Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening

Plant and Cell Physiology

Volumn 54, Issue 1, 2013, Pages 24-35

  Takemiya, Atsushi ^a   Yamauchi, Shota ^a   Yano, Takayuki ^a   Ariyoshi, Chie ^a   Shimazaki, Ken Ichiro ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Arabidopsis; Blue light; Phototropin; PP1; Protein phosphatase; Stomata

Indexed keywords

ARABIDOPSIS PROTEIN; NPH1 PROTEIN, ARABIDOPSIS; PHOSPHOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PHOT2 PROTEIN, ARABIDOPSIS; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PYRAN DERIVATIVE; SPIRO COMPOUND; TAUTOMYCIN;

ARABIDOPSIS; ARTICLE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; GENETICS; LIGHT; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT STOMA; PROTEIN MOTIF; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; VICIA FABA;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; LIGHT; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHOPROTEINS; PHYLOGENY; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; PROTEIN PHOSPHATASE 1; PROTEIN SUBUNITS; PROTON-TRANSLOCATING ATPASES; PYRANS; SIGNAL TRANSDUCTION; SPIRO COMPOUNDS; VICIA FABA;

ARABIDOPSIS; EUKARYOTA; VICIA FABA;

EID: 84872359577     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs073     Document Type: Article

References (60)

1. Aggen, J.B., Nairn, A.C. and Chamberlin, R. (2000) Regulation of protein phosphatase 1. Chem. Biol. 7: R13-R23
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 633-657
3. Assmann, S.M., Simoncini, L. and Schroeder, J.I. (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba. Nature 318: 285-287
4. Barford, D., Das, A.K. and Egloff, M.P. (1998) The structure and mechanism of protein phosphatases: Insights into catalysis and regulation. Annu. Rev. Biophys. Biomol. Struct. 27: 133-164
5. Bollen, M. (2001) Combinational control of protein phosphatase-1. Trends Biochem. Sci. 26: 426-431
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254
7. Caro, E., Castellano, M.M. and Gutierrez, C. (2007) A chromatin link that couples cell division to root epidermis patterning in Arabidopsis. Nature 447: 213-217
8. Ceulemans, H. and Bollen, M. (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84: 1-39
9. Christie, J.M. (2007) Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58: 21-45
10. Cohen, P.T.W. (2002) Protein phosphatase 1 - targeted in many directions. J. Cell Sci. 115: 241-256
11. DeLong, A. (2006) Switching the flip: Protein phosphatase roles in signaling pathways. Curr. Opin. Plant Biol. 9: 470-477
12. Doerks, T., Strauss, M., Brendel, M. and Bork, P. (2000) GRAM, a novel domain in glucosyltransferases, myotubularins and other putative membrane-associated proteins. Trends Biochem. Sci. 25: 483-485
13. Doi, M., Shigenaga, A., Emi, T., Kinoshita, T. and Shimazaki, K. (2004) A transgene encoding a blue-light receptor, phot1, restores blue-light responses in the Arabidopsis phot1 phot2 double mutant. J. Exp. Bot. 55: 517-523
14. Egloff, M.-P., Johnson, F., Moorhead, G., Cohen, P.T.W., Cohen, P. and Barford, D. (1997) Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J. 16: 1876-1887
15. Emi, T., Kinoshita, T. and Shimazaki, K. (2001) Specific binding of vf14- 3-3a isoform to the plasma membrane H+-ATPase in response to blue light and fusicoccin in guard cells of broad bean. Plant Physiol. 125: 1115-1125
16. Fan, L.M., Zhao, Z.X. and Assmann, S.M. (2004) Guard cells: A dynamic signaling model. Curr. Opin. Plant Biol. 7: 537-546
17. Farkas, I., Dombra'di, V., Miskei, M., Szabados, L. and Koncz, C. (2007) Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci. 12: 169-176
18. Favre, B., Turowski, P. and Hemmings, B.A. (1997) Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin A, okadaic acid, and tautomycin. J. Biol. Chem. 272: 13856-13863
19. Folta, K.M. and Spalding, E.P. (2001) Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J. 26: 471-478
20. Hayashi, M., Inoue, S., Takahashi, K. and Kinoshita, T. (2011) Immunohistochemical detection of blue light-induced phosphorylation of the plasma membrane H+-ATPase in stomatal guard cells. Plant Cell Physiol. 52: 1238-1248
21. Hayashi, Y., Nakamura, S., Takemiya, A., Takahashi, Y., Shimazaki, K. and Kinoshita, T. (2010) Biochemical characterization of in vitro phosphorylation and dephosphorylation of the plasma membrane H+-ATPase. Plant Cell Physiol. 51: 1186-1196
22. Huala, E., Oeller, P.W., Liscum, E., Han, I.S., Larsen, E. and Briggs, W.R. (1997) Arabidopsis NPH1: A protein kinase with a putative redox-sensing domain. Science 278: 2120-2123
23. Inada, S., Ohgishi, M., Mayama, T., Okada, K. and Sakai, T. (2004) RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16: 887-896
24. Inoue, S., Kinoshita, T., Matsumoto, M., Nakayama, K.I., Doi, M. and Shimazaki, K. (2008) Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc. Natl Acad. Sci. USA 105: 5626-5631
25. Inoue, S., Takemiya, A. and Shimazaki, K. (2010) Phototropin signaling and stomatal opening as a model case. Curr. Opin. Plant Biol. 13: 587-593
26. Jacob, T., Ritchie, S., Assmann, S.M. and Gilroy, S. (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc. Natl Acad. Sci. USA 96: 12192-12197
27. Jeon, B.W., Hwang, J.U., Hwang, Y., Song, W.Y., Fu, Y., Gu, Y. et al. (2008) The Arabidopsis small G protein ROP2 is activated by light in guard cells and inhibits light-induced stomatal opening. Plant Cell 20: 75-87
28. Jiang, S.Y., Ramamoorthy, R. and Ramachandran, S. (2008) Comparative transcriptional profiling and evolutionary analysis of the GRAM domain family in eukaryotes. Dev. Biol. 314: 418-432
29. Jones, J.A., Rawles, R. and Hannun, Y.A. (2005) Identification of a novel phosphatidic acid binding domain in protein phosphatase-1. Biochemistry 44: 13235-13245
30. Kagawa, T., Sakai, T., Suetsugu, N., Oikawa, K., Ishiguro, S., Kato, T. et al. (2001) Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141
31. Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M. and Shimazaki, K. (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414: 656-660
32. Kinoshita, T. and Shimazaki, K. (1999) Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J. 18: 5548-5558
33. Kinoshita, T. and Shimazaki, K. (2001) Analysis of the phosphorylation level in guard-cell plasma membrane H+-ATPase in response to fusicoccin. Plant Cell Physiol. 42: 424-432
34. Li, Y., Rosso, M.G., Viehoever, P. and Weisshaar, B. (2007) GABI-Kat SimpleSearch: An Arabidopsis thaliana T-DNA mutant database with detailed information for confirmed insertions. Nucleic Acids Res. 35: D874-D878
35. Lin, Q., Li, J., Smith, R.D. and Walker, J.C. (1998) Molecular cloning and chromosomal mapping of type one serine/threonine protein phosphatases in Arabidopsis thaliana. Mol. Plant Biol. 37: 471-481
36. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M. and Kobayashi, H. (1999) Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J. 18: 455-463
37. Roelfsema, M.R.G and Hedrich, R. (2005) In the light of stomatal opening: New insights into 'the Watergate'. New Phytol. 167: 665-691
38. Sakai, T., Wada, T., Ishiguro, S. and Okada, K. (2000) RPT2: A signal transducer of the phototropic response in Arabidopsis. Plant Cell 12: 225-236
39. Salomon, M., Knieb, E., von Zeppelin, T. and Rüdiger, W. (2003) Mapping of low- and high-fluence autophosphorylation sites in phototropin 1. Biochemistry 42: 4217-4225
40. Schroeder, J.I., Raschke, K. and Neher, E. (1987) Voltage dependence of K+ channels in guard cell protoplasts. Proc. Natl Acad. Sci. USA 84: 4108-4112
41. Schroeder, J.I., Allen, G.J., Hugouvieux, V., Kwak, J.M. and Waner, D. (2001) Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 627-658
42. Sessions, A., Burke, E., Presting, G., Aux, G., McElver, J., Patton, D. et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994
43. Shenolikar, S. and Nairn, A.C. (1991) Protein phosphatases: Recent progress. Adv. Second Messenger Phosphoprotein Res. 23: 1-121
44. Shimazaki, K., Doi, M., Assmann, S.M. and Kinoshita, T. (2007) Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58: 219-247
45. Shimazaki, K., Iino, M. and Zeiger, E. (1986) Blue light-dependent proton extrusion by guard-cell protoplasts of Vicia faba. Nature 319: 324-326
46. Takemiya, A., Ariyoshi, C. and Shimazaki, K. (2009) Identification and functional characterization of inhibitor-3, a regulatory subunit of protein phosphatase 1 in plants. Plant Physiol. 150: 144-156
47. Takemiya, A., Inoue, S., Doi, M., Kinoshita, T. and Shimazaki, K. (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17: 1120-1127
48. Takemiya, A., Kinoshita, T., Asanuma, M. and Shimazaki, K. (2006) Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba. Proc. Natl Acad. Sci. USA 103: 13549-13554
49. Takemiya, A. and Shimazaki, K. (2010) Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase 1. Plant Physiol. 153: 1555-1562
50. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599
51. Templeton, G.W., Nimick, M., Morrice, N., Campbell, D., Goudreault, M., Gingras, A.-C. et al. (2011) Identification and characterization of AtI-2, an Arabidopsis homologue of an ancient protein phosphatase 1 (PP1) regulatory subunit. Biochem. J. 435: 73-83
52. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680
53. Tokutomi, S., Matsuoka, D. and Zikihara, K. (2008) Molecular structure and regulation of phototropin kinase by blue light. Biochim. Biophys. Acta 1784: 133-142
54. Tseng, T.-S. and Briggs, W.R. (2010) The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell 22: 392-402
55. Ueno, K., Kinoshita, T., Inoue, S., Emi, T. and Shimazaki, K. (2005) Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant Cell Physiol. 46: 955-963
56. Vavasseur, A. and Raghavendra, A.S. (2005) Guard cell metabolism and CO2 sensing. New Phytol. 165: 665-682
57. Wang, Q.M., Guan, K.L., Roach, P.J. and DePaoli-Roach, A.A. (1995) Phosphorylation and activation of the ATP-Mg-dependent protein phosphatase by the mitogen-activated protein kinase. J. Biol. Chem. 270: 18352-18358
58. Zhang, W., Qin, C., Zhao, J. and Wang, X. (2004) Phospholipase Da1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc. Natl Acad. Sci. USA 101: 9508-9513
59. Zhang, X., Wang, H., Takemiya, A., Song, C.P., Kinoshita, T. and Shimazaki, K. (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol. 136: 4150-4158
60. Zhao, S. and Lee, E.Y.C. (1997) A protein phosphatase-1-binding motif identified by the panning of a random peptide display library. J. Biol. Chem. 272: 28368-28372