Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in arabidopsis

Plant and Cell Physiology

Volumn 50, Issue 12, 2009, Pages 2123-2132

  Fujita, Yasunari ^a   Nakashima, Kazuo ^a   Yoshida, Takuya ^a,b   Katagiri, Takeshi ^c   Kidokoro, Satoshi ^a,b   Kanamori, Norihito ^a   Umezawa, Taishi ^c   Fujita, Miki ^c   Maruyama, Kyonoshin ^a   Ishiyama, Kanako ^d   Kobayashi, Masatomo ^d   Nakasone, Shoko ^a,b   Yamada, Kohji ^a,b   Ito, Takuya ^c   Shinozaki, Kazuo ^c   Yamaguchi Shinozaki, Kazuko ^a,b  

^a JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

^d RIKEN TSUKUBA INSTITUTE   (Japan)

Author keywords

ABA signaling; Arabidopsis thaliana; Protein phosphatase 2C; SnRK2 protein kinase; Water stress

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; AREB1 PROTEIN, ARABIDOPSIS; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2C; PROTEIN SERINE THREONINE KINASE; SNRK2 PROTEIN, ARABIDOPSIS; WATER;

ARABIDOPSIS; ARTICLE; DEHYDRATION; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; TRANSGENIC PLANT;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CYCLOPENTANES; DEHYDRATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MUTAGENESIS, INSERTIONAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYLIPINS; PHOSPHOPROTEIN PHOSPHATASES; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 71049140992     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp147     Document Type: Article

References (39)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., et al. (2005) FD, a bZIP protein mediating signals from the fl oral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
2. Bartels, D. and Sunkar, R. (2005) Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24: 23-58.
3. Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., et al. (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fi ne-tune gene expression during late embryogenesis. Plant Cell 14: 1391-1403.
4. Boudsocq, M., Barbier-Brygoo, H. and Lauriere, C. (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279: 41758-41766.
5. Busk, P.K. and Pages, M. (1998) Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37: 425-435.
6. Finkelstein, R.R., Gampala, S.S. and Rock, C.D. (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14 Suppl: S15-S45.
7. Fujii, H., Verslues, P.E. and Zhu, J.K. (2007) 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.
8. Fujii, H. and Zhu, J.K. (2009) Arabidopsis mutant defi cient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl Acad. Sci. USA 106: 8380-8385.
9. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi,F., Narusaka, Y., Yamaguchi-Shinozaki, K., et al. (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9: 436-442.
10. Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M.M., Seki, M., et al. (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
11. Furihata, T., Maruyama, K., Fujita, Y., Umezawa, T., Yoshida, R., Shinozaki, K., et al. (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl Acad. Sci. USA 103: 1988-1993.
12. Giraudat, J. (1995) Abscisic acid signaling. Curr. Opin. Cell Biol. 7:232-238.
13. Himmelbach, A., Yang, Y. and Grill, E. (2003) Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol. 6: 470-479.
14. Hirayama, T. and Shinozaki, K. (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci. 12: 343-351.
15. Hundertmark, M. and Hincha, D.K. (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9: 118.
16. Iuchi, S., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2000) A stress-inducible genefor 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol. 123: 553-562.
17. Johnson, R.R., Wagner, R.L., Verhey, S.D. and Walker-Simmons, M.K. (2002) 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.
18. Kang, J.Y., Choi, H.I., Im, M.Y. and Kim, S.Y. (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14: 343-357.
19. Kobayashi, Y., Murata, M., Minami, H., Yamamoto, S., Kagaya, Y., Hobo, T., et al. (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J. 44: 939-949.
20. Kobayashi, Y., Yamamoto, S., Minami, H., Kagaya, Y. and Hattori, T. (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16: 1163-1177.
21. Koornneef, M., Reuling, G. and Karssen, C.M. (1984) The isolation and chracterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 61: 377-383.
22. Kwak, J.M., Moon, J.H., Murata, Y., Kuchitsu, K., Leonhardt, N., DeLong, A., etal. (2002)Disruptionofaguardcell-expressedproteinphosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 14: 2849-2861.
23. Leung, J., Bouvier-Durand, M., Morris, P.C., Guerrier, D., Chefdor, F. and Giraudat, J. (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448-1452.
24. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., et al. (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.
25. Mustilli, A.C., Merlot, S., Vavasseur, A., Fenzi, F. and 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.
26. Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., et al. (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50: 1345-1363.
27. Ooms, J., Leon-Kloosterziel, K.M., Bartels, D., Koornneef, M. and Karssen, C.M. (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana (a comparative study using abscisic acid-insensitive abi3 mutants). Plant Physiol. 102: 1185-1191.
28. Park, S.Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
29. Qin, F., Sakuma, Y., Tran, L.S., Maruyama, K., Kidokoro, S., Fujita, Y., et al. (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20: 1693-1707.
30. Schweighofer, A., Hirt, H. and Meskiene, I. (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci. 9: 236-243.
31. Shen, Q., Zhang, P. and Ho, T.H. (1996) Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and suffi cient for ABA induction of gene expression in barley. Plant Cell 8: 1107-1119.
32. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl Acad. Sci. USA 97: 11632-11637.
33. Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Näke, C., et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
34. Xie, X., Wang, Y., Williamson, L., Holroyd, G.H., Tagliavia, C., Murchie, E., et al. (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr. Biol. 16:882-887.
35. Yamaguchi-Shinozaki, K. and Shinozaki, K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57: 781-803.
36. Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., et al. (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43: 1473-1483.
37. Yoshida, R., Umezawa, T., Mizoguchi, T., Takahashi, S., Takahashi, F. and Shinozaki, K. (2006) 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.
38. Yoshida, T., Nishimura, N., Kitahata, N., Kuromori, T., Ito, T., Asami, T., et al. (2006) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol. 140: 115-126.
39. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621-2632.