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AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity.

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Jeanguenin, Linda [UCL] Alcon, Carine Duby, Geoffrey Boeglin, Martin Chérel, Isabelle Véry, Anne-Aliénor

A functional Shaker potassium channel requires assembly of four α-subunits encoded by a single gene or various genes from the Shaker family. In Arabidopsis thaliana, AtKC1, a Shaker α-subunit that is silent when expressed alone, has been shown to regulate the activity of AKT1 by forming heteromeric AtKC1-AKT1 channels. Here, we investigated whether AtKC1 is a general regulator of channel activity. Co-expression in Xenopus oocytes of a dominant negative (pore-mutated) AtKC1 subunit with the inward Shaker channel subunits KAT1, KAT2 or AKT2, or the outward subunits SKOR or GORK, revealed that the three inward subunits functionally interact with AtKC1 while the outward ones cannot. Localization experiments in plant protoplasts showed that KAT2 was able to re-locate AtKC1 fused to GFP from endomembranes to the plasma membrane, indicating that heteromeric AtKC1-KAT2 channels are efficiently targeted to the plasma membrane. Functional properties of heteromeric channels involving AtKC1 and KAT1, KAT2 or AKT2 were analysed by voltage clamp after co-expression of the respective subunits in Xenopus oocytes. AtKC1 behaved as a regulatory subunit within the heterotetrameric channel, reducing the macroscopic conductance and negatively shifting the channel activation potential. Expression studies showed that AtKC1 and its identified Shaker partners have overlapping expression patterns, supporting the hypothesis of a general regulation of inward channel activity by AtKC1 in planta. Lastly, AtKC1 disruption appeared to reduce plant biomass production, showing that AtKC1-mediated channel activity regulation is required for normal plant growth.

  1. Ache Peter, Becker Dirk, Ivashikina Natalya, Dietrich Petra, Roelfsema M.Rob G, Hedrich Rainer, GORK, a delayed outward rectifier expressed in guard cells ofArabidopsis thaliana, is a K+-selective, K+-sensing ion channel, 10.1016/s0014-5793(00)02248-1
  2. Baizabal-Aguirre V.M., Clemens S., Uozumi N., Schroeder J.I., Suppression of Inward-Rectifying K + Channels KAT1 and AKT2 by Dominant Negative Point Mutations in the KAT1 α-Subunit, 10.1007/s002329900476
  3. Bechtold, C. R. Acad. Sci. Paris, 316, 1194 (1993)
  4. Becker Detlef, Binary vectors which allow the exchange of plant selectable markers and reporter genes, 10.1093/nar/18.1.203
  5. BLATT MICHAEL R., LEYMAN BARBARA, GEELEN DANNY, Tansley Review No. 108, 10.1046/j.1469-8137.1999.00546.x
  6. Boursiac Y., Early Effects of Salinity on Water Transport in Arabidopsis Roots. Molecular and Cellular Features of Aquaporin Expression, 10.1104/pp.105.065029
  7. Cherel I., Physical and Functional Interaction of the Arabidopsis K+ Channel AKT2 and Phosphatase AtPP2CA, 10.1105/tpc.000943
  8. Daram P., Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain, 10.1093/emboj/16.12.3455
  9. Deeken Rosalia, Geiger Dietmar, Fromm Jörg, Koroleva Olga, Ache Peter, Langenfeld-Heyser Rosemarie, Sauer Norbert, May Sean, Hedrich Rainer, Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis, 10.1007/s00425-002-0895-1
  10. Dennison K. L., Robertson W. R., Lewis B. D., Hirsch R. E., Sussman M. R., Spalding E. P., Functions of AKT1 and AKT2 Potassium Channels Determined by Studies of Single and Double Mutants of Arabidopsis, 10.1104/pp.010193
  11. Dreyer I., Antunes S., Hoshi T., Müller-Röber B., Palme K., Pongs O., Reintanz B., Hedrich R., Plant K+ channel alpha-subunits assemble indiscriminately, 10.1016/s0006-3495(97)78857-x
  12. Dreyer Ingo, Michard Erwan, Lacombe Benoı̂t, Thibaud Jean-Baptiste, A plant Shaker-like K+channel switches between two distinct gating modes resulting in either inward-rectifying or ‘leak’ current, 10.1016/s0014-5793(01)02832-0
  13. Dreyer Ingo, Porée Fabien, Schneider Antje, Mittelstädt Jessica, Bertl Adam, Sentenac Hervé, Thibaud Jean-Baptiste, Mueller-Roeber Bernd, Assembly of Plant Shaker-Like Kout Channels Requires Two Distinct Sites of the Channel α-Subunit, 10.1529/biophysj.103.037671
  14. Duby Geoffrey, Hosy Eric, Fizames Cécile, Alcon Carine, Costa Alex, Sentenac Hervé, Thibaud Jean-Baptiste, AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+channels, 10.1111/j.1365-313x.2007.03324.x
  15. Gajdanowicz P., Michard E., Sandmann M., Rocha M., Correa L. G. G., Ramirez-Aguilar S. J., Gomez-Porras J. L., Gonzalez W., Thibaud J.-B., van Dongen J. T., Dreyer I., Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues, 10.1073/pnas.1009777108
  16. Gaymard Frédéric, Pilot Guillaume, Lacombe Benoît, Bouchez David, Bruneau Dominique, Boucherez Jossia, Michaux-Ferrière Nicole, Thibaud Jean-Baptiste, Sentenac Hervé, Identification and Disruption of a Plant Shaker-like Outward Channel Involved in K+ Release into the Xylem Sap, 10.1016/s0092-8674(00)81606-2
  17. Geiger Dietmar, Becker Dirk, Vosloh Daniel, Gambale Franco, Palme Klaus, Rehers Marion, Anschuetz Uta, Dreyer Ingo, Kudla Jörg, Hedrich Rainer, HeteromericAtKC1·AKT1 Channels inArabidopsisRoots Facilitate Growth under K+-limiting Conditions, 10.1074/jbc.m109.017574
  18. Grefen Christopher, Chen Zhonghua, Honsbein Annegret, Donald Naomi, Hills Adrian, Blatt Michael R., A Novel Motif Essential for SNARE Interaction with the K+Channel KC1 and Channel Gating inArabidopsis, 10.1105/tpc.110.077768
  19. Hirsch R. E., A Role for the AKT1 Potassium Channel in Plant Nutrition, 10.1126/science.280.5365.918
  20. Honsbein A., Sokolovski S., Grefen C., Campanoni P., Pratelli R., Paneque M., Chen Z., Johansson I., Blatt M. R., A Tripartite SNARE-K+ Channel Complex Mediates in Channel-Dependent K+ Nutrition in Arabidopsis, 10.1105/tpc.109.066118
  21. Hosy E., Vavasseur A., Mouline K., Dreyer I., Gaymard F., Poree F., Boucherez J., Lebaudy A., Bouchez D., Very A.-A., Simonneau T., Thibaud J.-B., Sentenac H., The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration, 10.1073/pnas.0733970100
  22. Hosy E, Duby G, Véry A-A, Costa A, Sentenac H, Thibaud J-B, 10.1186/1746-4811-1-14
  23. Ivashikina Natalya, Deeken Rosalia, Fischer Susanne, Ache Peter, Hedrich Rainer, AKT2/3 Subunits Render Guard Cell K+Channels Ca2+Sensitive, 10.1085/jgp.200409211
  24. Jeanguenin Linda, Lebaudy Anne, Xicluna Jérôme, Alcon Carine, Hosy Eric, Duby Geoffrey, Michard Erwan, Lacombe Benoît, Dreyer Ingo, Thibaud Jean Baptiste, Heteromerization of Arabidopsis Kv channel α-subunits : Data and prospects, 10.4161/psb.3.9.6209
  25. Jouanneau Jean-Pierre, Peaud-Lenoel Claude, Croissance et synthese des proteines de suspensions cellulaires de Tabac sensibles a la kinetine, 10.1111/j.1399-3054.1967.tb08371.x
  26. Kwak J. M., Murata Y., Baizabal-Aguirre V. M., Merrill J., Wang M., Kemper A., Hawke S. D., Tallman G., Schroeder J. I., Dominant Negative Guard Cell K+ Channel Mutants Reduce Inward-Rectifying K+ Currents and Light-Induced Stomatal Opening in Arabidopsis, 10.1104/pp.010428
  27. Lacombe B., A Shaker-like K+ Channel with Weak Rectification Is Expressed in Both Source and Sink Phloem Tissues of Arabidopsis, 10.1105/tpc.12.6.837
  28. Lagarde Delphine, Basset Mireille, Lepetit Marc, Conejero Genevieve, Gaymard Frederic, Astruc Suzette, Grignon Claude, Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition, 10.1046/j.1365-313x.1996.09020195.x
  29. Lebaudy A., Vavasseur A., Hosy E., Dreyer I., Leonhardt N., Thibaud J.-B., Very A.-A., Simonneau T., Sentenac H., Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels, 10.1073/pnas.0709732105
  30. Lebaudy Anne, Hosy Eric, Simonneau Thierry, Sentenac Hervé, Thibaud Jean-Baptiste, Dreyer Ingo, Heteromeric K+channels in plants, 10.1111/j.1365-313x.2008.03479.x
  31. Lebaudy Anne, Pascaud François, Véry Anne-Aliénor, Alcon Carine, Dreyer Ingo, Thibaud Jean-Baptiste, Lacombe Benoît, Preferential KAT1-KAT2 Heteromerization Determines Inward K+Current Properties inArabidopsisGuard Cells, 10.1074/jbc.m109.068445
  32. Li L., Kim B.-G., Cheong Y. H., Pandey G. K., Luan S., A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis, 10.1073/pnas.0605129103
  33. Liman Emily R., Tytgat Jan, Hess Peter, Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs, 10.1016/0896-6273(92)90239-a
  34. Ma D., Role of ER Export Signals in Controlling Surface Potassium Channel Numbers, 10.1126/science.291.5502.316
  35. Maathuis Frans J. M., Filatov Victor, Herzyk Pawel, C. Krijger Gerard, B. Axelsen Kristian, Chen Sixue, Green Brian J., Li Yi, Madagan Kathryn L., Sánchez-Fernández Rocío, Forde Brian G., Palmgren Michael G., Rea Philip A., Williams Lorraine E., Sanders Dale, Amtmann Anna, Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress, 10.1046/j.1365-313x.2003.01839.x
  36. Marten I., Hoth S., Deeken R., Ache P., Ketchum K. A., Hoshi T., Hedrich R., AKT3, a phloem-localized K+ channel, is blocked by protons, 10.1073/pnas.96.13.7581
  37. Michelsen Kai, Yuan Hebao, Schwappach Blanche, Hide and run, 10.1038/sj.embor.7400480
  38. Mikosch M., Hurst A. C., Hertel B., Homann U., Diacidic Motif Is Required for Efficient Transport of the K+ Channel KAT1 to the Plasma Membrane, 10.1104/pp.106.087064
  39. Mouline K., Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis, 10.1101/gad.213902
  40. Nakamura R. L., McKendree Jr W. L., Hirsch R. E., Sedbrook J. C., Gaber R. F., Sussman M. R., Expression of an Arabidopsis Potassium Channel Gene in Guard Cells, 10.1104/pp.109.2.371
  41. Papazian D., Schwarz T., Tempel B., Jan Y., Jan L., Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila, 10.1126/science.2441470
  42. Pilot Guillaume, Lacombe Benoı̂t, Gaymard Frédéric, Chérel Isabelle, Boucherez Jossia, Thibaud Jean-Baptiste, Sentenac Hervé, Guard Cell Inward K+Channel Activity inArabidopsisInvolves Expression of the Twin Channel Subunits KAT1 and KAT2, 10.1074/jbc.m007303200
  43. Pilot Guillaume, Gaymard Frédéric, Mouline Karine, Chérel Isabelle, Sentenac Hervé, 10.1023/a:1022597102282
  44. Reintanz Birgit, Szyroki Alexander, Ivashikina Natalya, Ache Peter, Godde Matthias, Becker Dirk, Palme Klaus, Hedrich Rainer, AtKC1, a silentArabidopsispotassium channel α-subunit modulates root hair K+influx, 10.1073/pnas.052677799
  45. Schwappach Blanche, Zerangue Noa, Jan Yuh Nung, Jan Lily Yeh, Molecular Basis for K ATP Assembly, 10.1016/s0896-6273(00)81146-0
  46. Sottocornola B., Gazzarrini S., Olivari C., Romani G., Valbuzzi P., Thiel G., Moroni A., 14-3-3 proteins regulate the potassium channel KAT1 by dual modes, 10.1111/j.1438-8677.2007.00028.x
  47. Sutter J.-U., Selective Mobility and Sensitivity to SNAREs Is Exhibited by the Arabidopsis KAT1 K+ Channel at the Plasma Membrane, 10.1105/tpc.105.038950
  48. 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, 10.1073/pnas.051616698
  49. Thomine Sébastien, Lelièvre Françoise, Debarbieux Elise, Schroeder Julian I., Barbier-Brygoo Hélène, AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency, 10.1046/j.1365-313x.2003.01760.x
  50. Urbach Serge, Cherel Isabelle, Sentenac Herve, Gaymard Frederic, Biochemical characterization of the Arabidopsis K+ channels KAT1 and AKT1 expressed or co-expressed in insect cells, 10.1046/j.1365-313x.2000.00828.x
  51. Véry Anne-Aliénor, Sentenac Hervé, MOLECULARMECHANISMS ANDREGULATION OFK+TRANSPORT INHIGHERPLANTS, 10.1146/annurev.arplant.54.031902.134831
  52. V�ry A. -A., Bosseux C., Gaymard F., Sentenac H., Thibaud J. -B., Level of expression inXenopus oocytes affects some characteristics of a plant inward-rectifying voltage-gated K+ channel, 10.1007/bf00724528
  53. Very Anne-Alienor, Gaymard Frederic, Bosseux Corinne, Sentenac Herve, Thibaud Jean-Baptiste, Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents, 10.1046/j.1365-313x.1995.7020321.x
  54. Wang Yi, He Liu, Li Hao-Dong, Xu Jiang, Wu Wei-Hua, Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress, 10.1038/cr.2010.74
  55. Xicluna Jérôme, Lacombe Benoît, Dreyer Ingo, Alcon Carine, Jeanguenin Linda, Sentenac Hervé, Thibaud Jean-Baptiste, Chérel Isabelle, Increased Functional Diversity of Plant K+Channels by Preferential Heteromerization of the Shaker-like Subunits AKT2 and KAT2, 10.1074/jbc.m607607200
  56. Xu Jiang, Li Hao-Dong, Chen Li-Qing, Wang Yi, Liu Li-Li, He Liu, Wu Wei-Hua, A Protein Kinase, Interacting with Two Calcineurin B-like Proteins, Regulates K+ Transporter AKT1 in Arabidopsis, 10.1016/j.cell.2006.06.011
  57. Zerangue Noa, Schwappach Blanche, Jan Yuh Nung, Jan Lily Yeh, A New ER Trafficking Signal Regulates the Subunit Stoichiometry of Plasma Membrane KATP Channels, 10.1016/s0896-6273(00)80708-4
Bibliographic reference Jeanguenin, Linda ; Alcon, Carine ; Duby, Geoffrey ; Boeglin, Martin ; Chérel, Isabelle ; et. al. AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity.. In: The Plant journal, Vol. 67, no. 4, p. 570-582 (2011)
Permanent URL http://hdl.handle.net/2078/138680