Planta

, Volume 221, Issue 2, pp 212–221 | Cite as

Rice K+ uptake channel OsAKT1 is sensitive to salt stress

  • Ines Fuchs
  • Sonja Stölzle
  • Natalya Ivashikina
  • Rainer Hedrich
Original Article

Abstract

Potassium ions constitute the most important macronutrients taken up by plants. To unravel the mechanisms of K+ uptake and its sensitivity to salt stress in the model plant rice, we isolated and functionally characterized OsAKT1, a potassium channel homologous to the Arabidopsis root inward rectifier AKT1. OsAKT1 transcripts were predominantly found in the coleoptile and in the roots of young rice seedlings. K+ channel mRNA decreases in response to salt stress, both in the shoot and in the root of 4-day-old rice seedlings. Following expression in HEK293 cells, we were able to characterize OsAKT1 as a voltage-dependent, inward-rectifying K+ channel regulated by extracellular Ca2+ and protons. Patch-clamp studies on rice root protoplasts identified a K+ inward rectifier with similar channel properties as heterologously expressed OsAKT1. In line with the transcriptional downregulation of OsAKT1 in response to salt stress, inward K+ currents were significantly reduced in root protoplasts. Thus, OsAKT1 seems to represent the dominant salt-sensitive K+ uptake channel in rice roots.

Keywords

AKT1 K+ channel Plant nutrition Rice Salt stress 

References

  1. Basset M, Conejero G, Lepetit M, Fourcroy P, Sentenac H (1995) Organization and expression of the gene coding for the potassium transport system AKT1 of Arabidopsis thaliana. Plant Mol Biol 29:947–958CrossRefPubMedGoogle Scholar
  2. Bauer CS, Hoth S, Haga K, Philippar K, Aoki N, Hedrich R (2000) Differential expression and regulation of K+ channels in the maize coleoptile: molecular and biophysical analysis of cells isolated from cortex and vasculature. Plant J 24:139–145CrossRefPubMedGoogle Scholar
  3. Bertl A, Reid J, Sentenac H, Slayman C (1997) Functional comparison of plant inward-rectifier channels expressed in yeast. J Exp Bot 48:405–413Google Scholar
  4. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745–2752PubMedGoogle Scholar
  5. Chi Lin C, Huei Kao C (2001) Relative importance of Na+, Cl, and abscisic acid in NaCl induced inhibition of root growth of rice seedlings. Plant Soil 237:165–171CrossRefGoogle Scholar
  6. Deeken R, Ivashikina N, Czirjak T, Philippar K, Becker D, Ache P, Hedrich R (2003) Tumour development in Arabidopsis thaliana involves the Shakerlike K+ channels AKT1 and AKT2/3. Plant J 34:778–787CrossRefPubMedGoogle Scholar
  7. Dietrich P, Dreyer I, Wiesner P, Hedrich R (1998) Cation sensitivity and kinetics of guard-cell potassium channels differ among species. Planta 205:277–287CrossRefGoogle Scholar
  8. Downey P, Szabo I, Ivashikina N, Negro A, Guzzo F, Ache P, Hedrich R, Terzi M, Schiavo FL (2000) KDC1, a novel carrot root hair K+ channel: cloning, characterization, and expression in mammalian cells. J Biol Chem 275:39420–39426CrossRefPubMedGoogle Scholar
  9. Dreyer I, Antunes S, Hoshi T, Mueller-Roeber B, Palme K, Pongs O, Reintanz B, Hedrich R (1997) Plant K+ channel alpha-subunits assemble indiscriminately. Biophys J 72:2143–2150PubMedGoogle Scholar
  10. Fairley-Grenot KA, Assmann SM (1992) Whole cell K+ current across the plasma membrane of guard cells from a grass: Zea mays. Planta 186:282–293CrossRefGoogle Scholar
  11. Fuchs I, Philippar K, Ljung K, Sandberg G, Hedrich R (2003) Blue light regulates an auxin-induced K+ channel gene in the maize coleoptile. Proc Natl Acad Sci USA 100:11795–11800CrossRefPubMedGoogle Scholar
  12. Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155PubMedGoogle Scholar
  13. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt 24 tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Phys 45:146–159CrossRefGoogle Scholar
  14. Gaymard F, Cerutti M, Horeau C, Lemaillet G, Urbach S, Ravallec M, Devauchelle G, Sentenac H, Thibaud JB (1996) The baculovirus/insect cell system as an alternative to Xenopus oocytes. First characterization of the AKT1 K+ channel from Arabidopsis thaliana. J Biol Chem 271:22863–22870CrossRefPubMedGoogle Scholar
  15. Golldack D, Su H, Quigley F, Kamasani UR, Munoz-Garay C, Balderas E, Popova OV, Bennett J, Bohnert HJ, Pantoja O (2002) Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J 31:529–542CrossRefPubMedGoogle Scholar
  16. Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81CrossRefPubMedGoogle Scholar
  17. Hartje S, Zimmermann S, Klonus D, Mueller-Roeber B (2000) Functional characterisation of LKT1, a K+ uptake channel from tomato root hairs, and comparison with the closely related potato inwardly rectifying K+ channel SKT1 after expression in Xenopus Oocytes. Planta 210:723–731CrossRefPubMedGoogle Scholar
  18. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921CrossRefPubMedGoogle Scholar
  19. Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27:129–138CrossRefPubMedGoogle Scholar
  20. Hoth S, Dreyer I, Dietrich P, Becker D, Muller-Rober B, Hedrich R (1997) Molecular basis of plant-specific acid activation of K+ uptake channels. Proc Natl Acad Sci USA 94:4806–4810Google Scholar
  21. Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Lett 508:463–469CrossRefPubMedGoogle Scholar
  22. Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H et al. (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice: the rice fulllength cDNA consortium. Science 301:376–379CrossRefPubMedGoogle Scholar
  23. Koyama ML, Levesley A, Koebner RMD, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol 125:406–422CrossRefPubMedGoogle Scholar
  24. Kronzucker HJ, Britto DT, Davenport RJ, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337CrossRefPubMedGoogle Scholar
  25. Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C (1996) Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9:195–203CrossRefPubMedGoogle Scholar
  26. Mouline K, Very AA, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev 16:339–350CrossRefPubMedGoogle Scholar
  27. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123–131Google Scholar
  28. Philippar K, Fuchs I, Lüthen H, Hoth S, Bauer C, Haga K, Thiel G, Ljung K, Sandberg G, Böttger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci USA 96:12186–12191CrossRefPubMedGoogle Scholar
  29. Philippar K, Buechsenschuetz K, Abshagen M, Fuchs I, Geiger D, Lacombe B, Hedrich R (2003) The K+ channel KZM1 mediates potassium uptake into the phloem and guard cells of the C4 grass Zea mays. J Biol Chem 278:16973–16981CrossRefPubMedGoogle Scholar
  30. Philippar K, Ivashikina N, Ache P, Christian M, Luthen H, Palme K, Hedrich R (2004) Auxin activates KAT1 and KAT2, two K+-channel genes expressed in seedlings of Arabidopsis thaliana. Plant J 37:815–827CrossRefPubMedGoogle Scholar
  31. Pilot G, Gaymard F, Mouline K, Cherel I, Sentenac H (2003) Regulated expression of Arabidopsis Shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol Biol 51:773–787CrossRefPubMedGoogle Scholar
  32. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441CrossRefPubMedGoogle Scholar
  33. Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R (2002) AtKC1, a silent Arabidopsis potassium channel á- subunit modulates root hair K+ influx. Proc Natl Acad Sci USA 99:4079–4084Google Scholar
  34. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155Google Scholar
  35. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd edn. Cold Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  36. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon CCloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665PubMedGoogle Scholar
  37. Shi H, Zhu JK (2002) Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol 50:543–550CrossRefPubMedGoogle Scholar
  38. Su H, Golldack D, Katsuhara M, Zhao C, Bohnert HJ (2001) Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol 125:604–614CrossRefPubMedGoogle Scholar
  39. Su H, Golldack D, Zhao C, Bohnert HJ (2002) The expression of HAK-Type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493CrossRefPubMedGoogle Scholar
  40. Szyroki A, Ivashikina N, Dietrich P, Roelfsema MRG, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, Palme K, Hedrich R (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA 98:2917–2921Google Scholar
  41. Tester M, Davenport RJ (2003) Na+ Tolerance and Na+ transport in higher plants. Ann Bot 91:503–527CrossRefPubMedGoogle Scholar
  42. Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259CrossRefPubMedGoogle Scholar
  43. Waller F, Furuya M, Nick P (2002) OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol Biol 50:415–425CrossRefPubMedGoogle Scholar
  44. Watad AEA, Reuveni M, Bressan RA, Hasegawa PM (1991) Enhanced net K+ uptake capacity of NaCl-adapted cells. Plant Physiol 95:1265–1269Google Scholar
  45. Wolt JD (1994) Soil solution chemistry: applications to environmental science and agriculture. Wiley, New YorkGoogle Scholar
  46. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedGoogle Scholar
  47. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar
  48. Zimmermann S, Talke I, Ehrhardt T, Nast G, Mueller-Roeber B (1998) Characterization of SKT1, an inwardly rectifying potassium channel from potato, by heterologous expression in insect cells. Plant Physiol 116:879–890CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Ines Fuchs
    • 1
  • Sonja Stölzle
    • 1
    • 2
  • Natalya Ivashikina
    • 1
    • 3
  • Rainer Hedrich
    • 1
  1. 1.Department of Molecular Plant Physiology and BiophysicsUniversity of WürzburgWürzburgGermany
  2. 2.Nanion TechnologiesMunichGermany
  3. 3.All-Russian Research Institute of AgrochemistryMoscowRussia

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