Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation

EMBO Journal

Volumn 22, Issue 5, 2003, Pages 1005-1013

  Liu, Kun Hsiang ^a,b   Tsay, Yi Fang ^b  

^a ACADEMIA SINICA   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

Affinity; Arabidopsis; Nitrate; Phosphorylation; Transporter

Indexed keywords

NITRATE TRANSPORTER; PROTEIN CHL1; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DEPHOSPHORYLATION; FEMALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

ANIMALS; ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MUTAGENESIS, SITE-DIRECTED; NITRATES; NITROGEN; OOCYTES; PHOSPHORYLATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; THREONINE; XENOPUS LAEVIS;

ANIMALIA; ARABIDOPSIS;

EID: 0037416191     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg118     Document Type: Article

References (52)

1. Adan, C.-C., Chen, D.L., Yeh, K.-C. and Abel, S. (2000) Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol., 124, 1728-1838.
2. Anderson, J.A., Huprikar, S.S., Kochian, L.V., Lucas, W.J. and Gaber, R.F. (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 89, 3736-3740.
3. Bechtold, N., Ellis, J. and Pelletier, G.C.R. (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris, 316, 1194-1199.
4. ATP channel: separate roles of Kir6.2 and SURI subunit phosphorylation. EMBO J., 18, 4722-4732.
5. Bibb, J.A. et al. (1999) Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signaling in neurons. Nature, 402, 669-671.
6. Blakely, R.D. and Bauman, A.L. (2000) Biogenic amine transporters: regulation in flux. Curr. Opin. Neurobiol., 10, 328-336.
7. Boll, M., Herget, M., Wagener, M., Weber, W.M., Markovich, D., Biber, J. and Clauss, W. (1996) Expression cloning and functional characterization of the kidney cortex high-affinity proton-coupled peptide transporter. Proc. Natl Acad. Sci. USA, 93, 284-289.
8. Cahalan, M.D. (2001) Cell biology. Channels as enzymes. Nature, 411, 542-543.
9. Covitz, K.M., Amidon, G.L. and Sadee, W. (1998) Membrane topology of the human dipeptide transporter, hPEPT1, determined by epitope insertions. Biochemistry, 37, 15214-15221.
10. 2+ channels. Nature, 411, 484-489.
11. Doddema, H. and Telkamp, G.P. (1979) Uptake of nitrate by mutants of Arabidopsis thaliana, disturbed in uptake or reduction of nitrate. Physiol. Plant, 45, 332-338.
12. Epstein, E. (1972) Mineral Nutrition of Plants: Principles and Perspectives. Wiley, New York, NY.
13. + channel modulated by a functionally associated protein kinase. Nature, 369, 563-565.
14. Fei, Y.-J., Kanai, Y., Nussberger, S., Ganapathy, V., Leibach, F.H., Romero, M.F., Singh, S.K., Boron, W.F. and Hediger, M.A. (1994) Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature, 368, 563-566.
15. + transporter from Arabidopsis. Plant Cell, 10, 63-73.
16. +-ATPase AHA2 involves the three C-terminal residues Tyr946-Thr-Val and requires phosphorylation of Thr947. J. Biol. Chem., 274, 36774-36780.
17. Glass, A.D.M. and Siddiqi, M.Y. (1995) Nitrogen absorption by plant roots. In Srivastava, H.S. and Singh, R.P. (eds), Nitrogen Nutrition in Higher Plants. Associated Publishing Co., New Delhi, India, pp. 21-56.
18. Gong, J., Xu, J., Bezanila, M., van Huizen, R., Derin, R. and Li, M. (1999) Differential stimulation of PKC phosphorylation of potassium channels by ZIP1 and ZIP2. Science, 285, 1565-1569.
19. Guo, F.Q., Wang, R., Chen, M. and Crawford, N.M. (2001) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell, 13, 1761-1777.
20. Hagting, A., vdVelde, J., Poolman, B. and Konings, W.N. (1997) Membrane topology of the di- and tripeptide transport protein of Lactococcus lactis. Biochemistry, 36, 6777-6785.
21. Higuchi, R. (1990) Recombinant PCR. In Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J. (eds), PCR protocols. Academic Press, San Diego, CA, pp. 177-183.
22. Hirsch, R.E., Lewis, B.D., Spalding, E.P. and Sussman, M.R. (1998) A role for the AKT1 potassium channel in plant nutrition. Science, 280, 918-921.
23. Huang, N.-C., Chiang, C.-S., Crawford, N.M. and Tsay, Y.-F. (1996) CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell, 8, 2183-2191.
24. Huang, N.-C., Liu, K.-H., Lo, H.-J. and Tsay, Y.-F. (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell, 11, 1381-1392.
25. 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.
26. Kochian, L.V. and Lucas, W.J. (1988) Potassium transport in roots. Adv. Bot. Res., 15, 93-178.
27. + channel function by the Kvb1.3 subunit. J. Biol. Chem., 274, 25355-25361.
28. Leibach, F.H. and Ganapathy, V. (1996) Peptide transporters in the intestine and the kidney. Annu. Rev. Nutr., 16, 99-119.
29. + channel determined by construction of multimeric cDNAs. Neuron, 9, 861-871.
30. 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.
31. +/peptide cotransporter family from human kidney. Biochim. Biophys. Acta, 1235, 461-466.
32. + channels. Plant Physiol., 114, 1141-1149.
33. Maurel, C., Kado, R.T., Guern, J. and Chrispeels, M.J. (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J., 14, 3028-3035.
34. Mehrens, T., Lelleck, S., Cetinkaya, I., Knollmann, M., Hohage, H., Gorboulev, V., Boknik, P., Koepsell, H. and Schlatter, E. (2000) The affinity of the organic cation transporter rOCT1 is increased by protein kinase C-dependent phosphorylation. J. Am. Soc. Nephrol., 11, 1216-1224.
35. Mengel, K. and Kirkby, E.A. (1987) Principles of Plant Nutrition. International Potash Institute, Bern, Switzerland.
36. Paulsen, I.T. and Skurray, R.A. (1994) The POT family of transport proteins. Trends Biochem. Sci., 19, 404.
37. Perraud, A.L. et al. (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature, 411, 595-599.
38. 2+ channel β3 subunit enhances voltage-dependent relief of G-protein inhibition induced by muscarinic receptor activation and Gβγ. J. Neurosci., 18, 4883-4890.
39. Runnels, L.W., Yue, L. and Clapham, D.E. (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science, 291, 1043-1047.
40. Saito, H., Terada, T., Okuda, M., Sasaki, S. and Inui, K. (1996) Molecular cloning and tissue distribution of rat peptide transporter PEPT2. Biochim. Biophys. Acta, 1280, 173-177.
41. Santa-Maria, G.E., Rubio, F., Dubcovsky, J. and Rodriguez-Navarro, A. (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell, 9, 2281-2289.
42. Schiff, M.L., Siderovski, D.P., Jordan, J.D., Brothers, G., Snow, B., De Vries, L., Ortiz, D.F. and Diverse-Pierluissi, M. (2000) Tyrosine kinase-dependent recruitment of RGS12 to the N-type calcium channel. Nature, 408, 723-727.
43. Sentenac, H., Bonneaud, N., Minet, M., Lacroute, F., Salmon, J.-M., Gaymard, F. and Grignon, C. (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science, 256, 663-665.
44. +-ATPase creates a binding site for the regulatory 14-3-3 protein. Plant Cell, 11, 2379-2392.
45. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
46. - fluxes in the chll-5 mutant of Arabidopsis thaliana. Plant Physiol., 114, 137-144.
47. 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.
48. 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.
49. Wang, R., Liu, D. and Crawford, N.M. (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl Acad. Sci. USA, 95, 15134-15139.
50. 2+-independent reduction of N-methyl-D-aspartate channel activity by protein tyrosin phosphatase. Proc. Natl Acad. Sci. USA, 93, 1721-1725.
51. Williams, L. and Miller, A. (2001) Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, 659-688.
52. + channel, ROMK, by cyclic AMP-dependent protein kinase. J. Biol. Chem., 271, 9313-9319.