Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1998 Nov;10(11):1957–1970. doi: 10.1105/tpc.10.11.1957

Voltage-dependent K+ channels as targets of osmosensing in guard cells

K Liu 1, S Luan 1
PMCID: PMC143957  PMID: 9811801

Abstract

Guard cell turgor responds to the osmogradient across the plasma membrane and controls the stomatal aperture. Here, we report that guard cells utilize voltage-dependent K+ channels as targets of the osmosensing pathway, providing a positive feedback mechanism for stomatal regulation. When exposed to a hypotonic condition, the inward K+ current (IKin) was highly activated, whereas the outward K+ current (IKout) was inactivated. In contrast, hypertonic conditions inactivated the IKin while activating IKout. Single-channel recording analyses indicated that an alteration in channel opening frequency was responsible for regulating IKin and IKout under different osmotic conditions. Further studies correlate osmoregulation of IKin with the pattern of organization of actin filaments, which may be a critical component in the osmosensing pathway in plant cells.

Full Text

The Full Text of this article is available as a PDF (351.5 KB).

Selected References

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

  1. Alexandre J., Lassalles J. P. Hydrostatic and osmotic pressure activated channel in plant vacuole. Biophys J. 1991 Dec;60(6):1326–1336. doi: 10.1016/S0006-3495(91)82170-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Baraban S. C., Bellingham M. C., Berger A. J., Schwartzkroin P. A. Osmolarity modulates K+ channel function on rat hippocampal interneurons but not CA1 pyramidal neurons. J Physiol. 1997 Feb 1;498(Pt 3):679–689. doi: 10.1113/jphysiol.1997.sp021892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bei Q., Luan S. Functional expression and characterization of a plant K+ channel gene in a plant cell model. Plant J. 1998 Mar;13(6):857–865. doi: 10.1046/j.1365-313x.1998.00084.x. [DOI] [PubMed] [Google Scholar]
  5. Cantiello H. F. Role of actin filament organization in cell volume and ion channel regulation. J Exp Zool. 1997 Dec 1;279(5):425–435. doi: 10.1002/(sici)1097-010x(19971201)279:5<425::aid-jez4>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Cossins A. R., Gibson J. S. Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J Exp Biol. 1997 Jan;200(Pt 2):343–352. doi: 10.1242/jeb.200.2.343. [DOI] [PubMed] [Google Scholar]
  8. Gosling M., Smith J. W., Poyner D. R. Characterization of a volume-sensitive chloride current in rat osteoblast-like (ROS 17/2.8) cells. J Physiol. 1995 Jun 15;485(Pt 3):671–682. doi: 10.1113/jphysiol.1995.sp020761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grinstein S., Foskett J. K. Ionic mechanisms of cell volume regulation in leukocytes. Annu Rev Physiol. 1990;52:399–414. doi: 10.1146/annurev.ph.52.030190.002151. [DOI] [PubMed] [Google Scholar]
  10. Hwang J. U., Suh S., Yi H., Kim J., Lee Y. Actin Filaments Modulate Both Stomatal Opening and Inward K+-Channel Activities in Guard Cells of Vicia faba L. Plant Physiol. 1997 Oct;115(2):335–342. doi: 10.1104/pp.115.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ilan N., Moran N., Schwartz A. The Role of Potassium Channels in the Temperature Control of Stomatal Aperture. Plant Physiol. 1995 Jul;108(3):1161–1170. doi: 10.1104/pp.108.3.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Karmanov V. G., Meleshchenko S. N., Savin V. N. Izuchenie dinamiki vodnogo obmena rasteniia i postroenie élektricheskogo analoga sistemy vodnogo obmena. Biofizika. 1966;11(1):147–155. [PubMed] [Google Scholar]
  13. Kim M., Hepler P. K., Eun S. O., Ha K. S., Lee Y. Actin Filaments in Mature Guard Cells Are Radially Distributed and Involved in Stomatal Movement. Plant Physiol. 1995 Nov;109(3):1077–1084. doi: 10.1104/pp.109.3.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Lang A. R., Klepper B., Cumming M. J. Leaf water balance during oscillation of stomatal aperture. Plant Physiol. 1969 Jun;44(6):826–830. doi: 10.1104/pp.44.6.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Luan S., Li W., Rusnak F., Assmann S. M., Schreiber S. L. Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2202–2206. doi: 10.1073/pnas.90.6.2202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maathuis F. J., Ichida A. M., Sanders D., Schroeder J. I. Roles of higher plant K+ channels. Plant Physiol. 1997 Aug;114(4):1141–1149. doi: 10.1104/pp.114.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mastrocola T., Lambert I. H., Kramhøft B., Rugolo M., Hoffmann E. K. Volume regulation in human fibroblasts: role of Ca2+ and 5-lipoxygenase products in the activation of the Cl- efflux. J Membr Biol. 1993 Oct;136(1):55–62. doi: 10.1007/BF00241489. [DOI] [PubMed] [Google Scholar]
  19. Maximov A. V., Vedernikova E. A., Hinssen H., Khaitlina S. Y., Negulyaev Y. A. Ca-dependent regulation of Na+-selective channels via actin cytoskeleton modification in leukemia cells. FEBS Lett. 1997 Jul 21;412(1):94–96. doi: 10.1016/s0014-5793(97)00754-0. [DOI] [PubMed] [Google Scholar]
  20. Morris C. E. Mechanosensitive ion channels. J Membr Biol. 1990 Feb;113(2):93–107. doi: 10.1007/BF01872883. [DOI] [PubMed] [Google Scholar]
  21. Morán J., Sabanero M., Meza I., Pasantes-Morales H. Changes of actin cytoskeleton during swelling and regulatory volume decrease in cultured astrocytes. Am J Physiol. 1996 Dec;271(6 Pt 1):C1901–C1907. doi: 10.1152/ajpcell.1996.271.6.C1901. [DOI] [PubMed] [Google Scholar]
  22. Negulyaev Y. A., Vedernikova E. A., Maximov A. V. Disruption of actin filaments increases the activity of sodium-conducting channels in human myeloid leukemia cells. Mol Biol Cell. 1996 Dec;7(12):1857–1864. doi: 10.1091/mbc.7.12.1857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Neher E. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 1992;207:123–131. doi: 10.1016/0076-6879(92)07008-c. [DOI] [PubMed] [Google Scholar]
  24. Pei Z. M., Kuchitsu K., Ward J. M., Schwarz M., Schroeder J. I. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell. 1997 Mar;9(3):409–423. doi: 10.1105/tpc.9.3.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pickard B. G., Ding J. P. The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control centre? Aust J Plant Physiol. 1993;20:439–459. doi: 10.1071/pp9930439. [DOI] [PubMed] [Google Scholar]
  26. Sachs F. Mechanical transduction by ion channels: how forces reach the channel. Soc Gen Physiol Ser. 1997;52:209–218. [PubMed] [Google Scholar]
  27. Schoenmakers T. J., Vaudry H., Cazin L. Osmo- and mechanosensitivity of the transient outward K+ current in a mammalian neuronal cell line. J Physiol. 1995 Dec 1;489(Pt 2):419–430. doi: 10.1113/jphysiol.1995.sp021062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Schroeder J. I., Ward J. M., Gassmann W. Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu Rev Biophys Biomol Struct. 1994;23:441–471. doi: 10.1146/annurev.bb.23.060194.002301. [DOI] [PubMed] [Google Scholar]
  30. Schwartz A., Wu W. H., Tucker E. B., Assmann S. M. Inhibition of inward K+ channels and stomatal response by abscisic acid: an intracellular locus of phytohormone action. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):4019–4023. doi: 10.1073/pnas.91.9.4019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schwiebert E. M., Mills J. W., Stanton B. A. Actin-based cytoskeleton regulates a chloride channel and cell volume in a renal cortical collecting duct cell line. J Biol Chem. 1994 Mar 11;269(10):7081–7089. [PubMed] [Google Scholar]
  32. Tilly B. C., Edixhoven M. J., Tertoolen L. G., Morii N., Saitoh Y., Narumiya S., de Jonge H. R. Activation of the osmo-sensitive chloride conductance involves P21rho and is accompanied by a transient reorganization of the F-actin cytoskeleton. Mol Biol Cell. 1996 Sep;7(9):1419–1427. doi: 10.1091/mbc.7.9.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ward J. M., Pei Z. M., Schroeder J. I. Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants. Plant Cell. 1995 Jul;7(7):833–844. doi: 10.1105/tpc.7.7.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wu W. H., Assmann S. M. Is ATP Required for K+ Channel Activation in Vicia Guard Cells? Plant Physiol. 1995 Jan;107(1):101–109. doi: 10.1104/pp.107.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Xu W. X., Kim S. J., So I., Kim K. W. Role of actin microfilament in osmotic stretch-induced increase of voltage-operated calcium channel current in guinea-pig gastric myocytes. Pflugers Arch. 1997 Aug;434(4):502–504. doi: 10.1007/s004240050428. [DOI] [PubMed] [Google Scholar]
  36. Yokoshiki H., Katsube Y., Sunugawa M., Seki T., Sperelakis N. Disruption of actin cytoskeleton attenuates sulfonylurea inhibition of cardiac ATP-sensitive K+ channels. Pflugers Arch. 1997 Jun;434(2):203–205. doi: 10.1007/s004240050384. [DOI] [PubMed] [Google Scholar]

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

RESOURCES