Skip to main content
Log in

Rice K+ uptake channel OsAKT1 is sensitive to salt stress

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 29:947–958

    Article  CAS  PubMed  Google Scholar 

  • 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 24:139–145

    Article  CAS  PubMed  Google Scholar 

  • Bertl A, Reid J, Sentenac H, Slayman C (1997) Functional comparison of plant inward-rectifier channels expressed in yeast. J Exp Bot 48:405–413

    CAS  Google Scholar 

  • Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745–2752

    CAS  PubMed  Google Scholar 

  • 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 237:165–171

    Article  Google Scholar 

  • 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 34:778–787

    Article  CAS  PubMed  Google Scholar 

  • Dietrich P, Dreyer I, Wiesner P, Hedrich R (1998) Cation sensitivity and kinetics of guard-cell potassium channels differ among species. Planta 205:277–287

    Article  CAS  Google Scholar 

  • 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 275:39420–39426

    Article  CAS  PubMed  Google Scholar 

  • 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 72:2143–2150

    CAS  PubMed  Google Scholar 

  • Fairley-Grenot KA, Assmann SM (1992) Whole cell K+ current across the plasma membrane of guard cells from a grass: Zea mays. Planta 186:282–293

    Article  CAS  Google Scholar 

  • 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 100:11795–11800

    Article  CAS  PubMed  Google Scholar 

  • Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155

    CAS  PubMed  Google Scholar 

  • 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 45:146–159

    Article  CAS  Google Scholar 

  • 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 271:22863–22870

    Article  CAS  PubMed  Google Scholar 

  • 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 31:529–542

    Article  CAS  PubMed  Google Scholar 

  • 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 51:71–81

    Article  CAS  PubMed  Google Scholar 

  • 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 210:723–731

    Article  CAS  PubMed  Google Scholar 

  • Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921

    Article  CAS  PubMed  Google Scholar 

  • 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 27:129–138

    Article  CAS  PubMed  Google Scholar 

  • 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 94:4806–4810

    Google Scholar 

  • 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 508:463–469

    Article  CAS  PubMed  Google Scholar 

  • 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 301:376–379

    Article  PubMed  Google Scholar 

  • 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 125:406–422

    Article  CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Britto DT, Davenport RJ, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337

    Article  CAS  PubMed  Google Scholar 

  • 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 9:195–203

    Article  CAS  PubMed  Google Scholar 

  • 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 16:339–350

    Article  CAS  PubMed  Google Scholar 

  • Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123–131

    CAS  Google Scholar 

  • 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 96:12186–12191

    Article  CAS  PubMed  Google Scholar 

  • 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 278:16973–16981

    Article  CAS  PubMed  Google Scholar 

  • 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 37:815–827

    Article  CAS  PubMed  Google Scholar 

  • 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 51:773–787

    Article  CAS  PubMed  Google Scholar 

  • 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 99:8436–8441

    Article  CAS  PubMed  Google Scholar 

  • 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 99:4079–4084

    Google Scholar 

  • 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 98:14150–14155

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd edn. Cold Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • 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 256:663–665

    CAS  PubMed  Google Scholar 

  • 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 50:543–550

    Article  CAS  PubMed  Google Scholar 

  • 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 125:604–614

    Article  CAS  PubMed  Google Scholar 

  • 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 129:1482–1493

    Article  CAS  PubMed  Google Scholar 

  • 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 98:2917–2921

    Google Scholar 

  • Tester M, Davenport RJ (2003) Na+ Tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • 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 122:1249–1259

    Article  CAS  PubMed  Google Scholar 

  • 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 50:415–425

    Article  CAS  PubMed  Google Scholar 

  • Watad AEA, Reuveni M, Bressan RA, Hasegawa PM (1991) Enhanced net K+ uptake capacity of NaCl-adapted cells. Plant Physiol 95:1265–1269

    CAS  Google Scholar 

  • Wolt JD (1994) Soil solution chemistry: applications to environmental science and agriculture. Wiley, New York

    Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

  • 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 116:879–890

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank D. Becker (University of Würzburg) for helpful discussions, P. Dietrich (University of Würzburg) and I. Marten (University of Würzburg) for critical reading and comments on the manuscript. We are also grateful to P. Nick (University of Karlsruhe) for providing a clone of OsARF1. This work was supported by a Körber European Science Award to R.H.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rainer Hedrich.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fuchs, I., Stölzle, S., Ivashikina, N. et al. Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221, 212–221 (2005). https://doi.org/10.1007/s00425-004-1437-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1437-9

Keywords

Navigation