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PMID: 21461660 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Systems biology approaches to abscisic acid signaling.

Journal of plant research ·Vol. 124 ·No. 4 ·2011-07-00 ·Pages 539-48

Umezawa T

Abstract

Recent advances in our understanding of abscisic acid (ABA) signaling have identified a core pathway consisting of receptors (PYR/PYL/RCAR), protein phosphatases (PP2C), protein kinases (SnRK2), and several downstream factors that will lead to the next stage of ABA research. Systems biology will be an important concept for further understanding ABA responses in plants. In this review, two practical approaches of systems biology to ABA signaling are presented: the one is 'transcriptome analysis', which covers coding genes as well as unannotated transcripts, and the other is 'phosphoproteomics'. The latter technology will offer an unprecedented overview of the regulatory networks involved in ABA signaling because protein phosphorylation/dephosphorylation is a major center of such regulation. Systematic studies will contribute to our understanding of the network structure and dynamics of ABA signaling; moreover, systems biology will facilitate ABA signaling studies as well as future biotechnological applications in crops or trees.

MeSH Terms
Abscisic Acid/metabolism GTP-Binding Proteins/metabolism Gene Expression Profiling Gene Expression Regulation, Plant Phosphoprotein Phosphatases/metabolism Phosphorylation Plant Growth Regulators/metabolism Plant Proteins/genetics,metabolism Plant Stomata/physiology Plants/metabolism Protein Serine-Threonine Kinases/metabolism Proteomics Signal Transduction Systems Biology Transcription Factors/metabolism
Chemicals
Plant Growth Regulators Plant Proteins Transcription Factors Abscisic Acid Protein Serine-Threonine Kinases Phosphoprotein Phosphatases GTP-Binding Proteins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Umezawa Taishi
Gene Discovery Research Group, RIKEN Plant Science Center, 3-1-1 Kouyadai, Tsukuba, Ibaraki 305-0074, Japan. umezawa@rtc.riken.jp
References (109)
109 references, click to expand
  1. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database.
    Plant Cell. 2004 Sep;16(9):2394-405 PMID: 15308754
  2. Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using TiO2-phosphopeptide enrichment and mass accuracy precursor alignment.
    Plant J. 2010 Jul 1;63(1):1-17 PMID: 20374526
  3. 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
  4. 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
  5. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant.
    J Cell Sci. 2002 Dec 15;115(Pt 24):4891-900 PMID: 12432076
  6. Emerging trends in the functional genomics of the abiotic stress response in crop plants.
    Plant Biotechnol J. 2007 May;5(3):361-80 PMID: 17430544
  7. A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11771-6 PMID: 14504388
  8. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array.
    Plant Cell Physiol. 2008 Aug;49(8):1135-49 PMID: 18625610
  9. Physical and functional interaction of the Arabidopsis K(+) channel AKT2 and phosphatase AtPP2CA.
    Plant Cell. 2002 May;14(5):1133-46 PMID: 12034902
  10. Systems biology: a brief overview.
    Science. 2002 Mar 1;295(5560):1662-4 PMID: 11872829
  11. Plant nuclear hormone receptors: a role for small molecules in protein-protein interactions.
    Annu Rev Cell Dev Biol. 2010;26:445-69 PMID: 20590451
  12. Sorghum bicolor's transcriptome response to dehydration, high salinity and ABA.
    Plant Mol Biol. 2005 Jul;58(5):699-720 PMID: 16158244
  13. Abscisic acid: emergence of a core signaling network.
    Annu Rev Plant Biol. 2010;61:651-79 PMID: 20192755
  14. Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA.
    Trends Plant Sci. 2007 Aug;12(8):343-51 PMID: 17629540
  15. Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal.
    J Exp Bot. 2008;59(1):37-43 PMID: 17595196
  16. ABA receptors: the START of a new paradigm in phytohormone signalling.
    J Exp Bot. 2010 Jul;61(12):3199-210 PMID: 20522527
  17. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed.
    Plant J. 2005 Mar;41(5):697-709 PMID: 15703057
  18. Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1.
    Plant Cell. 2002 Dec;14(12):3177-89 PMID: 12468735
  19. In vitro reconstitution of an abscisic acid signalling pathway.
    Nature. 2009 Dec 3;462(7273):660-4 PMID: 19924127
  20. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays.
    Genes Dev. 2009 Jan 1;23(1):80-92 PMID: 19095804
  21. Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses.
    Plant J. 2009 Aug;59(3):375-86 PMID: 19392690
  22. In planta changes in protein phosphorylation induced by the plant hormone abscisic acid.
    Proc Natl Acad Sci U S A. 2010 Sep 7;107(36):15986-91 PMID: 20733066
  23. 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
  24. Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays.
    Plant J. 2010 Apr 1;62(1):39-51 PMID: 20088898
  25. ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs.
    Plant Physiol. 2006 Jan;140(1):115-26 PMID: 16339800
  26. Phospholipase D alpha 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling.
    Proc Natl Acad Sci U S A. 2004 Jun 22;101(25):9508-13 PMID: 15197253
  27. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase.
    FEBS Lett. 2009 Sep 17;583(18):2982-6 PMID: 19716822
  28. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis.
    Mol Cell Proteomics. 2007 Jul;6(7):1198-214 PMID: 17317660
  29. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.
    Annu Rev Plant Biol. 2006;57:781-803 PMID: 16669782
  30. Recent advances and emerging trends in plant hormone signalling.
    Nature. 2009 Jun 25;459(7250):1071-8 PMID: 19553990
  31. Phosphoproteomics in Arabidopsis: moving from empirical to predictive science.
    J Exp Bot. 2006;57(7):1523-7 PMID: 16531460
  32. 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
  33. Transcriptome analysis reveals specific modulation of abscisic acid signaling by ROP10 small GTPase in Arabidopsis.
    Plant Physiol. 2005 Nov;139(3):1350-65 PMID: 16258012
  34. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future.
    Curr Opin Biotechnol. 2006 Apr;17(2):113-22 PMID: 16495045
  35. Stomagen positively regulates stomatal density in Arabidopsis.
    Nature. 2010 Jan 14;463(7278):241-4 PMID: 20010603
  36. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis.
    Mol Syst Biol. 2008;4:193 PMID: 18463617
  37. HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis.
    Plant Cell. 2008 Nov;20(11):2972-88 PMID: 19033529
  38. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access.
    Plant J. 2008 Aug;55(3):526-42 PMID: 18419781
  39. Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis.
    Plant Cell. 2002 Nov;14(11):2787-97 PMID: 12417701
  40. Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling.
    Plant Mol Biol. 2010 Jan;72(1-2):27-45 PMID: 19806323
  41. Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice.
    Plant J. 2006 Apr;46(1):1-13 PMID: 16553892
  42. 'Omics' analyses of regulatory networks in plant abiotic stress responses.
    Curr Opin Plant Biol. 2010 Apr;13(2):132-8 PMID: 20080055
  43. Co-expression tools for plant biology: opportunities for hypothesis generation and caveats.
    Plant Cell Environ. 2009 Dec;32(12):1633-51 PMID: 19712066
  44. G-protein coupled receptor signaling architecture of mammalian immune cells.
    PLoS One. 2009;4(1):e4189 PMID: 19142232
  45. 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
  46. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses.
    Plant J. 2007 Apr;50(2):347-63 PMID: 17376166
  47. Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism.
    Nucleic Acids Res. 2006 Jun 28;34(11):3267-78 PMID: 16807317
  48. Global and site-specific quantitative phosphoproteomics: principles and applications.
    Annu Rev Pharmacol Toxicol. 2009;49:199-221 PMID: 18834307
  49. ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed.
    Plant J. 2007 Jun;50(6):935-49 PMID: 17461784
  50. Large scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape.
    Mol Cell Proteomics. 2006 Nov;5(11):2044-59 PMID: 16825184
  51. Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana.
    Plant Cell Physiol. 2008 Oct;49(10):1580-8 PMID: 18779215
  52. 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
  53. 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
  54. Modulation of the Arabidopsis KAT1 channel by an activator of protein kinase C in Xenopus laevis oocytes.
    FEBS J. 2010 May;277(10):2318-28 PMID: 20423459
  55. Genomics approach to abscisic acid- and gibberellin-responsive genes in rice.
    DNA Res. 2003 Dec 31;10(6):249-61 PMID: 15029956
  56. Plant phosphoproteomics: an update.
    Proteomics. 2009 Feb;9(4):964-88 PMID: 19212952
  57. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs.
    Plant J. 2009 Nov;60(4):575-88 PMID: 19624469
  58. The AKT3 potassium channel protein interacts with the AtPP2CA protein phosphatase 2C.
    J Exp Bot. 2001 Jan;52(354):181-2 PMID: 11181729
  59. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses.
    Cell. 2006 Aug 11;126(3):467-75 PMID: 16901781
  60. A rice kinase-protein interaction map.
    Plant Physiol. 2009 Mar;149(3):1478-92 PMID: 19109415
  61. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis.
    Plant Cell. 2008 Jun;20(6):1678-92 PMID: 18586869
  62. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses.
    Plant J. 2007 Sep;51(5):931-40 PMID: 17651370
  63. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8023-8 PMID: 20385816
  64. G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells.
    Science. 2001 Jun 15;292(5524):2070-2 PMID: 11408655
  65. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis.
    Plant Cell. 2005 Apr;17(4):1105-19 PMID: 15772289
  66. Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics.
    Plant J. 2009 Mar;57(6):1065-78 PMID: 19036030
  67. Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action.
    Mol Syst Biol. 2010 Jun 8;6:372 PMID: 20531402
  68. 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
  69. Protein-protein interactions of tandem affinity purified protein kinases from rice.
    PLoS One. 2009 Aug 19;4(8):e6685 PMID: 19690613
  70. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport.
    Plant Cell Physiol. 2010 Nov;51(11):1821-39 PMID: 20980270
  71. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses.
    Plant Cell. 2006 Oct;18(10):2749-66 PMID: 16998070
  72. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis.
    Cell. 2006 Sep 22;126(6):1189-201 PMID: 16949657
  73. Research on plant abiotic stress responses in the post-genome era: past, present and future.
    Plant J. 2010 Mar;61(6):1041-52 PMID: 20409277
  74. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis.
    Plant J. 2010 Jan;61(2):290-9 PMID: 19874541
  75. 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. 2010 Feb;61(4):672-85 PMID: 19947981
  76. Proteomics approaches to understand protein phosphorylation in pathway modulation.
    Curr Opin Plant Biol. 2010 Jun;13(3):280-87 PMID: 20097120
  77. Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens.
    New Phytol. 2007;176(2):275-287 PMID: 17696978
  78. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought.
    EMBO J. 2009 Dec 2;28(23):3745-57 PMID: 19816401
  79. Regulators of PP2C phosphatase activity function as abscisic acid sensors.
    Science. 2009 May 22;324(5930):1064-8 PMID: 19407143
  80. 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
  81. 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. 2006 Feb 24;281(8):5310-8 PMID: 16365038
  82. ABA perception and signalling.
    Trends Plant Sci. 2010 Jul;15(7):395-401 PMID: 20493758
  83. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis.
    EMBO J. 2002 Jun 17;21(12):3029-38 PMID: 12065416
  84. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis.
    Plant Cell. 2004 Dec;16(12):3460-79 PMID: 15548743
  85. Identification of transcribed sequences in Arabidopsis thaliana by using high-resolution genome tiling arrays.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4453-8 PMID: 15755812
  86. Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes.
    Plant Physiol. 2010 Jan;152(1):19-28 PMID: 19923235
  87. Web-queryable large-scale data sets for hypothesis generation in plant biology.
    Plant Cell. 2009 Apr;21(4):1034-51 PMID: 19401381
  88. Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity.
    Plant Physiol. 2005 Dec;139(4):1750-61 PMID: 16299177
  89. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis.
    Dev Cell. 2002 Aug;3(2):233-44 PMID: 12194854
  90. Towards functional phosphoproteomics by mapping differential phosphorylation events in signaling networks.
    Proteomics. 2008 Nov;8(21):4453-65 PMID: 18972525
  91. 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
  92. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis.
    Plant Cell. 2007 May;19(5):1665-81 PMID: 17513501
  93. 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
  94. 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
  95. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions.
    Genes Dev. 2010 Aug 15;24(16):1695-708 PMID: 20713515
  96. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis.
    Cell. 2009 Jan 9;136(1):136-48 PMID: 19135895
  97. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition.
    Plant Cell. 2010 Jun;22(6):1909-35 PMID: 20543028
  98. Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response.
    J Exp Bot. 2010 Jul;61(12):3345-53 PMID: 20519338
  99. Abscisic acid biosynthesis and catabolism.
    Annu Rev Plant Biol. 2005;56:165-85 PMID: 15862093
  100. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants.
    Plant Physiol. 2010 Jul;153(3):1161-74 PMID: 20466843
  101. Bow ties, metabolism and disease.
    Trends Biotechnol. 2004 Sep;22(9):446-50 PMID: 15331224
  102. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis.
    Mol Cell Proteomics. 2007 Oct;6(10):1711-26 PMID: 17586839
  103. Tiling array-driven elucidation of transcriptional structures based on maximum-likelihood and Markov models.
    Plant J. 2005 Aug;43(4):611-21 PMID: 16098113
  104. Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase.
    Nature. 2002 Aug 15;418(6899):793-7 PMID: 12181571
  105. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis.
    Plant Cell. 2006 Oct;18(10):2733-48 PMID: 16980540
  106. Advances in the analysis of protein phosphorylation.
    J Proteome Res. 2008 May;7(5):1809-18 PMID: 18327898
  107. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.
    Plant Physiol. 2003 Dec;133(4):1755-67 PMID: 14645724
  108. The Mg-chelatase H subunit is an abscisic acid receptor.
    Nature. 2006 Oct 19;443(7113):823-6 PMID: 17051210
  109. Decoding signalling networks by mass spectrometry-based proteomics.
    Nat Rev Mol Cell Biol. 2010 Jun;11(6):427-39 PMID: 20461098
Article Info
Journal
Journal of plant research
Abbr.
J Plant Res
ISSN
1618-0860
Published
2011-07-00
Epub
2011-00-02
Pages
539-48
Language
English
Region
Japan
NLM ID
9887853
Subset
IM
Analysis Services
Analysis Services

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