The ascorbic acid redox state controls guard cell signaling and stomatal movement

Plant Cell

Volumn 16, Issue 5, 2004, Pages 1143-1162

  Chen, Zhong ^a   Gallie, Daniel R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACIDS; CATALYSIS; CELLS; ENZYME KINETICS; HYDROGEN PEROXIDE; REDOX REACTIONS; REDUCTION;

GUARD CELLS; REDOX STATE;

PLANTS (BOTANY);

NICOTIANA TABACUM; TRITICUM AESTIVUM;

EID: 2442495232     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.021584     Document Type: Article

References (57)

1. Aebi, H. (1984). Catalase in vitro. Methods Enzymol. 105, 121-126.
2. Asada, K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639.
3. Assmann, S.M. (1993). Signal transduction in guard cells. Annu. Rev. Cell Biol. 9, 345-375.
4. Assmann, S.M., and Wang, X.Q. (2001). From milliseconds to millions of years: Guard cells and environmental responses. Curr. Opin. Plant Biol. 4, 421-428.
5. Blatt, M.R. (2000). Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16, 221-241.
6. + channels of stomatal guard cells: Abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191, 330-341.
7. Bowler, C., Vanmontagu, M., and Inze, D. (1992). Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 83-116.
8. Bredford, 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.
9. Chen, Z., Young, T.E., Ling, J., Chang, S.-C., and Gallie, D.R. (2003). Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc. Natl. Acad. Sci. USA 100, 3525-3530.
10. Creissen, G., Firmin, J., Fryer, M., Kular, B., Leyland, N., Reynolds, H., Pastori, G., Wellburn, F., Baker, N., Wellburn, A., and Mullineaux, P. (1999). Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11, 1277-1292.
11. de Pinto, M.C., Tommasi, F., and De Gara, L. (2000). Enzymes of the ascorbate biosynthesis and ascorbate-glutathione cycle in cultured cells of tobacco Bright Yellow 2. Plant Physiol. Biochem. 38, 541-550.
12. Erdei, L., Szegeletes, Z.S., Barabas, K.N., Pestanacz, A., Fulop, K., Kalmar, L., Kovacs, A., Toth, B., and Der, A. (1998). Environmental stress and the biological clock in plants: Changes of rhythmic behaviour of carbohydrates, antioxidant enzymes and stomatal resistance by salinity. J. Plant Physiol. 152, 265-271.
13. Eskling, M., Arvidsson, P., and Akerlund, H.E. (1997). The xanthophyll cycle, its regulation and components. Physiol. Plant 100, 806-816.
14. Esterbauer, H., Grill, D., and Welt, R. (1990). Der jahreszeitliche Rhytmus des Acorbinsauresystems in Nadeln von Picea abies. Z. Pflanzenphysiol. 98, 393-402.
15. Foyer, C.H., Rowell, J., and Walker, D. (1983). Measurements of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157, 239-244.
16. Foyer, C.H., Souriau, N., Perret, S., Lelandais, M., Kunert, K.J., Pruvost, C., and Jouanin, L. (1995). Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol. 109, 1047-1057.
17. Gainnopolitis, C.N., and Pies, S.K. (1977). Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol. 59, 309-314.
18. Gómez-Cadenas, A., Tadeo, F.R., Talon, M., and Eduardo Primo-Millo, E. (1996). Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol. 112, 401-408.
19. Grabov, A., and Blatt, M.R. (1998). Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc. Natl. Acad. Sci. USA 95, 4778-4783.
20. 2 is the likely intermediary signaling molecule for the response. Plant J. 22, 87-95.
21. Hamilton, D.W., Hills, A., Kohler, B., and Blatt, M.R. (2000). Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc. Natl. Acad. Sci. USA 97, 4967-4972.
22. Havaux, M., Bonfils, J.P., Lutz, C., and Niyogi, K.K. (2000). Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol. 124, 273-284.
23. Horemans, N., Foyer, C.H., and Asard, H. (2000). Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci. 5, 263-267.
24. Hossain, M.A., and Asada, K. (1984). Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant Cell Physiol. 25, 85-92.
25. Ishikawa, H., Aizawa, H., Kishira, H., Ogawa, T., and Sakata, M. (1983). Light-induced changes of membrane potential in guard cells of Vicia faba. Plant Cell Physiol. 24, 769-772.
26. Kohler, B., and Blatt, M.R. (2002). Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant J. 32, 185-194.
27. Kohler, B., Hills, A., and Blatt, M.R. (2003). Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol. 131, 385-388.
28. Kruse, T., Tallman, G., and Zeiger, E. (1989). Isolation of guard cell protoplasts from mechanically prepared epidermis of vicia faba leaves. Plant Physiol. 90, 1382-1386.
29. Lee, S., Choi, H., Suh, S., Doo, I.S., Oh, K.Y., Choi, E.J., Schroeder Taylor, A.T., Low, P.S., and Lee, Y. (1999). Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 121, 147-152.
30. Leung, J., and Giraudat, J. (1998). Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 199-222.
31. MacRobbie, E.A. (2000). ABA activates multiple Ca(2+) fluxes in stomatal guard cells, triggering vacuolar K(+)(Rb(+)) release. Proc. Natl. Acad. Sci. USA 97, 12361-12368.
32. McAinsh, M.R., Clayton, H., Mansfield, T.A., and Hetherington, A.M. (1996). Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol. 111, 1031-1042.
33. Munne-Bosch, S., and Alegre, L. (2002). Plant aging increases oxidative stress in chloroplasts. Planta 214, 608-615.
34. Murata, Y., Pei, Z.M., Mori, I.C., and Schroeder, J. (2001). Abscisic acid activation of plasma membrane Ca(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.
35. Pastori, G.M., and Foyer, C.H. (2002). Common components, networks, and pathways of cross-tolerance to stress. The central role of "redox" and abscisic acid-mediated controls. Plant Physiol. 129, 460-468.
36. Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M., and Schroeder, J.I. (1997). Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9, 409-423.
37. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and Schroeder, J.I. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406, 731-734.
38. Pignocchi, C., Fletcher, J.M., Wilkinson, J.E., Barnes, J.D., and Foyer, C.H. (2003). Function of ascorbate oxidase in tobacco. Plant Physiol. 132, 1631-1641.
39. Polidoros, A.N., and Scandalios, J.G. (1998). Circadian expression of the maize Cat3 catalase gene is highly conserved among diverse maize genotypes with structurally different promoters. Genetics 149, 405-415.
40. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J., and Knight, M.R. (1994). Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6, 1301-1310.
41. Redinbaugh, M.G., Sabre, M., and Scandalios, J.G. (1990). Expression of the maize Cat3 catalase gene is under the influence of a circadian rhythm. Proc. Natl. Acad. Sci. USA 87, 6853-6857.
42. Scandalios, J.G. (1993). Oxygen stress and superoxide dismutases. Plant Physiol. 101, 7-12.
43. Schroeder, J.I., Allen, G.J., Hugouvieux, V., Kwak, J.M., and Waner, D. (2001a). Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-658.
44. Schroeder, J.I., Kwak, J.M., and Allen, G.J. (2001b). Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410, 327-330.
45. Schupp, R., and Rennenberg, H. (1988). Diurnal changes in the glutathione content of spruce needles (Picea abies L). Plant Sci. 57, 113-117.
46. Shimaoka, T., Yokota, A., and Miyake, C. (2000). Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant Cell Physiol. 41, 1110-1118.
47. Smirnoff, N. (2000). Ascorbic acid: Metabolism and functions of a multifaceted molecule. Curr. Opin. Plant Biol. 3, 229-235.
48. Smirnoff, N., and Pallanca, J.E. (1996). Ascorbate metabolism in relation to oxidative stress. Biochem. Soc. Trans. 24, 472-478.
49. Sutherland, M.W., and Learmonth, B.A. (1997). The tetrazolium dyes MTS and XTT provide new quantitative assay for superoxide and superoxide dismutase. Free Radic. Res. 27, 283-289.
50. Tamaoki, M., Mukai, F., Asai, N., Nakajima, N., Kubo, A., Aono, M., and Saji, H. (2003). Light-controlled expression of a gene encoding L-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis. Plant Sci. 164, 1111-1117.
51. Thiel, G., MacRobbie, E.A., and Blatt, M.R. (1992). Membrane transport in stomatal guard cells: The importance of voltage control. J. Membr. Biol. 126, 1-18.
52. Veljovic-Jovanovic, S.D., Pignocchi, C., Noctor, G., and Foyer, C.H. (2001). Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 127, 426-435.
53. Wildi, B., and Lutz, C. (1996). Antioxidant composition of selected high alpine plant species from different altitudes. Plant Cell Environ. 19, 138-146.
54. Zeiger, E. (2000). Sensory transduction of blue light in guard cells. Trends Plant Sci. 5, 183-185.
55. Zhang, X., Zhang, L., Dong, F., Gao, J., 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.
56. Zhong, H.H., and McClung, C.R. (1996). The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol. Gen. Genet. 251, 196-203.
57. Zhong, H.H., Painter, J.E., Salome, P.A., Straume, M., and McClung, C.R. (1998). Imbibition, but not release from stratification, sets the circadian clock in Arabidopsis seedlings. Plant Cell 10, 2005-2018.