Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase

Plant Physiology

Volumn 135, Issue 1, 2004, Pages 549-560

  Shane, Michael W ^a   Cramer, Michael D ^a,b   Funayama Noguchi, Sachiko ^a,c   Cawthray, Gregory R ^a   Millar, A Harvey ^a   Day, David A ^a   Lambers, Hans ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; ENZYMES; OXYGEN; PHOSPHORUS; PHYSIOLOGY; SYNTHESIS (CHEMICAL);

CLUSTER ROOTS; ELECTRON TRANSPORT; MITOCHONDRIA;

PLANTS (BOTANY);

HAKEA; HAKEA PROSTRATA; PROTEACEAE;

EID: 2442684437     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.035659     Document Type: Article

References (54)

1. 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: 233-240
2. Chollet R, Vidal J, O'Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273-298
3. Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM, Wiskich JT (1996) The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiol 110: 1-2
4. Day DA, Neuburger M, Douce R (1985) Biochemical characterisation of chlorophyll-free mitochondria from pea leaves. Aust J Plant Physiol 12: 219-228
5. Dell B, Kuo J, Thomson CJ (1980) Development of proteoid roots in Hakea obliqua R.Br. (Proteaceae) grown in water culture. Aust J Bot 28: 27-37
6. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid root clusters and other root clusters. Bot Acta 108: 183-200
7. Dinkelaker B, Hengeler C, Neumann G, Eltrop L, Marschner H (1997) Root exudates and mobilization of nutrients. In H Rennenberg, W Eschrich, H Ziegler, eds, Trees: Contributions to Modern Tree Physiology. Backhuys Publishers, Leiden, The Netherlands, pp 441-452
8. Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol 89: 1311-1317
9. Gardner W, Barber D, 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
10. Gerke J (1992) Phosphate, aluminium and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Z Pflanzenernaehr Bodenk 155: 339-342
11. Grierson PF, Attiwill PM (1989) Chemical characteristics of the proteoid root mat of Banksia integrifolia L. f. Aust J Bot 37: 137-143
12. Guy RD, Berry JA, Fogel ML, Turpin DH, Weger HG (1992) Fractionation of the stable isotopes of oxygen during respiration by plants - the basis of a new technique to estimate partitioning to the alternative path. In H Lambers, LHW Van der Plas, eds, Plant Respiration. Molecular, Biochemical and Physiological Aspects. SPB Academic Publishing, The Hague, The Netherlands, pp 443-453
13. 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
14. Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35: 241-289
15. Hoffland E, Findenegg GR, Nelemans JA (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
16. Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104: 657-665
17. Johnson JF, Allan DL, Vance CP, 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
18. Johnson JF, Vance CP, Allan DL (1996b) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol 112: 31-41
19. Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205: 25-44
20. Kania A, Langlade N, Martinoia E, Neumann G (2003) Phosphorus deficiency-induced modifications in citrate catabolism and in cytosolic pH as related to citrate exudation in cluster roots of white lupin. Plant Soil 248: 117-127
21. Kearns A, Whelan J, Young S, Elthon TE, Day DA (1992) Tissue-specific expression of the alternative oxidase in soybean and siratro. Plant Physiol 99: 712-717
22. Keerthisinghe G, Hocking P, Ryan PR, 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
23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
24. Lambers H (1997) Oxidation of mitochondrial NADH and the synthesis of ATP. In DT Dennis, DH Turpin, DD Lefebrve, DB Layzell, eds, Plant Metabolism. Longman Singapore Publishers, Singapore, pp 200-219
25. Lambers H, Atkin OA, Millenaar FF (2002b) Respiratory patterns in roots. In Y Waisel, A Eshel, U Kafkafi, eds, Plant Roots the Hidden Half, Ed 3. Marcel Dekker, New York, pp 521-552
26. Lambers H, Cramer MD, Shane MW, Wouterlood M, Poot P, Veneklaas EJ (2003) Structure and functioning of cluster roots and plant responses to phosphate deficiency. Plant Soil 248: ix-xix
27. Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martinez E (2002a) 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
28. Lambers H, Van der Werf A, Bergkotte M (1993) Assessment of the capacity and activity of the alternative respiratory pathway in intact tissues. In GAF Hendry, JP Grime, eds, Methods in Comparative Plant Ecology - A Laboratory Manual. Chapman and Hall, London, pp 140-144
29. Lamont B (1972) The morphology and anatomy of proteoid roots in the genus Hakea. Aust J Bot 20: 155-174
30. Lamont BB (2003) Structure, ecology and physiology of root clusters-a review. Plant Soil 248: 1-19
31. Massonneau A, Langlade N, Léon 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 231: 534-542
32. McCully ME (1975) The development of lateral roots. In JG Torrey, DT Clarkson, eds, The Development and Function of Roots, Third Cabot Symposium. Academic Press, New York, pp 105-124
33. McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol 50: 695-718
34. Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5: 2-15
35. Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate blue and malachite green. Analyst 108: 361-367
36. Myets N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858
37. Neumann G, Martinoia E (2002) Cluster roots - an underground adaptation for survival in extreme environments. Trends Plant Sci 7: 162-167
38. 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
39. Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211: 121-130
40. Pate JS, Bell TL (1999) Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agrofor Syst 45: 303-341
41. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83: 346-356
42. 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
43. Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24: 891-904
44. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52: 527-560
45. Rychter AM, Mikulska M (1990) The relationship between phosphate status and cyanide-resistant respiration in bean roots. Physiol Plant 79: 663-667
46. Sanchez R, Cejudo FJ (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132: 949-957
47. Schuller KA, Turpin DH, Plaxton WC (1990) Metabolite regulation of partially purified soybean nodule phosphoenolpyruvate carboxylase. Plant Physiol 94: 1429-1435
48. Shane MW, De Vos M, De Roock S, Cawthray GR, Lambers H (2003) 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: 209-219
49. Smith FW, Jackson WA, Vanden-Berg PJ (1990) Internal phosphorus flows during development of phosphorus stress in Stylosanthes hamata. Aust J Plant Physiol 17: 451-464
50. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, London
51. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101: 339-344
52. Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248: 99-116
53. 2 concentration. Plant Physiol 120: 705-716
54. Watt M, Evans JR (1999b) Proteoid roots: physiology and development. Plant Physiol 121: 317-323