Abstract
K+ is the most abundant cation in cells of higher plants, and it plays vital roles in plant growth and development. Extensive studies on the kinetics of K+ uptake in roots have shown that K+ uptake is mediated by at least two transport mechanisms, one with a high and one with a low affinity for K+. However, the precise molecular mechanisms of K+ uptake from soils into root epidermal cells remain unknown. In the present study we have pursued the biophysical identification and characterization of mechanisms of K+ uptake into single root hairs of wheat (Triticum aestivum L.), since root hairs constitute an important site of nutrient uptake from the soil. These patch-clamp studies showed activation of a large inward current carried by K+ ions into root hairs at membrane potentials more negative than -75 mV. This K+ influx current was mediated by hyperpolarization-activated K+-selective ion channels, with a selectivity sequence for monovalent cations of K+ > Rb+ [almost equal to] NH4+ >> Na+ [almost equal to] Li+ > Cs+. Kinetic analysis of K+ channel currents yielded an apparent K+ equilibrium dissociation constant (Km) of [almost equal to]8.8 mM, which closely correlates to the major component of low-affinity K+ uptake. These channels did not inactivate during prolonged stimulation and would thus enable long-term K+ uptake driven by the plasma membrane proton-extruding pump. Aluminum, which is known to inhibit cation uptake at the root epidermis, blocked these inward-rectifying K+ channels with half-maximal current inhibition at [almost equal to]8 [mu]M free Al3+. Aluminum block of K+ channels at these Al3+ concentrations correlates closely to Al3+ phytotoxicity. It is concluded that inward-rectifying K+ channels in root hairs can function as both a physiologically important mechanism for low-affinity K+ uptake and as regulators of membrane potential. The identification of this mechanism is a major step toward a detailed molecular characterization of the multiple components involved in K+ uptake, transport, and membrane potential control in root epidermal cells.
Full Text
The Full Text of this article is available as a PDF (1.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barry P. H., Lynch J. W. Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol. 1991 Apr;121(2):101–117. doi: 10.1007/BF01870526. [DOI] [PubMed] [Google Scholar]
- Elzenga J. T., Keller C. P., Van Volkenburgh E. Patch clamping protoplasts from vascular plants : method for the quick isolation of protoplasts having a high success rate of gigaseal formation. Plant Physiol. 1991 Dec;97(4):1573–1575. doi: 10.1104/pp.97.4.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Epstein E., Rains D. W. CARRIER-MEDIATED CATION TRANSPORT IN BARLEY ROOTS: KINETIC EVIDENCE FOR A SPECTRUM OF ACTIVE SITES. Proc Natl Acad Sci U S A. 1965 Jun;53(6):1320–1324. doi: 10.1073/pnas.53.6.1320. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fernando M., Mehroke J., Glass A. D. De Novo Synthesis of Plasma Membrane and Tonoplast Polypeptides of Barley Roots during Short-Term K Deprivation : In Search of the High-Affinity K Transport System. Plant Physiol. 1992 Nov;100(3):1269–1276. doi: 10.1104/pp.100.3.1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher R. F., Long S. R. Rhizobium--plant signal exchange. Nature. 1992 Jun 25;357(6380):655–660. doi: 10.1038/357655a0. [DOI] [PubMed] [Google Scholar]
- Gassmann W., Ward J. M., Schroeder J. I. Physiological Roles of Inward-Rectifying K+ Channels. Plant Cell. 1993 Nov;5(11):1491–1493. doi: 10.1105/tpc.5.11.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godbold D. L., Fritz E., Hüttermann A. Aluminum toxicity and forest decline. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3888–3892. doi: 10.1073/pnas.85.11.3888. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kochian L. V., Lucas W. J. Potassium Transport in Corn Roots : II. The Significance of the Root Periphery. Plant Physiol. 1983 Oct;73(2):208–215. doi: 10.1104/pp.73.2.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kochian L. V., Lucas W. J. Potassium transport in corn roots : I. Resolution of kinetics into a saturable and linear component. Plant Physiol. 1982 Dec;70(6):1723–1731. doi: 10.1104/pp.70.6.1723. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kochian L. V., Xin-Zhi J., Lucas W. J. Potassium Transport in Corn Roots : IV. Characterization of the Linear Component. Plant Physiol. 1985 Nov;79(3):771–776. doi: 10.1104/pp.79.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Leonard R. T., Hotchkiss C. W. Cation-stimulated Adenosine Triphosphatase Activity and Cation Transport in Corn Roots. Plant Physiol. 1976 Sep;58(3):331–335. doi: 10.1104/pp.58.3.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lew R. R. Electrogenic transport properties of growing Arabidopsis root hairs : the plasma membrane proton pump and potassium channels. Plant Physiol. 1991 Dec;97(4):1527–1534. doi: 10.1104/pp.97.4.1527. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Newman I. A., Kochian L. V., Grusak M. A., Lucas W. J. Fluxes of h and k in corn roots : characterization and stoichiometries using ion-selective microelectrodes. Plant Physiol. 1987 Aug;84(4):1177–1184. doi: 10.1104/pp.84.4.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rains D. W., Epstein E. Sodium absorption by barley roots: role of the dual mechanisms of alkali cation transport. Plant Physiol. 1967 Mar;42(3):314–318. doi: 10.1104/pp.42.3.314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodriguez-Navarro A., Blatt M. R., Slayman C. L. A potassium-proton symport in Neurospora crassa. J Gen Physiol. 1986 May;87(5):649–674. doi: 10.1085/jgp.87.5.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samuels A. L., Fernando M., Glass A. D. Immunofluorescent Localization of Plasma Membrane H-ATPase in Barley Roots and Effects of K Nutrition. Plant Physiol. 1992 Aug;99(4):1509–1514. doi: 10.1104/pp.99.4.1509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Thiel G., MacRobbie E. A., Blatt M. R. Membrane transport in stomatal guard cells: the importance of voltage control. J Membr Biol. 1992 Feb;126(1):1–18. doi: 10.1007/BF00233456. [DOI] [PubMed] [Google Scholar]
- Van Duijn B., Ypey D. L., Libbenga K. R. Whole-Cell K+ Currents across the Plasma Membrane of Tobacco Protoplasts from Cell-Suspension Cultures. Plant Physiol. 1993 Jan;101(1):81–88. doi: 10.1104/pp.101.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]