Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors

Plant Journal

Volumn 44, Issue 6, 2005, Pages 939-949

  Kobayashi, Yuhko ^a   Murata, Michiharu ^b   Minami, Hideyuki ^a   Yamamoto, Shuhei ^a   Kagaya, Yasuaki ^b   Hobo, Tokunori ^b,c   Yamamoto, Akiko ^a   Hattori, Tsukaho ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b MIE UNIVERSITY   (Japan)

^c Research Institute for Biological Science OKAYAMA   (Japan)

Author keywords

Abscisic acid; Abscisic acid response element; Osmotic stress; Protein kinase; Rice

Indexed keywords

ACTIVATION ANALYSIS; ENZYME KINETICS; GENES; IMMUNOLOGY; PRECIPITATION (CHEMICAL);

ABSCISIC ACID; ABSCISIC ACID RESPONSE ELEMENT; OSMOTIC STRESS; PROTEIN KINASE;

PROTEINS;

ACTIVATION; ENZYMATIC ACTIVITY; PROTEINS;

ABSCISIC ACID; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; PHYTOHORMONE; PROTEIN SERINE THREONINE KINASE; RECOMBINANT PROTEIN; SERINE; TRAB1 PROTEIN, PLANT; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; OSMOTIC PRESSURE; PHOSPHORYLATION; RICE; SIGNAL TRANSDUCTION;

ABSCISIC ACID; AMINO ACID SEQUENCE; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; KINETICS; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; OSMOTIC PRESSURE; PHOSPHORYLATION; PLANT GROWTH REGULATORS; PLANT PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; RESPONSE ELEMENTS; SERINE; SIGNAL TRANSDUCTION;

EID: 32444442926     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02583.x     Document Type: Article

References (55)

1. Boudsocq M. Barbier-Brygoo H. 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.
2. Bray E.A. ( 1997) Plant responses to water deficit. Trends Plant Sci. 2, 48.
3. Brinkworth R.I. Breinl R.A. Kobe B. ( 2003) From the cover: structural basis and prediction of substrate specificity in protein serine/threonine kinases. Proc. Natl Acad. Sci. USA, 100, 74 79.
4. Busk P.K. Pages M. ( 1998) Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37, 425 435.
5. Choi H.-I. Hong J.-H. Ha J.-O. Kang J.-Y. Kim S.Y. ( 2000) ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723 1730.
6. DeWald D.B. Torabinejad J. Jones C.A. Shope J.C. Cangelosi A.R. Thompson J.E. Prestwich G.D. Hama H. ( 2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol. 126, 759 769.
7. Finkelstein R.R. Lynch T.J. ( 2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell, 12, 599 610.
8. Finkelstein R.R. Gampala S.S.L. Rock C.D. ( 2002) Abscisic acid signaling in seeds and seedlings. Plant Cell, 14, S15 45.
9. Gomez-Cadenas A. Verhey S.D. Holappa L.D. Shen Q. Ho T.-H.D. Walker-Simmons M.K. ( 1999) An abscisic acid-induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers. Proc. Natl Acad. Sci. USA, 96, 1767 1772.
10. Gomez-Cadenas A. Zentella R. Walker-Simmons M.K. Ho T.-H.D. ( 2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. Plant Cell, 13, 667 679.
11. Hattori T. Totsuka M. Hobo T. Kagaya Y. Yamamoto-Toyoda A. ( 2002) Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol. 43, 136 140.
12. Himmelbach A. Yang Y. Grill E. ( 2003) Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol. 6, 470 479.
13. Hobo T. Asada M. Kowyama Y. Hattori T. ( 1999a) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J. 19, 679 689.
14. Hobo T. Kowyama Y. Hattori T. ( 1999b) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc. Natl Acad. Sci. USA, 96, 15348 15353.
15. Hrabak E.M. Chan C.W.M. Gribskov M. et al. ( 2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132, 666 680.
16. Hugouvieux V. Kwak J.M. Schroeder J.I. ( 2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell, 106, 477 487.
17. Johnson R.R. Wagner R.L. Verhey S.D. Walker-Simmons M.K. ( 2002) The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol. 130, 837 846.
18. Kagaya Y. Hobo T. Murata M. Ban A. Hattori T. ( 2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell, 14, 3177 3189.
19. Kang J.-Y. Choi H.-I. Im M.-Y. Kim S.Y. ( 2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell, 14, 343 357.
20. Kelner A. Pekala I. Kaczanowski S. Muszynska G. Hardie D.G. Dobrowolska G. ( 2004) Biochemical characterization of the tobacco 42-kD protein kinase activated by osmotic stress. Plant Physiol. 136, 3255 3265.
21. Kobayashi Y. Yamamoto S. Minami H. Kagaya Y. 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.
22. Koiwa H. Barb A.W. Xiong L. et al. ( 2002) C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc. Natl Acad. Sci. USA, 99, 10893 10898.
23. Kuhn J.M. Schroeder J.I. ( 2003) Impacts of altered RNA metabolism on abscisic acid signaling. Curr. Opin. Plant Biol. 6, 463.
24. Kwak J.M. Moon J.-H. Murata Y. Kuchitsu K. Leonhardt N. DeLong A. Schroeder J.I. ( 2002) disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell, 14, 2849 2861.
25. Lang V. Palva E.T. ( 1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant. Mol. Biol. 20, 951 962.
26. Lang V. Mantyla E. Welin B. Sundberg B. Palva E.T. ( 1994) Alterations in water status, endogenous abscisic acid content, and expression of rab18 gene during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol. 104, 1341 1349.
27. Leonhardt N. Kwak J.M. Robert N. Waner D. Leonhardt G. Schroeder J.I. ( 2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell, 16, 596 615.
28. Leung J. Merlot S. Giraudat J. ( 1997) 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.
29. Li J. Kinoshita T. Pandey S. Ng C.K.Y. Gygi S.P. Shimazaki K.-I. Assmann S.M. ( 2002) Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature, 418, 793.
30. Lopez-Molina L. Chua N.H. ( 2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol. 41, 541 547.
31. Lopez-Molina L. Mongrand S. Chua N.-H. ( 2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl Acad. Sci. USA, 98, 4782 4787.
32. Lu C. Fedoroff N. ( 2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell, 12, 2351 2366.
33. Lu C. Han M.H. Guevara-Garcia A. Fedoroff N.V. ( 2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc. Natl Acad. Sci. USA, 99, 15812 15817.
34. MacRobbie E. ( 1997) Signalling in guard cells and regulation of ion channel activity. J. Exp. Bot. 48, 515 528.
35. McCarty D.R. ( 1995) Genetic control and integration of maturation and germination pathways in seed development. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46, 71 93.
36. McCourt P. ( 2001) Plant hormone signaling: getting the message out. Mol. Cell, 8, 1157 1158.
37. Munnik T. Irvine R.F. Musgrave A. ( 1998) Phospholipid signalling in plants. Biochim. Biophys. Acta Lipids Lipid Metab. 1389, 222 272.
38. Munnik T. Ligterink W. Meskiene I. Calderini O. Beyerly J. Musgrave A. Hirt H. ( 1999) Distinct osmosensing protein kinase pathways are involved in signalling moderate and severe hyperosmotic stress. Plant J. 20, 381 388.
39. Munnik T. Meijer H.J.G. ter Riet B. Hirt H. Frank W. Bartels D. Musgrave A. ( 2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. 22, 147 154.
40. 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.
41. Ng C.K.Y. Kinoshita T. Pandey S. Shimazaki K.-I. Assmann S.M. ( 2004) Abscisic acid induces rapid subnuclear reorganization in guard cells. Plant Physiol. 134, 1327 1331.
42. Pedro L.R. Martin P.L. Erwin G. ( 1998) Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2. Plant Mol. Biol. 38, 879.
43. Pei Z.M. Murata Y. Benning G. Thomine S. Klusener 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.
44. Pical C. Westergren T. Dove S.K. Larsson C. Sommarin M. ( 1999) Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J. Biol. Chem. 274, 38232 38240.
45. Saez A. Apostolova N. Gonzalez-Guzman M. Gonzalez-Garcia M.P. Nicolas C. Lorenzo O. Rodriguez P.L. ( 2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signaling. Plant J. 37, 354 369.
46. Shen Q. Ho T.H.D. ( 1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-Box and a novel cis-acting element. Plant Cell, 7, 295 307.
47. Shen Q. Zhang P. Ho T.H.D. ( 1996) Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell, 8, 1107 1119.
48. Shinozaki K. Yamaguchi-Shinozaki K. ( 2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant. Biol. 3, 217.
49. Uno Y. Furihata T. Abe H. Yoshida R. Shinozaki K. 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.
50. Wang X. ( 1999) The role of phospholipase D in signaling cascades. Plant Physiol. 120, 645 652.
51. Welin B.V. Olson A. Nylander M. Palva E.T. ( 1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol. Biol. 26, 131 144.
52. Xiong L. Lee H. Ishitani M. Zhu J.-K. ( 2002a) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J. Biol. Chem. 277, 8588 8596.
53. Xiong L. Schumaker K.S. Zhu J.-K. ( 2002b) Cell signaling during cold, drought, and salt stress. Plant Cell, 14, S165 183.
54. Yoshiba Y. Nanjo T. Miura S. Yamaguchi-Shinozaki K. Shinozaki K. ( 1999) Stress-responsive and developmental regulation of delta1-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 261, 766.
55. Yoshida R. Hobo T. Ichimura K. Mizoguchi T. Takahashi F. Aronso 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.