Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in Vicia guard cells

Plant and Cell Physiology

Volumn 48, Issue 5, 2007, Pages 715-723

  Zhang, Xiao ^a,b   Takemiya, Atsushi ^a   Kinoshita, Toshinori ^a   Shimazaki, Ken Ichiro ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b HENAN UNIVERSITY   (China)

Author keywords

Abscisic acid; Blue light; H+ pumping; Nitric oxide; Stomatal opening

Indexed keywords

2 PHENYL 4,4,5,5 TETRAMETHYLIMIDAZOLINE 1 OXYL 3 OXIDE; 2-PHENYL-4,4,5,5-TETRAMETHYLIMIDAZOLINE-1-OXYL-3-OXIDE; ABSCISIC ACID; AMINE OXIDE; HYDROGEN PEROXIDE; IMIDAZOLE DERIVATIVE; NITRIC OXIDE; NITRIC OXIDE DONOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SCAVENGER; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BEAN; CYTOLOGY; DRUG EFFECT; LIGHT; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLANT EPIDERMIS; RADIATION EXPOSURE; SIGNAL TRANSDUCTION;

ABSCISIC ACID; CYCLIC N-OXIDES; FREE RADICAL SCAVENGERS; HYDROGEN PEROXIDE; IMIDAZOLES; LIGHT; NITRIC OXIDE; NITRIC OXIDE DONORS; PHOSPHORYLATION; PLANT EPIDERMIS; PLANT PROTEINS; PROTON-TRANSLOCATING ATPASES; SIGNAL TRANSDUCTION; VICIA;

VICIA;

EID: 34548401341     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcm039     Document Type: Article

References (54)

1. Assmann, S.M. and Shimazaki, K. (1999) The multisensory guard cell, stomatal responses to blue light and abscisic acid. Plant Physiol. 119: 809-815.
2. 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.
3. 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.
4. Briggs, W.R., Beck, C.F., Cashmore, A.R., Christie, J.M., Hughes, J., et al. (2001) The phototropin family of photoreceptors. Plant Cel 13: 993-997.
5. Briggs, W.R. and Christie, J.M. (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7: 204-210.
6. 2 synthesis. Plant J. 45: 113-122.
7. Christie, J.M., Reymond, P., Powell, G.K., Bernasconi, P., Raibekas, A.A., Liscum, E. and Briggs, W.R. (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282: 1698-1701.
8. Delledonne, M., Xia, Y., Dixon, R.A. and Lamb, C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585-588.
9. Desikan, R., Griffiths, R., Hancock, J.T. and Neill, S.J. (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99: 16314-16318.
10. Folta, K.M., Lieg, E.J., Durham, T. and Spalding, E.P. (2003) Primary inhibition of hypocotyl growth and phototropism depend differently on phototropin-mediated increases in cytoplasmic calcium induced by blue light. Plant Physiol. 133: 1464-1470.
11. Furchgott, R.F. (1995) Special topic: nitric oxide. Annu. Rev. Physiol. 57: 695-682.
12. - channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl Acad. Sci. USA 100: 11116-11121.
13. Garcia-Mata, C. and Lamattina, L. (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126: 1196-1204.
14. Garcia-Mata, C. and Lamattina, L. (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128: 790-792.
15. Garcia-Mata, C. and Lamattina, L. (2003) Abscisic acid, nitric oxide and stomatal closure. Is nitrate reductase one of the missing links? Trends Plant Sci. 8: 20-26.
16. + pumping by abscisic acid in Vicia guard-cell protoplasts. Plant Physiol. 111: 433-440.
17. Gould, K.S., Lamotte, O., Klinguer, A., Pugin, A. and Wendehenne, D. (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26: 1851-1862.
18. 2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc. Natl Acad. Sci. USA 97: 4967-4972.
19. 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.
20. 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 phototropin1 in Arabidopsis thaliana. Plant Cell 16: 887-896.
21. Inoue, S., Kinoshita, T. and Shimazaki, K. (2005) Possible involvement of phototropins in leaf movement of kidney bean in response to blue light. Plant Physiol. 138: 1994-2004.
22. Kagawa, T., Sakai, T., Suetsugu, N., Oikawa, K., Ishiguro, S., Kato, T., Tabata, S., Okada, K. and Wada, M. (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141.
23. 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.
24. Kinoshita, T., Emi, T., Tominaga, M., Sakamoto, K., Shigenaga, A., Doi, M. and Shimazaki, K. (2003) Blue-light- and phosphorylationdependent binding of a 14-3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiol. 133: 1453-1463.
25. +-ATPase in guard cells of fava bean. Plant Cell 7: 1333-1342.
26. Kinoshita, T. and Shimazaki, K. (1997) Involvement of calyculin A- and okadaic acid-sensitive protein phosphatase in the blue light response of stomatal guard cells. Plant Cell Physiol. 38: 1281-1285.
27. +-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J. 18: 5548-5558.
28. +-ATPase in response to fusicoccin. Plant Cell Physiol. 42: 424-432.
29. +-ATPase by blue light. Plant Cell Physiol. 43: 1359-1365.
30. 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. and Schroeder, J.I. (2003) NADPH oxidase AtbohD and AtbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22: 2623-2633.
31. +-ATPase from beet root is inhibited by a calcium-dependent phosphorylation. Planta 204: 352-359.
32. 2 in ABA-induced stomatal closure in Vicia faba L. J. Plant Physiol. Mol. Biol. 31: 62-70.
33. 2+- permeable channels and stomatal closure. PLoS Biol. 4: 1749-1762.
34. Neill, S.J., Desikan, R., Clarke, A. and Hancock, J.T. (2002a) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cell. Plant Physiol. 128: 13-16.
35. Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D. and Hancock, J.T. (2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53: 1237-1247.
36. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E. and Schroeder, J.L. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406: 731-734.
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. Roelfsema, M.R.G., Steinmeyer, R., Staal, M. and Hedrich, R. (2001) Single guard cell recordings in intact plants: light-induced hyperpolarization of the plasma membrane. Plant J. 26: 1-13.
39. Sakai, T., Kagawa, T., Kasahara, M., Swartz, T.E., Christie, J.M., Briggs, W.R., Wada, M. and Okada, K. (2001) Arabidospsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl Acad. Sci. USA 98: 6969-6974.
40. Sakamoto, K. and Briggs, W.R. (2002) Cellular and subcellular location of phototropin1. Plant Cell 14: 1723-1735.
41. Salomon, M., Christie, J.M., Knieb, E., Lempert, U. and Briggs, W.R. (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39: 9401-9410.
42. 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.
43. Shimazaki, K., Doi, M., Assmann, S.M. and Kinoshita, T. (2007) Light regulation of stomatal movement. Ann. Rev. Plant Biol. 58: 219-247.
44. 2+ in blue light-dependent proton pumping in guard cell protoplasts from Vicia faba. Physiol. Plant 105: 554-561.
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. + pumping by guard cell protoplasts from Vicia faba L. Plant Physiol. 99: 1416-1421.
47. + channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol. 136: 4275-4284.
48. 2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J. 43: 520-529.
49. +-ATPase creates a binding site for the regulatory 14-3-3 protein. Plant Cell 11: 2379-2391.
50. Takemiya, A., Kinoshita, T., Asanuma, M. and Shimazaki, K. (2006) Protein phosphatase 1 positively regulates stomatal opening to blue light in Vicia faba. Proc. Natl Acad. Sci. USA 103: 13549-13554.
51. Taylor, A.R. and Assmann, S.M. (2001) Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells. Plant Physiol. 125: 329-338.
52. 2 sensing. New Phytol. 165: 665-682.
53. +-ATPase in guard cell protoplasts. Plant Physiol. 136: 4150-4158.
54. Zhang, X., Zhang, L., Dong, F.C., Gao, J.F., Galbraith, D.W. and Song, C.P. (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126: 1438-1448.