Ion Channels Meet Auxin Action

Abstract

The regulation of cell division and elongation in plants is accomplished by the action of different phytohormones. Auxin as one of these growth regulators is known to stimulate cell elongation growth in the aerial parts of the plant. Here, auxin enhances cell enlargement by increasing the extensibility of the cell wall and by facilitating the uptake of osmolytes such as potassium ions into the cell. Starting in the late 1990s, the auxin regulation of ion channels mediating K⁺ import into the cell has been studied in great detail. In this article we will focus on the molecular mechanisms underlying the modulation of K⁺ transport by auxin and present a model to explain how the regulation of K⁺ channels is involved in auxin-induced cell elongation growth.

Key words

Auxin - K⁺ channel - elongation growth - tropisms - maize - Arabidopsis thaliana.

References

• 1 Arend M., Stinzing A., Wind C., Langer K., Latz A., Ache P., Fromm J., Hedrich R.. Polar-localised poplar K⁺ channel capable of controlling electrical properties of wood-forming cells.  Planta. (2005);  223 140-148
• 2 Basset M., Conejero G., Lepetit M., Fourcroy P., Sentenac H.. Organization and expression of the gene coding for the potassium transport system AKT1 of Arabidopsis thaliana.  Plant Molecular Biology. (1995);  29 947-958
• 3 Bauer C. S., Hoth S., Haga K., Philippar K., Aoki N., Hedrich R.. Differential expression and regulation of K⁺ channels in the maize coleoptile: molecular and biophysical analysis of cells isolated from cortex and vasculature.  The Plant Journal. (2000);  24 139-145
• 4 Becker D., Hedrich R.. Channelling auxin action: modulation of ion transport by indole-3-acetic acid.  Plant Molecular Biology. (2002);  49 349-356
• 5 Blatt M. R., Thiel G.. K⁺ channels of stomatal guard cells: bimodal control of the K⁺ inward-rectifier evoked by auxin.  The Plant Journal. (1994);  5 55-68
• 6 Briggs W. R., Beck C. F., Cashmore A. R., Christie J. M., Hughes J., Jarillo J. A., Kagawa T., Kanegae H., Liscum E., Nagatani. et al. . The phototropin family of photoreceptors.  Plant Cell. (2001);  13 993-997
• 7 Catala C., Rose J. K. C., Bennett A. B.. Auxin regulation and spatial localization of an endo-1,4-β‐D-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls.  The Plant Journal. (1997);  12 417-426
• 8 Catala C., Rose J. K. C., Bennett A. B.. Auxin-regulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth.  Plant Physiology. (2000);  122 527-534
• 9 Cholodny N.. Beiträge zur hormonalen Theorie von Tropismen.  Planta. (1928);  6 118-134
• 10 Claussen M., Lüthen H., Blatt M., Böttger M.. Auxin-induced growth and its linkage to potassium channels.  Planta. (1997);  201 227-234
• 11 Cleland R. E.. The outer epidermis of Avena and maize coleoptiles is not a unique target for auxin in elongation growth.  Planta. (1991);  186 75-80
• 12 Cosgrove D. J.. Expansive growth of plant cell walls.  Plant Physiology and Biochemistry. (2000);  38 109-124
• 13 Darwin C.. The Power of Movements in Plants. London; John Murray (1880)
• 14 Deeken R., Geiger D., Fromm J., Koroleva O., Ache P., Langenfeld-Heyser R., Sauer N., May S., Hedrich R.. Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis.  Planta. (2002);  216 334-344
• 15 Deeken R., Sanders C., Ache P., Hedrich R.. Developmental and light-dependent regulation of a phloem-localised K⁺ channel of Arabidopsis thaliana.  The Plant Journal. (2000);  23 285-290
• 16 Dharmasiri N., Dharmasiri S., Estelle M.. The F‐box protein TIR1 is an auxin receptor.  Nature. (2005 a);  435 441-445
• 17 Dharmasiri N., Dharmasiri S., Weijers D., Lechner E., Yamada M., Hobbie L., Ehrismann J. S., Jürgens G., Estelle M.. Plant development is regulated by a family of auxin receptor F box proteins.  Developmental Cell. (2005 b);  9 109-119
• 18 Dietrich P., Sanders D., Hedrich R.. The role of ion channels in light-dependent stomatal opening.  Journal of Experimental Botany. (2001);  52 1959-1967
• 19 Dreyer I., Antunes S., Hoshi T., Müller-Röber B., Palme K., Pongs O., Reintanz B., Hedrich R.. Plant K⁺ channel alpha-subunits assemble indiscriminately.  Biophysical Journal. (1997);  72 2143-2150
• 20 Elumalai R. P., Nagpal P., Reed J. W.. A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion.  Plant Cell. (2002);  14 119-131
• 21 Esmon C. A., Pedmale U. V., Liscum E.. Plant tropisms: providing the power of movement to a sessile organism.  The International Journal of Developmental Biology. (2005);  49 665-674
• 22 Felle H., Peters W., Palme K.. The electrical response of maize to auxins.  Biochimica et Biophysica Acta. (1991);  1064 199-204
• 23 Frias I., Caldeira M. T., Perez-Castineira J. R., Navarro-Avino J. P., Culianez-Macia F. A., Kuppinger O., Stransky H., Pages M., Hager A., Serrano R.. A major isoform of the maize plasma membrane H⁺-ATPase: characterization and induction by auxin in coleoptiles.  Plant Cell. (1996);  8 1533-1544
• 24 Friml J.. Auxin transport - shaping the plant.  Current Opinion in Plant Biology. (2003);  6 7-12
• 25 Friml J., Wisniewska J., Benkova E., Mendgen K., Palme K.. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis.  Nature. (2002);  415 806-809
• 26 Fry S. C., Smith R. C., Renwick K. F., Martin D. J., Hodge S. K., Matthews K. J.. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants.  Biochemical Journal. (1992);  282 821-828
• 27 Fuchs I., Philippar K., Ljung K., Sandberg G., Hedrich R.. Blue light regulates an auxin-induced K⁺ channel gene in the maize coleoptile.  Proceedings of the National Academy of Sciences of the USA. (2003);  100 11795-11800
• 28 Fuchs I., Stölzle S., Ivashikina N., Hedrich R.. Rice K⁺ uptake channel OsAKT1 is sensitive to salt stress.  Planta. (2005);  221 212-221
• 29 Greenwood M. S., Shaw S., Hillman J. R., Ritchie A., Wilkins M. B.. Identification of auxin from Zea coleoptile tips by mass spectrometry.  Planta. (1972);  108 179-183
• 30 Hager A.. Role of the plasma membrane H⁺-ATPase in auxin-induced elongation growth: historical and new aspects.  Journal of Plant Research. (2003);  116 483-505
• 31 Hager A., Brich M.. Blue-light-induced phosphorylation of a plasma-membrane protein from phototropically sensitive tips of maize coleoptiles.  Planta. (1993);  189 567-576
• 32 Hager A., Debus G., Edel H. G., Stransky H., Serrano R.. Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane proton ATPase.  Planta. (1991);  185 527-537
• 33 Hager A., Menzel H., Krauss A.. Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum.  Planta. (1971);  100 47-75
• 34 Haschke H. P., Lüttge U.. β-Indolylessigsäure (IES)-abhängiger K⁺-H⁺-Austauschmechanismus und Streckungswachstum bei Avena-Koleoptilen.  Zeitschrift für Naturforschung. (1973);  28C 555-558
• 35 Haschke H. P., Lüttge U.. Stoichiometric correlation of malate accumulation with auxin-dependent K⁺-H⁺ exchange and growth in Avena coleoptile segments.  Plant Physiology. (1975);  56 696-698
• 36 Hoth S., Hedrich R.. Distinct molecular bases for pH sensitivity of the guard cell K⁺ channels KST1 and KAT1.  Journal of Biological Chemistry. (1999);  274 11599-11603
• 37 Hutchison K. W., Singer P. B., McInnis S., Diaz-Sala C., Greenwood M. S.. Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin.  Plant Physiology. (1999);  120 827-832
• 38 Iino M.. Gravitropism and phototropism of maize coleoptiles: evaluation of the Cholodny-Went theory and through effects of auxin application and decapitation.  Plant and Cell Physiology. (1995);  36 361-367
• 39 Iino M.. Mediation of tropisms by lateral translocation of endogenous IAA in maize coleoptiles.  Plant, Cell and Environment. (1991);  14 279-286
• 40 Jahn T., Johansson F., Lüthen H., Volkmann D., Larsson C.. Reinvestigation of auxin and fusicoccin stimulation of the plasma-membrane H⁺-ATPase activity.  Planta. (1996);  199 359-365
• 41 Kaldenhoff R., Iino M.. Restoration of phototropic responsiveness in decapitated maize coleoptiles.  Plant Physiology. (1997);  114 1267-1272
• 42 Kepinski S., Leyser O.. The Arabidopsis F‐box protein TIR1 is an auxin receptor.  Nature. (2005);  435 446-451
• 43 Kiss J. Z., Guisinger M. M., Miller A. J., Stackhouse K. S.. Reduced gravitropism in hypocotyls of starch-deficient mutants of Arabidopsis.  Plant and Cell Physiology. (1997);  38 518-525
• 44 Kiss J. Z., Hertel R., Sack F. D.. Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana.  Planta. (1989);  177 198-206
• 45 Ljung K., Bhalerao R. P., Sandberg G.. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth.  The Plant Journal. (2001);  28 465-474
• 46 Lohse G., Hedrich R.. Characterization of the plasma membrane proton ATPase from Vicia faba guard cells: modulation by extracellular factors and seasonal changes.  Planta. (1992);  188 206-214
• 47 Marten I., Lohse G., Hedrich R.. Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells.  Nature. (1991);  353 758-762
• 48 Mäser P., Thomine S., Schroeder J. I., Ward J. M., Hirschi K., Sze H., Talke I. N., Amtmann A., Maathuis F. J. M., Sanders D., Harper J. F., Tchieu J., Gribskov M., Persans M. W., Salt D. E., Kim S. A., Guerinot M. L.. Phylogenetic relationships within cation transporter families of Arabidopsis.  Plant Physiology. (2001);  126 1646-1667
• 49 Mulkey T. J., Kuzmanoff K. M., Evans M. L.. Correlations between proton-efflux patterns and growth patterns during geotropism and phototropism in maize and sunflower.  Planta. (1981);  152 239-241
• 50 Nelles A.. Short-term effects of plant hormones on membrane potential and membrane permeability of dwarf maize coleoptile cells (Zea mays L. d ₁) in comparison with growth responses.  Planta. (1977);  137 293-298
• 51 Parker K. E., Briggs W. R.. Transport of IAA during gravitropism in intact maize coleoptiles.  Plant Physiology. (1990);  94 1763-1769
• 52 Peters W. S., Richter U., Felle H. H.. Auxin-induced H⁺-pump stimulation does not depend on the presence of epidermal cells in corn coleoptiles.  Planta. (1992);  186 313-316
• 53 Philippar K., Büchsenschütz K., Edwards D., Löffler J., Lüthen H., Kranz E., Edwards K. J., Hedrich R.. The auxin-induced K⁺ channel gene ZMK1 in maize functions in coleoptile growth and is required for embryo development.  Plant Molecular Biology. (2006); 
• 54 Philippar K., Fuchs I., Lüthen H., Hoth S., Bauer C., Haga K., Thiel G., Ljung K., Sandberg G., Böttger M., Becker D., Hedrich R.. Auxin-induced K⁺ channel expression represents an essential step in coleoptile growth and gravitropism.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 12186-12191
• 55 Philippar K., Ivashikina N., Ache P., Christian M., Lüthen H., Palme K., Hedrich R.. Auxin activates KAT1 and KAT2, two K⁺-channel genes expressed in seedlings of Arabidopsis thaliana.  The Plant Journal. (2004);  37 815-827
• 56 Pilot G., Lacombe B., Gaymard F., Cherel I., Boucherez J., Thibaud J. B., Sentenac H.. Guard cell inward K⁺ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2.  Journal of Biological Chemistry,. (2001);  276 3215-3221
• 57 Quintero F. J., Blatt M. R.. A new family of K⁺ transporters from Arabidopsis that are conserved across phyla.  FEBS Letters. (1997);  415 206-211
• 58 Reintanz B., Szyroki A., Ivashikina N., Ache P., Godde M., Becker D., Palme K., Hedrich R.. AtKC1, a silent Arabidopsis potassium channel alpha-subunit modulates root hair K⁺ influx.  Proceedings of the National Academy of Sciences of the USA. (2002);  99 4079-4084
• 59 Rose J. K. C., Braam J., Fry S. C., Nishitani K.. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature.  Plant and Cell Physiology. (2002);  43 1421-1435
• 60 Rück A., Palme K., Venis M. A., Napier R. M., Felle H. H.. Patch-clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts.  The Plant Journal. (1993);  4 41-46
• 61 Sano T., Higaki T., Handa K., Kadota Y., Kuchitsu K., Hasezawa S., Hoffmann A., Endter J., Zimmermann U., Hedrich R., Roitsch T.. Calcium ions are involved in the delay of plant cell cycle progression by abiotic stresses.  FEBS Letters. (2006);  580 597-602
• 62 Schachtman D. P., Schroeder J. I., Lucas W. J., Anderson J. A., Gaber R. F.. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA.  Science. (1992);  258 1654-1658
• 63 Swarup R., Friml J., Marchant A., Ljung K., Sandberg G., Palme K., Bennett M.. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex.  Genes and Development. (2001);  15 2648-2653
• 64 Swarup R., Kramer E. M., Perry P., Knox K., Leyser H. M. O., Haseloff J., Beemster G. T. S., Bhalerao R., Bennett M. J.. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.  Nature Cell Biology. (2005);  7 1057-1065
• 65 Szyroki A., Ivashikina N., Dietrich P., Roelfsema M. R. G., Ache P., Reintanz B., Deeken R., Godde M., Felle H., Steinmeyer R., Palme K., Hedrich R.. KAT1 is not essential for stomatal opening.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 2917-2921
• 66 Thiel G., Weise R.. Auxin augments conductance of K⁺ inward rectifier in maize coleoptile protoplasts.  Planta. (1999);  208 38-45
• 67 Very A. A., Sentenac H.. Cation channels in the Arabidopsis plasma membrane.  Trends in Plant Science. (2002);  7 168-175
• 68 Very A. A., Sentenac H.. Molecular Mechanisms and Regulation of K⁺ Transport in higher Plants.  Annual Review of Plant Biology. (2003);  54 575-603
• 69 Went F. W.. Wuchsstoff und Wachstum.  Receuil des Travaux Botaniques Neerlandais. (1928);  25 1-116
• 70 Went F. W., Thimann K. V.. Phytohormones. New York; Macmillan (1937)

Guest Editor: R. Reski