Plant and Soil

, 304:169

Impact of phosphorus mineral source (Al–P or Fe–P) and pH on cluster-root formation and carboxylate exudation in Lupinus albus L.

  • M. W. Shane
  • H. Lambers
  • G. R. Cawthray
  • A. J. Kuhn
  • U. Schurr
Regular Article

Abstract

Lupinus albus L. were grown in rhizoboxes containing a soil amended with sparingly available Fe–P or Al–P (100 μg P g−1 soil/resin mixture). Root halves of individual plants were supplied with nutrient solution (minus P) buffered at either pH 5.5 or 7.5, to assess whether the source of mineral-bound P and/or pH influence cluster-root growth and carboxylate exudation. The P-amended soil was mixed 3:1 (w/w) with anion-exchange resins to allow rapid fixation of carboxylates. Treatments lasted 10 weeks. Forty percent and 30% of the root mass developed as cluster roots in plants grown on Fe–P and Al–P respectively, but cluster-root growth was the same on root-halves grown at pH 5.5 or 7.5. Mineral-bound P source (Al– or Fe–P) had no influence on the types of carboxylates measured in soil associated with cluster roots—citrate (and trace amounts of malate and fumarate) was the only major carboxylate detected. The [citrate] in the rhizosphere of cluster roots decreased with increased shoot P status (suggesting a systemic effect) and also, only for plants grown on Al–P, with decreased pH in the root environment (suggesting a local effect). In a separate experiment using anion exchange resins pre-loaded with malate or citrate, we measured malate (50%) and citrate (79%) recovery after 30 days in soil. We therefore, also conclude that measurements of [citrate] and [malate] at the root surface may be underestimated and would be greater than the 40- and 1.6-μmol g−1 root DM, respectively estimated by us and others because of decomposition of carboxylates around roots prior to sampling.

Keywords

Citrate P-deficiency Proteoid roots Split-root design Systemic signal White lupin 

References

  1. Braum SM, Helmke PA (1995) White lupin utilises soil phosphorus that is unavailable to soybean. Plant Soil 176:95–100CrossRefGoogle Scholar
  2. Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromatogr A 1011:233–240PubMedCrossRefGoogle Scholar
  3. Clements JC, White PF, Buirchell BJ (1993) The root morphology of Lupinus angustifolius in relation to other Lupinus species. Aust J Agr Res 44:1367–1375CrossRefGoogle Scholar
  4. Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292CrossRefGoogle Scholar
  5. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid root clusters and other root clusters. Bot Acta 108:183–200Google Scholar
  6. Dinkelaker B, Hengeler G, 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, The Netherlands, pp 441–452Google Scholar
  7. Gardner WK, Parbery DG, Barber DA (1981) Proteoid root morphology and function in Lupinus albus. Plant Soil 60:143–147CrossRefGoogle Scholar
  8. Gardner WK, Parbery DG, Barber DA (1982a) The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil/root interface. Plant Soil 68:19–32CrossRefGoogle Scholar
  9. Gardner WK, Parbery DG, Barber DA (1982b) The acquisition of phosphorus by Lupinus albus L. II. The effect of varying phosphorus supply and soil type on some characteristics of the soil/root interface. Plant Soil 68:33–41CrossRefGoogle Scholar
  10. 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 aluminum in the proteoid rhizosphere in samples of an oxisol and a luvisol. Z Pflanzenernähr Bodenkd 157:289–294CrossRefGoogle Scholar
  11. Gilbert GA, Allan DA, Vance CP (1997) Phosphorus deficiency in white lupin alters root development and metabolism. In: Flores HE, Lynch JP, Eissenstat D (eds) Radical biology: advances and perspectives on the function of plant roots. American Society of Plant Physiologists, Rockville, USA, pp 92–103Google Scholar
  12. 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
  13. Hocking P, Jeffery S (2004) Cluster root production and organic anion exudation in a group of old world lupins and a new world lupin. Plant Soil 258:135–150CrossRefGoogle Scholar
  14. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  15. Jones DL, Prabowo AM, Kochain LV (1996) Kinetics of malate transport and decomposition in acid soils and isolated bacterial populations: the effect of microorganisms on root exudation of malate under Al stress. Plant Soil 182:239–247Google Scholar
  16. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils—misconceptions and knowledge gaps. Plant Soil 248:31–41CrossRefGoogle Scholar
  17. Keerthisinghe G, Hocking P, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ 21:467–478CrossRefGoogle Scholar
  18. Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martinez E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant Soil 238:111–122CrossRefGoogle Scholar
  19. Lamont B (1972) The morphology and anatomy of proteoid roots in the genus Hakea. Aust J Bot 20:155–174CrossRefGoogle Scholar
  20. Liang R, Li C (2003) Differences in cluster-root formation and carboxylate exudation in Lupinus albus L. under different nutrient deficiencies. Plant Soil 248:221–227CrossRefGoogle Scholar
  21. Longnecker N, Brennan R, Robson A (1998) Lupin nutrition. In: Gladstones JS, Atkins C, Hamblin J (eds) Lupin as crop plants. Biology, production and utilization. CAB International, Wallingford, Oxfordshire, UK, pp 121–148Google Scholar
  22. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, UKGoogle Scholar
  23. Marschner H, Römheld V, Horst WJ, Martin P (1986) Root-induced changes in the rhizosphere: Importance for the mineral nutrition of plants. Z Pflanzenernähr Bodenkd 149:441–456CrossRefGoogle Scholar
  24. Marschner H, Römheld V, Cakmak I (1987) Root-induced changes of nutrient availability in the rhizosphere. J Plant Nutr 10:1175–1184CrossRefGoogle Scholar
  25. McCluskey J, Herdman L, Skene KR (2004) Iron deficiency induces changes in metabolism of citrate in lateral roots and cluster roots of Lupinus albus. Physiol Plant 121:586–594CrossRefGoogle Scholar
  26. Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate blue and malachite green. Analyst 108:361–367CrossRefGoogle Scholar
  27. Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167PubMedCrossRefGoogle Scholar
  28. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382CrossRefGoogle Scholar
  29. Pate JS, Dell B (1984) Economy of mineral nutrients in sandplain species. In: Pate JS, Beard JS (eds) Kwongan—plant life of the sandplain. University of Western Australia Press, Nedlands, Australia, pp 227–252Google Scholar
  30. Peiter E, Yan F, Schubert S (2001) Proteoid root formation of Lupinus albus L. is triggered by high pH of the root medium. J Appl Bot 75:50–52Google Scholar
  31. Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500PubMedCrossRefGoogle Scholar
  32. Shane MW, Lambers H (2005a) Cluster roots: a curiosity in context. Plant Soil 274:101–125CrossRefGoogle Scholar
  33. Shane MW, Lambers H (2005b) Manganese accumulation in leaves of Hakea prostrata R.Br. (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 274:441–450CrossRefGoogle Scholar
  34. Shane MW, Lambers H (2006) Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of ‘P toxicity’. J Exp Bot 57:413–423PubMedCrossRefGoogle Scholar
  35. Shane MW, de Vos M, de Roock S, Lambers H (2003a) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26:265–273CrossRefGoogle Scholar
  36. Shane MW, De Vos M, De Roock S, Cawthray GR, Lambers H (2003b) Effect of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. Plant Soil 248:209–219CrossRefGoogle Scholar
  37. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in Harsh Hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560PubMedCrossRefGoogle Scholar
  38. Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H (2006) Specialised ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ 29:1989–1999PubMedCrossRefGoogle Scholar
  39. Shu L, Shen JU, Rengel Z, Tang C, Zhang F, Cawthray GR (2007) Formation of cluster roots and citrate exudation by Lupinus albus in response to localised application of different phosphorus sources. Plant Sci 172:1017–1024CrossRefGoogle Scholar
  40. Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86:1060–1064CrossRefGoogle Scholar
  41. Skene KR (2000) Pattern formation in cluster roots: some developmental and evolutionary considerations. Ann Bot 85:901–908CrossRefGoogle Scholar
  42. Ström L, Olsson T, Tyler G (1994) Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic-acids. Plant Soil 167:239–245CrossRefGoogle Scholar
  43. Trinick MJ (1977) Vesicular–arbuscular infection and soil phosphorus utilization in Lupinus spp. New Phytol 78:297–304CrossRefGoogle Scholar
  44. Vance CP, Uhde-Stone C, Allen DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable source. New Phytol 157:423–447CrossRefGoogle Scholar
  45. Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197CrossRefGoogle Scholar
  46. Walker BA, Pate JS (1986) Morphological variation between seedling progenies of Viminaria juncea (Schrad. & Wendl.) Hoffmans. (Fabaceae) and its physiological significance. Aust J Plant Physiol 13:305–319CrossRefGoogle Scholar
  47. Watt M, Evans JR (1999) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716PubMedCrossRefGoogle Scholar
  48. Zhu Y, Yan F, Zörb C, Schubert (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.). Plant Cell Physiol 46:892–901PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • M. W. Shane
    • 1
    • 2
  • H. Lambers
    • 1
  • G. R. Cawthray
    • 1
  • A. J. Kuhn
    • 2
  • U. Schurr
    • 2
  1. 1.School of Plant Biology, Faculty of Natural and Agricultural SciencesThe University of Western AustraliaCrawleyAustralia
  2. 2.ICG-3 (Phytosphere)Research Centre JülichJülichGermany

Personalised recommendations