A brand new START: Abscisic acid perception and transduction in the guard cell

Science Signaling

Volumn 4, Issue 201, 2011, Pages

  Joshi Saha, Archana ^a   Valon, Christiane ^a   Leung, Jeffrey ^a  

^a INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ABSCISIC ACID RECEPTOR; AMINO ACID; CARRIER PROTEIN; CELL PROTEIN; CPK21 KINASE; CPK23 KINASE; HYDROGEN PEROXIDE; NADPH OXIDASE RESPIRATORY BURST OXIDASE PROTEIN F; OPEN STOMATA 1; OXIDOREDUCTASE; PHOSPHOPROTEIN PHOSPHATASE 2; PHOSPHOPROTEIN PHOSPHATASE 2C; PHOSPHOTRANSFERASE; POTASSIUM ION; RECEPTOR; SNF1 RELATED KINASE; STEROIDOGENIC ACUTE REGULATORY RELATED LIPID TRANSFER PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CARBON DIOXIDE; INWARDLY RECTIFYING POTASSIUM CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; PROTEIN SERINE THREONINE KINASE; PYL2 PROTEIN, ARABIDOPSIS; SNRK2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CELL MEMBRANE; GUARD CELL; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON DIOXIDE; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; PHOSPHORYLATION; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 82555198807     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002164     Document Type: Review

References (128)

1. A. M. Hetherington, F. I. Woodward, The role of stomata in sensing and driving environmental change. Nature 424, 901-908 (2003).
2. A. Lebaudy, A. Vavasseur, E. Hosy, I. Dreyer, N. Leonhardt, J.-B. Thibaud, A.-A. Véry, T. Simonneau, H. Sentenac, Plant adaptation to fl uctuating environment and biomass production are strongly dependent on guard cell potassium channels. Proc. Natl. Acad. Sci. U.S.A. 105, 5271-5276 (2008).
3. 2+ signaling. Annu. Rev. Plant Biol. 61, 561-591 (2010).
4. T. Vahisalu, I. Puzõrjova, M. Brosché, E. Valk, M. Lepiku, H. Moldau, P. Pechter, Y.-S. Wang, O. Lindgren, J. Salojärvi, M. Loog, J. Kangasjärvi, H. Kollist, Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J. 62, 442-453 (2010).
5. D. Cho, D. Shin, B. W. Jeon, J. M. Kwak, ROS-mediated ABA signaling. J. Plant Biol. 52, 102-113 (2009).
6. M. R. Blatt, Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16, 221-241 (2000).
7. J. I. Schroeder, G. J. Allen, V. Hugouvieux, J. M. Kwak, D. Waner, Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-658 (2001).
8. M. R. G. Roelfsema, R. Hedrich, In the light of stomatal opening: New insights into 'the Watergate'. New Phytol. 167, 665-691 (2005).
9. S. Pandey, W. Zhang, S. M. Assmann, Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett. 581, 2325-2336 (2007).
10. C. Sirichandra, A. Wasilewska, F. Vlad, C. Valon, J. Leung, The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J. Exp. Bot. 60, 1439-1463 (2009).
11. +-ATPase in guard cells of fava bean. Plant Cell 7, 1333-1342 (1995).
12. J. I. Schroeder, B. U. Keller, Two types of anion channel currents in guard cells with distinct voltage regulation. Proc. Natl. Acad. Sci. U.S.A. 89, 5025-5029 (1992).
13. M. R. Roelfsema, V. Levchenko, R. Hedrich, ABA depolarizes guard cells in intact plants, through a transient activation of R- and S-type anion channels. Plant J. 37, 578-588 (2004).
14. C. Schmidt, J. I. Schroeder, Anion selectivity of slow anion channels in the plasma membrane of guard cells (large nitrate permeability). Plant Physiol. 106, 383-391 (1994).
15. B. U. Keller, R. Hedrich, K. Raschke, Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341, 450-453 (1989).
16. E. A. C. MacRobbie, ABA-induced ion effl ux in stomatal guard cells: Multiple actions of ABA inside and outside the cell. Plant J. 7, 565-576 (1995).
17. + channels and stomatal response by abscisic acid: An intracellular locus of phytohormone action. Proc. Natl. Acad. Sci. U.S.A. 91, 4019-4023 (1994).
18. W. Hartung, The site of action of abscisic acid at the guard cell plasmalemma of Valerianella locusta. Plant Cell Environ. 6, 427-428 (1983).
19. B. E. Anderson, J. M. Ward, J. I. Schroeder, Evidence for an extracellular reception site for abscisic acid in Commelina guard cells. Plant Physiol. 104, 1177-1183 (1994).
20. S. Gilroy, R. L. Jones, Perception of gibberellin and abscisic acid at the external face of the plasma membrane of barley (Hordeum vulgare L.) aleurone protoplasts. Plant Physiol. 104, 1185-1192 (1994).
21. + outward rectifying channels depend on an extracellular perception of ABA in Arabidopsis thaliana suspension cells. Plant J. 18, 13-22 (1999).
22. T. F. Schultz, R. S. Quatrano, Evidence for surface perception of abscisic acid by rice suspension cells as assayed by Em gene expression. Plant Sci. 130, 63-71 (1997).
23. D. Yamazaki, S. Yoshida, T. Asami, K. Kuchitsu, Visualization of abscisic acid-perception sites on the plasma membrane of stomatal guard cells. Plant J. 35, 129-139 (2003).
24. M. Schwarz, J. I. Schroeder, Abscisic acid maintains S-type anion channel activity in ATP-depleted Vicia faba guard cells. FEBS Lett. 428, 177-182 (1998).
25. A. B. Ogunkanmi, D. J. Tucker, T. A. Mansfi eld, An improved bioassay for abscisic acid and other antitranspirants. New Phytol. 72, 277-282 (1973).
26. N. W. Paterson, J. D. B. Weyers, R. A. Brook, The effect of pH on stomatal sensitivity to abscisic acid. Plant Cell Environ. 11, 83-89 (1988).
27. A. C. Allan, M. D. Fricker, J. L. Ward, M. H. Beale, A. J. Trewavas, Two transduction pathways mediate rapid effects of abscisic acid in Commelina guard cells. Plant Cell 6, 1319-1328 (1994).
28. C. Hornberg, E. W. Weiler, High-affi nity binding sites for abscisic acid on the plasmalemma of Vicia faba guard cells. Nature 310, 321-324 (1984).
29. P. McCourt, R. Creelman, The ABA receptors -We report you decide. Curr. Opin. Plant Biol. 11, 474-478 (2008).
30. L. B. Sheard, N. Zheng, Plant biology: Signal advance for abscisic acid. Nature 462, 575-576 (2009).
31. The News Staff, Breakthrough of the year: The runners-up. Science 326, 1600-1607 (2009).
32. S.-Y. Park, P. Fung, N. Nishimura, D. R. Jensen, H. Fujii, Y. Zhao, S. Lumba, J. Santiago, A. Rodrigues, T.-F. Chow, S. E. Alfred, D. Bonetta, R. Finkelstein, N. J. Provart, D. Desveaux, P. L. Rodriguez, P. McCourt, J.-K. Zhu, J. I. Schroeder, B. F. Volkman, S. R. Cutler, Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071 (2009).
33. C. Radauer, P. Lackner, H. Breiteneder, The Bet v 1 fold: An ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol. Biol. 8, 286 (2008).
34. J. Leung, M. Bouvier-Durand, P.-C. Morris, D. Guerrier, F. Chefdor, J. Giraudat, Arabidopsis ABA response gene ABI1: Features of a calcium-modulated protein phosphatase. Science 264, 1448-1452 (1994).
35. K. Meyer, M. P. Leube, E. Grill, A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452-1455 (1994).
36. J. Leung, S. Merlot, J. Giraudat, The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9, 759-771 (1997).
37. P. L. Rodriguez, G. Benning, E. Grill, ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett. 421, 185-190 (1998).
38. A. Saez, N. Apostolova, M. Gonzalez-Guzman, M. P. Gonzalez-Garcia, C. Nicolas, O. Lorenzo, P. L. Rodriguez, Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 37, 354-369 (2004).
39. J. Santiago, A. Rodrigues, A. Saez, S. Rubio, R. Antoni, F. Dupeux, S.-Y. Park, J. A. Márquez, S. R. Cutler, P. L. Rodriguez, Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60, 575-588 (2009).
40. N. Leonhardt, J. M. Kwak, N. Robert, D. Waner, G. Leonhardt, J. I. Schroeder, Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16, 596-615 (2004).
41. Y. Ma, I. Szostkiewicz, A. Korte, D. Moes, Y. Yang, A. Christmann, E. Grill, Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068 (2009).
42. S. R. Cutler, P. L. Rodriguez, R. R. Finkelstein, S. R. Abrams, Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679 (2010).
43. K. E. Hubbard, N. Nishimura, K. Hitomi, E. D. Getzoff, J. I. Schroeder, Early abscisic acid signal transduction mechanisms: Newly discovered components and newly emerging questions. Genes Dev. 24, 1695-1708 (2010).
44. K. Melcher, L.-M. Ng, X. E. Zhou, F.-F. Soon, Y. Xu, K. M. Suino-Powell, S.-Y. Park, J. J. Weiner, H. Fujii, V. Chinnusamy, A. Kovach, J. Li, Y. Wang, J. Li, F. C. Peterson, D. R. Jensen, E.-L. Yong, B. F. Volkman, S. R. Cutler, J.-K. Zhu, H. E. Xu, A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462, 602-608 (2009).
45. K. Melcher, Y. Xu, L.-M. Ng, X. E. Zhou, F.-F. Soon, V. Chinnusamy, K. M. Suino-Powell, A. Kovach, F. S. Tham, S. R. Cutler, J. Li, E.-L. Yong, J.- K. Zhu, H. E. Xu, Identifi cation and mechanism of ABA receptor antagonism. Nat. Struct. Mol. Biol. 17, 1102-1108 (2010).
46. K. Melcher, X.-E. Zhou, H. E. Xu, Thirsty plants and beyond: Structural mechanisms of abscisic acid perception and signaling. Curr. Opin. Struct. Biol. 20, 722-729 (2010).
47. A. S. Raghavendra, V. K. Gonugunta, A. Christmann, E. Grill, ABA perception and signalling. Trends Plant Sci. 15, 395-401 (2010).
48. T. Umezawa, K. Nakashima, T. Miyakawa, T. Kuromori, M. Tanokura, K. Shinozaki, K. Yamaguchi-Shinozaki, Molecular basis of the core regulatory network in ABA responses: Sensing, signaling and transport. Plant Cell Physiol. 51, 1821-1839 (2010).
49. F. C. Peterson, E. S. Burgie, S.-Y. Park, D. R. Jensen, J. J. Weiner, C. A. Bingman, C.-E. A. Chang, S. R. Cutler, G. N. Phillips Jr., B. F. Volkman, Structural basis for selective activation of ABA receptors. Nat. Struct. Mol. Biol. 17, 1109-1113 (2010).
50. N. Nishimura, K. Hitomi, A. S. Arvai, R. P. Rambo, C. Hitomi, S. R. Cutler, J. I. Schroeder, E. D. Getzoff, Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326, 1373-1379 (2009).
51. P. Yin, H. Fan, Q. Hao, X. Yuan, D. Wu, Y. Pang, C. Yan, W. Li, J. Wang, N. Yan, Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat. Struct. Mol. Biol. 16, 1230-1236 (2009).
52. F. Dupeux, J. Santiago, K. Betz, J. Twycross, S.-Y. Park, L. Rodriguez, M. Gonzalez-Guzman, M. R. Jensen, N. Krasnogor, M. Blackledge, M. Holdsworth, S. R. Cutler, P. L. Rodriguez, J. A. Márquez, A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO J. 30, 4171-4184 (2011).
53. K.-i. Miyazono, T. Miyakawa, Y. Sawano, K. Kubota, H.-J. Kang, A. Asano, Y. Miyauchi, M. Takahashi, Y. Zhi, Y. Fujita, T. Yoshida, K. S. Kodaira, K. Yamaguchi-Shinozaki, M. Tanokura, Structural basis of abscisic acid signalling. Nature 462, 609-614 (2009).
54. I. Szostkiewicz, K. Richter, M. Kepka, S. Demmel, Y. Ma, A. Korte, F. F. Assaad, A. Christmann, E. Grill, Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J. 61, 25-35 (2010).
55. F. Dupeux, R. Antoni, K. Betz, J. Santiago, M. Gonzalez-Guzman, L. Rodriguez, S. Rubio, S.-Y. Park, S. R. Cutler, P. L. Rodriguez, J. A. Márquez, Modulation of abscisic acid signaling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiol. 156, 106-116 (2011).
56. R. R. Johnson, R. L. Wagner, S. D. Verhey, M. K. Walker-Simmons, The abscisic acid-responsive kinase PKABA1 interacts with a seed-specifi c abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol. 130, 837-846 (2002).
57. J. Li, S. M. Assmann, An abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8, 2359-2368 (1996).
58. J. Li, X.-Q. Wang, M. B. Watson, S. M. Assmann, Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287, 300-303 (2000).
59. R. Yoshida, T. Hobo, K. Ichimura, T. Mizoguchi, F. Takahashi, J. Aronso, J. R. Ecker, K. Shinozaki, ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43, 1473-1483 (2002).
60. A.-C. Mustilli, S. Merlot, A. Vavasseur, F. Fenzi, J. Giraudat, 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 (2002).
61. R. Yoshida, T. Umezawa, T. Mizoguchi, S. Takahashi, F. Takahashi, K. Shinozaki, The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J. Biol. Chem. 281, 5310-5318 (2006).
62. M. Boudsocq, H. Barbier-Brygoo, C. Laurière, Identifi cation of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279, 41758-41766 (2004).
63. H. Fujii, P. E. Verslues, J.-K. Zhu, Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, 1717-1722 (2011).
64. H. Fujii, J.-K. Zhu, Arabidopsis mutant defi cient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl. Acad. Sci. U.S.A. 106, 8380-8385 (2009).
65. T. Umezawa, N. Sugiyama, M. Mizoguchi, S. Hayashi, F. Myouga, K. Yamaguchi-Shinozaki, Y. Ishihama, T. Hirayama, K. Shinozaki, Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 17588-17593 (2009).
66. F. Vlad, S. Rubio, A. Rodrigues, C. Sirichandra, C. Belin, N. Robert, J. Leung, P. L. Rodriguez, C. Laurière, S. Merlot, Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21, 3170-3184 (2009).
67. N. Nishimura, A. Sarkeshik, K. Nito, S. Y. Park, A. Wang, P. C. Carvalho, S. Lee, D. F. Caddell, S. R. Cutler, J. Chory, J. R. Yates, J. I. Schroeder, PYR/PYL/RCAR family members are major invivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61, 290-299 (2010).
68. H. Fujii, V. Chinnusamy, A. Rodrigues, S. Rubio, R. Antoni, S.-Y. Park, S. R. Cutler, J. Sheen, P. L. Rodriguez, J.-K. Zhu, In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660-664 (2009).
69. X. Xie, Y. Wang, L. Williamson, G. H. Holroyd, C. Tagliavia, E. Murchie, J. Theobald, M. R. Knight, W. J. Davies, H. M. O. Leyser, A. M. Hetherington, The identifi cation of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr. Biol. 16, 882-887 (2006).
70. H. Fujii, P. E. Verslues, J.-K. Zhu, Identifi cation of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19, 485-494 (2007).
71. T. Yoshida, Y. Fujita, H. Sayama, S. Kidokoro, K. Maruyama, J. Mizoi, K. Shinozaki, K. Yamaguchi- Shinozaki, AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685 (2010).
72. T. Furihata, K. Maruyama, Y. Fujita, T. Umezawa, R. Yoshida, K. Shinozaki, K. Yamaguchi- Shinozaki, Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl. Acad. Sci. U.S.A. 103, 1988-1993 (2006).
73. C. Sirichandra, M. Davanture, B. E. Turk, M. Zivy, B. Valot, J. Leung, S. Merlot, The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5, e13935 (2010).
74. A. Sato, Y. Sato, Y. Fukao, M. Fujiwara, T. Umezawa, K. Shinozaki, T. Hibi, M. Taniguchi, H. Miyake, D. B. Goto, N. Uozumi, 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. 424, 439-448 (2009).
75. G. P. Bienert, A. L. Møller, K. A. Kristiansen, A. Schulz, I. M. Møller, J. K. Schjoerring, T. P. Jahn, Specifi c aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192 (2007).
76. D. Cho, D. Shin, B. W. Jeon, J. M. Kwak, ROS-mediated ABA signaling. J. Plant Biol. 52, 102-113 (2009).
77. J. M. Kwak, I. C. Mori, Z. M. Pei, N. Leonhardt, M. A. Torres, J. L. Dangl, R. E. Bloom, S. Bodde, J. D. Jones, J. I. Schroeder, NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633 (2003).
78. C. Sirichandra, D. Gu, H.-C. Hu, M. Davanture, S. Lee, M. Djaoui, B. Valot, M. Zivy, J. Leung, S. Merlot, J. M. Kwak, Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583, 2982-2986 (2009).
79. C. Schmidt, I. Schelle, Y.-J. Liao, J. I. Schroeder, Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. Proc. Natl. Acad. Sci. U.S.A. 92, 9535-9539 (1995).
80. J. Negi, O. Matsuda, T. Nagasawa, Y. Oba, H. Takahashi, M. Kawai-Yamada, H. Uchimiya, M. Hashimoto, K. Iba, CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483-486 (2008).
81. T. Vahisalu, H. Kollist, Y.-F. Wang, N. Nishimura, W.-Y. Chan, G. Valerio, A. Lamminmäki, M. Brosché, H. Moldau, R. Desikan, J. I. Schroeder, J. Kangasjärvi, SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452, 487-491 (2008).
82. S. Saji, S. Bathula, A. Kubo, M. Tamaoki, M. Kanna, M. Aono, N. Nakajima, T. Nakaji, T. Takeda, M. Asayama, H. Saji, Disruption of a gene encoding C4-dicarboxylate transporter-like protein increases ozone sensitivity through deregulation of the stomatal response in Arabidopsis thaliana. Plant Cell Physiol. 49, 2-10 (2008).
83. S. Thomine, S. Zimmermann, J. Guern, H. Barbier-Brygoo, ATP-dependent regulation of an anion channel at the plasma membrane of protoplasts from epidermal cells of Arabidopsis hypocotyls. Plant Cell 7, 2091-2100 (1995).
84. T. Sasaki, I. C. Mori, T. Furuichi, S. Munemasa, K. Toyooka, K. Matsuoka, Y. Murata, Y. Yamamoto, Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol. 51, 354-365 (2010).
85. S. Meyer, P. Mumm, D. Imes, A. Endler, B. Weder, K. A. S. Al-Rasheid, D. Geiger, I. Marten, E. Martinoia, R. Hedrich, AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J. 63, 1054-1062 (2010).
86. O. A. Hoekenga, L. G. Maron, M. A. Piñeros, G. M. A. Cançado, J. Shaff, Y. Kobayashi, P. R. Ryan, B. Dong, E. Delhaize, T. Sasaki, H. Matsumoto, Y. Yamamoto, H. Koyama, L. V. Kochian, AtALMT1, which encodes a malate transporter, is identifi ed as one of several genes critical for aluminum tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 9738-9743 (2006).
87. T. Sasaki, Y. Yamamoto, B. Ezaki, M. Katsuhara, S. J. Ahn, P. R. Ryan, E. Delhaize, H. Matsumoto, A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645-653 (2004).
88. Y. H. Chen, L. Hu, M. Punta, R. Bruni, B. Hillerich, B. Kloss, B. Rost, J. Love, S. A. Siegelbaum, W. A. Hendrickson, Homologue structure of the SLAC1 anion channel for closing stomata in leaves. Nature 467, 1074-1080 (2010).
89. D. Geiger, S. Scherzer, P. Mumm, A. Stange, I. Marten, H. Bauer, P. Ache, S. Matschi, A. Liese, K. A. Al-Rasheid, T. Romeis, R. Hedrich, Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl. Acad. Sci. U.S.A. 106, 21425-21430 (2009).
90. 2+ affinities. Proc. Natl. Acad. Sci. U.S.A. 107, 8023-8028 (2010).
91. S. C. Lee, W.-Z. Lan, B. B. Buchanan, S. Luan, A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. U.S.A. 106, 21419-21424 (2009).
92. D. Geiger, T. Maierhofer, K. A. S. Al-Rasheid, S. Scherzer, P. Mumm, A. Liese, P. Ache, C. Wellmann, I. Marten, E. Grill, T. Romeis, R. Hedrich, Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci. Signal. 4, ra32 (2011).
93. S.-Y. Ma, W.-H. Wu, AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol. Biol. 65, 511-518 (2007).
94. S. Franz, B. Ehlert, A. Liese, J. Kurth, A.-C. Cazalé, T. Romeis, Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol. Plant. 4, 83-96 (2011).
95. 2+)-permeable channels and stomatal closure. PLoS Biol. 4, e327 (2006).
96. 2 signal transduction in guard cell. EMBO J. 30, 1645-1658 (2011).
97. E. Hosy, A. Vavasseur, K. Mouline, I. Dreyer, F. Gaymard, F. Porée, J. Boucherez, A. Lebaudy, D. Bouchez, A.-A. Véry, T. Simonneau, J.-B. Thibaud, H. Sentenac, The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl. Acad. Sci. U.S.A. 100, 5549-5554 (2003).
98. 2-controlled stomatal movements in guard cells. Nat. Cell Biol. 12, 87-93, 1-18 (2010).
99. 2 sensing. New Phytol. 165, 665-682 (2005).
100. 2) diffusion across the plasma membrane. Plant Cell Physiol. 43, 70-78 (2002).
101. 2 pore with physiological functions. Nature 425, 734-737 (2003).
102. J. Flexas, M. Ribas-Carbó, A. Diaz-Espejo, J. Galmés, H. Medrano, Mesophyll conductance to CO2: Current knowledge and future prospects. Plant Cell Environ. 31, 602-621 (2008).
103. T. Mrinalini, Y. K. Latha, A. S. Raghavendra, V. S. R. Das, Stimulation and inhibition by bicarbonate of stomatal opening in epidermal strips of Commelina benghalensis. New Phytol. 91, 413-418 (1982).
104. T. Kuromori, T. Miyaji, H. Yabuuchi, H. Shimizu, E. Sugimoto, A. Kamiya, Y. Moriyama, K. Shinozaki, ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc. Natl. Acad. Sci. U.S.A. 107, 2361-2366 (2010).
105. J. Kang, J.-U. Hwang, M. Lee, Y.-Y. Kim, S. M. Assmann, E. Martinoia, Y. Lee, PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. U.S.A. 107, 2355-2360 (2010).
106. J. Smalle, J. Kurepa, P. Yang, T. J. Emborg, E. Babiychuk, S. Kushnir, R. D. Vierstra, The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specifi c function in abscisic acid signaling. Plant Cell 15, 965-980 (2003).
107. P. D. Hare, H. S. Seo, J. Y. Yang, N. H. Chua, Modulation of sensitivity and selectivity in plant signaling by proteasomal destabilization. Curr. Opin. Plant Biol. 6, 453-462 (2003).
108. +)-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J. 26, 3216-3226 (2007).
109. M. Haruta, H. L. Burch, R. B. Nelson, G. Barrett-Wilt, K. G. Kline, S. B. Mohsin, J. C. Young, M. S. Otegui, M. R. Sussman, Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J. Biol. Chem. 285, 17918-17929 (2010).
110. S. Pandey, D. C. Nelson, S. M. Assmann, Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136, 136-148 (2009).
111. F.-Q. Wu, Q. Xin, Z. Cao, Z.-Q. Liu, S.-Y. Du, C. Mei, C.-X. Zhao, X.-F. Wang, Y. Shang, T. Jiang, X.-F. Zhang, L. Yan, R. Zhao, Z.-N. Cui, R. Liu, H.-L. Sun, X.-L. Yang, Z. Su, D.-P. Zhang, The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol. 150, 1940-1954 (2009).
112. Y. Shang, L. Yan, Z.-Q. Liu, Z. Cao, C. Mei, Q. Xin, F.-Q. Wu, X.-F. Wang, S.-Y. Du, T. Jiang, X.-F. Zhang, R. Zhao, H.-L. Sun, R. Liu, Y.-T. Yu, D.-P. Zhang, The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22, 1909-1935 (2010).
113. T. Tsuzuki, K. Takahashi, S.-i. Inoue, Y. Okigaki, M. Tomiyama, M. A. Hossain, K.-i. Shimazaki, Y. Murata, T. Kinoshita, Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J. Plant Res. 124, 527-538 (2011).
114. Y.-Y. Shen, X.-F. Wang, F.-Q. Wu, S.-Y. Du, Z. Cao, Y. Shang, X.-L. Wang, C.-C. Peng, X.-C. Yu, S.-Y. Zhu, R.-C. Fan, Y.-H. Xu, D.-P. Zhang, The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443, 823-826 (2006).
115. B. V. Milborrow, A distinction between the fast and slow responses to abscisic acid. Aust. J. Plant Physiol. 7, 749-754 (1980).
116. M. Bucholc, A. Ciesielski, G. Goch, A. Anielska-Mazur, A. Kulik, E. Krzywi ska, G. Dobrowolska, SNF1-related protein kinases 2 are negatively regulated by a plant-specifi c calcium sensor. J. Biol. Chem. 286, 3429-3441 (2011).
117. R. E. Sharp, M. E. LeNoble, M. A. Else, E. T. Thorne, F. Gherardi, Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: Evidence for an interaction with ethylene. J. Exp. Bot. 51, 1575-1584 (2000).
118. M. E. LeNoble, W. G. Spollen, R. E. Sharp, Maintenance of shoot growth by endogenous ABA: Genetic assessment of the involvement of ethylene suppression. J. Exp. Bot. 55, 237-245 (2004).
119. M. Ghassemian, E. Nambara, S. Cutler, H. Kawaide, Y. Kamiya, P. McCourt, Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12, 1117-1126 (2000).
120. J. M. Barrero, P. Piqueras, M. González-Guzmán, R. Serrano, P. L. Rodríguez, M. R. Ponce, J. L. Micol, A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J. Exp. Bot. 56, 2071-2083 (2005).
121. J. Wigger, J. Phillips, M. Peisker, W. Hartung, U. zur Nieden, O. Artsaenko, U. Fiedler, U. Conrad, Prevention of stomatal closure by immunomodulation of endogenous abscisic acid and its reversion by abscisic acid treatment: Physiological behaviour and morphological features of tobacco stomata. Planta 215, 413-423 (2002).
122. D. M. Priest, S. J. Ambrose, F. E. Vaistij, L. Elias, G. S. Higgins, A. R. Ross, S. R. Abrams, D. J. Bowles, Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J. 46, 492-502 (2006).
123. A. Christmann, T. Hoffmann, I. Teplova, E. Grill, A. Müller, Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol. 137, 209-219 (2005).
124. M. J. Harris, W. H. Outlaw Jr., Rapid adjustment of guard-cell abscisic Acid levels to current leaf-water status. Plant Physiol. 95, 171-173 (1991).
125. S. Q. Zhang, W. H. Outlaw Jr., K. Aghoram, Relationship between changes in the guard cell abscisic-acid content and other stress-related physiological parameters in intact plants. J. Exp. Bot. 52, 301-308 (2001).
126. I. Chen, ABA receptor diversity. PSI-Nature Structural Biology Knowledgebase (2010); http://sbkb.org/update/2010/11/full/sbkb.2010.49. html.
127. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
128. + -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19, 1617-1634 (2007).