Biologia plantarum 55:507-521, 2011 | DOI: 10.1007/s10535-011-0117-4

Arabidopsis Ca2+-dependent protein kinase CPK3 mediates relationship of putative inositol triphosphate receptor with slow-type anion channel

A. Cousson1,2,3,*
1 CEA, DSV, IBEB, Lab. Echanges Membran et Signalisation, Saint-Paul-lez-Durance, France
2 CNRS, UMR, Biol. Veget. et Microbiol. Environ., Saint-Paul-lez-Durance, France
3 Aix-Marseille Université, Saint-Paul-lez-Durance, France

It has been suggested in Arabidopsis thaliana (L.) Heynh. cv. Columbia that, contrary to 30 μM abscisic acid (ABA), 20 μM ABA induces guard cell Ca2+ mobilization through activating phosphoinositide-specific phospholipase C (PI-PLC)-dependent inositol 1,4,5-triphosphate (IP3) production. Here, it was investigated whether Ca2+-dependent protein kinase, CPK3 or CPK6 would mediate ABA-induced stomatal closure downstream of IP3 production. In the knockout cpk3-1 mutant, the PLC inhibitor (U73122) adjusted 20 μM ABA-induced stomatal closure to the extent observed in the knockout cpk6-1 and cpk3-1cpk6-1 mutants and the wild type, whereas, in the wild type, the inhibitor of IP3-induced Ca2+ mobilization, xestospongin C (XeC), adjusted this closure to the extent observed in the cpk3-1 mutant. The Ca2+ buffer, EGTA and XeC positively interacted with the slow anion channel blocker, anthracene-9-carboxylic acid (9-AC) to inhibit 20 μM ABA-induced stomatal closure, which was suppressed in the dexamethasone-inducible AtPLC1 antisense transgene or the knockout cpk3-1, cpk6-1, cpk3-1cpk6-1 and NADPH oxidase atrbohD/F mutants. Discrete concentrations of 9-AC or another slow anion channel blocker (probenecid) negatively interacted with the Ca2+ buffer, BAPTA or the inhibitor of cyclic ADP-ribose-induced Ca2+ mobilization, ruthenium red, to inhibit 30 μM ABAinduced stomatal closure in the wild type but not in the cpk6-1, cpk3-1cpk6-1 and atrbohD/F mutants. Based on so far revealed features of the tested compounds and plant materials, interpretation of the results confirmed that guard cell ABA concentration discriminates between two Ca2+ mediations and outlined that one of them sequentially implicates CPK6, PLC1, a putative IP3 receptor homologue, CPK3, and the slow anion channel, whereas the other one excludes AtPLC1-dependent IP3 production and CPK3.

Keywords: abscisic acid concentration; anion channel blockers; Ca2+-dependent protein phosphorylation; intracellular Ca2+ modulators; phospholipase C; stomatal closure

Received: November 19, 2009; Accepted: June 8, 2010; Published: September 1, 2011Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Cousson, A. (2011). Arabidopsis Ca2+-dependent protein kinase CPK3 mediates relationship of putative inositol triphosphate receptor with slow-type anion channel. Biologia plantarum55(3), 507-521. doi: 10.1007/s10535-011-0117-4.
Download citation

References

  1. Aarhus, R., Graeff, R.M., Dickey, D.M., Walseth, T.F., Lee, H.C.: ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. - J. biol. Chem. 270: 30327-30333, 1995. Go to original source...
  2. Albrecht, V., Weinl, S., Blazevic, D., D'Angelo, C., Batistic, O., Kolukisaoglu, Ü., Bock, R., Schulz, B., Harter, K., Kudla, J.: The calcium sensor CBL1 integrates plant responses to abiotic stresses. - Plant J. 36: 457-470, 2003. Go to original source...
  3. Allen, G.J., Chu, S.P., Harrington, C.L., Schumacher, K., Hoffmann, T., Tang, Y.Y., Grill, E., Schroeder, J.I.: A defined range of guard cell oscillation parameters encodes stomatal movements. - Nature 411: 1053-1057, 2001. Go to original source...
  4. Allen, G.J., Muir, S.R., Sanders, D.: Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADPribose. - Science 268: 735-737, 1995. Go to original source...
  5. Aoyama, T., Chua, N.-H.: A glucocorticoid-mediated transcriptional induction system in transgenic plants. - Plant J. 11: 605-612, 1997. Go to original source...
  6. Armstrong, F., Blatt, M.R.: Evidence for K+ channel control in Vicia guard cells coupled by G-proteins to a 7TMS receptor mimetic. - Plant J. 8: 187-198, 1995. Go to original source...
  7. Assmann, S.M., Schwartz, A.: Synergistic effect of light and fusicoccin on stomatal opening. - Plant Physiol. 98: 1349-1355, 1992. Go to original source...
  8. Berridge, M.J.: Inositol triphosphate and calcium signalling. - Nature 361: 315-325, 1993. Go to original source...
  9. Blatt, M.R., Armstrong, F.: K+ channels of stomatal guard cells: abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH. - Planta 191: 330-341, 1993. Go to original source...
  10. Burnette, R.N., Gunesekera, B.M., Gillaspy, G.E.: An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling. - Plant Physiol. 132: 1011-1019, 2003. Go to original source...
  11. Chen, J.-G., Gao, Y., Jones, A.M.: Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. - Plant Physiol. 141: 887-897, 2006. Go to original source...
  12. Cousson, A.: Pharmacological study of two potential Ca2+ signalling pathways within stomatal closing in response to abscisic acid in Commelina communis L. - Plant Sci. 145:67-74, 1999. Go to original source...
  13. Cousson, A.: Carbon dioxide and ferricyanide parallel each other to inhibit Commelina stomatal opening in a putative Ca2+-independent fashion. - J. Plant Physiol. 159: 281-291, 2002. Go to original source...
  14. Cousson, A.: Two potential Ca2+-mobilising processes depend on the abscisic acid concentration and growth temperature in the Arabidopsis stomatal guard cell. - J. Plant Physiol. 160: 493-501, 2003. Go to original source...
  15. Cousson, A.: Pharmacological evidence for a putative mediation of cyclic GMP and cytosolic Ca2+ within auxin-induced de novo root formation in the monocot plant Commelina communis (L.). - Plant Sci. 166: 1117-1124, 2004. Go to original source...
  16. Cousson, A.: Two Ca2+ mobilizing pathways implicated within abscisic acid-induced stomatal closing in Arabidopsis thaliana (L.) Heynh. (Columbia-4 ecotype). - Biol. Plant. 51: 285-291, 2007. Go to original source...
  17. Cousson, A.: Putative primary involvement of Arabidopsis phosphoinositide-specific phospholipase C1 within abscisic acid-induced stomatal closing. - Biol. Plant. 52: 493-501, 2008. Go to original source...
  18. Cousson, A.: Involvement of phospholipase C-independent calcium-mediated abscisic acid signalling during Arabidopsis response to drought. - Biol. Plant. 53: 53-62, 2009. Go to original source...
  19. Cousson, A., Cotelle, V., Vavasseur, A.: Induction of stomatal closure by vanadate or a light/dark transition involves Ca2+-calmodulin-dependent protein phosphorylations. - Plant Physiol. 109: 491-497, 1995. Go to original source...
  20. Cousson, A., Vavasseur, A.: Putative involvement of cytosolic Ca2+ and GTP-binding proteins in cyclic GMP-mediated induction of stomatal opening by auxin in Commelina communis L. - Planta 206: 308-314, 1998a. Go to original source...
  21. Cousson, A., Vavasseur, A.: Two potential Ca2+-dependent transduction pathways in stomatal closing in response to abscisic acid. - Plant Physiol. Biochem. 36: 257-262, 1998b. Go to original source...
  22. Davies, W.J., Mansfield, T.A.: Auxins and stomata. - In: Zeiger, E., Farquhar, G.D., Cowan, I.C. (ed.): Stomatal Function. Pp. 293-309. Stanford University Press, Stanford 1987.
  23. De Smet, P., Parys, J.B., Callewaert, G., Weidema, A.F., Hill, E., De Smedt, H., Erneux, C., Sorrentino, V., Missiaen, L.: Xestospongin C is an equally potent inhibitor of the inositol 1,4,5-triphosphate receptor and the endoplasmic reticulum Ca2+ pumps. - Cell Calcium 26: 9-13, 1999. Go to original source...
  24. Dolmetsch, R.E., Lewis, R.S., Goodnow, C.C., Healy, J.I.: Differential activation of transcription factors induced by Ca2+ response amplitude and duration. - Nature 386: 855-858, 1997. Go to original source...
  25. Forestier, C., Bouteau, F., Leonhardt, N., Vavasseur, A.: Pharmacological properties of slow anion currents in intact guard cells of Arabidopsis. Application of the discontinuous single-electrode voltage-clamp to different species. - Eur J. Physiol. 436: 920-927, 1998. Go to original source...
  26. Gaedeke, N., Klein, M., Kolukisaoglu, M., Forestier, C., Müller, A., Ansorge, M., Becker, D., Mamnun, Y., Kuchler, K., Schulz, B., Mueller-Roeber, B., Martinoia, E.: The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomatal movement. - EMBO J. 20:1875-1887, 2001. Go to original source...
  27. Gabriel, S.E., Clarke, L.L., Boucher, R.C., Stutts, M.J.: CFTR and outward rectifying chloride channels are distinct proteins with a regulatory relationship. - Nature 363: 263-266, 1993. Go to original source...
  28. Gafni, J., Munsch, J.A., Lam, T.H., Catlin, M.C., Costa, L.G., Molinski, T.F., Pessah, L.N.: Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-triphosphate receptor. - Neuron 19: 723-733, 1997. Go to original source...
  29. Galione, A.: Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling. - Mol. cell. Endocrinol. 98:125-131, 1994. Go to original source...
  30. Galione, A., Lee, H.C., Busa, W.B.: Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADPribose. - Science 253: 1143-1146, 1991. Go to original source...
  31. Gilroy, S., Read, N.D., Trewavas, A.J.: Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. - Nature 346: 769-771, 1990. Go to original source...
  32. Grabov, A., Blatt, M.R.: Parallel control of the inward-rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells. - Planta 201: 84-95, 1997. Go to original source...
  33. Grabov, A., Blatt, M.R.: Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. - Proc. nat. Acad. Sci. USA 95: 4778-4783, 1998. Go to original source...
  34. Grabov, A., Blatt, M.R.: A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in guard cells. - Plant Physiol. 119: 277-287, 1999. Go to original source...
  35. Grabov, A., Leung, J., Giraudat, J., Blatt, M.R.: Alteration of anion channel kinetics in wild type and abi1-1 transgenic Nicotiana benthamiana guard cells by abscisic acid. - Plant J. 12: 203-213, 1997. Go to original source...
  36. Guo, Y., Xiong, L., Song, C.P., Gong, D., Halfter, U., Zhu, J.K.: A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. - Dev. Cell. 3: 233-244, 2002. Go to original source...
  37. Hajdukiewicz, P., Svab, Z., Maliga, P.: The small, versatile pPZP family of Agrobacterium vectors for plant transformation. - Plant mol. Biol. 25: 989-994, 1994. Go to original source...
  38. Harper, J.F., Breton, G., Harmon, A.: Decoding Ca2+ signals through plant protein kinases. - Annu. Rev. Plant Biol. 55:263-288, 2004. Go to original source...
  39. Hirayama, T., Ohto, C., Mizoguchi, T., Shinozaki, K.: A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 92: 3903-3907, 1995. Go to original source...
  40. Howard, M., Grimaldi, J.C., Bazan, J.F., Lund, F.E., Santos-Argumedo, L., Parkhouse, R.M., Walseth, T.F., Lee, H.C.: Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. - Science 262: 1056-1059, 1993. Go to original source...
  41. Hunt, L., Mills, L.N., Pical, C., Leckie, C.P., Aitken, F.L., Kopka, J., Mueller-Roeber, B., McAinsh, M.R., Hetherington, A.M., Gray, J.E.: Phospholipase C is required for the control of stomatal aperture by ABA. - Plant J. 34:47-55, 2003. Go to original source...
  42. Ishige, F., Takaishi, M., Foster, R., Chua, N-H., Oeda, K.: A G-box motif (GCCACGTGCC) tetramer confers high levels of constitutive expression in dicot and monocot. - Plant J. 18: 443-448, 1999. Go to original source...
  43. Kinoshita, T., Nishimura, M., Shimazaki, K.-I.: Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of fava bean. - Plant Cell 7: 1333-1342, 1995. Go to original source...
  44. Klein, M., Perfus-Barbeoch, L., Frelet, A., Gaedeke, N., Reinhardt, D., Mueller-Roeber, B., Martinoia, E., Forestier, C.: The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. - Plant J. 33: 119-129, 2003. Go to original source...
  45. Kwak, J.M., Moon, J-H., Murata, Y., Kuchitsu, K., Leonhardt, N., DeLong, A., Schroeder, J.I.: Disruption of a guard cellexpressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. - Plant Cell 14: 2849-2861, 2002. Go to original source...
  46. Kwak, J.M., Mori, I.C., Pei, Z-M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D.G., Schroeder, J.I.: NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. - EMBO J. 22: 2623-2633, 2003. Go to original source...
  47. Larsen, P.B., Tai, C.Y., Kochian, L.V., Howell, S.H.: Arabidopsis mutants with increased sensitivity to aluminum. - Plant Physiol. 110: 743-751, 1996. Go to original source...
  48. Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., Hetherington, A.M.: Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. - Proc. nat. Acad. Sci. USA 95: 15837-15842, 1998. Go to original source...
  49. Lee, H.C.: Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. - J. biol. Chem. 268:293-299, 1993.
  50. Lee, J.Y., Yoo, B.C., Harmon, A.C.: Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. - Biochem 37: 6801-6809, 1998. Go to original source...
  51. Lee, K.H., Piao, H.L., Kim, H-Y., Choi, S.M., Jiang, F., Hartung, W., Hwang, I., Kwak, J.M., Lee, I-J., Hwang, I.: Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. - Cell 126:1109-1120, 2006. Go to original source...
  52. Lee, Y., Choi, Y.B., Suh, S., Lee, J., Assmann, S.M., Joe, C.O., Kelleher, J.F., Crain, R.C.: Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. - Plant Physiol. 110: 987-996, 1996. Go to original source...
  53. Leonhardt, N., Bazin, I., Richaud, P., Marin, E., Vavasseur, A., Forestier, C.: Antibodies to CFTR modulate the turgor pressure of guard cell protoplasts via slow anion channels. - FEBS Lett. 494: 15-18, 2001. Go to original source...
  54. Leymarie, J., Lascève, G., Vavasseur, A.: Interaction of stomatal responses to ABA and CO2 in Arabidopsis thaliana. - Aust J. Plant Physiol. 25: 785-791, 1998. Go to original source...
  55. Marten, I., Zeilinger, C., Redhead, C., Landry, D.W., Al-Awqati, Q., Hedrich, R.: Identification and modulation of a voltage-dependent anion channel in the plasma membrane of guard cells by high-affinity ligands. - EMBO J 11: 3569-3575, 1992. Go to original source...
  56. McAinsh, M.R., Brownlee, C., Hetherington, A.M.: Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. - Nature 343: 186-188, 1990. Go to original source...
  57. Mori, I.C., Murata, Y., Yang, Y., Munemasa, S., Wang, Y.-F., Andreoli, S., Tiriac, H., Alonso, J.M., Harper, J.F., Ecker, J.R., Kwak, J.M., Schroeder, JI.: CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. - PLoS Biol. 4(10): e327, 2006. Go to original source...
  58. Mueller-Roeber, B., Pical, C.: Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. - Plant Physiol. 130: 22-46, 2002. Go to original source...
  59. Muir, S.R., Bewell, M.A., Sanders, D., Allen, G.J.: Ligandgated Ca2+ channels and Ca2+ signalling in higher plants. - J. exp. Bot. 48: 589-597, 1997. Go to original source...
  60. Pandey, G.K., Cheong, Y.H., Kim, K-N., Grant, J.J., Li, L., Hung, W., D'Angelo, C., Weinl, S., Kudla, J., Luan, S.: The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. - Plant Cell 16: 1912-1924, 2004.
  61. 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 9: 409-423, 1997. Go to original source...
  62. Pei, Z.-M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., Schroeder, J.I.: Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. - Nature 406: 731-734, 2000. Go to original source...
  63. Pineros, M., Tester, M.: Calcium channels in higher plant cells: selectivity, regulation and pharmacology. - J. exp. Bot. 48: 551-577, 1997. Go to original source...
  64. Pratt, S., Shepard, R.L., Kandasamy, R.A., Johnston, P.A., Perry III, W., Dantzig, A.H.: The multidrug resistance protein 5 (ABCC5) confers resistance to 5-fluorouracil and transports its monophosphorylated metabolites. - Mol. Cancer Therapy 4: 855-863, 2005. Go to original source...
  65. Raschke, K., Shabahang, M., Wolf, R.: The slow and rapid anion conductance in whole guard cells: their voltage-dependent alternation, and the modulation of their activities by abscisic acid and CO2. - Planta 217: 639-650, 2003. Go to original source...
  66. Roelfsema, M.R.G., Levchenko, V., Hedrich, R.: ABA depolarizes guard cells in intact plants, through a transient activation of R- and S-type anion channels. - Plant J. 37: 578-588, 2004. Go to original source...
  67. Sanchez, J.-P., Chua, N.-H.: Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. - Plant Cell 13: 1143-1154, 2001. Go to original source...
  68. Sanchez, J.-P., Duque, P., Chua, N.-H.: ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. - Plant Cell 38: 381-395, 2004.
  69. Sanders, D., Pelloux, J., Brownlee, C., Harper, J.F.: Calcium at the crossroads of signaling. - Plant Cell 14(Suppl.): S401-S417, 2002. Go to original source...
  70. Schmidt, C., Schelle, I., Liao, Y.-J., Schroeder, J.I.: Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. - Proc. nat. Acad. Sci. USA 92: 9535-9539, 1995. Go to original source...
  71. Schroeder, J.I., Hagiwara, D.: Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. - Nature 338: 427-430, 1989. Go to original source...
  72. Schulz-Lessdorf, B., Lohse, G., Hedrich, R.: GCAC1 recognizes the pH gradient across the plasma membrane: a pH-sensitive and ATP-dependent anion channel links guard cell membrane potential to acid and energy metabolism. - Plant J. 10: 993-1004, 1996. Go to original source...
  73. Schwartz, A., Ilan, N., Schwarz, M., Scheaffer, J., Assmann, S.M., Schroeder, J.I.: Anion-channel blockers inhibit S-type anion channels and abscisic acid responses in guard cells. - Plant Physiol. 109: 651-658, 1995. Go to original source...
  74. Schwarz, M., Schroeder, J.I.: Abscisic acid maintains S-type anion channel activity in ATP-depleted Vicia faba guard cells. - FEBS Lett. 428: 177-182, 1998. Go to original source...
  75. Sethi, J.K., Empson, R.M., Galione, A.: Nicotinamide inhibits cyclic ADP-ribose-mediated calcium signalling in sea urchin eggs. - Biochem J. 319: 613-617, 1996. Go to original source...
  76. Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., Hetherington, A.M., McAinsh, M.R.: Abscisic acid induces oscillations in guard cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. - Proc. nat. Acad. Sci. USA 96: 1779-1784, 1999. Go to original source...
  77. Suh, S.J., Wang, Y.F., Frelet, A., Leonhardt, N., Klein, M., Forestier, C., Mueller-Roeber, B., Cho, M.H., Martinoia, E., Schroeder, J.I.: The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. - J. biol. Chem. 282: 1916-1924, 2007.
  78. Thiel, G., MacRobbie, E.A.C., Blatt, M.R.: Membrane transport in stomatal guard cells: the importance of voltage control. - J. Membrane Biol. 126: 1-18, 1992. Go to original source...
  79. Thompson, A.K., Mostafapour, S.P., Denlinger, L.C., Bleasdale, J.E., Fisher, S.K.: The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation. - J. biol. Chem. 266: 23856-23862, 1991.
  80. Wang, X.-Q., Ullah, H., Jones, A.M., Assmann, S.M.: G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. - Science 292: 2070-2072, 2001. Go to original source...
  81. Wu, Y., Kuzma, J., Maréchal, E., Graeff, R., Lee, H.C., Foster, R., Chua, N-H.: Abscisic acid signaling through cyclic ADP-ribose in plants. - Science 278: 2126-2130, 1997. Go to original source...