novel flavins accumulating in the roots of iron-deficient sugar beet (Beta vulgaris). J Biol Chem 268:20958–20965PubMedGoogle Scholar
  112. Susin S, Abian J, Paleato ML, Sanchez-Baeza F, Abadia A, Gelpi E, Abadia J (1994) Flavin excretion from roots of iron-deficient sugar beet (Beta vulgaris L). Planta 193:514–519CrossRefGoogle Scholar
  113. Tamura S, Chang C, Suzuki A, Kumai S (1969) Chemical studies on “clover sickness.” I. Isolation and structural elucidation of two new isoflavonoids in red clover. Agric Biol Chem 33:391–397Google Scholar
  114. Tang CS, Young CC (1982) Collection and identification of allelopathic compounds from the undisturbed root system of bigalte lompograss (Hemarthia altissima). Plant Physiol 69:155–161PubMedCrossRefGoogle Scholar
  115. Timonin MI (1946) Mircoflora of the rhizosphere in relation to the manganese-deficiency disease of oats. Proc Soil Sci Soc Am 11:284–292Google Scholar
  116. Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New YorkGoogle Scholar
  117. Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40:1971–1974CrossRefGoogle Scholar
  118. Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465–475PubMedCrossRefGoogle Scholar
  119. Treeby M, Uren N (1993) Iron deficiency stress responses amongst citrus rootstocks. J Plant Nutr Soil Sci 156:75–81CrossRefGoogle Scholar
  120. Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591PubMedCrossRefGoogle Scholar
  121. Tsanuo MK, Hassanali A, Hooper AM, Khan Z, Kaberia F, Pckette JA, Wadhams LJ (2003) Isoflavanones from the allelopathic aqueous root exudate of Desmodium uncinatum. Phytochemistry 64:265–273PubMedCrossRefGoogle Scholar
  122. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to P deficiency. Plant Physiol 131:1064–1079PubMedCrossRefGoogle Scholar
  123. van Hees PAW, Lundström US (2000) Equilibrium models of alluminium and iron complexation with different organic acids in soil solution. Geoderma 94:201–221CrossRefGoogle Scholar
  124. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397PubMedCrossRefGoogle Scholar
  125. von Wiren 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 106:71–77Google Scholar
  126. von Wiren N, Khodr H, Hider RC (2000) Hydroxylated phytosiderophores species possess an enhanced chelate stability and affinity for iron(III). Plant Physiol 124:1149–1157CrossRefGoogle Scholar
  127. Walker T, Bias H, Grotewold E, Vivanco J (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedCrossRefGoogle Scholar
  128. Weisskopf L, Tomasi N, Santelia D, Martinoia E, Langlade NB, Tabacchi R, Abou-Mansour E (2006a) Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage. New Phytol 171:657–668PubMedGoogle Scholar
  129. Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006b) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927PubMedCrossRefGoogle Scholar
  130. Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82CrossRefGoogle Scholar
  131. Werner D (2001) Organic signals between plants and microorganisms. In: Pinton R, Varanini Z, Nannipieri Z (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 197–222Google Scholar
  132. Werner D (2007) Molecular biology and physiology of the rhizobia-legume symbiosis. In: Pinton R, Varanini Z, Nannipieri Z (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC, Boca Raton, pp 237–266Google Scholar
  133. Wojtaszek P, Stobiecki M, Gulewicz K (1993) Role of nitrogen and plant growth regulators in the exudation and accumulation of isoflavonoids by roots of intact white lupin (Lupinus albus L.) plants. J Plant Physiol 142:689–694Google Scholar
  134. Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307PubMedCrossRefGoogle Scholar
  135. 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
  136. Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136:3771–3783PubMedCrossRefGoogle Scholar
  137. Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 21:2323–2340PubMedCrossRefGoogle Scholar
  138. Zheng SJ, Tang C, Arakawa Y, Masaoka Y (2003) The responses of red clover (Trifolium pretense L.) to iron deficiency: a root Fe(III) chelate reductase. Plant Sci 164:679–687CrossRefGoogle Scholar
  139. Zuanazzi JAS, Clergeot PH, Quirion JC, Husson HP, Kondorosi A, Ratet P (1998) Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol Plant Microbe Interact 11:784–794CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Stefano Cesco
    • 1
    Email author
  • Guenter Neumann
    • 2
  • Nicola Tomasi
    • 1
  • Roberto Pinton
    • 1
  • Laure Weisskopf
    • 3
  1. 1.Dipartimento di Scienze Agrarie e AmbientaliUniversity of UdineUdineItaly
  2. 2.Institute of Plant NutritionUniversity of HohenheimStuttgartGermany
  3. 3.Department of Microbiology, Botanical InstituteUniversity of ZürichZürichSwitzerland

Personalised recommendations