High-affinity k+ transport in arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions

Plant Physiology

Volumn 153, Issue 2, 2010, Pages 863-875

  Pyo, Young Jae ^a   Gierth, Markus ^b   Schroeder, Julian I ^c   Cho, Myeon Haeng ^a  

^a Yonsei University   (South Korea)

^b UNIVERSITY OF COLOGNE   (Germany)

^c SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77953218015     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.154369     Document Type: Article

References (63)

1. Ahn SJ, Shin R and Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134: 1135-1145
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
3. Anderson JA, Huprikar SS, Kochian LV, Lucas WJ and Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89: 3736-3740
4. Armengaud P, Breitling R and Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136: 2556-2576
5. Ashley MK, Grant M and Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57: 425-436
6. Bentsink L and Koornneef M (2008) Seed dormancy and germination. In The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, pp 1-18
7. Bewley JD and Black M (1994) Seeds: Physiology of Development and Germination. Plenum Press, New York
8. Bregante M, Yang Y, Formentin E, Carpaneto A, Schroeder JI, Gambale F, Lo SF and Costa A (2008) KDC1, a carrot Shaker-like potassium channel, reveals its role as a silent regulatory subunit when expressed in plant cells. Plant Mol Biol 66: 61-72
9. Buschmann PH, Vaidyanathan R, Gassmann W and Schroeder JI (2000) Enhancement of Na+ uptake currents, time-dependent inward-rectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiol 122: 1387-1397
10. Desbrosses G, Josefsson C, Rigas S, Hatzopoulos P and Dolan L (2003) AKT1 and TRH1 are required during root hair elongation in Arabidopsis. J Exp Bot 54: 781-788
11. Duby G, Hosy E, Fizames C, Alcon C, Costa A, Sentenac H and Thibaud JB (2008) AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+ channels. Plant J 53: 115-123
12. Elumalai RP, Nagpal P and Reed JW (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14: 119-131
13. Epstein E and Bloom AJ (2005) Mineral Nutrition of Plants: Principles and Perspectives. Sinauer Associates, Sunderland, MA
14. Epstein E, Rains DW and Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49: 684-692
15. Fu HH and Luan S (1998) AtKuP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10: 63-73
16. Fulgenzi FR, Peralta ML, Mangano S, Danna CH, Vallejo AJ, Puigdomenech P and Santa-Maria GE (2008) The ionic environment controls the contribution of the barley HvHAK1 transporter to potassium acquisition. Plant Physiol 147: 252-262
17. Gassmann W and Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat: a mechanism for aluminum-sensitive low-affinity K+ uptake and membrane potential control. Plant Physiol 105: 1399-1408
18. Geiger D, Becker D, Vosloh D, Gambale F, Palme K, Rehers M, Anschuetz U, Dreyer I, Kudla J and Hedrich R (2009) Heteromeric AtKC1/AKT1 channels in Arabidopsis roots facilitate growth under K+ limiting conditions. J Biol Chem 284: 21288-21295
19. Gierth M and Mäser P (2007) Potassium transporters in plants: involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581: 2348-2356
20. Gierth M, Mäser P and Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137: 1105-1114
21. Glass ADM (1983) Regulation of ion-transport. Annu Rev Plant Physiol Plant Mol Biol 34: 311-326
22. Hirsch RE, Lewis BD, Spalding EP and Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280: 918-921
23. Jain A, Poling MD, Smith AP, Nagarajan VK, Lahner B, Meagher RB and Raghothama KG (2009) Variations in the composition of gelling agents affect morphophysiological and molecular responses to deficiencies of phosphate and other nutrients. Plant Physiol 150: 1033-1049
24. Kim EJ, Kwak JM, Uozumi N and Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10: 51-62
25. Kochian LV and Lucas WJ (1982) Potassium transport in corn roots. 1. Resolution of kinetics into a saturable and linear component. Plant Physiol 70: 1723-1731
26. Koornneef M, Alonso-Blanco C and Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55: 141-172
27. Kourie J and Goldsmith MHM (1992) K+ channels are responsible for an inwardly-rectifying current in the plasma membrane of mesophyll protoplasts of Avena sativa. Plant Physiol 98: 1087-1097
28. Kwak JM, Murata Y, Baizabal-Aguirre VM, Merrill J, Wang M, Kemper A, Hawke SD, Tallman G and Schroeder JI (2001) Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol 127: 473-485
29. Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S and Grignon C (1996) Tissue specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9: 195-203
30. Lebaudy A, Very AA and Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581: 2357-2366
31. Li L, Kim BG, Cheong YH, Pandey GK and Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103: 12625-12630
32. Maathuis FJ (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12: 250-258
33. Maathuis FJ and Sanders D (1999) Plasma membrane transport in context: making sense out of complexity. Curr Opin Plant Biol 2: 236-243
34. Maathuis FJM and Sanders D (1995) Contrasting roles in ion transport of two K+-channel types in root cells of Arabidopsis thaliana. Planta 197: 456-464
35. MacKinnon R (2003) Potassium channels. FEBS Lett 555: 62-65
36. Martinez-Cordero MA, Vicente M and Francisco R (2004) Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Mol Biol 56: 413-421
37. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126: 1646-1667
38. Moran N and Satter RL (1989) K+ channels in plasmalemma of motor cells of Samanea saman. In J Dainty, MI Michelis, E Marré and F Rasi-Coldogno, eds, Plant Membrane Transport. Elsevier, Amsterdam, pp 529-530
39. Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ and Schachtman DP (2008) The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. J Exp Bot 59: 595-607
40. Quintero FJ and Blatt MR (1997) A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett 415: 206-211
41. Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K and Hedrich R (2002) AtKC1, a silent Arabidopsis potassium channel alpha-subunit modulates root hair K+ influx. Proc Natl Acad Sci USA 99: 4079-4084
42. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann K, Grabov A, Dolan L and Hatzopoulos P (2001) Trh1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13: 139-151
43. Rubio F, Aleman F, Nieves-Cordones M and Martinez V (2010) Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K uptake. Physiol Plant (in press)
44. Rubio F, Nieves-Cordones M, Aleman F and Martinez V (2008) Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Plant 134: 598-608
45. Rubio F, Santa-Maria GE and Rodriguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109: 34-43
46. Sambrook J and Russell DW (2001) Molecular Cloning: A Laboratory Manual, Ed 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
47. Santa-Maria GE, 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
48. Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA and Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258: 1654-1658
49. Schroeder JI and Fang HH (1991) Inward-rectifying K+ channels in guard cells provide a mechanism for low-affinity K+ uptake. Proc Natl Acad Sci USA 88: 11583-11587
50. Schroeder JI, Hedrich R and Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312: 361-362
51. Schroeder JI, Raschke K and Neher E (1987) Voltage dependence of K+ channels in guard-cell protoplasts. Proc Natl Acad Sci USA 84: 4108-4112
52. Schroeder JI, Ward JM and Gassmann W (1994) Perspectives in the physiology and structure of inward rectifying K+ channels in higher-plants: biophysical implications for K+ uptake. Annu Rev Biophys Biomol Struct 23: 441-471
53. Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge UI and Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131: 16-26
54. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F and Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256: 663-665
55. Shin R and Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101: 8827-8832
56. Siddiqi MY and Glass ADM (1983) Studies of the growth and mineral nutrition of barley varieties. 2. Potassium uptake and its regulation. Can J Bot 61: 1551-1558
57. Siddiqi MY, Glass ADM, Ruth TJ and Rufty TW (1990) Studies of the uptake of nitrate in barley. I. Kinetics of nitrogen-13-labeled nitrate influx. Plant Physiol 93: 1426-1432
58. Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR and Lewis BD (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
59. Sten-Knudsen O and Ussing HH (1981) The flux ratio equation under nonstationary conditions. J Membr Biol 63: 233-242
60. Ussing HH (1969) The interpretation of tracer fluxes in terms of membrane structure. Q Rev Biophys 1: 365-376
61. Wang YH, Garvin DF and Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots: evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130: 1361-1370
62. Ward JM, Mäser P and Schroeder JI (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71: 59-82
63. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L and Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 1347-1360