Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin

Plant, Cell and Environment

Volumn 32, Issue 5, 2009, Pages 465-475

  Tomasi, Nicola ^a   Kretzschmar, Tobias ^b   Espen, Luca ^c   Weisskopf, Laure ^b   Fuglsang, Anja Thoe ^d   Palmgren, Michael Gjedde ^d   Neumann, Günter ^e   Varanini, Zeno ^f   Pinton, Roberto ^a   Martinoia, Enrico ^b   Cesco, Stefano ^a  

^a UNIVERSITY OF UDINE   (Italy)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF HOHENHEIM   (Germany)

^f UNIVERSITY OF VERONA   (Italy)

Author keywords

Carboxylate release; Lupinus albus; Malate; Organic acids; pH; Phosphorus; Proton pump; Rhizosphere; Root exudates

Indexed keywords

DICOTYLEDON; ENZYME; GENE EXPRESSION; NUCLEAR MAGNETIC RESONANCE; ORGANIC ACID; PH; RHIZOSPHERE; ROOT;

LUPINUS ALBUS;

EID: 64149090457     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2009.01938.x     Document Type: Article

References (51)

1. Bradford M.M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72, 248 254.
2. + uptake, electric potential difference and membrane ATPase activities of higher plant tissues. Plant Science Letters 17, 391 400.
3. Davies J., Briarty L.G. Rieley J.O. (1973) Observations on swollen lateral roots of Cyperaceae. New Phytologist 72, 167 174.
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 & Environment 12, 285 292.
5. Espen L., Dell'Orto M., De Nisi P. Zocchi G. (2000) Metabolic responses in cucumber (Cucumis sativus L.) roots under Fe-deficiency: a P-31-nuclear magnetic resonance in-vivo study. Planta 210, 985 992.
6. +-transport-competent plasma-membrane vesicles from corn roots by discontinuous sucrose gradient centrifugation - effect of membrane protectant agents. Journal of Plant Physiology 144, 505 512.
7. Forbush B. (1983) Assay of Na,K-Atpase in plasma-membrane preparations - increasing the permeability of membrane-vesicles using sodium dodecyl-sulfate buffered with bovine serum-albumin. Analytical Biochemistry 128, 159 163.
8. +-ATPase AHA2 involves the three C-terminal residues Tyr(946)-Thr-Val and requires phosphorylation of Thr(947). Journal of Biological Chemistry 274, 36774 36780.
9. Furukawa J., Yamaji N., Wang H., Mitani N., Murata Y., Sato K., Katsuhara M., Takeda K. Ma J.F. (2007) An aluminum-activated citrate transporter in barley. Plant and Cell Physiology 48, 1081 1091.
10. Gardner W.K., Parbery D.G. Barber D.A. (1981) Proteoid root morphology and function in Lupinus albus. Plant and Soil 60, 143 147.
11. Gardner W.K., Parbery D.G. Barber D.A. (1982) The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of soil/root interface. Plant and Soil 68, 19 32.
12. Gogstad G.O. Krutnes M.B. (1982) Measurement of protein in cell-suspensions using the coomassie brilliant blue dye-binding assay. Analytical Biochemistry 126, 355 359.
13. Handreck K.A. (1997) Phosphorus requirements of Australian native plants. Australian Journal of Soil Research 35, 241 289.
14. Hocking P.J. Jeffery S. (2004) Cluster-root production and organic anion exudation in a group of old-world lupins and a new-world lupin. Plant and Soil 258, 135 150.
15. +-ATPase by a mechanism involving the c-terminal inhibitory domain. The Plant Cell 5, 321 327.
16. Johnson J.F., Vance C.P. Allan D.L. (1996) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiology 112, 31 41.
17. Jones D.L. Darrah P. (1994) Role of root derived organic acid in the mobilization of nutrients from the rhizosphere. Plant and Soil 166, 247 257.
18. Kania A., Neumann G., Cesco S., Pinton R., Römheld V. (2001) Use of plasma membrane vesicles for examination of phosphorus deficiency-induced root excretion of citrate in cluster roots of white lupin (Lupinus albus L.). In Plant Nutrition: Food Security and Sustainability of Agro-Ecosystems through Basic and Applied Research. XIV International Plant Nutrition Colloquium (eds W.J. Horst, M.K. Schenk, A. Bürket, et al. pp. 546 547. Kluwer Academic Publishers, Dordrecht, the Netherlands.
19. Keerthisinghe G., Hocking P.J., Ryan P.R. Delhaize E. (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant, Cell & Environment 21, 467 478.
20. 31P nuclear magnetic-resonance to higher plant tissue. Journal of Experimental Botany 33, 656 669.
21. Lambers H., Juniper D., Cawthray G.R., Veneklaas E.J. 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 and Soil 238, 111 122.
22. Lamont B. (1974) Biology of dauciform roots in sedge Cyathochaete- Avenacea. New Phytologist 73, 985 996.
23. +-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Functional Plant Biology 31, 1075 1083.
24. Ma Y., Jakowitsch J., Maier T.L., Bayer M.G., Muller N.E., Schenk H.E.A. Loffelhardt W. (2001) ATP citrate lyase in the glaucocystophyte alga Cyanophora paradoxa is a cytosolic enzyme: characterisation of the gene for the large subunit at the cDNA and genomic levels. Molecular Genetics and Genomics 266, 231 238.
25. Maniatis T., Sambrook J. Fritsch E.F. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, NY, USA.
26. Marschner H. (1995) Mineral Nutrition of Higher Plants. Academic Press, London, UK.
27. 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.
28. Michelet B., Lukaszewicz M., Dupriez V. Boutry M. (1994) A plant plasma-membrane proton-atpase gene is regulated by development and environment and shows signs of a translational regulation. The Plant Cell 6, 1375 1389.
29. Neumann G. Martinoia E. (2002) Cluster roots - an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162 167.
30. Neumann G., Massonneau A., Martinoia E. Römheld V. (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208, 373 382.
31. Neumann G., Massonneau A., Langlade N., Dinkelaker B., Hengeler C., Römheld V. Martinoia E. (2000) Physiological aspect of cluster root function and development in phosphorus-deficient White Lupin (Lupinus albus L.). Annals of Botany 85, 909 919.
32. Ohno T., Koyama H. Hara T. (2003) Characterization of citrate transport through the plasma membrane in a carrot mutant cell line with enhanced citrate excretion. Plant and Cell Physiology 44, 156 162.
33. +-ATPase is protected by fusicoccin-induced 14-3-3 binding. Plant Physiology 118, 551 555.
34. +-ATPase. Advances in Botanical Research 28, 1 70.
35. Purnell H.M. (1960) Studies of the family Proteaceae. Anatomy and morphology of the roots of some Victorian species. Australian Journal of Botany 8, 38 50.
36. +-ATPase: yeast as a model system for solute transport across the plant plasma membrane. The Plant Cell 7, 1655 1666.
37. Ritz C. Spiess A.N. (2008) qpcR: an R package for sigmoidal model selection in quantitative real-time polymerase chain reaction analysis. Bioinformatics 24, 1549 1551.
38. Roberts J.K.M., Ray P.M., Wadejardetzky N. Jardetzky O. (1980) Estimation of cytoplasmic and vacuolar pH in higher-plant cells by P-31 NMR. Nature 283, 870 872.
39. Roberts J.K.M., Wadejardetzky N. Jardetzky O. (1981) Intracellular pH measurements by P-31 nuclear magnetic-resonance influence of factors other than pH on P-31 chemical-shifts. Biochemistry 20, 5389 5394.
40. - Uptake. Plant Physiology 109, 1277 1283.
41. +-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant Physiology and Biochemistry 43, 287 292.
42. Sas L., Rengel Z. Tang C. (2001) Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. Plant Science 160, 1191 1198.
43. Shane M.W., De Vos M., De Roock S. Lambers H. (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant, Cell & Environment 26, 265 273.
44. Shane M.W., Dixon K.W. Lambers H. (2005) The occurrence of dauciform roots amongst Western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae). New Phytologist 165, 887 898.
45. +-ATPase. Plant Physiology 138, 287 296.
46. 31P nuclear magnetic resonance study. Plant Physiology 99, 856 863.
47. 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 Biology and Biochemistry 40, 1971 1974.
48. 2 concentration. Plant Physiology 120, 705 716.
49. +-ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiology 129, 50 63.
50. Zhang W.H., Ryan P.R. Tyerman S.D. (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiology 136, 3771 3783.
51. Zhu Y., Yan F., Zorb C. Schubert S. (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant and Cell Physiology 46, 892 901.