Plant and Soil

, Volume 248, Issue 1–2, pp 209–219

Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br.

  • Michael W. Shane
  • Martin de Vos
  • Sytze de Roock
  • Gregory R. Cawthray
  • Hans Lambers
Article

Abstract

The response of internal phosphorus concentration, cluster-root initiation, and growth and carboxylate exudation to different external P supplies was investigated in Hakea prostrata R.Br. using a split-root design. After removal of most of the taproot, equal amounts of laterals were allowed to grow in two separate pots fastened together at the top, so that the separate root halves could be exposed to different conditions. Plants were grown for 10 weeks in this system; one root half was supplied with 1 μM P while the other halves were supplied with 0, 1, 25 or 75 μM P. Higher concentrations of P supplied to one root half significantly increased the P concentration of those roots and in the shoots. The P concentrations in root halves supplied with 1 μM P were invariably low, regardless of the P concentration supplied to the other root half. Cluster root initiation was completely suppressed on root halves supplied with 25 or 75 μM P, whereas it continued on the other halves supplied with 1 μM P indicating that cluster-root initiation was regulated by local root P concentration. Cluster-root growth (dry mass increment) on root halves supplied with 1 μM P was significantly reduced when the other half was either deprived of P or supplied with 25 or 75 μM P. Cluster-root growth was favoured by a low shoot P status at a root P supply that was adequate for increased growth of roots and shoots without increased tissue P concentrations. The differences in cluster-root growth on root halves with the same P supply suggest that decreased cluster-root growth was systemically regulated. Carboxylate-exudation rates from cluster roots on root halves supplied with 1 μM P were the same, whether the other root half was supplied with 1, 25 or 75 μM P, but were approximately 30 times faster when the other half was deprived of P. Estimates of root P-uptake rates suggest a rather limited capacity for down-regulating P uptake when phosphate was readily available.

carboxylate exudation cluster roots Hakea prostrata proteoid roots phosphorus Proteaceae split-root design 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. A. O. A. C. 1975 Official Methods of Analysis. 12th edn. Association of Official Analytical Chemists, Washington, DC.Google Scholar
  2. Bates T R and Lynch J P 1996 Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ. 19, 529-538.Google Scholar
  3. Brouwer R 1963 Some aspects of the equilibrium between overground and underground plant parts. Meded. Inst. Biol. Scheikd. Onderzoek Landbouwgewassen. 213, 31-39.Google Scholar
  4. Bolan N D, Elliot J, Gregg P E H and Weil S 1997 Enhanced dissolution of phosphate rocks in the rhizosphere. Biol. Fertil. Soils 24, 169-174.Google Scholar
  5. De Groot C C, Marcelis R F M, Van Den Boogaard R and Lambers H 2001 Growth and dry-mass partitioning in tomato as affected by phosphorus nutrition and light. Plant Cell Environ. 24Google Scholar
  6. Dinkelaker B, Romheld V and Marschner H 989 Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus). Plant Cell Environ. 12, 285-292.Google Scholar
  7. Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid root clusters and other root clusters. Bot. Acta 108, 183-200.Google Scholar
  8. Gardner W, Parbery D and Barber D 1982 The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil/root interface. Plant Soil 68, 19-32.Google Scholar
  9. Gardner W, Barber D and Parbery D 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.Google Scholar
  10. Gerke J 1994 Kinetics of soil phosphate desorption as affected by citric acid. Z. Bodenk. Pflanzenernaehr. 157, 17-22.Google Scholar
  11. Gilbert G A, Knight J D, Vance C P and Allan D L 2000 Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann. Bot. 85, 921-928.Google Scholar
  12. Grierson P F 1992 Organic acids in the rhizosphere of Banksia integrifolia L.f. Plant Soil 144, 259-265.Google Scholar
  13. Grose M J 1989 Phosphorus nutrition of seedlings of the waratah Telopea speciosissima (Sm.) R. Br. (Proteaceae). Aust. J. Bot. 37, 313-320.Google Scholar
  14. Handreck K A 1991 Interactions between iron and phosphorus in the nutrition of Banksia ericifolia L. f. var. ericifolia (Proteaceae) in soil-less potting media. Aust. J. Bot. 39, 373-384.Google Scholar
  15. Handreck K A 1997 Phosphorus requirements of Australian native plants. Aust. J. Soil Res. 35, 241-289.Google Scholar
  16. Hinsinger P 1998 How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. Adv. Agron. 64, 225-265Google Scholar
  17. Hoffland E, Findenegg G R and Nelemans J A 1989 Solubilization of rock phosphate by rape. II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113, 161-165.Google Scholar
  18. Jeffrey D W 1967 Phosphate nutrition of Australian heath plants. I. The importance of proteoid roots in Banksia (Proteaceae). Aust. J. Bot. 15, 403-411.Google Scholar
  19. Jones D L 1998 Organic acids in the rhizosphere-a critical review. Plant Soil 205, 25-44.Google Scholar
  20. Jones D L and Darrah P R 1994 Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166, 247-257.Google Scholar
  21. Jungk A O 1996 Dynamics of nutrient movement at the soil-root interface. In Plant Roots: The Hidden Half, 2nd edn. Eds Y Waisel, A Eshel & U Kafkaki. pp. 529-556. Marcel Dekker, New York.Google Scholar
  22. Keerthisinghe G, Hocking P, Ryan PR and Delhaize, E 1998 Proteoid roots of lupin (Lupinus albus L.): Effect of phosphorus supply on formation and spatial variation in citrate efflux and enzyme activity. Plant Cell Environ. 21, 467-478.Google Scholar
  23. Kirk G J D, Santos E E and Santos M B 1999 Phosphate solubilization by organic anion excretion from rice roots in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH, and effects on phosphate solubility. New Phytol. 142, 185-200.Google Scholar
  24. Kuiper D, Schuit J and Kuiper P J C 1988 Effect of internal and external cytokinin concentrations on root growth and root to shoot ratio of Plantago major ssp. pleiosperma at different nutrient concentrations. Plant Soil 111, 231-236.Google Scholar
  25. Kuiper D, Kuiper P J C, Lambers H, Schuit J and Staal M 1989 Cytokinin concentration in relation to mineral nutrition and benzyladenine treatment in Plantago major ssp. pleiosperma. Physiol. Plant. 75, 511-517.Google Scholar
  26. Lambers H, Stuart Chapin F III and Pons T L 1998 Plant Physiological Ecology.Springer, New York.Google Scholar
  27. Lambers H, Juniper D, Cawthray G R, Veneklaas E J and Martinez-Ferri 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, 111-122.Google Scholar
  28. Lamont B 1971 The effect of soil nutrients on the production of proteoid roots by Hakea species. Aust. J. Bot. 20, 27-40.Google Scholar
  29. Lamont B 1972 The morphology and anatomy of proteoid roots in the genus Hakea. Aust. J. Bot. 20, 155-174.Google Scholar
  30. Lamont B 1973 Factors affecting the distribution of proteoid roots within the root systems of two Hakea species Aust. J. Bot. 21, 165-187.Google Scholar
  31. Lamont B 1982 Mechanisms for enhancing nutrient uptake in plant with particular reference to Mediterranean South Africa and Western Australia. Bot. Rev. 48, 597-689.Google Scholar
  32. Lamont B 1993 Why are hairy root clusters so abundant in the most nutrient-impoverished soils of Australia? Plant Soil 155/156, 269-272.Google Scholar
  33. Lamont B 2002 Structure and ecology of proteoid root clusters. Plant Soil 248, 1-19.Google Scholar
  34. Lamont B, Brown G and Mitchell DT 1984 Structure, environmental effects on their formation, and function of proteoid roots in Leucadendron laureolum (Proteaceae). New Phytol. 97, 381-390.Google Scholar
  35. Ma Z, Bielenberg D G, Brown K M and Lynch J P 2001 Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 24, 459-467.Google Scholar
  36. Marschner H 1995 Mineral Nutrition of Higher Plants. 2nd edn. Academic Press, London.Google Scholar
  37. Neumann G and Martinoia E 2002 Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci. 7, 162-167.PubMedGoogle Scholar
  38. Parks S E., Haigh A M. and Creswell G C 2000 Stem tissue phosphorus as an index of the phosphorus status of Banksia ericifolia L. Plant Soil 227, 59-65.Google Scholar
  39. Purnell HM 1960 Studies of the family Proteaceae. 1. Anatomy and morphology of the roots of some Victorian species. Aust. J. Bot. 8, 38-50.Google Scholar
  40. Raaimakers D, Boot R G A, Dijkstra P, Pot S and Pons T 1995 Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia. 102, 120-125.Google Scholar
  41. Reddell P, Yun Y and Shipton W A 1997 Cluster roots and mycorrhizae in Casuarina cunninghamiana: Their occurrence and formation in relation to phosphorus supply. Aust. J. Bot. 45, 41-51.Google Scholar
  42. Roelofs R F R, Rengel Z, Cawthray G R, Dixon K W and Lambers H 2001 Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ. 24, 891-904.Google Scholar
  43. Shane MW, McCully ME and Canny MJ 2000 The vascular system of maize stems revisited: Implications for water transport and xylem safety. Ann. Bot. 86, 245-258.Google Scholar
  44. Smith F W, Jackson W A and Vanden Berg P J 1990 Internal phosphorus flows during development of phosphorus stress in Stylosanthes hamata. Aust. J. Plant Physiol. 17, 451-464.Google Scholar
  45. Stitt M 1997 The flux of carbon between the chloroplast and the cytoplasm. In Plant Metabolism. Eds. D T Denis, D H Turpin, D D Lefebvre and D B Layzell. pp. 382-400. Longman Scientific and Technical, Singapore.Google Scholar
  46. Torrey J G 1986 Endogenous and exogenous influences in the regulation of lateral root formation. In New Root Formation in Plants and Cuttings. Ed. AB Jackson. pp. 31-66. Marinus Nijhoff, Dordrecht.Google Scholar
  47. Watt M and Evans J R 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, 705-716.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Michael W. Shane
    • 1
  • Martin de Vos
    • 1
    • 2
  • Sytze de Roock
    • 1
    • 2
  • Gregory R. Cawthray
    • 1
  • Hans Lambers
    • 1
    • 2
  1. 1.School of Plant Biology, Faculty of Natural and Agricultural SciencesThe University of Western AustraliaCrawleyAustralia
  2. 2.Plant EcophysiologyUtrecht UniversityThe Netherlands

Personalised recommendations