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PMID: 21220313 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo.

Fujii H, Verslues PE, Zhu JK

Abstract

Osmotic stress associated with drought or salinity is a major factor that limits plant productivity. Protein kinases in the SNF1-related protein kinase 2 (SnRK2) family are activated by osmotic stress, suggesting that the kinases are involved in osmotic stress signaling. However, due to functional redundancy, their contribution to osmotic stress responses remained unclear. In this report, we constructed an Arabidopsis line carrying mutations in all 10 members of the SnRK2 family. The decuple mutant snrk2.1/2/3/4/5/6/7/8/9/10 grew poorly under hyperosmotic stress conditions but was similar to the wild type in culture media in the absence of osmotic stress. The mutant was also defective in gene regulation and the accumulation of abscisic acid (ABA), proline, and inositol 1,4,5-trisphosphate under osmotic stress. In addition, analysis of mutants defective in the ABA-activated SnRK2s (snrk2.2/3/6) and mutants defective in the rest of the SnRK2s (snrk2.1/4/5/7/8/9/10) revealed that SnRK2s are a merging point of ABA-dependent and -independent pathways for osmotic stress responses. These results demonstrate critical functions of the SnRK2s in mediating osmotic stress signaling and tolerance.

MeSH Terms
Abscisic Acid/pharmacology Amino Acid Sequence Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Enzyme Activation/drug effects Gene Expression Profiling Inositol 1,4,5-Trisphosphate/metabolism Molecular Sequence Data Mutation Oligonucleotide Array Sequence Analysis Osmotic Pressure/physiology Plant Growth Regulators/pharmacology Proline/metabolism Protein Kinases/genetics,metabolism Protein Serine-Threonine Kinases/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Sequence Homology, Amino Acid Signal Transduction/physiology
Chemicals
Arabidopsis Proteins Plant Growth Regulators SnRK2 protein, Arabidopsis Abscisic Acid Inositol 1,4,5-Trisphosphate Proline Protein Kinases SnRK2.10 protein, Arabidopsis OST1 protein, Arabidopsis Protein Serine-Threonine Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Fujii Hiroaki
Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA.
Verslues Paul E
Zhu Jian-Kang
References (54)
54 references, click to expand
  1. The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis.
    Plant Physiol. 2010 May;153(1):99-113 PMID: 20200070
  2. In vitro reconstitution of an abscisic acid signalling pathway.
    Nature. 2009 Dec 3;462(7273):660-4 PMID: 19924127
  3. Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis.
    J Biol Chem. 2002 Mar 8;277(10):8588-96 PMID: 11779861
  4. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci.
    Plant J. 1996 Oct;10(4):655-61 PMID: 8893542
  5. 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. 2009 Dec 10;424(3):439-48 PMID: 19785574
  6. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21425-30 PMID: 19955405
  7. Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10183-7 PMID: 1438207
  8. 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. 2009 Dec 15;106(50):21419-24 PMID: 19955427
  9. Interaction of SOS2 with nucleoside diphosphate kinase 2 and catalases reveals a point of connection between salt stress and H2O2 signaling in Arabidopsis thaliana.
    Mol Cell Biol. 2007 Nov;27(22):7771-80 PMID: 17785451
  10. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17588-93 PMID: 19805022
  11. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
    Science. 2009 May 22;324(5930):1068-71 PMID: 19407142
  12. Hormone signalling from a developmental context.
    J Exp Bot. 2004 Jan;55(395):247-51 PMID: 14673027
  13. Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2.
    Plant Cell. 2001 May;13(5):1205-19 PMID: 11340192
  14. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase.
    Science. 2000 Jan 14;287(5451):300-3 PMID: 10634783
  15. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1.
    Proc Natl Acad Sci U S A. 2006 Feb 7;103(6):1988-93 PMID: 16446457
  16. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase.
    FEBS Lett. 2009 Sep 17;583(18):2982-6 PMID: 19716822
  17. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3730-4 PMID: 10725382
  18. Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress.
    Plant J. 1995 May;7(5):751-60 PMID: 7773306
  19. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis.
    Plant Cell Physiol. 2009 Dec;50(12):2123-32 PMID: 19880399
  20. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells.
    Plant Cell. 2000 Jan;12(1):165-78 PMID: 10634915
  21. Ca2+-dependent protein kinases and stress signal transduction in plants.
    Science. 1996 Dec 13;274(5294):1900-2 PMID: 8943201
  22. New developments in abscisic acid perception and metabolism.
    Curr Opin Plant Biol. 2007 Oct;10(5):447-52 PMID: 17875396
  23. Molecular aspects of seed dormancy.
    Annu Rev Plant Biol. 2008;59:387-415 PMID: 18257711
  24. Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression.
    Plant Cell Physiol. 2010 May;51(5):842-7 PMID: 20375108
  25. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  26. Regulation of levels of proline as an osmolyte in plants under water stress.
    Plant Cell Physiol. 1997 Oct;38(10):1095-102 PMID: 9399433
  27. 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. 2009 Jul;50(7):1345-63 PMID: 19541597
  28. TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis.
    J Exp Bot. 2010 Mar;61(3):683-96 PMID: 20022921
  29. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.
    Plant J. 2006 Feb;45(4):523-39 PMID: 16441347
  30. Hormone interactions in stomatal function.
    Plant Mol Biol. 2009 Mar;69(4):451-62 PMID: 19031047
  31. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress.
    Proc Natl Acad Sci U S A. 2009 May 19;106(20):8380-5 PMID: 19420218
  32. Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid.
    Plant Mol Biol. 2007 Mar;63(4):491-503 PMID: 17103012
  33. Arabidopsis PLC1 is required for secondary responses to abscisic acid signals.
    Plant Cell. 2001 May;13(5):1143-54 PMID: 11340187
  34. The Arabidopsis CDPK-SnRK superfamily of protein kinases.
    Plant Physiol. 2003 Jun;132(2):666-80 PMID: 12805596
  35. Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray.
    Plant Mol Biol. 2004 Sep;56(1):29-55 PMID: 15604727
  36. SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17306-11 PMID: 15561775
  37. Phosphoproteomic identification of targets of the Arabidopsis sucrose nonfermenting-like kinase SnRK2.8 reveals a connection to metabolic processes.
    Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6460-5 PMID: 17404219
  38. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  39. Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid.
    Plant Cell. 2004 May;16(5):1163-77 PMID: 15084714
  40. ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis.
    Plant Cell Physiol. 2002 Dec;43(12):1473-83 PMID: 12514244
  41. Regulators of PP2C phosphatase activity function as abscisic acid sensors.
    Science. 2009 May 22;324(5930):1064-8 PMID: 19407143
  42. 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. 2005 Dec;44(6):939-49 PMID: 16359387
  43. An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling.
    Plant Physiol. 2003 Jun;132(2):1011-9 PMID: 12805629
  44. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis.
    Plant Cell. 2009 Oct;21(10):3170-84 PMID: 19855047
  45. A versatile strategy to define the phosphorylation preferences of plant protein kinases and screen for putative substrates.
    Plant J. 2008 Jul;55(1):104-17 PMID: 18363786
  46. The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity.
    Plant Cell. 2008 Oct;20(10):2729-45 PMID: 18941053
  47. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production.
    Plant Cell. 2002 Dec;14(12):3089-99 PMID: 12468729
  48. Linear models and empirical bayes methods for assessing differential expression in microarray experiments.
    Stat Appl Genet Mol Biol. 2004;3:Article3 PMID: 16646809
  49. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis.
    Plant Cell. 2007 Feb;19(2):485-94 PMID: 17307925
  50. Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress.
    Plant Cell Environ. 2006 Oct;29(10):2000-8 PMID: 16930325
  51. Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture.
    Plant Cell Physiol. 2001 Feb;42(2):214-22 PMID: 11230576
  52. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling.
    Annu Rev Plant Biol. 2010;61:561-91 PMID: 20192751
  53. Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana.
    J Biol Chem. 2004 Oct 1;279(40):41758-66 PMID: 15292193
  54. A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling.
    Plant Mol Biol. 2007 Jan;63(2):151-69 PMID: 16977424
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-01-25
Epub
2011-00-10
Pages
1717-22
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3029766
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059138 · United States
NIGMS NIH HHS · R01GM059138 · United States
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