Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1995 Jan;107(1):101–109. doi: 10.1104/pp.107.1.101

Is ATP Required for K+ Channel Activation in Vicia Guard Cells?

W H Wu 1, S M Assmann 1
PMCID: PMC161172  PMID: 12228345

Abstract

In vivo, K+ entry into guard cells via inward-rectifying K+ channels is indirectly driven by ATP via an H+-ATPase that hyperpolarizes the membrane potential. However, whether activation of the K+ channels of guard cells requires ATP remains unknown. In the present study, both whole-cell and single-channel patch-clamp techniques were used to address this question. Exogenous ATP, ADP, and adenosine-5[prime]-O-(3-thiotriphosphate) applied to the cytoplasm had no effect on whole-cell K+ currents of Vicia faba L. guard cells. Azide, an inhibitor of oxidative phosphorylation, also had no effect. However, an ATP-scavenging system, glucose plus hexokinase, inhibited whole-cell inward K+ currents by 30 to 40%. Single-channel results acquired from cytoplasm-free inside-out membrane patches showed definite activation of inward K+ channels by ATP. Other nucleotides, such as ADP, adenosine-5[prime]-O(3-thiotriphosphate), and GTP, did not increase channel activity in the membrane patches. Inward K+ channel activity in membrane patches preactivated by exogenous ATP was inhibited by glucose plus hexokinase. These results suggest that a low concentration of ATP is required for activation of the inward K+ channels of the guard-cell plasma membrane. The issue of how ATP as a signal regulates these K+ channels is discussed.

Full Text

The Full Text of this article is available as a PDF (881.6 KB).

Selected References

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

  1. Assmann S. M. Signal transduction in guard cells. Annu Rev Cell Biol. 1993;9:345–375. doi: 10.1146/annurev.cb.09.110193.002021. [DOI] [PubMed] [Google Scholar]
  2. Blatt M. R. K+ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH. J Gen Physiol. 1992 Apr;99(4):615–644. doi: 10.1085/jgp.99.4.615. [DOI] [PMC free article] [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. Dang Y., Lowe G. M., Edwards S. W., Galvani D. W. The effects of GM-CSF on myeloperoxidase release in normal and myelodysplastic neutrophils. Leuk Res. 1993 Dec;17(12):1037–1044. doi: 10.1016/0145-2126(93)90160-m. [DOI] [PubMed] [Google Scholar]
  5. Fairley-Grenot K. A., Assmann S. M. Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells. J Membr Biol. 1992 Jun;128(2):103–113. doi: 10.1007/BF00231883. [DOI] [PubMed] [Google Scholar]
  6. Gratecos D., Fischer E. H. Adenosine 5'-O(3-thiotriphosphate) in the control of phosphorylase activity. Biochem Biophys Res Commun. 1974 Jun 18;58(4):960–967. doi: 10.1016/s0006-291x(74)80237-8. [DOI] [PubMed] [Google Scholar]
  7. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  8. Jeppsson S., Karlsson S., Kullander S. Gonadal steroids, gonadotropins and endometrial histology in postmenopausal women with malignant ovarian tumors. Acta Obstet Gynecol Scand. 1986;65(3):207–210. doi: 10.3109/00016348609155172. [DOI] [PubMed] [Google Scholar]
  9. Kondo T., Kiriyama T., Kato Y., Kogame Y., Kaneko K., Hishida H., Mizuno Y., Ejiri K., Kawai K., Takeuchi A. [Clinical reliability and limitation of 99m Tc-pyrophosphate myocardial scintigraphy for the assessment of acute myocardial infarction--with special reference to evaluation of the area affected by infarction]. Kaku Igaku. 1982 Jul;19(6):871–879. [PubMed] [Google Scholar]
  10. Kruse T., Tallman G., Zeiger E. Isolation of Guard Cell Protoplasts from Mechanically Prepared Epidermis of Vicia faba Leaves. Plant Physiol. 1989 Aug;90(4):1382–1386. doi: 10.1104/pp.90.4.1382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Li W., Assmann S. M. Characterization of a G-protein-regulated outward K+ current in mesophyll cells of vicia faba L. Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):262–266. doi: 10.1073/pnas.90.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Marten I., Zeilinger C., Redhead C., Landry D. W., al-Awqati Q., Hedrich R. Identification and modulation of a voltage-dependent anion channel in the plasma membrane of guard cells by high-affinity ligands. EMBO J. 1992 Oct;11(10):3569–3575. doi: 10.1002/j.1460-2075.1992.tb05440.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Poffenroth M., Green D. B., Tallman G. Sugar Concentrations in Guard Cells of Vicia faba Illuminated with Red or Blue Light : Analysis by High Performance Liquid Chromatography. Plant Physiol. 1992 Apr;98(4):1460–1471. doi: 10.1104/pp.98.4.1460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pusch M., Neher E. Rates of diffusional exchange between small cells and a measuring patch pipette. Pflugers Arch. 1988 Feb;411(2):204–211. doi: 10.1007/BF00582316. [DOI] [PubMed] [Google Scholar]
  15. Schroeder J. I., Fang H. H. Inward-rectifying K+ channels in guard cells provide a mechanism for low-affinity K+ uptake. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11583–11587. doi: 10.1073/pnas.88.24.11583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schroeder J. I. K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J Gen Physiol. 1988 Nov;92(5):667–683. doi: 10.1085/jgp.92.5.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Schroeder J. I., Keller B. U. Two types of anion channel currents in guard cells with distinct voltage regulation. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5025–5029. doi: 10.1073/pnas.89.11.5025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schroeder J. I. Quantitative analysis of outward rectifying K+ channel currents in guard cell protoplasts from Vicia faba. J Membr Biol. 1989 Mar;107(3):229–235. doi: 10.1007/BF01871938. [DOI] [PubMed] [Google Scholar]
  19. Schroeder J. I., Raschke K., Neher E. Voltage dependence of K channels in guard-cell protoplasts. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4108–4112. doi: 10.1073/pnas.84.12.4108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Shimazaki K., Zeiger E. Cyclic and Noncyclic Photophosphorylation in Isolated Guard Cell Chloroplasts from Vicia faba L. Plant Physiol. 1985 Jun;78(2):211–214. doi: 10.1104/pp.78.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shimazaki K., Zeiger E. Cyclic and Noncyclic Photophosphorylation in Isolated Guard Cell Chloroplasts from Vicia faba L. Plant Physiol. 1985 Jun;78(2):211–214. doi: 10.1104/pp.78.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Spalding E. P., Goldsmith MHM. Activation of K+ Channels in the Plasma Membrane of Arabidopsis by ATP Produced Photosynthetically. Plant Cell. 1993 Apr;5(4):477–484. doi: 10.1105/tpc.5.4.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wu W. H., Assmann S. M. A membrane-delimited pathway of G-protein regulation of the guard-cell inward K+ channel. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6310–6314. doi: 10.1073/pnas.91.14.6310. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES