CPK13, A noncanonical Ca2+-Dependent protein kinase, Specifically inhibits KAT2 and KAT1 shaker K+channels and reduces stomatal opening

Plant Physiology

Volumn 166, Issue 1, 2014, Pages 314-326

  Ronzier, Elsa ^a   Corratgé Faillie, Claire ^a   Sanchez, FréDéRic ^a   Prado, Karine ^a   Brière, Christian ^b,c   Leonhardt, Nathalie ^d   Thibaud, Jean Baptiste ^a   Xiong, Tou Cheu ^a  

^a INRA   (France)

^b CNRS   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d University of Aix Marseille   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; CPK13 PROTEIN, ARABIDOPSIS; INWARDLY RECTIFYING POTASSIUM CHANNEL; KAT1 PROTEIN, ARABIDOPSIS; KAT2 PROTEIN, ARABIDOPSIS; PROTEIN KINASE; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL; ARABIDOPSIS; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; PATCH CLAMP TECHNIQUE; PHOSPHORYLATION; PLANT STOMA; XENOPUS LAEVIS;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; MICROSCOPY, FLUORESCENCE; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PLANT STOMATA; POTASSIUM CHANNELS, INWARDLY RECTIFYING; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN KINASES; XENOPUS LAEVIS;

EID: 84907057033     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.240226     Document Type: Article

References (82)

1. Acharya BR, Jeon BW, Zhang W, Assmann SM (2013) Open Stomata 1 (OST1) is limiting in abscisic acid responses of Arabidopsis guard cells. New Phytol 200: 1049-1063.
2. Batistic O, Waadt R, Steinhorst L, Held K, Kudla J (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J 61: 211-222.
3. Benetka W, Mehlmer N, Maurer-Stroh S, Sammer M, Koranda M, Neumüller R, Betschinger J, Knoblich JA, Teige M, Eisenhaber F (2008) Experimental testing of predicted myristoylation targets involved in asymmetric cell division and calcium-dependent signalling. Cell Cycle 7: 3709-3719.
4. Berkowitz G, Zhang X, Mercie R, Leng Q, Lawton M (2000) Co-expression of calcium-dependent protein kinase with the inward rectified guard cell K+ channel KAT1 alters current parameters in Xenopus laevis oocytes. Plant Cell Physiol 41: 785-790.
5. Blatt MR (1991) Ion channel gating in plants: physiological implications and integration for stomatal function. J Membr Biol 124: 95-112.
6. +channels of stomatal guard cells: characteristics of the inward rectifier and its control by pH. J Gen Physiol 99: 615-644.
7. 2+signalling and control of guard-cell volume in stomatal movements. Curr Opin Plant Biol 3: 196-204.
8. Boudsocq M, Droillard MJ, Regad L, Laurière C (2012) Characterization of Arabidopsis calcium-dependent protein kinases: activated or not by calcium? Biochem J 447: 291-299.
9. 2+sensor protein kinases. Nature 464: 418-422.
10. Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1. PP2C phosphatase action. Proc Natl Acad Sci USA 109: 10593-10598.
11. Chen L, Wang QQ, Zhou L, Ren F, Li DD, Li XB (2013) Arabidopsis CBLinteracting protein kinase (CIPK6) is involved in plant response to salt/ osmotic stress and ABA. Mol Biol Rep 40: 4759-4767.
12. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases: the Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129: 469-485.
13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
14. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/ NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110: 8744-8749.
15. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629.
16. 2+affinities. Proc Natl Acad Sci USA 107: 8023-8028.
17. Gibbs CS, Zoller MJ (1991) Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J Biol Chem 266: 8923-8931.
18. Grabov A, Blatt MR (1999) A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in guard cells. Plant Physiol 119: 277-288.
19. 2+signal? Trends Plant Sci 5: 154-159.
20. 2+signals through plant protein kinases. Annu Rev Plant Biol 55: 263-288.
21. Harper JF, Huang JF, Lloyd SJ (1994) Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33: 7267-7277.
22. Hedrich R (2012) Ion channels in plants. Physiol Rev 92: 1777-1811.
23. Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratgé-Faillie C, Offenborn JN, Lacombe B, Dreyer I, Thibaud JB, et al (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21: 1116-1130.
24. Hetherington AM (2001) Guard cell signaling. Cell 107: 711-714.
25. 2+signals in plants. Annu Rev Plant Biol 55: 401-427.
26. +channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100: 5549-5554.
27. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57: 264-278.
28. Hubbard KE, Siegel RS, Valerio G, Brandt B, Schroeder JI (2012) Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses. Ann Bot (Lond) 109: 5-17.
29. Imes D, Mumm P, Böhm J, Al-Rasheid KA, Marten I, Geiger D, Hedrich R (2013) Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant J 74: 372-382.
30. Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89: 1790-1794.
31. Islam MM, Hossain MA, Jannat R, Munemasa S, Nakamura Y, Mori IC, Murata Y (2010) Cytosolic alkalization and cytosolic calcium oscillation in Arabidopsis guard cells response to ABA and MeJA. Plant Cell Physiol 51: 1721-1730.
32. 2+sensor priming hypothesis. Curr Opin Plant Biol 9: 654-663.
33. Jeanguenin L, Lebaudy A, Xicluna J, Alcon C, Hosy E, Duby G, Michard E, Lacombe B, Dreyer I, Thibaud JB (2008) Heteromerization of Arabidopsis Kv channel alpha-subunits: data and prospects. Plant Signal Behav 3: 622-625.
34. Kanchiswamy CN, Takahashi H, Quadro S, Maffei ME, Bossi S, Bertea C, Zebelo SA, Muroi A, Ishihama N, Yoshioka H, et al (2010) Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPKmediated calcium signaling. BMC Plant Biol 10: 97.
35. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347-363.
36. +-ATPase of camelina and rapeseed. J Plant Physiol 170: 828-837.
37. +currents and light-induced stomatal opening in Arabidopsis. Plant Physiol 127: 473-485.
38. Laanemets K, Brandt B, Li J, Merilo E, Wang YF, Keshwani MM, Taylor SS, Kollist H, Schroeder JI (2013) Calcium-dependent and -independent stomatal signaling network and compensatory feedback control of stomatal opening via Ca2+ sensitivity priming. Plant Physiol 163: 504-513.
39. Lan WZ, Lee SC, Che YF, Jiang YQ, Luan S (2011) Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions. Mol Plant 4: 527-536.
40. +channels in plants. Plant J 54: 1076-1082.
41. +current properties in Arabidopsis guard cells. J Biol Chem 285: 6265-6274.
42. Lebaudy A, Vavasseur A, Hosy E, Dreyer I, Leonhardt N, Thibaud JB, Véry AA, Simonneau T, Sentenac H (2008b) Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels. Proc Natl Acad Sci USA 105: 5271-5276.
43. +channel activity in plants: genes, regulations and functions. FEBS Lett 581: 2357-2366.
44. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16: 596-615.
45. Li J, Lee YR, Assmann SM (1998) Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 116: 785-795.
46. Liese A, Romeis T (2013) Biochemical regulation of in vivo function of plant calcium-dependent protein kinases (CDPK). Biochim Biophys Acta 1833: 1582-1589.
47. Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124: 1315-1326.
48. Lu SX, Hrabak EM (2013) The myristoylated amino-terminus of an Arabidopsis calcium-dependent protein kinase mediates plasma membrane localization. Plant Mol Biol 82: 267-278.
49. Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14: 37-42.
50. +channels in guard cells. Proc Natl Acad Sci USA 90: 2202-2206.
51. 2+and cell signalling in guard cells. Semin Cell Biol 4: 113-122.
52. MacRobbie EA (1998) Signal transduction and ion channels in guard cells.Philos Trans R Soc Lond B Biol Sci 353: 1475-1488.
53. 2+-dependent and -independent abscisic acid activation of plasma membrane anion channels in guard cells of Nicotiana tabacum. Plant Physiol 143: 28-37.
54. Martín ML, Busconi L (2000) Membrane localization of a rice calciumdependent protein kinase(CDPK)is mediated by myristoylation and palmitoylation. Plant J 24: 429-435.
55. McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111: 1031-1042.
56. 2+-permeable channels and stomatal closure. PLoS Biol 4: e327.
57. Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2011) The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol 155: 553-561.
58. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14: 3089-3099.
59. Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y, et al (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71: 2095-2100.
60. +channel KAT2 determine its subcellular localization and activity at the plasma membrane. Plant Physiol 164: 1415-1429.
61. Nilson SE, Assmann SM (2007) The control of transpiration: insights from Arabidopsis. Plant Physiol 143: 19-27.
62. Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581: 2325-2336.
63. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
64. +channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J Biol Chem 276: 3215-3221.
65. Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114: 1-28.
66. Scherzer S, Maierhofer T, Al-Rasheid KA, Geiger D, Hedrich R (2012) Multiple calcium-dependent kinases modulate ABA-activated guard cell anion channels. Mol Plant 5: 1409-1412.
67. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
68. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52: 627-658.
69. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonateand abscisic acid-induced stomatal closure. Plant Physiol 134: 1536-1545.
70. Szyroki A, Ivashikina N, Dietrich P, Roelfsema MR, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, et al (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA 98: 2917-2921.
71. Thiel G, MacRobbie EA, Blatt MR (1992) Membrane transport in stomatal guard cells: the importance of voltage control. J Membr Biol 126: 1-18.
72. +channel in Xenopus oocytes: analysis of macroscopic currents. Plant J 7: 321-332.
73. Véry AA, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci 7: 168-175.
74. +transport in higher plants. Annu Rev Plant Biol 54: 575-603.
75. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292: 2070-2072.
76. Webb AA, Larman MG, Montgomery LT, Taylor JE, Hetherington AM (2001) The role of calcium in ABA-induced gene expression and stomatal movements. Plant J 26: 351-362.
77. 2+-decoding signaling network: function and perspectives. New Phytol 184: 517-528.
78. Wilkinson S, Clephan AL, Davies WJ (2001) Rapid low temperatureinduced stomatal closure occurs in cold-tolerant Commelina communis leaves but not in cold-sensitive tobacco leaves, via a mechanism that involves apoplastic calcium but not abscisic acid. Plant Physiol 126: 1566-1578.
79. +channels by preferential heteromerization of the shaker-like subunits AKT2 and KAT2. J Biol Chem 282: 486-494.
80. +transporter AKT1 in Arabidopsis. Cell 125: 1347-1360.
81. Zhao Z, Zhang W, Stanley BA, Assmann SM (2008) Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20: 3210-3226.
82. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, et al (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19: 3019-3036