Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism

Plant and Soil

Volumn 248, Issue 1-2, 2003, Pages 99-116

  Uhde Stone, Claudia ^a   Gilbert, Glena ^a,c   Johnson, Jane M F ^a,d   Litjens, Ralph ^a,e   Zinn, Kelly E ^a   Temple, Stephen J ^a,f   Vance, Carroll P ^a,b   Allan, Deborah L ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c VITERBO UNIVERSITY   (United States)

^d U S DEPARTMENT OF AGRICULTURE   (United States)

^e Higher Inst for Prof Educ Venlo   (Netherlands)

^f Forage Genetics International   (United States)

Author keywords

Cluster root; Lupinus albus L.; Malate dehydrogenase; Phosphoenolpyruvate carboxylase; Phosphorus deficiency; Proteoid root

Indexed keywords

ACCLIMATION; METABOLISM; ORGANIC ACID; PHOSPHORUS; ROOT SYSTEM;

EMBRYOPHYTA; EUKARYOTA; LUPINUS; LUPINUS ALBUS;

EID: 0012771652     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022335519879     Document Type: Article

References (69)

1. Aono T, Kanada N, Ijima A and Oyaizu H 2001 The response of the phosphate uptake system and the organic acid exudation system to phosphate starvation in Sesbania rostrata. Plant Cell Physiol. 15, 1253-1264.
2. Avio L, Sbrana C and Giovannetti M 1990 The response of different species of Lupinus to VAM endophytes. Symbiosis 42, 321-323.
3. 4 plants. Biochem Biophys. Res. Com. 286, 1158-1162.
4. Bradford M M 1976 A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
5. Braum S and Helmke P A 1995 White lupin utilizes soil phosphorus that is unavailable to soybean. Plant Soil 176, 95-100.
6. Braun W and Abraham R 1989 Modified diffusion blotting for rapid and efficient protein transfer with PhastSystem. Electrophoresis 10, 249-253.
7. Chollet R, Vidal J and O'Leary M H 1996 Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol, 47, 273-298.
8. Cretin C, Luchetta P, Joly C, Miginiac-Maslow M, Decottignies P, Jacquot J, Vidal J and Gadal P 1988 Identification of cDNA clone from sorghum leaf malate dehydrogenase (NADP). Eur. J. Biochem. 174, 497-501.
9. Devereux J, Haeberli P and Smithies O 1984 Sequence analysis programs for the VAX, Nucleic Acids Res. 12, 387-395.
10. Dinkelaker B, Romheld V and Marschner H 1989 Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ. 12, 285-292.
11. Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid roots and other root clusters. Botanica Acta. 108, 169-276.
12. 4-form enzyme. Plant Cell Physiol. 39, 865-873.
13. 4 phosophoenolpyruvate carboxylase. Planta 213, 379-89.
14. Fleming A J, Mandel T, Roth I and Kuhlemeier C 1993 The patterns of gene expression in the tomato shoot apical meristem. Plant Cell 5, 297-309.
15. Frank J, Claarke R J, Vater J and Holzwarth J F 2001 Influence of allosteric effectors on the kinetics and equilibrium binding of phosphoenolpyruvate (PEP) to phosphoenolpyruvate carboxylase (PEPC) from Zea mays. Biophys. Chem. 92, 53-64.
16. Gardner W K, Parbery D G and Barber D A 1982 The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil/root interface. Plant Soil 68, 19-32.
17. Gardner W K, Barber D A and Parbery D G 1983 The acquisition of phosphorus by Lupinus albas L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70, 107-124.
18. Gietl C 1992 Malate dehydrogenase isoenzymes: Cellular location and role in the flow of metabolites between cytoplasm and cell organelles. Biochim. Biophys. Acta 110, 217-234.
19. Gilbert G A, Knight J D, Vance C P and Allan D L 1999 Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ. 22, 801-810.
20. 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.
21. Guex N, Henry H, Flach J, Richter H and Widmer F 1995 Glyoxysomal malate dehydrogenase and malate synthase from soybean cotyledons (Glycine max L.): enzyme association, antibody production and cDNA cloning. Planta 197, 369-375.
22. Hartwell J, Gill A, Nimmo G A, Wilkins M B, Jenkins G I and Nimmo H G 1999 Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J. 20, 333-42.
23. Heukeshovewn J and Demick R 1988 Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9, 28-32.
24. Huber S C, Huber J L and McMichael R W Jr 1994 Control of plant enzyme activity by reversible protein phosphorylation. Int. Rev. Cytol. 149, 47-98.
25. 2-fixing and nitrate- and urea-dependent soybean plants. Plant Physiol. 112, 171-178.
26. 4 plants. Proc. Natl. Acad. Sci. USA. 88, 2712-2715.
27. Johnson J F, Allan D L, Vance C P and Weiblen G 1996a Root carbon dioxide fixation by phosphorus-deficient Lupinus albus. Contribution to organic acid exudation by proteoid roots. Plant Physiol. 112, 19-30.
28. Johnson J F, Vance C P and Allan D L 1996b Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112, 31-41.
29. Kim D J and Smith S M 1994 Expression of a single gene encoding microbody NAD-malate dehydrogenase during glyoxysome and peroxisome development in cucumber. Plant Mol. Biol. 26, 1833-1841.
30. Lance C and Rustin P 1984 The central role of malate in plant metabolism. Physiol. Veg. 22, 625-641.
31. 3 plants. Physiol. Veg. 21, 805-815.
32. Lepiniec L, Vidal J, Chollet R, Gadal P and Cretin C 1994 Phosphoenolpyruvate carboxylase: structure, regulation and evolution. Plant Sci. 99, 111-124.
33. Liu J, Uhde-Stone C, Li A, Vance C and Allan D 2001 A phosphate transporter with enhanced expression in proteoid roots of white lapin (Lupinus albus L.), Plant Soil 237, 257-266.
34. Marczewski W 1989 Kinetic properties of phosphoenolpyruvate carboxylase from lupin nodules and roots. Physiol Planta. 76, 539-543.
35. Marschner H V, Romheld V, Horst W J and Martin P 1986 Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. Z, Pflanzenernaehr Bodenk. 149, 441-456.
36. Marschner H, Romheld V and Cakmak I 1987 Root-induced changes of nutrient availability in the rhizosphere. J. Plant Nutr. 10, 1175-1184.
37. Marschner H 1995 Mineral Nutrition of Higher Plants, 2nd edition. Academic Press Inc., San Diego, CA.
38. Massonneau A, Langlade N, Leon S, Smutny J, Vogt E, Neumann G and 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, 534-42.
39. 2 MS. University of Minnesota, St Paul, Minn.
40. McCloud S A, Smith R G and Schuller K A 2001. Partial purification and characterization of pyruvate kinase from the plant fraction of soybean root nodules. Physiol. Plant. 111, 283-290.
41. 3 plants. Plant Physiol. 84, 58-60.
42. Metzler M C, Rothermel B A and Nelson T 1989 Maize NADP-malate dehydrogenase: cDNA cloning, sequence and mRNA characterization. Plant Mol. Biol. 12, 712-722.
43. Miller S S, Discroll B T, Gregerson R G, Gantt J S and Vance C P 1998 Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J. 15, 173-185.
44. Miller S S, Liu J, Allan D L, Menzhuber C J, Fedorova M and Vance C P 2001 Molecular control of acid phosphatase secreted into the rhizosphere of proteoid roots from phosphorus stressed white lupin. Plant Physiol. 127, 594-606.
45. Moraes T F and Plaxton W C 2000 Purification and characterization of phosphoenolpyruvate carboxylase from Brassica napus (rapeseed) suspension cell cultures: implications for phosphoenolpyruvate carboxylase regulation during phosphate starvation, and the integration of glycolysis with nitrogen assimilation. Eur. J. Biochem. 267, 4465-4476.
46. Musrati R A, Kollarova M, Mernik N and Mikulasova D 1998 Malate dehydrogenase: distribution, function and properties. Gen. Physiol. Biophys. 17, 193-210.
47. Neumann G, Massonneau A, Martinoia E and Romheld V 1999 Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208, 373-382.
48. Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Romheld V and Martinoia E 2000 Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann. Bot. 85, 909-919.
49. Pathirana S M, Vance C P, Miller S S and Gantt J S 1992 Alfalfa root nodule phosphoenolpyruvate carboxylase: characterization of the cDNA and expression in effective and plant-controlled ineffective nodules. Plant Mol. Biol. 20, 437-450
50. Pilbeam D J, Cakman I, Marschner H and Kirkby E A 1993 Effect of withdrawal of phosphorus on nitrate assimilation and PEP carboxylase activity in tomato. Plant Soil 154, 111-117.
51. Raghothama K G 1999 Phosphate acquisition. Ann. Rev. Plant. Physiol. Plant. Mol. Biol. 50, 665-693.
52. Sambrook J, Fritch E and Maniatis T 1989 Molecular Cloning. Cold Spring Harbour Laboratory Press. Cold Spring Harbour, NY.
53. Schuller K A, Turpin D H and Plaxton W C 1990 Metabolite regulation of partially purified soybean nodule phosphoenolpyruvate carboxylase. Plant Physiol. 94, 1429-1435.
54. Schuller K A and Werner D 1993 Phosphorylation of soybean nodule phosphoenolpyruvate carboxylase in vitro decreases sensitivity to inhibition by L-malate. Plant Physiol. 101, 1267-1273.
55. Scrutton M C and Fatebene F 1975 An assay system for localization of pyruvate and phosphoenolpyruvate carboxylase activity on polyacrylamide gels and its application of detection of these enzymes in tissue and extracts. Anal Biochem. 69, 247-260.
56. Skene K R 1998b Cluster roots: some ecological considerations. J. Ecol. 86. 1060-1064.
57. Sugimoto T, Kawasaki T, Kato T, Whittier R F, Shibata D and Kawamura Y 1992 cDNA sequence and expression of a phosphoenolpyruvate carboxylase gene from soybean. Plant Mol. Biol. 20, 743-747.
58. Tadano T and Sakai H 1991 Secretion of acid phosphatase by roots of several crop species under phosphorus-deficient conditions. Soil Sci. Plant Nutr. 37, 129-140.
59. Taybi T, Patil S, Chollet R and Cushman J C 2000 A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in crassulacean acid metabolism-induced leaves of the common ice plant. Plant Physiol. 123, 1471-1482.
60. Theodorou M E, Cornel F A, Duff S M G and Plaxton W C 1992 Phosphate starvation-inducible synthesis of the α-subunit of the pyrophosphate-dependent phosphofructokinase in black mustard suspension cells. J. Biol. Chem. 267, 21901-21905.
61. Theodoru M E and Plaxton W C 1993 Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant. Physiol. 101, 339-344.
62. Ting I D and Osmond C B 1973 Multiple forms of plant PEP carboxylase associated with different metabolic pathways. Plant Physiol. 51, 448-453.
63. Trinick M J 1977 Vesicular-arbuscular infection and soil phosphorus utilization in Lupinus spp. New Phytol. 78, 297-304.
64. Vance C P, Stade S and Maxwell C A 1983 Alfalfa root nodule carbon dioxide fixation: I. Association with nitrogen fixation and incorporation into amino acids. Plant Physiol. 72, 469-473.
65. Wang Y H and Chollet R 1993 In vitro phosphorylation of purified tobacco-leaf phosphoenolpyruvate carboxylase. FEBS Lett. 328, 215-218.
66. 2 concentration. Plant Physiol. 120, 705-716.
67. Watt M and Evans J R 1999b. Proteoid roots. Physiology and development. Plant Physiol. 121, 317-323.
68. Zhang X Q, Li B and Chollet R 1995 In vivo regulatory phosphorylation of soybean-nodule phosphoenolpyruvate carboxylase. Plant Physiol. 108, 1561-1568.
69. Zhang X Q and Chollet R 1997 Phosphoenolpyruvate carboxylase protein kinase from soybean root nodules: partial purification, characterization, and up/down-regulation by photosynthate supply from the shoots. Arch Biochem Biophys. 15, 260-268.