Potassium transport systems in the moss Physcomitrella patens: pphak1 plants reveal the complexity of potassium uptake

Plant Journal

Volumn 52, Issue 6, 2007, Pages 1080-1093

  Garciadeblas, Blanca ^a   Barrero Gil, Javier ^a   Benito, Begoña ^a   Rodríguez Navarro, Alonso ^a  

^a UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

HAK transporters; Mutants; Physcomitrella; Potassium; Potassium channels; Yeast expression

Indexed keywords

HAK TRANSPORTERS; PHYSCOMITRELLA; POTASSIUM CHANNELS; YEAST EXPRESSION;

COMPLEXATION; DATABASE SYSTEMS; GENES; MUTAGENESIS; PLANTS (BOTANY); YEAST;

POTASSIUM COMPOUNDS;

CATION TRANSPORT PROTEIN; HAK1 PROTEIN, PLANT; POTASSIUM; SODIUM; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; BIOLOGY; BRYOPSIDA; EXPRESSED SEQUENCE TAG; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; RICE; SEQUENCE HOMOLOGY; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; ARABIDOPSIS; BIOLOGICAL TRANSPORT; BRYOPSIDA; CATION TRANSPORT PROTEINS; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POTASSIUM; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM;

ARABIDOPSIS; BRYOPHYTA; FUNGI; MAGNOLIOPHYTA; ORYZA SATIVA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 36949013887     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03297.x     Document Type: Article

References (72)

1. + uptake. Plant Physiol. 134, 1135 1145.
2. Alonso-Blanco, C., Peeters, A.J.M., Koornneef, M., Lister, C., Dean, C., Bosch, N.v.d., Pot, J. Kuiper, M.T.R. (1998) Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J. 14, 259 271.
3. Amrutha, R.N., Sekhar, P.N., Varshney, R.V. Kishor, P.B.K. (2007) Genome-wide analysis and identification of genes related to potassium transporter families in rice (Oryza sativa). Plant Sci. 172, 708 721.
4. Ashton, N.W., Cove, D.J. Featherstone, D.R. (1979) The isolation and physiological analysis of mutants of the moss Physcomitrella patens. Planta, 144, 437 442.
5. Bañuelos, M.A., Garciadeblas, B., Cubero, B. Rodríguez- Navarro, A. (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol. 130, 784 795.
6. Benito, B., Garciadeblás, B., Schreier, P. Rodríguez- Navarro, A. (2004) Novel P-type ATPases mediate high-affinity potassium or sodium uptake in fungi. Eukaryot. Cell, 3, 359 368.
7. Borsics, T., Webb, D., Andeme-Ondzighi, C., Staehelin, L.A. Christopher, D.A. (2007) The cyclic nucleotide-gated calmodulin-binding channel AtCNGC10 localizes to the plasma membrane and influences numerous growth responses and starch accumulation in Arabidopsis thaliana. Planta, 225, 563 573.
8. + transport system. J. Exp. Bot. 52, 839 844.
9. Broadley, M.R., Bowen, H.C., Cotterill, H.L., Hammond, J.P., Meacham, M.C., Mead, A. White, P.J. (2004) Phylogenetic variations in the shoot mineral concentration of angiosperms. J. Exp. Bot. 55, 321 336.
10. Brunelli, J.P. Pall, M.L. (1993) A series of yeast/Escherichia coli l expression vectors designed for directional cloning of cDNAs and cre/lox-mediated plasmid excision. Yeast, 9, 1309 1318.
11. Camacho, M., Ramos, J. Rodríguez-Navarro, A. (1981) Potassium requirements of Saccharomyces cerevisiae. Curr. Microbiol. 6, 295 299.
12. Choe, H., Sackin, H. Palmer, L.G. (2000) Permeation properties of inward-rectifier potassium channels and their molecular determinants. J. Gen. Physiol. 115, 391 404.
13. Cove, D., Bezanilla, M., Harries, P. Quatrano, R. (2006) Mosses as model systems for the study of metabolism and development. Annu. Rev. Plant Biol. 57, 497 520.
14. Daram, P., Urbach, S., Gaymard, F., Sentenac, H. Chérel, I. (1997) Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain. EMBO J. 16, 3455 3463.
15. Dennison, K.L., Robertson, W.R., Lewis, B.D., Hirsch, R.E., Sussman, M.R. Spalding, E.P. (2001) Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol. 127, 1012 1019.
16. Dreyer, I., Horeau, C., Lemaillet, G., Zimmermann, S., Bush, D.R., Rodríguez-Navarro, A., Schachtman, D.P., Spalding, E.P., Sentenac, H. Gaber, R.F. (1999) Identification and characterization of plant transporters using heterologous expression systems. J. Exp. Bot. 50, 1073 1078.
17. Elumalai, R.P., Nagpal, P. Reed, J.W. (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell, 14, 119 131.
18. Ermolayeva, E., Hohmeyer, H., Johannes, E. Sanders, D. (1996) Calcium-dependent membrane depolarisation activated by phytochrome in the moss Physcomitrella patens. Planta, 199, 352 358.
19. Ermolayeva, E., Sanders, D. Johannes, E. (1997) Ionic mechanism and role of phytochrome-mediated membrane depolarization in caulonemal side branch initial formation in the moss Physcomitrella patens. Planta, 201, 109 118.
20. Frank, W., Decker, E.L. Reski, R. (2005) Molecular tools to study Physcomitrella patens. Plant Biol, 7, 220 227.
21. Gambale, P. Uozumi, N. (2006) Properties of Shaker-type potassium channels in higher plants. J. Membrane Biol. 210, 1 19.
22. + uptake kinetics in Arabidopsis roots. Plant Physiol. 137, 1105 1114.
23. Gobert, A., Park, G., Amtmann, A., Sanders, D. Maathuis, F. (2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. J. Exp. Bot. 57, 791 800.
24. Goremykin, V.V. Hellwing, F.H. (2005) Evidence for the most basal split in land plants dividing bryophyte and tracheophyte lineages. Plant Syst. Evol. 254, 93 103.
25. Hamilton, R., Watanabe, C.K. Boer, H.A.d. (1987) Compilation and comparison of the sequence context around the AUG startcodons in Saccharomyces cerevisiae mRNAs. Nucleic Acid Res. 15, 3581 3593.
26. Harada, H. Leigh, R.A. (2006) Genetic mapping of natural variation in potassium concentration in shoots of Arabidopsis thaliana. J. Exp. Bot. 57, 953 960.
27. D helix of the TRK1 potassium transporter of Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1613, 1 6.
28. Haro, R., Bañuelos, M.A., Senn, M.E., Barrero-Gil, J. Rodríguez-Navarro, A. (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol. 139, 1495 1506.
29. Hirsch, R.E., Lewis, B.D., Spalding, E.P. Sussman, M.R. (1998) A role for the AKT1 potassium channel in plant nutrition. Science, 280, 918 921.
30. Hohe, A., Egener, T., Lucht, J.M., Holtof, H., Reinhard, C., Schween, G. Reski, R. (2004) An improved and highly standardized transformation procedure allows efficient production of single and multiple targeted gene-knockouts in a moss, Physcomitrella patens. Curr. Genet. 44, 339 347.
31. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J. Bourguignon, J. (2007) A proteomic dissection of Arabidopsis thaliana vacoules isolated from cell culture. Mol. Cell. Proteomics, 6, 394 412.
32. Johannes, E., Ermolayeva, E. Sanders, D. (1997) Red light-induced membrane potential transients in the moss Physcomitella patens: ion channel interaction in phytochrome signalling. J. Exp. Bot. 48, 599 608.
33. Kleffmann, T., Russenberger, W., Zychlinski, A.v., Christopher, W., Sjölander, K., Gruissem, W. Baginsky, S. (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354 362.
34. Klein, M., Frommer, W.B. Ludewig, U. (2003) Various ion channels in leaf protoplasts from the moss Physcomitrella patens. Plant Sci. 164, 657 664.
35. + channel. Planta, 225, 1179 1191.
36. Leng, Q., Mercier, R.W., Hua, B.-G., Fromm, H. Berkowitz, G.A. (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 128, 400 410.
37. Li, X.L., Borsics, T., Harrington, H.M. Christopher, D.A. (2005) Arabidopsis AtCNGC10 rescues potassium channel mutants of E. coli. yeast and Arabidopsis and is regulated by calcium/calmodulin and cyclic GMP in E. coli. Funct. Plant Biol. 32, 643 653.
38. + response in Arabidopsis. Proc. Natl Acad. Sci. USA, 103, 12625 12630.
39. Marschner, H. 1995) Mineral Nutrition of Higher Plants. London : Academic Press.
40. + transporter HAK1 of pepper. Plant Mol. Biol. 56, 413 421.
41. + uptake in pepper plants. J. Exp. Bot. 56, 1553 1562.
42. Mäser, P., Thomine, S., Schroeder, J.I. et al. (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126, 1646 1667.
43. Mäser, P., Gierth, M. Schroeder, J.I. (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil, 247, 43 54.
44. Nishiyama, T., Fujita, T., Shin, T. et al. (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc. Natl Acad. Sci. USA, 24, 8007 8012.
45. Oborn, I., Andrist-Rangel, Y., Askekaard, M., Grant, C.A., Watson, C.A. Edwards, A.C. (2005) Critical aspects of potassium management in agricultural systems. Soil Use Manag. 21, 102 112.
46. Palmer, J.D., Soltis, D.E. Chase, M.W. (2004) The plant tree of life: an overview and some points of view. Am. J. Bot. 91, 1437 1445.
47. Payne, K.A., Bowen, H.C., Hammond, J.P., Hampton, C.R., Lynn, J.R., Mead, A., Swarup, K., Bennett, M.J., White, P.J. Broadley, M.R. (2004) Natural genetic variation in caesium (Cs) accumulation by Arabidopsis thaliana. New Phytol. 162, 535 548.
48. Peltier, J.-B., Ytterberg, A.J., Sun, Q. Wijk, K.J.v. (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J. Biol. Chem. 279, 49367 49383.
49. + channel family in higher plants. J. Mol. Evol. 56, 418 434.
50. Qiu, Y.L., Li, L., Wang, B. et al. (2006) The deepest divergence in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA, 103, 15511 15516.
51. + homeostasis. Proc. Natl Acad. Sci. USA, 99, 9061 9066.
52. Reski, R. (2005) Do we need another model plant? Plant Biol. 7, 219.
53. Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K.A., Grabov, A., Dolan, L. Hatzopoulos, P. (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell, 13, 139 151.
54. Rodríguez-Navarro, A. (2000) Potassium transport in fungi and plants. Biochim. Biophys. Acta, 1469, 1 30.
55. Rodríguez-Navarro, A. Ramos, J. (1984) Dual system for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 159, 940 945.
56. Rodríguez-Navarro, A. Rubio, F. (2006) High-affinity potassium and sodium transport systems in plants. J. Exp. Bot. 57, 1149 1160.
57. Rubio, F., Santa-María, G.E. Rodríguez-Navarro, A. (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol. Plant. 109, 34 43.
58. Rubio-Somoza, I., Martinez, M., Diaz, I. Carbonero, P. (2006) HvMCD1, a R1MYB transcription factor from barley with antagonistic regulatory functions during development and germination. Plant J. 45, 17 30.
59. Santa-María, G.E., Rubio, F., Dubcovsky, J. Rodríguez- 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.
60. Santa-María, G.E., Danna, C.H. Czibener, C. (2000) High-affinity potassium transport in barley roots. Ammonium-sensitive and -insensitive pathways. Plant Physiol. 123, 297 306.
61. Schaefer, D.G. Zyrd, J.-P. (2001) The moss Physcomitrella patens, now and then. Plant Physiol. 127, 1430 1438.
62. Schneider, A. (2003) Characterization of soil potassium supply as derived from sorption-desorption experiments. Plant Soil, 251, 331 341.
63. Senn, M.E., Rubio, F., Bañuelos, M.A. Rodríguez-Navarro, A. (2001) Comparative functional features of plant potassium HvHAK1 and HvHAK2 transporters. J. Biol. Chem. 276, 44563 44569.
64. Spalding, E.P., Hirsch, R.E., Lewis, D.R., Qi, Z., Sussman, M.R. Lewis, B.D. (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity. Inhibition by ammonium and stimulation by sodium. J. Gen. Physiol. 113, 909 918.
65. + cycling and pool-size dynamics define low-affinity potassium transport in barley. Plant Physiol. 141, 1494 1507.
66. + transport in higher plants. Annu. Rev. Plant Biol. 54, 575 603.
67. Vreugdenhil, D., Aarts, M.G., Koornneef, M., Nelissen, H. Ernst, W.H.O. (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant Cell Environ. 27, 828 839.
68. White, P.J. (1999) The molecular mechanism of sodium influx to root cells. Trends Plant Sci. 4, 245 246.
69. White, P.J. Broadley, M.R. (2000) Mechanisms of caesium uptake by plants. New Phytol. 147, 241 256.
70. + transporter AKT1 in Arabidopsis. Cell, 125, 1347 1360.
71. Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G. Bhattacharya, D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21, 809 818.
72. Zhu, Y.-G. Smolders, E. (2000) Plant uptake of radiocaesium: a review of mechanisms, regulation and application. J. Exp. Bot. 51, 1635 1645.