ABA-mediated transcriptional regulation in response to osmotic stress in plants

Journal of Plant Research volume 124, pages509–525(2011)Cite this article

Abstract

The plant hormone abscisic acid (ABA) plays a pivotal role in a variety of developmental processes and adaptive stress responses to environmental stimuli in plants. Cellular dehydration during the seed maturation and vegetative growth stages induces an increase in endogenous ABA levels, which control many dehydration-responsive genes. In Arabidopsis plants, ABA regulates nearly 10% of the protein-coding genes, a much higher percentage than other plant hormones. Expression of the genes is mainly regulated by two different families of bZIP transcription factors (TFs), ABI5 in the seeds and AREB/ABFs in the vegetative stage, in an ABA-responsive-element (ABRE) dependent manner. The SnRK2-AREB/ABF pathway governs the majority of ABA-mediated ABRE-dependent gene expression in response to osmotic stress during the vegetative stage. In addition to osmotic stress, the circadian clock and light conditions also appear to participate in the regulation of ABA-mediated gene expression, likely conferring versatile tolerance and repressing growth under stress conditions. Moreover, various other TFs belonging to several classes, including AP2/ERF, MYB, NAC, and HD-ZF, have been reported to engage in ABA-mediated gene expression. This review mainly focuses on the transcriptional regulation of ABA-mediated gene expression in response to osmotic stress during the vegetative growth stage in Arabidopsis.

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References

  1. Abdeen A, Schnell J, Miki B (2010) Transcriptome analysis reveals absence of unintended effects in drought-tolerant transgenic plants overexpressing the transcription factor ABF3. BMC Genomics 11:69

    PubMed  Article  CAS  Google Scholar 

  2. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    PubMed  CAS  Article  Google Scholar 

  3. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    PubMed  CAS  Article  Google Scholar 

  4. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    PubMed  CAS  Article  Google Scholar 

  5. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    PubMed  CAS  Article  Google Scholar 

  6. Ascenzi R, Gantt JS (1997) A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol Biol 34:629–641

    PubMed  CAS  Article  Google Scholar 

  7. Bartels D, Sour E (2004) Molecular responses of higher plants to dehydration. In: Heribert H, Shinozaki K (eds) Plant responses to abiotic stress. Springer, Berlin, pp 13–37

  8. Bassaganya-Riera J, Skoneczka J, Kingston DG, Krishnan A, Misyak SA, Guri AJ, Pereira A, Carter AB, Minorsky P, Tumarkin R, Hontecillas R (2010) Mechanisms of action and medicinal applications of abscisic acid. Curr Med Chem 17:467–478

    PubMed  CAS  Article  Google Scholar 

  9. Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403

    PubMed  CAS  Article  Google Scholar 

  10. Bensmihen S, Giraudat J, Parcy F (2005) Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation. J Exp Bot 56:597–603

    PubMed  CAS  Article  Google Scholar 

  11. Berendzen KW, Stuber K, Harter K, Wanke D (2006) Cis-motifs upstream of the transcription and translation initiation sites are effectively revealed by their positional disequilibrium in eukaryote genomes using frequency distribution curves. BMC Bioinformatics 7:522

    PubMed  Article  CAS  Google Scholar 

  12. Bossi F, Cordoba E, Dupre P, Mendoza MS, Roman CS, Leon P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant J 59:359–374

    PubMed  CAS  Article  Google Scholar 

  13. Bruzzone S, Moreschi I, Usai C, Guida L, Damonte G, Salis A, Scarfi S, Millo E, De Flora A, Zocchi E (2007) Abscisic acid is an endogenous cytokine in human granulocytes with cyclic ADP-ribose as second messenger. Proc Natl Acad Sci USA 104:5759–5764

    PubMed  CAS  Article  Google Scholar 

  14. Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18:756–767

    PubMed  CAS  Article  Google Scholar 

  15. Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D, Li C (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150:463–481

    PubMed  CAS  Article  Google Scholar 

  16. Busk PK, Pagès M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    PubMed  CAS  Article  Google Scholar 

  17. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    PubMed  CAS  Article  Google Scholar 

  18. Cernac A, Andre C, Hoffmann-Benning S, Benning C (2006) WRI1 is required for seed germination and seedling establishment. Plant Physiol 141:745–757

    PubMed  CAS  Article  Google Scholar 

  19. Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500

    PubMed  CAS  Article  Google Scholar 

  20. Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    PubMed  CAS  Article  Google Scholar 

  21. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    PubMed  CAS  Article  Google Scholar 

  22. Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761

    PubMed  CAS  Article  Google Scholar 

  23. Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53:53–64

    PubMed  CAS  Article  Google Scholar 

  24. Corrêa LG, Riano-Pachon DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS One 3:e2944

    PubMed  Article  CAS  Google Scholar 

  25. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    PubMed  CAS  Article  Google Scholar 

  26. de Pater S, Pham K, Memelink J, Kijne J (1997) RAP-1 is an Arabidopsis MYC-like R protein homologue, that binds to G-box sequence motifs. Plant Mol Biol 34:169–174

    PubMed  Article  Google Scholar 

  27. De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon L, Smeekens SC, Pieterse CM (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1:305–311

    PubMed  Article  Google Scholar 

  28. Denekamp M, Smeekens SC (2003) Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiol 132:1415–1423

    PubMed  CAS  Article  Google Scholar 

  29. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    PubMed  CAS  Article  Google Scholar 

  30. Dong CJ, Liu JY (2010) The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biol 10:47

    PubMed  Article  CAS  Google Scholar 

  31. Drechsel G, Raab S, Hoth S (2010) Arabidopsis zinc-finger protein 2 is a negative regulator of ABA signaling during seed germination. J Plant Physiol 167:1418–1421

    PubMed  CAS  Article  Google Scholar 

  32. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    PubMed  CAS  Article  Google Scholar 

  33. Elhiti M, Stasolla C (2009) Structure and function of homodomain-leucine zipper (HD-Zip) proteins. Plant Signal Behav 4:86–88

    PubMed  CAS  Article  Google Scholar 

  34. Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2 H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39

    PubMed  Article  CAS  Google Scholar 

  35. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    PubMed  CAS  Article  Google Scholar 

  36. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054

    PubMed  CAS  Article  Google Scholar 

  37. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45

    PubMed  CAS  Google Scholar 

  38. Finkelstein R, Gampala SS, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol Biol 59:253–267

    PubMed  CAS  Article  Google Scholar 

  39. Foster R, Izawa T, Chua NH (1994) Plant bZIP proteins gather at ACGT elements. FASEB J 8:192–200

    PubMed  CAS  Google Scholar 

  40. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    PubMed  CAS  Article  Google Scholar 

  41. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385

    PubMed  CAS  Article  Google Scholar 

  42. Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494

    PubMed  CAS  Article  Google Scholar 

  43. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664

    PubMed  CAS  Article  Google Scholar 

  44. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    PubMed  CAS  Article  Google Scholar 

  45. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    PubMed  CAS  Article  Google Scholar 

  46. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (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

    PubMed  Article  Google Scholar 

  47. Fujita M, Fujita Y, Takahashi F, Yamaguchi-Shinozaki K, Shinozaki K (2009a) Stress physiology of higher plants: cross-talk between abiotic and biotic stress signaling. In: Hirt H (ed) Plant stress biology: from genomics to systems biology. Wiley, New Jersey, pp 67–89

  48. Fujita Y, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K (2009b) Transcription factors involved in the crosstalk between abiotic and biotic stress-signaling networks. In: Yoshioka K, Shinozaki, K. (ed) Signal crosstalk in plant stress responses. Wiley-Blackwell, pp 43–58

  49. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009c) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132

    PubMed  CAS  Article  Google Scholar 

  50. Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993

    PubMed  CAS  Article  Google Scholar 

  51. Garcia ME, Lynch T, Peeters J, Snowden C, Finkelstein R (2008) A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol Biol 67:643–658

    PubMed  CAS  Article  Google Scholar 

  52. Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, Ogawa M, Yamauchi Y, Preston J, Aoki K, Kiba T, Takatsuto S, Fujioka S, Asami T, Nakano T, Kato H, Mizuno T, Sakakibara H, Yamaguchi S, Nambara E, Kamiya Y, Takahashi H, Hirai MY, Sakurai T, Shinozaki K, Saito K, Yoshida S, Shimada Y (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55:526–542

    PubMed  CAS  Article  Google Scholar 

  53. Gómez-Porras JL, Riaño-Pachón DM, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genomics 8:260

    PubMed  Article  CAS  Google Scholar 

  54. Greve K, La Cour T, Jensen MK, Poulsen FM, Skriver K (2003) Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochem J 371:97–108

    PubMed  CAS  Article  Google Scholar 

  55. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK (2002) A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell 3:233–244

    PubMed  CAS  Article  Google Scholar 

  56. Gusmaroli G, Tonelli C, Mantovani R (2002) Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. Gene 283:41–48

    PubMed  CAS  Article  Google Scholar 

  57. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    PubMed  CAS  Article  Google Scholar 

  58. Hanano S, Domagalska MA, Nagy F, Davis SJ (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11:1381–1392

    PubMed  CAS  Article  Google Scholar 

  59. Hattori T, Terada T, Hamasuna S (1995) Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7:913–925

    PubMed  CAS  Article  Google Scholar 

  60. 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

    PubMed  CAS  Article  Google Scholar 

  61. He P, Chintamanani S, Chen Z, Zhu L, Kunkel BN, Alfano JR, Tang X, Zhou JM (2004) Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J 37:589–602

    PubMed  CAS  Article  Google Scholar 

  62. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    PubMed  CAS  Article  Google Scholar 

  63. Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20:735–747

    PubMed  CAS  Article  Google Scholar 

  64. Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engstrom P, Söderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139:509–518

    PubMed  CAS  Article  Google Scholar 

  65. Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21:3029–3038

    PubMed  CAS  Article  Google Scholar 

  66. Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689

    PubMed  CAS  Article  Google Scholar 

  67. Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708

    PubMed  CAS  Article  Google Scholar 

  68. Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    PubMed  CAS  Article  Google Scholar 

  69. Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by an NAC (NAM-ATAF1, 2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 56:867–880

    PubMed  CAS  Article  Google Scholar 

  70. Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure–function relationships and determinants of ANAC019 stress signalling. Biochem J 426:183–196

    PubMed  CAS  Article  Google Scholar 

  71. Jiang CJ, Aono M, Tamaoki M, Maeda S, Sugano S, Mori M, Takatsuji H (2008) SAZ, a new SUPERMAN-like protein, negatively regulates a subset of ABA-responsive genes in Arabidopsis. Mol Genet Genomics 279:183–192

    PubMed  CAS  Article  Google Scholar 

  72. Johannesson H, Wang Y, Hanson J, Engström P (2003) The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 51:719–729

    PubMed  CAS  Article  Google Scholar 

  73. Jung C, Lyou SH, Yeu S, Kim MA, Rhee S, Kim M, Lee JS, Choi YD, Cheong JJ (2007) Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Rep 26:1053–1063

    PubMed  CAS  Article  Google Scholar 

  74. Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635

    PubMed  CAS  Article  Google Scholar 

  75. Jung C, Shim JS, Seo JS, Lee HY, Kim CH, Choi YD, Cheong JJ (2010) Non-specific phytohormonal induction of AtMYB44 and suppression of jasmonate-responsive gene activation in Arabidopsis thaliana. Mol Cells 29:71–76

    PubMed  CAS  Article  Google Scholar 

  76. 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

    PubMed  CAS  Article  Google Scholar 

  77. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    PubMed  CAS  Article  Google Scholar 

  78. Kempa S, Krasensky J, Dal Santo S, Kopka J, Jonak C (2008) A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3:e3935

    PubMed  Article  CAS  Google Scholar 

  79. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    PubMed  CAS  Article  Google Scholar 

  80. Kim SY (2006) The role of ABF family bZIP class transcription factors in stress response. Physiol Plant 126:519–527

    CAS  Google Scholar 

  81. Kim SY, Ma J, Perret P, Li Z, Thomas TL (2002) Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol 130:688–697

    PubMed  CAS  Article  Google Scholar 

  82. Kim S, Choi HI, Ryu HJ, Park JH, Kim MD, Kim SY (2004a) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136:3639–3648

    PubMed  CAS  Article  Google Scholar 

  83. Kim S, Kang JY, Cho DI, Park JH, Kim SY (2004b) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87

    PubMed  CAS  Article  Google Scholar 

  84. Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    PubMed  CAS  Article  Google Scholar 

  85. Kim JM, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588

    PubMed  CAS  Article  Google Scholar 

  86. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–1057

    PubMed  CAS  Article  Google Scholar 

  87. Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33:604–611

    PubMed  Article  CAS  Google Scholar 

  88. Kirchler T, Briesemeister S, Singer M, Schutze K, Keinath M, Kohlbacher O, Vicente-Carbajosa J, Teige M, Harter K, Chaban C (2010) The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors. Eur J Cell Biol 89:175–183

    PubMed  CAS  Article  Google Scholar 

  89. Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189

    PubMed  CAS  Article  Google Scholar 

  90. Klempnauer KH, Gonda TJ, Bishop JM (1982) Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell 31:453–463

    PubMed  CAS  Article  Google Scholar 

  91. Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107:15986–15991

    PubMed  CAS  Article  Google Scholar 

  92. Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717

    PubMed  CAS  Article  Google Scholar 

  93. 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

    PubMed  CAS  Article  Google Scholar 

  94. Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (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

    PubMed  CAS  Article  Google Scholar 

  95. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–276

    PubMed  CAS  Article  Google Scholar 

  96. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    PubMed  CAS  Article  Google Scholar 

  97. Lee YH, Chun JY (1998) A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol Biol 37:377–384

    PubMed  CAS  Article  Google Scholar 

  98. Lee SJ, Cho DI, Kang JY, Kim SY (2009) An ARIA-interacting AP2 domain protein is a novel component of ABA signaling. Mol Cells 27:409–416

    PubMed  CAS  Article  Google Scholar 

  99. Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010a) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22:1716–1732

    PubMed  CAS  Article  Google Scholar 

  100. Lee SJ, Cho DI, Kang JY, Kim MD, Kim SY (2010b) AtNEK6 interacts with ARIA and is involved in ABA response during seed germination. Mol Cells 29:559–566

    PubMed  CAS  Article  Google Scholar 

  101. Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY (2010c) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 153:716–727

    PubMed  CAS  Article  Google Scholar 

  102. Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28:3745–3757

    PubMed  CAS  Article  Google Scholar 

  103. Li H, Sun J, Xu Y, Jiang H, Wu X, Li C (2007) The bHLH-type transcription factor AtAIB positively regulates ABA response in Arabidopsis. Plant Mol Biol 65:655–665

    PubMed  CAS  Article  Google Scholar 

  104. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    PubMed  CAS  Article  Google Scholar 

  105. Liu H, Stone SL (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22:2630–2641

    PubMed  CAS  Article  Google Scholar 

  106. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    PubMed  CAS  Article  Google Scholar 

  107. Lopez-Molina L, Chua NH (2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol 41:541–547

    PubMed  CAS  Google Scholar 

  108. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    PubMed  CAS  Article  Google Scholar 

  109. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17:410–418

    PubMed  CAS  Article  Google Scholar 

  110. Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    PubMed  CAS  Article  Google Scholar 

  111. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626

    PubMed  CAS  Article  Google Scholar 

  112. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    PubMed  CAS  Article  Google Scholar 

  113. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149

    PubMed  CAS  Article  Google Scholar 

  114. Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    PubMed  CAS  Article  Google Scholar 

  115. Menkens AE, Cashmore AR (1994) Isolation and characterization of a fourth Arabidopsis thaliana G-box-binding factor, which has similarities to Fos oncoprotein. Proc Natl Acad Sci USA 91:2522–2526

    PubMed  CAS  Article  Google Scholar 

  116. Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci 20:506–510

    PubMed  CAS  Article  Google Scholar 

  117. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 106:5418–5423

    PubMed  CAS  Article  Google Scholar 

  118. Mizuno T, Yamashino T (2008) Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol 49:481–487

    PubMed  CAS  Article  Google Scholar 

  119. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    PubMed  CAS  Article  Google Scholar 

  120. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665

    PubMed  CAS  Article  Google Scholar 

  121. Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60:51–68

    PubMed  CAS  Article  Google Scholar 

  122. Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (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

    PubMed  CAS  Article  Google Scholar 

  123. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    PubMed  CAS  Article  Google Scholar 

  124. Nambara E, Suzuki M, Abrams S, McCarty DR, Kamiya Y, McCourt P (2002) A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana. Genetics 161:1247–1255

    PubMed  CAS  Google Scholar 

  125. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    PubMed  CAS  Article  Google Scholar 

  126. Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475

    PubMed  CAS  Article  Google Scholar 

  127. Nováková M, Motyka V, Dobrev PI, Malbeck J, Gaudinová A, Vanková R (2005) Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Exp Bot 56:2877–2883

    PubMed  Article  Google Scholar 

  128. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    PubMed  CAS  Article  Google Scholar 

  129. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    PubMed  CAS  Article  Google Scholar 

  130. Pandey GK, Grant JJ, Cheong YH, Kim BG, Li L, Luan S (2005) ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol 139:1185–1193

    PubMed  CAS  Article  Google Scholar 

  131. Pauwels L, Goossens A (2008) Fine-tuning of early events in the jasmonate response. Plant Signal Behav 3:846–847

    PubMed  Article  Google Scholar 

  132. Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, Inzé D, Goossens A (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci USA 105:1380–1385

    PubMed  CAS  Article  Google Scholar 

  133. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    PubMed  CAS  Article  Google Scholar 

  134. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    PubMed  CAS  Article  Google Scholar 

  135. Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429

    Google Scholar 

  136. Romanel EA, Schrago CG, Counago RM, Russo CA, Alves-Ferreira M (2009) Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS One 4:e5791

    PubMed  Article  CAS  Google Scholar 

  137. Rushton PJ, Reinstadler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14:749–762

    PubMed  CAS  Article  Google Scholar 

  138. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    PubMed  CAS  Article  Google Scholar 

  139. Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell 20:2972–2988

    PubMed  CAS  Article  Google Scholar 

  140. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    PubMed  CAS  Article  Google Scholar 

  141. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    PubMed  CAS  Article  Google Scholar 

  142. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    PubMed  CAS  Article  Google Scholar 

  143. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291

    PubMed  CAS  Article  Google Scholar 

  144. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151:275–289

    PubMed  CAS  Article  Google Scholar 

  145. Shen Q, Zhang P, Ho TH (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

    PubMed  CAS  Article  Google Scholar 

  146. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    PubMed  CAS  Article  Google Scholar 

  147. Siefers N, Dang KK, Kumimoto RW, Bynum WE 4th, Tayrose G, Holt BF 3rd (2009) Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol 149:625–641

    PubMed  CAS  Article  Google Scholar 

  148. Skriver K, Olsen FL, Rogers JC, Mundy J (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88:7266–7270

    PubMed  CAS  Article  Google Scholar 

  149. Smalle J, Kurepa J, Yang P, Emborg TJ, Babiychuk E, Kushnir S, Vierstra RD (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15:965–980

    PubMed  CAS  Article  Google Scholar 

  150. Söderman E, Mattsson J, Engström P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10:375–381

    PubMed  Article  Google Scholar 

  151. Söderman E, Hjellström M, Fahleson J, Engström P (1999) The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Mol Biol 40:1073–1083

    PubMed  Article  Google Scholar 

  152. Sokol A, Kwiatkowska A, Jerzmanowski A, Prymakowska-Bosak M (2007) Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta 227:245–254

    PubMed  CAS  Article  Google Scholar 

  153. Son O, Hur YS, Kim YK, Lee HJ, Kim S, Kim MR, Nam KH, Lee MS, Kim BY, Park J, Lee SC, Hanada A, Yamaguchi S, Lee IJ, Kim SK, Yun DJ, Soderman E, Cheon CI (2010) ATHB12, an ABA-inducible homeodomain-leucine zipper (HD-Zip) protein of Arabidopsis, negatively regulates the growth of the inflorescence stem by decreasing the expression of a gibberellin 20-oxidase gene. Plant Cell Physiol 51:1537–1547

    PubMed  CAS  Article  Google Scholar 

  154. Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    PubMed  CAS  Article  Google Scholar 

  155. Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133

    PubMed  CAS  Article  Google Scholar 

  156. Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18:3415–3428

    PubMed  CAS  Article  Google Scholar 

  157. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    PubMed  CAS  Article  Google Scholar 

  158. Suzuki M, McCarty DR (2008) Functional symmetry of the B3 network controlling seed development. Curr Opin Plant Biol 11:548–553

    PubMed  CAS  Article  Google Scholar 

  159. Suzuki M, Kao CY, McCarty DR (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9:799–807

    PubMed  CAS  Article  Google Scholar 

  160. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 8:1749–1770

    Article  CAS  Google Scholar 

  161. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    PubMed  CAS  Article  Google Scholar 

  162. Tran LS, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, Maruyama K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2007) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49:46–63

    PubMed  CAS  Article  Google Scholar 

  163. 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

    PubMed  CAS  Article  Google Scholar 

  164. Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078

    PubMed  CAS  Article  Google Scholar 

  165. Wang Y, Zhang W, Li K, Sun F, Han C, Wang Y, Li X (2008) Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana. J Plant Res 121:87–96

    PubMed  Article  Google Scholar 

  166. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217

    PubMed  CAS  Article  Google Scholar 

  167. Weiner JJ, Peterson FC, Volkman BF, Cutler SR (2010) Structural and functional insights into core ABA signaling. Curr Opin Plant Biol 13:495–502

    PubMed  CAS  Article  Google Scholar 

  168. Yadav V, Mallappa C, Gangappa SN, Bhatia S, Chattopadhyay S (2005) A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell 17:1953–1966

    PubMed  CAS  Article  Google Scholar 

  169. Yamagishi K, Tatematsu K, Yano R, Preston J, Kitamura S, Takahashi H, McCourt P, Kamiya Y, Nambara E (2009) CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant Cell Physiol 50:330–340

    PubMed  CAS  Article  Google Scholar 

  170. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    PubMed  CAS  Article  Google Scholar 

  171. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    PubMed  CAS  Article  Google Scholar 

  172. Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    PubMed  Article  CAS  Google Scholar 

  173. Yano R, Kanno Y, Jikumaru Y, Nakabayashi K, Kamiya Y, Nambara E (2009) CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid-mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiol 151:641–654

    PubMed  CAS  Article  Google Scholar 

  174. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) 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 61:672–685

    PubMed  CAS  Article  Google Scholar 

  175. Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082

    PubMed  CAS  Article  Google Scholar 

  176. Zhang W, Ruan J, Ho TH, You Y, Yu T, Quatrano RS (2005) Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid- and abiotic stress-responsive genes in Arabidopsis thaliana. Bioinformatics 21:3074–3081

    PubMed  CAS  Article  Google Scholar 

  177. Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    PubMed  CAS  Article  Google Scholar 

  178. Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21:2563–2577

    PubMed  CAS  Article  Google Scholar 

  179. Zhou X, Hua D, Chen Z, Zhou Z, Gong Z (2009) Elongator mediates ABA responses, oxidative stress resistance and anthocyanin biosynthesis in Arabidopsis. Plant J 60:79–90

    PubMed  CAS  Article  Google Scholar 

  180. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    PubMed  CAS  Article  Google Scholar 

  181. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    PubMed  CAS  Article  Google Scholar 

  182. Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12

    PubMed  CAS  Article  Google Scholar 

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Acknowledgments

We would like to thank Masami Toyoshima (JIRCAS) for skillful editorial assistance and for helping to prepare the figures and table as well as Junro Mogami and Naohiko Ohama for helping to gather the information. We also thank Takuya Yoshida and Hironori Takasaki for comments. This work was supported by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN); the Ministry of Agriculture, Forestry and Fisheries (MAFF); Grants-in-Aid for Scientific Research by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) and the Japan Society for the Promotion of Science (JSPS).

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  1. Biological Resources Division, Japan International Research Center for Agricultural Sciences (JIRCAS), 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan

    Yasunari Fujita & Kazuko Yamaguchi-Shinozaki

  2. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Yasunari Fujita

  3. Plant Science Center, RIKEN Yokohama Institute, Yokohama, Kanagawa, 230-0045, Japan

    Miki Fujita & Kazuo Shinozaki

  4. Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657, Japan

    Kazuko Yamaguchi-Shinozaki

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  1. Yasunari Fujita
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  2. Miki Fujita
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  3. Kazuo Shinozaki
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Correspondence to Kazuko Yamaguchi-Shinozaki.

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Fujita, Y., Fujita, M., Shinozaki, K. et al. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124, 509–525 (2011). https://doi.org/10.1007/s10265-011-0412-3

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Keywords

  • Abscisic acid (ABA)
  • Arabidopsis
  • Dehydration
  • Osmotic stress
  • Stress response
  • Transcription factor