Skip to main content

Advertisement

SpringerLink
Log in

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

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

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Amann C, Amberger A (1988) Verringerung der Phosphatsorption durch Zusatz organischer Verbindungen zu Böden in Abhängigkeit vom pH Wert. Z Pflanzenernahr Bodenkd 151:41–46

    Article  CAS  Google Scholar 

  • 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 39:785–795

    Article  CAS  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    Article  CAS  PubMed  Google Scholar 

  • 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 179:209–223

    Article  CAS  PubMed  Google Scholar 

  • 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 146:762–771

    Article  CAS  PubMed  Google Scholar 

  • 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 58:821–825

    PubMed  Google Scholar 

  • 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 8:252–258

    Google Scholar 

  • Bienfait HF (1985) Regulated redox processes at the plasmalemma of plant root cells and their function in iron uptake. J Bioenerg Biomembranes 17:73–83

    Article  CAS  Google Scholar 

  • Bienfait HF, Van den Briel W, Mesland-Mul NT (1985) Free space iron pools in roots: generation and mobilization. Plant Physiol 78:596–600

    Article  CAS  PubMed  Google Scholar 

  • 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 10:339–346

    Article  Google Scholar 

  • Bors W, Heller W, Michel C, Saran M (1990) Flavonoids as antioxidants: determination of radical-scavenging efficiencies. Methods Enzymol 186:343–355

    Article  CAS  PubMed  Google Scholar 

  • Brown MH, Paulsen IT, Skurray RA (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:393–401

    Article  Google Scholar 

  • 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 13:693–698

    Article  CAS  Google Scholar 

  • Cakmak I, Marschner H (1988) Increase in membrane permeability and exudation in roots of zinc deficient plants. J Plant Physiol 132:356–361

    CAS  Google Scholar 

  • 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 33:398–408

    CAS  Google Scholar 

  • Chobot V, Huber C, Trettenhahn G, Hadacek F (2009) (±)-catechin: chemical weapon, antioxidant, or stress regulator? J Chem Ecol 35:980–996

    Article  CAS  PubMed  Google Scholar 

  • Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 409:346–349

    Article  CAS  PubMed  Google Scholar 

  • D’Arcy-Lameta (1986) Study of soybean and lentil root exudates. II. Identification of some polyphenolic compounds, relation with plantlet physiology. Plant Soil 92:113–123

    Article  Google Scholar 

  • 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 26:1909–1926

    Article  CAS  Google Scholar 

  • Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Lett 581:2255–2262

    Article  CAS  PubMed  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200

    Google Scholar 

  • 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 441–452

    Google Scholar 

  • Eckhardt NA (2006) The role of flavonoids in root nodule development and auxin transport in Medicago truncatula. Plant Cell 18:1539–1540

    Article  Google Scholar 

  • El Hajji H, Nkhili E, Tomao V, Dangles O (2006) Interactions of quercitin with iron and copper ions: complexation and autoxidation. Free Radic Res 40:303–320

    Article  PubMed  CAS  Google Scholar 

  • 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 6:45–48

    CAS  Google Scholar 

  • 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 403–459

    Google Scholar 

  • 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 128:726–733

    Article  CAS  PubMed  Google Scholar 

  • Gagnon H, Ibrahim RK (1997) Effects of various elicitors on the accumulation and secretion of isoflavonoids in white lupin. Phytochemistry 44:1463–1467

    Article  CAS  Google Scholar 

  • 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 100:76–79

    Article  CAS  PubMed  Google Scholar 

  • 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 68:19–32

    Article  CAS  Google Scholar 

  • 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 70:107–124

    Article  CAS  Google Scholar 

  • 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 155:339–343

    Article  Google Scholar 

  • 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 163:207–212

    Article  CAS  Google Scholar 

  • 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 163:213–219

    Article  CAS  Google Scholar 

  • Gollany HT, Schumacher TE, Rue RR, Liu SY (1993) A carbon dioxide microelectrode for in situ pCO2 measurement. Microchem J 48:42–49

    Article  CAS  Google Scholar 

  • 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 150:402–415

    Article  CAS  PubMed  Google Scholar 

  • Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826

    Article  CAS  PubMed  Google Scholar 

  • Graham TL (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 39:2208–2221

    Article  CAS  Google Scholar 

  • 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 232:81–90

    Article  Google Scholar 

  • 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 271–308

    Chapter  Google Scholar 

  • 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 98:59–78

    Google Scholar 

  • 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 248:43–59

    Article  CAS  Google Scholar 

  • 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 82:193–198

    CAS  Google Scholar 

  • 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 77:1311–1315

    Article  CAS  Google Scholar 

  • Hungria M, Joseph CM, Phillips DA (1991) Rhizobium-nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris). Plant Physiol 97:759–764

    Article  CAS  PubMed  Google Scholar 

  • 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 4:278–279

    Article  CAS  Google Scholar 

  • Iwashina T (2003) Flavonoid function and activity to other plants and microorganisms. Bol Sci Space 17:24–44

    Article  Google Scholar 

  • 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 131:1169–1177

    Article  CAS  PubMed  Google Scholar 

  • 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 144:278–285

    Article  CAS  PubMed  Google Scholar 

  • Kalinova J, Vrchotova N, Triska J (2007) Exudation of allelopathic substances in buckwheat (Fagopyrum esculentum Moench). J Agric Food Chem 55:6453–6459

    Article  CAS  PubMed  Google Scholar 

  • 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 58:1705–1710

    CAS  PubMed  Google Scholar 

  • Kape R, Wex K, Parniske M, Görge E, Wetzel A, Werner D (1992b) Legume root metabolites and VA-mycorrhiza development. J Plant Physiol 141:54–60

    Google Scholar 

  • 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 52:1339–1352

    Article  CAS  PubMed  Google Scholar 

  • 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 21:289–304

    Article  CAS  PubMed  Google Scholar 

  • Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580:1112–1122

    Article  CAS  PubMed  Google Scholar 

  • 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 50:1553–1559

    Article  CAS  Google Scholar 

  • Kraemer SM, Crowley DE, Kretzschmar R (2006) Geochemical aspects of phytosiderophores-promoted iron acquisition by plants. Adv Agron 91:1–46

    Article  CAS  Google Scholar 

  • Lane GA, Biggs D, Sutherland ORW, Skipp RA (1987) Isoflavonoids as feeding deterrents and antifungal components from root of Lupinus angustifolius. J Chem Ecol 13:771–783

    Article  CAS  Google Scholar 

  • 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 159:1329–1339

    Article  CAS  Google Scholar 

  • Leon-Barrios M, Dakora FD, Joseph CM, Phillips DA (1993) Isolation of rhizobium meliloti nod gene inducers from alfalfa rhizosphere soil. Appl Environ Microbiol 59:636–639

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 89–112

    Google Scholar 

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

    CAS  Google Scholar 

  • 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 225:301–310

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Irani NG, Grotewold E (2005) Covalent attachment of the plant natural product naringenin to small glass and ceramic beads. BMC Chem Biol 5:3–12

    Article  PubMed  CAS  Google Scholar 

  • Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit Rev Plant Sci 24:267–281

    Article  CAS  Google Scholar 

  • 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 205:1–12

    Article  CAS  Google Scholar 

  • 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 267:1–12

    Article  CAS  Google Scholar 

  • 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 19:2023–2038

    Article  CAS  PubMed  Google Scholar 

  • 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 191–204

    Google Scholar 

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

    Google Scholar 

  • 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 263–296

    Google Scholar 

  • 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):75–78

    Article  Google Scholar 

  • 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 213:534–542

    Article  CAS  PubMed  Google Scholar 

  • Maxwell CA, Phillips DA (1990) Concurrent synthesis and release of nod-gene-inducing flavonoids from alfalfa roots. Plant Physiol 93:1552–1558

    Article  CAS  PubMed  Google Scholar 

  • 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 36:1199–1208

    Article  CAS  PubMed  Google Scholar 

  • 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 132:146–153

    Article  CAS  PubMed  Google Scholar 

  • 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 317–318

    Google Scholar 

  • Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167

    Article  CAS  PubMed  Google Scholar 

  • 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 23–72

    Google Scholar 

  • Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorous deficiency during proteoid root development in white lupin. Planta 208:373–382

    Article  CAS  Google Scholar 

  • 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 85:909–920

    Article  CAS  Google Scholar 

  • Neumann G, George TS, Plassard C (2009) Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant Soil 321:431–456

    Article  CAS  Google Scholar 

  • Olsen RA, Bennett JH, Blume D, Brown JC (1981) Chemical aspects of the Fe stress response mechanism in tomatoes. J Plant Nutr 3:905–921

    Article  CAS  Google Scholar 

  • 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 38:205–209

    Article  CAS  PubMed  Google Scholar 

  • 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 297–330

    Google Scholar 

  • 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 25:29–40

    Article  CAS  Google Scholar 

  • 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 229–238

  • 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 117:599–608

    Article  CAS  PubMed  Google Scholar 

  • Rao AS (1990) Root flavonoids. Bot Rev 56:1–84

    Article  Google Scholar 

  • Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in rhizobium. Nature 323:632–635

    Article  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

    Article  CAS  Google Scholar 

  • 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 183:269–277

    Article  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Marschner H (1986) Mobilization of iron in the rhizosphere of different plant species. Adv Plant Nutr 2:155–204

    Google Scholar 

  • Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193

    Article  CAS  PubMed  Google Scholar 

  • 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 7:384–390

    CAS  Google Scholar 

  • Schwab AP, Lindsay WL (1989) A computer simulation of Fe(III) and Fe(II) complexation in nutrient solution. II. Exp Soil Sci Am J 53:34–38

    Article  CAS  Google Scholar 

  • Smit AL, Bengough AG, Engels C, Van Noordwijk M, Pellerin S, Van de Geijn SC (2000) Root methods. A handbook. Springer, Heidelberg

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, New York

    Google Scholar 

  • Steele HL, Werner D, Cooper JE (1999) Flavonoids in seed and root exudates of Lotus pedunculatus and their biotransformation by Mesorhizobium loti. Physiol Plant 107:251–258

    Article  CAS  Google Scholar 

  • 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 12:1290–1306

    Article  CAS  PubMed  Google Scholar 

  • 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 144:2000–2008

    Article  CAS  PubMed  Google Scholar 

  • 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 219:225–232

    Article  CAS  PubMed  Google Scholar 

  • 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 268:20958–20965

    CAS  PubMed  Google Scholar 

  • 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 193:514–519

    Article  CAS  Google Scholar 

  • 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 33:391–397

    CAS  Google Scholar 

  • Tang CS, Young CC (1982) Collection and identification of allelopathic compounds from the undisturbed root system of bigalte lompograss (Hemarthia altissima). Plant Physiol 69:155–161

    Article  CAS  PubMed  Google Scholar 

  • Timonin MI (1946) Mircoflora of the rhizosphere in relation to the manganese-deficiency disease of oats. Proc Soil Sci Soc Am 11:284–292

    Google Scholar 

  • Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New York

    Google Scholar 

  • 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 40:1971–1974

    Article  CAS  Google Scholar 

  • 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 32:465–475

    Article  CAS  PubMed  Google Scholar 

  • Treeby M, Uren N (1993) Iron deficiency stress responses amongst citrus rootstocks. J Plant Nutr Soil Sci 156:75–81

    Article  CAS  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  CAS  PubMed  Google Scholar 

  • 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 64:265–273

    Article  CAS  PubMed  Google Scholar 

  • 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 131:1064–1079

    Article  CAS  PubMed  Google Scholar 

  • van Hees PAW, Lundström US (2000) Equilibrium models of alluminium and iron complexation with different organic acids in soil solution. Geoderma 94:201–221

    Article  Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  CAS  PubMed  Google Scholar 

  • 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 106:71–77

    Google Scholar 

  • von Wiren N, Khodr H, Hider RC (2000) Hydroxylated phytosiderophores species possess an enhanced chelate stability and affinity for iron(III). Plant Physiol 124:1149–1157

    Article  Google Scholar 

  • Walker T, Bias H, Grotewold E, Vivanco J (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  CAS  PubMed  Google Scholar 

  • 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 171:657–668

    CAS  PubMed  Google Scholar 

  • 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 29:919–927

    Article  CAS  PubMed  Google Scholar 

  • Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82

    Article  CAS  Google Scholar 

  • 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 197–222

    Google Scholar 

  • 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 237–266

    Google Scholar 

  • 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 142:689–694

    CAS  Google Scholar 

  • Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136:3771–3783

    Article  CAS  PubMed  Google Scholar 

  • 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 21:2323–2340

    Article  CAS  PubMed  Google Scholar 

  • 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 164:679–687

    Article  CAS  Google Scholar 

  • 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 11:784–794

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze Agrarie e Ambientali, University of Udine, Via delle Scienze 208, 33100, Udine, Italy

    Stefano Cesco, Nicola Tomasi & Roberto Pinton

  2. Institute of Plant Nutrition, University of Hohenheim, 70593, Stuttgart, Germany

    Guenter Neumann

  3. Department of Microbiology, Botanical Institute, University of Zürich, Zollikerstrasse 107, 8008, Zürich, Switzerland

    Laure Weisskopf

Authors
  1. Stefano Cesco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guenter Neumann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicola Tomasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roberto Pinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laure Weisskopf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefano Cesco.

Additional information

Responsible Editor: Yongguan Zhu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cesco, S., Neumann, G., Tomasi, N. et al. Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329, 1–25 (2010). https://doi.org/10.1007/s11104-009-0266-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0266-9

Keywords

Search

Navigation