Identification of Two Protein Kinases Required for Abscisic Acid Regulation of Seed Germination, Root Growth, and Gene Expression in Arabidopsis[W]

Abscisic acid (ABA) is an important phytohormone regulating various plant processes, including seed germination. Although phosphorylation has been suggested to be important, the protein kinases required for ABA signaling during seed germination and seedling growth remain elusive. Here, we show that two protein kinases, SNF1-RELATED PROTEIN KINASE2.2 (SnRK2.2) and SnRK2.3, control responses to ABA in seed germination, dormancy, and seedling growth in Arabidopsis thaliana. A snrk2.2 snrk2.3 double mutant, but not snrk2.2 or snrk2.3 single mutants, showed strong ABA-insensitive phenotypes in seed germination and root growth inhibition. Changes in seed dormancy and ABA-induced Pro accumulation consistent with ABA insensitivity were also observed. The snrk2.2 snrk2.3 double mutant had a greatly reduced level of a 42-kD kinase activity capable of phosphorylating peptides from ABF (for ABA Response Element Binding Factor) transcription factors. ABA-induced expression of several genes whose promoters contain an ABA response element (ABRE) was reduced in snrk2.2 snrk2.3, suggesting that the mechanism of SnRK2.2 and SnRK2.3 action in ABA signaling involves the activation of ABRE-driven gene expression through the phosphorylation of ABFs. Together, these results demonstrate that SnRK2.2 and SnRK2.3 are redundant but key protein kinases that mediate a major part of ABA signaling in Arabidopsis.

[1]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[2]  K. Shinozaki,et al.  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* , 2006, Journal of Biological Chemistry.

[3]  K. Shinozaki,et al.  Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Jianhua Zhu,et al.  Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. , 2006, The Plant journal : for cell and molecular biology.

[5]  Shuhei Yamamoto,et al.  Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. , 2005, The Plant journal : for cell and molecular biology.

[6]  K. Halliday,et al.  Cold and Light Control Seed Germination through the bHLH Transcription Factor SPATULA , 2005, Current Biology.

[7]  Xianwu Zheng,et al.  HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Marie Boudsocq,et al.  Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana* , 2004, Journal of Biological Chemistry.

[9]  Shûhei Yamamoto,et al.  Differential Activation of the Rice Sucrose Nonfermenting1–Related Protein Kinase2 Family by Hyperosmotic Stress and Abscisic Acid , 2004, The Plant Cell Online.

[10]  P. McCourt,et al.  Hormone signalling from a developmental context. , 2003, Journal of experimental botany.

[11]  Yong Li,et al.  An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics , 2003, Plant Molecular Biology.

[12]  I. D. Teare,et al.  Rapid determination of free proline for water-stress studies , 1973, Plant and Soil.

[13]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[14]  M. Gribskov,et al.  The Arabidopsis CDPK-SnRK Superfamily of Protein Kinases , 2003, Plant Physiology.

[15]  S. Assmann.  OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells. , 2003, Trends in plant science.

[16]  K. Shinozaki,et al.  ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. , 2002, Plant & cell physiology.

[17]  Alain Vavasseur,et al.  Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007906. , 2002, The Plant Cell Online.

[18]  R. L. Wagner,et al.  The Abscisic Acid-Responsive Kinase PKABA1 Interacts with a Seed-Specific Abscisic Acid Response Element-Binding Factor, TaABF, and Phosphorylates TaABF Peptide Sequences1 , 2002, Plant Physiology.

[19]  E. Bray.  Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. , 2002, Plant, cell & environment.

[20]  S. Gibson,et al.  ABA and sugar interactions regulating development: cross-talk or voices in a crowd? , 2002, Current opinion in plant biology.

[21]  Soo Young Kim,et al.  Arabidopsis Basic Leucine Zipper Proteins That Mediate Stress-Responsive Abscisic Acid Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010362. , 2002, The Plant Cell Online.

[22]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings , 2002 .

[23]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[24]  L. Lopez-Molina,et al.  A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Julian I. Schroeder,et al.  Guard cell abscisic acid signalling and engineering drought hardiness in plants , 2001, Nature.

[26]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  T. Lynch,et al.  The Arabidopsis Abscisic Acid Response Gene ABI5 Encodes a Basic Leucine Zipper Transcription Factor , 2000, Plant Cell.

[28]  S. Kim,et al.  ABFs, a Family of ABA-responsive Element Binding Factors* , 2000, The Journal of Biological Chemistry.

[29]  X. Q. Wang,et al.  Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. , 2000, Science.

[30]  K. Shinozaki,et al.  Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. , 1999, Biochemical and biophysical research communications.

[31]  C. Vannini,et al.  The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid. , 1999, The Plant journal : for cell and molecular biology.

[32]  H. Goodman,et al.  The Arabidopsis Abscisic Acid Response Locus ABI4 Encodes an APETALA2 Domain Protein , 1998, Plant Cell.

[33]  J. Sheen.  Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  K. Shinozaki,et al.  Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. , 1997, The Plant cell.

[35]  S. Merlot,et al.  The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. , 1997, The Plant cell.

[36]  S. Jacobsen,et al.  Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. , 1996, The Plant journal : for cell and molecular biology.

[37]  F. Parcy,et al.  Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. , 1994, The Plant cell.

[38]  E. Grill,et al.  A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. , 1994, Science.

[39]  J. Giraudat,et al.  Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. , 1994, Science.

[40]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[41]  C. M. Karssen,et al.  Acquisition of Desiccation Tolerance and Longevity in Seeds of Arabidopsis thaliana (A Comparative Study Using Abscisic Acid-Insensitive abi3 Mutants) , 1993, Plant physiology.

[42]  M. Walker-Simmons,et al.  Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[43]  H. Goodman,et al.  Isolation of the Arabidopsis ABI3 gene by positional cloning. , 1992, The Plant cell.

[44]  C. Somerville,et al.  Three Classes of Abscisic Acid (ABA)-Insensitive Mutations of Arabidopsis Define Genes that Control Overlapping Subsets of ABA Responses. , 1990, Plant physiology.

[45]  R S Quatrano,et al.  A plant leucine zipper protein that recognizes an abscisic acid response element. , 1990, Science.

[46]  C. M. Karssen,et al.  The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana , 1984 .