Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1

Plant Journal

Volumn 62, Issue 3, 2010, Pages 442-453

  Vahisalu, Triin ^a,b   Puzõrjova, Irina ^b   Brosché, Mikael ^a   Valk, Ervin ^b   Lepiku, Martin ^b   Moldau, Heino ^b   Pechter, Priit ^b   Wang, Yuh Shuh ^b   Lindgren, Ove ^b   Salojärvi, Jarkko ^a   Loog, Mart ^b   Kangasjärvi, Jaakko ^a   Kollist, Hannes ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

OST1; Ozone; Reactive oxygen species; Signaling; SLAC1; Stomata

Indexed keywords

AIR POLLUTANTS; ANION CHANNELS; ARABIDOPSIS; DOMINANT-NEGATIVE MUTANTS; GUARD CELLS; ION CHANNEL; PHOSPHORYLATION SITES; PHYSICAL INTERACTIONS; PROTEIN KINASE; PROTEIN PHOSPHATASE; RAPID TRANSIENTS; REACTIVE OXYGEN SPECIES; SERINE RESIDUES; SIGNALING COMPONENTS; SITE DIRECTED MUTAGENESIS; STOMATAL CLOSURES; STOMATAL CONDUCTANCE; STOMATAL RESPONSE;

AMINO ACIDS; CELL MEMBRANES; IONS; ORGANIC ACIDS; OZONE; PHOSPHATASES; PHOSPHORYLATION; PLANTS (BOTANY); PROTEINS; RESONANT TUNNELING; SEMICONDUCTOR DIODES; SIGNALING; TEMPERATURE MEASURING INSTRUMENTS;

AIR POLLUTION;

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; OST1 PROTEIN, ARABIDOPSIS; OZONE; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; SLAC1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLANT STOMA; SITE DIRECTED MUTAGENESIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; OZONE; PHOSPHORYLATION; PLANT STOMATA; PROTEIN KINASES; REACTIVE OXYGEN SPECIES;

ARABIDOPSIS;

EID: 77950961702     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04159.x     Document Type: Article

References (55)

1. Ahlfors, R., Lång, S., Overmyer, K. et al. (2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell, 16, 1925 1937.
2. 2+. Proc. Natl Acad. Sci. USA, 96, 13554 13559.
3. Belin, C., de Franco, P.O., Bourbousse, C., Chaignepain, S., Schmitter, J.M., Vavasseur, A., Giraudat, J., Barbier-Brygoo, H. Thomine, S. (2006) Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 141, 1316 1327.
4. Clayton, H., Knight, M.R., Knight, H., McAinsh, M.R. Hetherington, A.M. (1999) Dissection of the ozone-induced calcium signature. Plant J. 17, 575 579.
5. Desikan, R., Last, K., Harrett-Williams, R., Tagliavia, C., Harter, K., Hooley, R., Hancock, J.T. Neill, S.J. (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J. 47, 907 916.
6. Evans, N.H., McAinsh, M.R., Hetherington, A.M. Knight, M.R. (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J. 41, 615 626.
7. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L. Zhu, J.K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature, doi :.
8. Geiger, D., Scherzer, S., Mumm, P. et al. (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl Acad. Sci. USA, 106, 21425 21430.
9. Grabov, A., Leung, J., Giraudat, J. Blatt, M.R. (1997) Alteration of anion channel kinetics in wild-type and abi1-1 transgenic Nicotiana benthamiana guard cells by abscisic acid. Plant J. 12, 203 213.
10. 2. Nat. Cell Biol. 8, 391 397.
11. 2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO J. 9, 3889 3892.
12. Hopkin, M. (2007) Carbon sinks threatened by increasing ozone. Nature, 448, 396 397.
13. + channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl Acad. Sci. USA, 100, 5549 5554.
14. Johnsson, N. Varshavsky, A. (1994) Split ubiquitin as a sensor of protein interactions in vivo. Proc. Natl Acad. Sci. USA, 91, 10340 10344.
15. Joo, J.H., Wang, S., Chen, J.G., Jones, A.M. Federoff, N.V. (2005) Different signaling and cell death roles of heterotrimeric G protein α and subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell, 17, 957 970.
16. Kangasjärvi, J., Jaspers, P. Kollist, H. (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ. 28, 1021 1036.
17. Keller, U.B., Hedrich, R. Raschke, K. (1989) Voltage dependent anion channels in the plasma membrane of guard cells. Nature, 341, 450 452.
18. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell Proteomics, 5, 749 757.
19. Kolla, V.A., Vavasseur, A. Raghavendra, A.S. (2007) Hydrogen peroxide production is an early event during bicarbonate induced stomatal closure in abaxial epidermis of Arabidopsis. Planta, 225, 1421 1429.
20. Kollist, T., Moldau, H., Rasulov, B., Oja, V., Rämma, H., Hüve, K., Jaspers, P., Kangasjärvi, J. Kollist, H. (2007) A novel device detects a rapid ozone-induced transient stomatal closure in intact Arabidopsis and its absence in abi2 mutant. Physiol. Plant. 129, 796 803.
21. 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. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623 2633.
22. + channels in plants. Plant J. 54, 1076 1082.
23. Lee, S., Choi, H., Suh, S., Doo, I.-S., Oh, K.-Y., Choi, E.J., Schroeder Taylor, A.T., Low, P.S. Lee, Y. (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reaction oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 121, 147 152.
24. Lee, S.C., Lan, W., Buchanan, B.B. Luan, S. (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl Acad. Sci. USA, 106, 21419 21424.
25. Li, S., Assmann, S.M. Albert, R. (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic signaling. PLoS Biol. 4, 1732 1748.
26. MacRobbie, E.A.C. (1998) Signal transduction and ion channels in guard cells. Philos. Trans. R. Soc. Lond. B, 353, 1475 1488.
27. Mori, I.C., Pinontoan, R., Kawano, T. Muto, S. (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol. 42, 1383 1388.
28. 2+-permeable channels and stomatal closure. PLoS Biol. 4, 1749 1762.
29. Munemasa, S., Oda, K., Watanabe-Sugimoto, M., Nakamura, Y., Shimoishi, Y. Murata, Y. (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol. 143, 1398 1407.
30. 2- channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell, 13, 2513 2523.
31. Mustilli, A.-C., 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.
32. 2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature, 452, 483 486.
33. Pandey, S., Zhang, W. Assmann, S.M. (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett. 581, 2325 2336.
34. 2+ in Arabidopsis thaliana guard cells. Proc. Natl Acad. Sci. USA, 95, 6548 6553.
35. Pei, Z.-M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E. Schroeder, J.I. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731 734.
36. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J. Knight, M.R. (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell, 6, 1301 1310.
37. 2. Planta, 217, 639 650.
38. Rentel, M.C., Lecourieux, D., Ouaked, F. et al. (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature, 427, 858 861.
39. Roelfsema, M.R.G. Prins, H.B.A. (1997) Ion channels in guard cells of Arabidopsis thaliana (L.) Heynh. Planta, 202, 18 27.
40. Sato, A., Sato, Y., Fukao, Y. et al. (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem. J. doi :.
41. Schmidt, C., Schelle, I., Liao, Y.J. Schroeder, J.I. (1995) Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. Proc. Natl Acad. Sci. USA, 92, 9535 9539.
42. Schroeder, J.I. Hagiwara, S. (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature, 338, 427 430.
43. Sirichandra, C., Gu, D., Hu, H.C. et al. (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase". FEBS Lett. 583, 2982 2986.
44. Sitch, S., Cox, P.M., Collins, W.J. Huntingford, C. (2007) Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature, 448, 791 794.
45. 2+ channel activities in Arabidopsis guard cells. J. Biol. Chem. 282, 1916 1924.
46. Till, B.J., Reynolds, S.H., Greene, A., Codomo, C.A., Enns, L.C., Johnson, J.E., Burtner, C., Odden, A.R., Young, K. Taylor, N.E. (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res. 13, 524 530.
47. phox). Plant J. 14, 365 370.
48. Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., Ishihama, Y., Hirayama, T. Shinozaki, K. (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 17588 17593.
49. Vahisalu, T., Kollist, H., Wang, Y.F. et al. (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature, 452, 487 491.
50. Vlad, F., Rubio, S., Rodrigues, A., Sirichandra, C., Belin, C., Robert, N., Leung, J., Rodriguez, P.L., Laurière, C. Merlot, S. (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell, doi :.
51. Voinnet, O., Rivas, S., Mestre, P. Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949 956. (Pubitemid 36339384)
52. Wang, X.Q., Ullah, H., Jones, A.M. Assmann, S.M. (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science, 292, 2070 2072. (Pubitemid 32691571)
53. Ward, J.M., Mäser, P. Schroeder, J.I. (2008) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71, 59 82.
54. Wrzaczek, M., Brosché, M., Kollist, H. Kangasjärvi, J. (2009) Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS. Proc. Natl Acad. Sci. USA, 106, 5412 5417.
55. Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Alonso, J., Ecker, J.R. Shinozaki, K. (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43, 1473 1483. (Pubitemid 36100984)