Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments

Plant Journal

Volumn 39, Issue 4, 2004, Pages 629-642

  Shin, Heungsop ^a   Shin, Hwa Soo ^a   Dewbre, Gary R ^a   Harrison, Maria J ^b  

^a PLANT BIOLOGY DIVISION   (United States)

^b United States Department of Agriculture   (United States)

Author keywords

Membrane protein; Mineral nutrition; Phosphorus; Roots

Indexed keywords

GENES; METABOLISM; PHOSPHATES;

ARABIDOPSIS; CELLULAR METABOLISMS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; PHOSPHATE;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PLANT ROOT; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MUTATION; PHOSPHATES; PLANT ROOTS; SIGNAL TRANSDUCTION;

GENES; METABOLISM; PHOSPHATES; PLANTS;

ARABIDOPSIS;

EID: 4143054697     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02161.x     Document Type: Article

References (73)

1. Abel, S., Nurnberger, T., Ahnert, V., Krauss, G.-J. and Glund, K. (2000) Induction of an extracellular cyclic nucleotide phosphodiesterase as an accessory ribonucleolytic activity during phosphate starvation of cultured tomato cells. Plant Physiol. 122, 543-552.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
3. Ames, B.N. (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Meth. Enzymol. 8, 115-118.
4. Arnon, D.I. and Hoagland, D.R. (1940) Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci. 50, 463-483.
5. Bariola, P.A., Howard, C.J., Taylor, C.B., Verburg, M.T., Jaglan, V.D. and Green, P.J. (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 6, 673-685.
6. Bieleski, R.L. (1973) Phosphate pools, phosphate transport and phosphate availability. Ann. Rev. Plant Physiol. 24, 225-252.
7. Bieleski, R.L. and Ferguson, I.B. (1983) Physiology and metabolism of phosphate and its compounds. In Encyclopedia of Plant Physiology (Lauchi, A. and Bieleski, R.L., eds). New York: Springer-Verlag, pp. 422-449.
8. Bucher, M., Rausch, C. and Daram, P. (2001) Molecular and biochemical mechanisms of phosphorus uptake into plants. J. Plant Nutr. Soil Sci. 164, 209-217.
9. Bun-ya, M., Nishimura, M., Harashima, S. and Oshima, Y. (1991) The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol. Cell. Biol. 11, 3229-3238.
10. Burleigh, S.H. and Harrison, M.J. (1998) Expression of phosphate transporters and the phosphate starvation-inducible gene Mt4 in mycorrhizal roots. In Phosphorous in Plant Biology: Regulatory Roles in Molecular Cellular, Organismic, and Ecosystem Processes (Lynch, J.P. and Deikman, J., eds). Rockville, MD: American Society of Plant Physiologists, pp. 261-270.
11. Burleigh, S.H. and Harrison, M.J. (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol. 119, 241-248.
12. Caspari, T., Stadler, R., Sauer, N. and Tanner, W. (1994) Structure/function relationship of the Chlorella glucose/H+ symporter. J. Biol. Chem. 269, 3498-3502.
13. Chiou, T.J., Liu, H. and Harrison, M.J. (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J. 25, 1-15.
14. Chiu, W.-I., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.
15. Clark, G.T., Dunlop, J. and Phung, H.T. (2000) Phosphate absorption by Arabidopsis thaliana: interactions between phosphorus status and inhibition by arsenate. Aust. J. Agric. Res. 27, 959-965.
16. Clarkson, D.T. and Scattergood, C.B. (1982) Growth and phosphate transport in barley and tomato plants during the development of, and recovery from, phosphate-stress. J. Exp. Bot. 33, 865-875.
17. Cogliatti, H.H. and Clarkson, D.T. (1983) Physiological changes in, and phosphate uptake by potato plants during development of, and recovery from phosphate deficiency. Physiol. Plant. 58, 287-294.
18. Daram, P., Brunner, S., Persson, B.L., Amrhein, N. and Bucher, M. (1998) Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta, 206, 225-233.
19. Drew, M. (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75, 479-490.
20. Duff, S.M., Plaxton, W.c. and Lefebvre, D.D. (1991) Phosphate-starvation response in plant cells: de novo synthesis and degradation of acid phosphatases. Proc. Natl Acad. Sci. USA, 88, 9538-9542.
21. Dunlop, J., Phung, H.T., Meeking, R. and White, D.W.R. (1997) The kinetics associated with phosphate absorption by Arabidopsis and its regulation by phosphorus status. Aust. J. Plant Physiol. 24, 623-629.
22. Epstein, E. (1972) Mineral Nutrition of Plants: Principles and Perspectives. New York: John Wiley and Sons, Inc., pp. 132-141.
23. Fu, H.-H. and Luan, S. (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell, 10, 63-74.
24. Harrison, M.J. (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 50, 361-389.
25. Harrison, M.J. and van Buuren, M.L. (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature, 378, 626-629.
26. Harrison, M.J., Dewbre, G.R. and Liu, J. (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell, 14, 2413-2429.
27. Hebert, D. and Carruthers, A. (1992) Glucose transporter oligomeric structure determines transporter function. Reversible redox-dependent interconversions of tetrameric and dimeric GLUT1. J. Biol. Chem. 267, 23829-23838.
28. Hirsch, R., Lewis, B., Spalding, E. and Sussman, M. (1998) A role for the AKT1 potassium channel in plant nutrition. Science, 280, 918-921.
29. Holford, I.C.R. (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust. J. Soil Res. 35, 227-239.
30. Karthikeyan, A.S., Varadarajan, D.K., Mukatira, U.T., D'Urzo, M.P., Damsz, B. and Raghothama, K.G. (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol. 130, 221-233.
31. Kim, E.J., Kwak, J.M., Uozumi, N. and Schroeder, J.I. (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell, 10, 51-62.
32. Lee, D.A., Chen, A. and Schroeder, J.I. (2003) ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J. 35, 637-646.
33. Leggewie, G., Willmitzer, L. and Riesmeier, J.W. (1997) Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell, 9, 381-392.
34. Liu, K. and Tsay, Y.-F. (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22, 1005-1013.
35. Liu, C., Muchhal, U.S. and Raghothama, K.G. (1997) Differential expression of TPS11, a phosphate starvation-induced gene in tomato. Plant Mol. Biol. 33, 867-874.
36. Liu, C., Muchhal, U.S., Uthappa, M., Kononowicz, A.K. and Raghothama, K.G. (1998a) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol. 116, 91-99.
37. Liu, H., Trieu, A.T., Blaylock, L.A. and Harrison, M.J. (1998b) Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (aM) fungi. Mol. Plant Microbe Interact. 11, 14-22.
38. Liu, K.-H., Huang, C.-Y. and Tsay, Y.-F. (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell, 11, 865-874.
39. Lynch, J. (1995) Root architecture and plant productivity. Plant Physiol. 109, 7-13.
40. Ma, Z., Baskin, T.I., Brown, K.M. and Lynch, J.P. (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol. 131, 1381-1390.
41. Marschner, H. (1995) Mineral Nutrition of Higher Plants. London: London Academic Press.
42. Meharg, A.A. and Hartley-Whitaker, J. (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol. 154, 29-44.
43. Meharg, A.A. and Macnair, M.R. (1990) An altered phosphate uptake system in arsenate-tolerant Holcus lanatus L. New Phytol. 116, 29-35.
44. Meharg, A.A. and Macnair, M.R. (1992) Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J. Exp. Bot. 43, 519-524.
45. Mitsukawa, N., Okumura, S., Shirano, Y., Sato, S., Kato, T., Harashima, S. and Shibata, D. (1997) Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proc. Natl Acad. Sci. USA, 94, 7098-7102.
46. Muchhal, U.S. and Raghothama, K.G. (1999) Transcriptional regulation of plant phosphate transporters. Proc. Natl Acad. Sci. USA, 96, 5868-5872.
47. Muchhal, U.S., Pardo, J.M. and Raghothama, K.G. (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 93, 101519-110523.
48. Mudge, S.R., Rae, A.L., Diatloff, E. and Smith, F.W. (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J. 31, 341-353.
49. Okumura, S., Mitsukawa, N., Shirano, Y. and Shibata, D. (1998) Phosphate transporter gene family of Arabidopsis thaliana. DNA Res. 5, 261-269.
50. Oparka, K.J. (1994) Plasmolysis - new insights into an old process. New Phytol. 126, 571-591.
51. Oparka, K.J., Prior, D.A.M., and Crawford, J.W. (1994) Behavior of plasma-membrane, cortical Er and plasmodesmata during plasmolysis of onion epidermal-cells. Plant Cell Environ. 17, 163-171.
52. Pao, S.S., Paulsen, I.T. and Saier, M.H., (1998) Major facilitator superfamily. Microbiol. Mol. Biol. 62, 1-34.
53. Paszkowski, U., Kroken, S., Roux, C. and Briggs, S.P. (2002) Rice phosphate transporters include an evolutionary divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA, 99, 13324-13329.
54. Poirier, Y., Thoma, S., Somerville, C. and Schiefelbein, J. (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 97, 1087-1093.
55. Raghothama, K. (1999) Phosphate acquisition. Annu. Rev. Plant Physiol. Mol. Biol. 50, 665-693.
56. Rausch, C. and Bucher, M. (2002) Molecular mechanisms of phosphate transport in plants. Planta, 216, 23-37.
57. Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., Amrhein, N. and Bucher, M. (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature, 414, 462-466.
58. Reinders, A., Schulze, W., Kuhn, C., Barker, L., Schulz, A., Ward, J.M. and Frommer, W.B. (2002) Protein-protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell, 14, 1567-1577.
59. Richardson, A.E. (1994) Soil microorganisms and phosphorus availability. In Soil biota management in sustainable farming systems (Prankhurst, B.D.C.E., Gupta, V.V.S.R. and Grace, P.R., eds). Melbourne: CSIRO, pp. 50-62.
60. Robinson, D. (1994) Tansley Review No. 73: the responses of plants to non-uniform supplies of nutrients. New Phytol. 127, 635-674.
61. Schachtman, D.P., Reid, R.J. and Ayling, S.M. (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116, 447-453.
62. Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbiosis. San Diego, CA: Academic Press, Inc.
63. Smith, F.W., Ealing, P.M., Dong, B. and Delhaize, E. (1997) The cloning of two Arabidopsis genes belonging to a phosphate transporter family. Plant J. 11, 83-92.
64. Ticconi, C.A., Delatorre, C.A., Lahner, B., Salt, D.E. and Abel, S. (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J. 37, 801-814.
65. Trueman, L.J., Richardson, A. and Forde, B.G. (1996) Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene, 175, 223-231.
66. Tsay, Y.-F., Schroeder, J.I., Feldmann, K.A. and Crawford, N.M. (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell, 72, 705-713.
67. + gene of Neurospora crassa. Gene, 153, 135-139.
68. Versaw, W.K. and Harrison, M.J. (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell, 14, 1751-1766.
69. Wang, R., Liu, D. and Crawford, N.M. (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. PNAS, 95, 15134-15139.
70. Will, A., Grassl, R., Erdmenger, J., Caspari, T. and Tanner, W. (1998) Alteration of substrate affinities and specificities of the Chlorella hexose/H+ symporters by mutations and construction of chimeras. J. Biol. Chem. 273, 11456-11462.
71. Williamson, L.C., Ribrioux, S.P.C.P., Fitter, A.M. and Ottoline Leyser, H.M. (2001) Phosphate availability regulates root system architecture in arabidopsis. Plant Physiol. 126, 875-882.
72. Wykoff, D.D. and O'Shea, E.K. (2001) Phosphate transport and sensing in Saccharomyces cerevisiae. Genetics, 159, 1491-1499.
73. Zhao, L., Versaw, W.K., Liu, J. and Harrison, M.J. (2003) A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. New Phytol. 157, 291-302.