Evidence for the existence of a sulfonylurea-receptor-like protein in plants: modulation of stomatal movements and guard cell potassium channels by sulfonylureas and potassium channel openers.

Limitation of water loss and control of gas exchange is accomplished in plant leaves via stomatal guard cells. Stomata open in response to light when an increase in guard cell turgor is triggered by ions and water influx across the plasma membrane. Recent evidence demonstrating the existence of ATP-binding cassette proteins in plants led us to analyze the effect of compounds known for their ability to modulate ATP-sensitive potassium channels (K-ATP) in animal cells. By using epidermal strip bioassays and whole-cell patch-clamp experiments with Vicia faba guard cell protoplasts, we describe a pharmacological profile that is specific for the outward K+ channel and very similar to the one described for ATP-sensitive potassium channels in mammalian cells. Tolbutamide and glibenclamide induced stomatal opening in bioassays and in patch-clamp experiments, a specific inhibition of the outward K+ channel by these compounds was observed. Conversely, application of potassium channel openers such as cromakalim or RP49356 triggered stomatal closure. An apparent competition between sulfonylureas and potassium channel openers occurred in bioassays, and outward potassium currents, previously inhibited by glibenclamide, were partially recovered after application of cromakalim. By using an expressed sequence tag clone from an Arabidopsis thaliana homologue of the sulfonylurea receptor, a 7-kb transcript was detected by Northern blot analysis in guard cells and other tissues. Beside the molecular evidence recently obtained for the expression of ATP-binding cassette protein transcripts in plants, these results give pharmacological support to the presence of a sulfonylurea-receptor-like protein in the guard-cell plasma membrane tightly involved in the outward potassium channel regulation during stomatal movements.

[1]  U. Panten,et al.  Sulfonylurea receptors and mechanism of sulfonylurea action. , 2009, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[2]  P. A. Rea,et al.  AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  N. Provart,et al.  Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation. , 1997, The Plant journal : for cell and molecular biology.

[4]  Y. Horio,et al.  Sulphonylurea receptor 2B and Kir6.1 form a sulphonylurea‐sensitive but ATP‐insensitive K+ channel. , 1997, The Journal of physiology.

[5]  S. Assmann,et al.  A Membrane-delimited Effect of Internal pH on the K+ Outward Rectifier of Vicia Faba Guard Cells , 1996, The Journal of Membrane Biology.

[6]  Alain Vavasseur,et al.  A reassessment of the intervention of calmodulin in the regulation of stomatal movement , 1996 .

[7]  D. Escande,et al.  ATP-binding cassette proteins as targets for drug discovery. , 1996, Trends in pharmacological sciences.

[8]  G. Giebisch,et al.  Sensitivity of a renal K+ channel (ROMK2) to the inhibitory sulfonylurea compound glibenclamide is enhanced by coexpression with the ATP-binding cassette transporter cystic fibrosis transmembrane regulator. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Martinoia,et al.  Old Enzymes for a New Job (Herbicide Detoxification in Plants) , 1996, Plant physiology.

[10]  J. Inazawa,et al.  Reconstitution of IKATP: An Inward Rectifier Subunit Plus the Sulfonylurea Receptor , 1995, Science.

[11]  C. Higgins,et al.  The ABC of channel regulation , 1995, Cell.

[12]  M. Vivaudou,et al.  Modification by protons of frog skeletal muscle KATP channels: effects on ion conduction and nucleotide inhibition. , 1995, The Journal of physiology.

[13]  S. Assmann,et al.  Is ATP Required for K+ Channel Activation in Vicia Guard Cells? , 1995, Plant physiology.

[14]  David J. Triggle,et al.  ATP‐sensitive K+ channels: Pharmacologic properties, regulation, and therapeutic potential , 1993 .

[15]  F. Ashcroft,et al.  The sulfonylurea receptor. , 1992, Biochimica et biophysica acta.

[16]  M. Welsh,et al.  Effect of ATP-sensitive K+ channel regulators on cystic fibrosis transmembrane conductance regulator chloride currents , 1992, The Journal of general physiology.

[17]  I Findlay,et al.  Inhibition of ATP-sensitive K+ channels in cardiac muscle by the sulphonylurea drug glibenclamide. , 1992, The Journal of pharmacology and experimental therapeutics.

[18]  M. Blatt,et al.  K+ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH , 1992, The Journal of general physiology.

[19]  R. Dudler,et al.  Structure of an mdr-like gene from Arabidopsis thaliana. Evolutionary implications. , 1992, The Journal of biological chemistry.

[20]  N. Standen Potassium channels: Structure, classification, function and therapeutic potential , 1990 .

[21]  M. Tazawa,et al.  ATP-Regulated Ion Channels in the Plasma Membrane of a Characeae Alga, Nitellopsis obtusa. , 1990, Plant physiology.

[22]  A. Hoekema,et al.  A small-scale procedure for the rapid isolation of plant RNAs. , 1989, Nucleic acids research.

[23]  S. Hagiwara,et al.  Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells , 1989, Nature.

[24]  M. Sanguinetti,et al.  BRL 34915 (cromakalim) activates ATP-sensitive K+ current in cardiac muscle. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[25]  N. Castle,et al.  Effect of channel blockers on potassium efflux from metabolically exhausted frog skeletal muscle. , 1987, The Journal of physiology.

[26]  J. Schroeder,et al.  Potassium-selective single channels in guard cell protoplasts of Vicia faba , 1984, Nature.

[27]  A. Noma,et al.  ATP-regulated K+ channels in cardiac muscle , 1983, Nature.

[28]  T. Ray The mode of action of chlorsulfuron: A new herbicide for cereals , 1982 .

[29]  K. Lawson Potassium channel activation: a potential therapeutic approach? , 1996, Pharmacology & therapeutics.

[30]  S. Assmann,et al.  Signal transduction in guard cells. , 1993, Annual review of cell biology.

[31]  F. Ashcroft,et al.  Properties and functions of ATP-sensitive K-channels. , 1990, Cellular signalling.