Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1993 Apr;5(4):477–484. doi: 10.1105/tpc.5.4.477

Activation of K+ Channels in the Plasma Membrane of Arabidopsis by ATP Produced Photosynthetically.

EP Spalding 1, M Goldsmith 1
PMCID: PMC160286  PMID: 12271073

Abstract

Light activates a K+ channel and transiently depolarizes the plasma membrane of Arabidopsis mesophyll cells. Genetically or chemically impairing photosynthesis abolished this electrical response to light. These results indicate that illuminated chloroplasts produce a factor that activated K+ channels in the plasma membrane. By patch clamping at the single-channel level, we have obtained evidence that ATP is one such factor. Application of 0.2 to 2 mM ATP to the cytoplasmic side of excised patches of membrane reversibly activated the type of channel that was activated by light in cell-attached patches. In addition, an outward-rectifying K+ channel and an outward-rectifying nonselective cation channel were similarly activated by ATP, whereas a nonselective stretch-activated channel was unaffected by this treatment. This novel mechanism for controlling the permeability of the plasma membrane to K+ may be important to photosynthetic metabolism.

Full Text

The Full Text of this article is available as a PDF (676.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson J. A., Huprikar S. S., Kochian L. V., Lucas W. J., Gaber R. F. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3736–3740. doi: 10.1073/pnas.89.9.3736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blatt M. R. Ion channel gating in plants: physiological implications and integration for stomatal function. J Membr Biol. 1991 Nov;124(2):95–112. doi: 10.1007/BF01870455. [DOI] [PubMed] [Google Scholar]
  3. Cosgrove D. J., Hedrich R. Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta. 1991 Dec;186(1):143–153. doi: 10.1007/BF00201510. [DOI] [PubMed] [Google Scholar]
  4. Fairley-Grenot K., Assmann S. M. Evidence for G-Protein Regulation of Inward K+ Channel Current in Guard Cells of Fava Bean. Plant Cell. 1991 Sep;3(9):1037–1044. doi: 10.1105/tpc.3.9.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gustin M. C., Zhou X. L., Martinac B., Kung C. A mechanosensitive ion channel in the yeast plasma membrane. Science. 1988 Nov 4;242(4879):762–765. doi: 10.1126/science.2460920. [DOI] [PubMed] [Google Scholar]
  6. Hampp R., Goller M., Ziegler H. Adenylate Levels, Energy Charge, and Phosphorylation Potential during Dark-Light and Light-Dark Transition in Chloroplasts, Mitochondria, and Cytosol of Mesophyll Protoplasts from Avena sativa L. Plant Physiol. 1982 Feb;69(2):448–455. doi: 10.1104/pp.69.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hedrich R., Busch H., Raschke K. Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO J. 1990 Dec;9(12):3889–3892. doi: 10.1002/j.1460-2075.1990.tb07608.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Heineke D., Riens B., Grosse H., Hoferichter P., Peter U., Flügge U. I., Heldt H. W. Redox Transfer across the Inner Chloroplast Envelope Membrane. Plant Physiol. 1991 Apr;95(4):1131–1137. doi: 10.1104/pp.95.4.1131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jaffe L. F. The role of ionic currents in establishing developmental pattern. Philos Trans R Soc Lond B Biol Sci. 1981 Oct 7;295(1078):553–566. doi: 10.1098/rstb.1981.0160. [DOI] [PubMed] [Google Scholar]
  10. Katsuhara M., Mimura T., Tazawa M. ATP-Regulated Ion Channels in the Plasma Membrane of a Characeae Alga, Nitellopsis obtusa. Plant Physiol. 1990 May;93(1):343–346. doi: 10.1104/pp.93.1.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kourie J., Goldsmith M. H. K Channels Are Responsible for an Inwardly Rectifying Current in the Plasma Membrane of Mesophyll Protoplasts of Avena sativa. Plant Physiol. 1992 Mar;98(3):1087–1097. doi: 10.1104/pp.98.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Moran N., Ehrenstein G., Iwasa K., Mischke C., Bare C., Satter R. L. Potassium Channels in Motor Cells of Samanea saman: A Patch-Clamp Study. Plant Physiol. 1988 Nov;88(3):643–648. doi: 10.1104/pp.88.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mummert H., Gradmann D. Action potentials in Acetabularia: measurement and simulation of voltage-gated fluxes. J Membr Biol. 1991 Dec;124(3):265–273. doi: 10.1007/BF01994359. [DOI] [PubMed] [Google Scholar]
  14. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8;305(5930):147–148. doi: 10.1038/305147a0. [DOI] [PubMed] [Google Scholar]
  15. Santarius K. A., Heber U. Changes in the intracellular levels of ATP, ADP, AMP and P1 and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim Biophys Acta. 1965 May 25;102(1):39–54. doi: 10.1016/0926-6585(65)90201-3. [DOI] [PubMed] [Google Scholar]
  16. Schroeder J. I., Hedrich R. Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biochem Sci. 1989 May;14(5):187–192. doi: 10.1016/0968-0004(89)90272-7. [DOI] [PubMed] [Google Scholar]
  17. Sentenac H., Bonneaud N., Minet M., Lacroute F., Salmon J. M., Gaymard F., Grignon C. Cloning and expression in yeast of a plant potassium ion transport system. Science. 1992 May 1;256(5057):663–665. doi: 10.1126/science.1585180. [DOI] [PubMed] [Google Scholar]
  18. Serrano E. E., Zeiger E., Hagiwara S. Red light stimulates an electrogenic proton pump in Vicia guard cell protoplasts. Proc Natl Acad Sci U S A. 1988 Jan;85(2):436–440. doi: 10.1073/pnas.85.2.436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Spalding E. P., Slayman C. L., Goldsmith M. H., Gradmann D., Bertl A. Ion channels in Arabidopsis plasma membrane : transport characteristics and involvement in light-induced voltage changes. Plant Physiol. 1992 May;99(1):96–102. doi: 10.1104/pp.99.1.96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Spruce A. E., Standen N. B., Stanfield P. R. Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature. 1985 Aug 22;316(6030):736–738. doi: 10.1038/316736a0. [DOI] [PubMed] [Google Scholar]
  21. Tsuchiya K., Wang W., Giebisch G., Welling P. A. ATP is a coupling modulator of parallel Na,K-ATPase-K-channel activity in the renal proximal tubule. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6418–6422. doi: 10.1073/pnas.89.14.6418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Weiss J. N., Lamp S. T. Glycolysis preferentially inhibits ATP-sensitive K+ channels in isolated guinea pig cardiac myocytes. Science. 1987 Oct 2;238(4823):67–69. doi: 10.1126/science.2443972. [DOI] [PubMed] [Google Scholar]
  23. Wu W., Berkowitz G. A. Stromal pH and Photosynthesis Are Affected by Electroneutral K and H Exchange through Chloroplast Envelope Ion Channels. Plant Physiol. 1992 Feb;98(2):666–672. doi: 10.1104/pp.98.2.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Zhou X. L., Kung C. A mechanosensitive ion channel in Schizosaccharomyces pombe. EMBO J. 1992 Aug;11(8):2869–2875. doi: 10.1002/j.1460-2075.1992.tb05355.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Zhou X. L., Stumpf M. A., Hoch H. C., Kung C. A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces. Science. 1991 Sep 20;253(5026):1415–1417. doi: 10.1126/science.1716786. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES