Microarray Analysis for Studying the Abiotic Stress Responses in Plants

  • Motoaki SekiEmail author
  • Masanori Okamoto
  • Akihiro Matsui
  • Jong-Myong Kim
  • Yukio Kurihara
  • Junko Ishida
  • Taeko Morosawa
  • Makiko Kawashima
  • Taiko Kim To
  • Kazuo Shinozaki


Plants respond and adapt to drought, high-salinity and cold stresses in order to survive. Molecular and genomic studies have shown that many genes with various functions are induced by drought, high-salinity and cold stresses, and that the various signaling factors including transcription factors are involved in the stress responses. The development of microarray-based expression profiling methods has allowed significant progress in the characterization of the plant stress response. Genetic engineering of the stress-inducible genes has become one of the promising strategies for the molecular breeding of the stress-tolerant plants. In this review, we highlight the application of the microarray analysis to the understanding of the plant abiotic stress responses and tolerance.


Transgenic Plant Cold Acclimation Freezing Tolerance Late Embryogenesis Abundant Abiotic Stress Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported in part by a grant for Genome Research from RIKEN, the Program for Promotion of Basic Research Activities for Innovative Biosciences, the Special Coordination Fund of the Science and Technology Agency, and a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MECSST) to K.S. It was also supported in part by a Grant-in-Aid for Scientific Research on Priority Areas “Systems Genomics” from MECSST and the President Discretionary Fund from RIKEN to M.S


  1. Abe H, Yamaguchi-Shinozaki K, Urao T et al. (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic-acid-regulated gene expression. Plant Cell 9:1859–1868PubMedCrossRefGoogle Scholar
  2. Abe H, Urao T, Ito T et al. (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78PubMedCrossRefGoogle Scholar
  3. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  4. Behnam B, Kikuchi A, Celebi-Toprak F et al. (2007) Arabidopsis rd29A::DREB2A enhances freezing tolerance in transgenic potato. Plant Cell Rep 26:1275–1282PubMedCrossRefGoogle Scholar
  5. Bhatnagar-Mathur P, Devi MJ, Reddy DS et al. (2007) Stress-inducible expression of AtDREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082PubMedCrossRefGoogle Scholar
  6. Boudsocq M, Lauriere C (2005) Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194PubMedCrossRefGoogle Scholar
  7. Bray EA (2002) Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot 89:803–811PubMedCrossRefGoogle Scholar
  8. Brazma A, Parkinson H, Sarkans U et al. (2003) ArrayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res 31:68–71PubMedCrossRefGoogle Scholar
  9. Brosche M, Vinocur B, Alatalo ER et al. (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101CrossRefGoogle Scholar
  10. Buchanan CD, Lim S, Salzman RA et al. (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58:699–720PubMedCrossRefGoogle Scholar
  11. Chandra Babu R, Zhang J, Blumc A et al. (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166:855–862CrossRefGoogle Scholar
  12. Chen W, Provart NJ, Glazebrook J et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574PubMedCrossRefGoogle Scholar
  13. Cheong YH, Chang HS, Gupta R et al. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677PubMedCrossRefGoogle Scholar
  14. Chini A, Grant J, Seki M et al. (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822PubMedCrossRefGoogle Scholar
  15. Chinnusamy V, Ohta M, Kannar S et al. (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054PubMedCrossRefGoogle Scholar
  16. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signaling in plants. J Exp Bot 55:225–236PubMedCrossRefGoogle Scholar
  17. Choi H, Hong JH, Ha J et al. (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730PubMedCrossRefGoogle Scholar
  18. Christensen CA, Feldmann KA (2007) Biotechnology approaches to engineering drought tolerant crops. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Dordrecht, pp 333–357CrossRefGoogle Scholar
  19. Cominelli E, Galbiati M, Vavasseur A et al. (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200PubMedCrossRefGoogle Scholar
  20. Cominelli E, Sala T, Calvi D et al. (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 15:1196–1200Google Scholar
  21. Cook D, Fowler S, Fiehn O et al. (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci U S A 101:15243–15248PubMedCrossRefGoogle Scholar
  22. Cramer GR, Ergul A, Grimplet J et al. (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134PubMedCrossRefGoogle Scholar
  23. Davletova S, Schlauch K, Coutu J et al. (2005) The Zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856PubMedCrossRefGoogle Scholar
  24. De Block M, Verduyn C, Brouwer DD et al. (2005) Poly (ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95–106PubMedCrossRefGoogle Scholar
  25. Dubouzet JG, Sakuma Y, Ito Y et al. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763PubMedCrossRefGoogle Scholar
  26. Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210Google Scholar
  27. 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 14:1675–1690PubMedCrossRefGoogle Scholar
  28. Fujita M, Fujita Y, Maruyama K et al. (2004) A dehydration-induced NAC protein, RD26 is involved in ABA-dependent stress signaling pathway. Plant J 39:863–876PubMedCrossRefGoogle Scholar
  29. Fujita Y, Fujita M, Sato R et al. (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488PubMedCrossRefGoogle Scholar
  30. Fujita M, Mizukado S, Fujita Y et al. (2007) Identification of stress-tolerance-related transcription-­factor genes via mini-scale full-length cDNA over-expressor (FOX) gene hunting system. Biochem Biophys Res Commun 364:250–257PubMedCrossRefGoogle Scholar
  31. Furihata T, Maruyama K, Fujita Y et al. (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993PubMedCrossRefGoogle Scholar
  32. Gong Q, Li P, Ma S et al. (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839PubMedCrossRefGoogle Scholar
  33. Gu R, Fonseca S, Puskas LG et al. (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276PubMedGoogle Scholar
  34. Gulick PJ, Drouin S, Yu Z et al. (2005) Transcriptome comparison of winter and spring wheat responding to low temperature. Genome 48:913–923PubMedGoogle Scholar
  35. Hazen SP, Wu Y, Kreps JA (2003) Gene expression profiling of plant responses to abiotic stress. Funct Integr Genomics 3:105–111PubMedCrossRefGoogle Scholar
  36. Hong B, Tong Z, Ma N et al. (2006) Heterologous expression of the AtDREB1A gene in chrysanthemum increases drought and salt stress tolerance. Sci China C Life Sci 49:436–445PubMedCrossRefGoogle Scholar
  37. Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487PubMedCrossRefGoogle Scholar
  38. Hwang EW, Kim KA, Park SC et al. (2005) Expression profiles of hot pepper (Capsicum annuum) genes under cold stress conditions. J Biosci 30:657–667PubMedCrossRefGoogle Scholar
  39. Iida K, Seki M, Sakurai T et al. (2004) Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res 32:5096–5103PubMedCrossRefGoogle Scholar
  40. Iida K, Seki M, Sakurai T et al. (2005) RARTF: database and tools for complete sets of Arabidopsis transcription factors. DNA Res 12:247–256PubMedCrossRefGoogle Scholar
  41. Inan G, Zhang Q, Li P et al. (2004) Salt Cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737PubMedCrossRefGoogle Scholar
  42. Ito Y, Katsura K, Maruyama K et al. (2006) Functional analysis of rice DREB1/CBF-type transcription factors Involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153PubMedCrossRefGoogle Scholar
  43. Iuchi S, Kobayashi M, Taji T et al. (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis, in Arabidopsis. Plant J 27:325–333PubMedCrossRefGoogle Scholar
  44. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG et al. (1998) Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280:104–106PubMedCrossRefGoogle Scholar
  45. Jaglo-Ottosen KR, Kleff S, Amundsen KL et al. (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917CrossRefGoogle Scholar
  46. Kamei A, Seki M, Umezawa T et al. (2005) Analysis of gene expression profiles in Arabidopsis salt overly sensitive mutants, sos2 and sos3 mutants. Plant Cell Environ 28:1267–1275CrossRefGoogle Scholar
  47. Kang JY, Choi HI, Im MY et al. (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357PubMedCrossRefGoogle Scholar
  48. Kasuga M, Liu Q, Miura S et al. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291PubMedCrossRefGoogle Scholar
  49. Kasukabe Y, He L, Nada K et al. (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and upregulates the expression of various stress-­regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722PubMedCrossRefGoogle Scholar
  50. Kawasaki S, Borchert C, Deyholos M et al. (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905PubMedCrossRefGoogle Scholar
  51. Kawaura K, Mochida K, Yamazaki Y et al. (2006) Transcriptome analysis of salinity stress responses in common wheat using a 22k oligo-DNA microarray. Funct Integr Genomics 6:132–142PubMedCrossRefGoogle Scholar
  52. Kim JM, Kim-To T, Ishida J et al. (2008) Alterations of lysine modifications on histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588PubMedCrossRefGoogle Scholar
  53. Kreps JA, Wu Y, Chang HS et al. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141PubMedCrossRefGoogle Scholar
  54. Lan L, Li M, Lai Y et al. (2005) Microarray analysis reveals similarities and variations in genetic programs controlling pollination/fertilization and stress responses in rice (Oryza sativa L.). Plant Mol Biol 59:151–164PubMedCrossRefGoogle Scholar
  55. Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175PubMedCrossRefGoogle Scholar
  56. Lee BH, Kapoor A, Zhu J et al. (2006) STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18:1736–1749PubMedCrossRefGoogle Scholar
  57. Liu Q, Kasuga M, Sakuma Y et al. (1998) The 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 10:1391–1406PubMedCrossRefGoogle Scholar
  58. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945PubMedCrossRefGoogle Scholar
  59. Liu J, Ishitani M, Halfter U et al. (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A 97:3730–3734PubMedCrossRefGoogle Scholar
  60. Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA-binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366PubMedCrossRefGoogle Scholar
  61. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  62. Mantri NL, Ford R, Coram TE et al. (2007) Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics 8:303PubMedCrossRefGoogle Scholar
  63. Margulies M, Egholm M, Altman WE et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  64. Maruyama K, Sakuma Y, Kasuga M et al. (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993PubMedCrossRefGoogle Scholar
  65. Matsui A, Ishida J, Morosawa T et al. (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149PubMedCrossRefGoogle Scholar
  66. Nishimura N, Kitahata N, Seki M et al. (2005) Analysis of ABA Hypersensitive Germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984PubMedCrossRefGoogle Scholar
  67. Noutoshi Y, Ito T, Seki M et al. (2005) A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY type disease resistance protein SLH1 (SENSITIVE TO LOW HUMIDITY 1) causes activation of defense responses and hypersensitive cell death. Plant J 43:873–888PubMedCrossRefGoogle Scholar
  68. Obayashi T, Kinoshita K, Nakai K et al. (2006) ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res 35:D863–D869CrossRefGoogle Scholar
  69. Osakabe Y, Maruyama K, Seki M et al. (2005) An LRR receptor kinase, RPK1, is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17:1105–1119PubMedCrossRefGoogle Scholar
  70. Oztur ZN, Talame V, Deyholos M et al. (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573PubMedCrossRefGoogle Scholar
  71. Papp I, Mur LA, Dalmadi A et al. (2004) A mutation in the Cap Binding Protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol Biol 55:679–686PubMedCrossRefGoogle Scholar
  72. Rabbani MA, Maruyama K, Abe H et al. (2003) Monitoring expression profiles of rice (Oryza sativa L.) genes under cold, drought and high-salinity stresses, and ABA application using both cDNA microarray and RNA gel blot analyses. Plant Physiol 133:1755–1767PubMedCrossRefGoogle Scholar
  73. Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151PubMedCrossRefGoogle Scholar
  74. Rensink WA, Lobst S, Hart A et al. (2005) Gene expression profiling of potato responses to cold, heat, and salt stress. Funct Integr Genomics 5:201–207PubMedCrossRefGoogle Scholar
  75. Richmond T, Somerville S (2000) Chasing the dream: plant EST microarrays. Curr Opin Plant Biol 3:108–116PubMedCrossRefGoogle Scholar
  76. Riechmann JL, Heard J, Martin G et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110PubMedCrossRefGoogle Scholar
  77. Rizhsky L, Liang H, Shuman J et al. (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Proc Natl Acad Sci U S A 134:1683–1696Google Scholar
  78. Sahin-Cevik M, Moore GA (2006) Identification and expression analysis of cold-regulated genes from the cold-hardy Citrus relative Poncirus trifoliate (L.) Raf. Plant Mol Biol 62:83–97PubMedCrossRefGoogle Scholar
  79. Sakuma Y, Liu Q, Dubouzet JG et al. (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 290:998–1009PubMedCrossRefGoogle Scholar
  80. Sakuma Y, Maruyama K, Osakabe Y et al. (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedCrossRefGoogle Scholar
  81. Sakuma Y, Maruyama K, Qin F et al. (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci U S A 103:18822–18827PubMedCrossRefGoogle Scholar
  82. Savitch LV, Allard G, Seki M et al. (2005) The effects of overexpression of two Brassica CBF/DREB1-like transcription factors on phytosynthetic capacity and freezing tolerance in Brassica napus. Plant Cell Physiol 46:1525–1539PubMedCrossRefGoogle Scholar
  83. Seki M, Narusaka M, Abe H et al. (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses using a full-length cDNA microarray. Plant Cell 13:61–72PubMedCrossRefGoogle Scholar
  84. Seki M, Narusaka M, Ishida J et al. (2002a) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold, and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedCrossRefGoogle Scholar
  85. Seki M, Ishida J, Narusaka M et al. (2002b) Monitoring the expression pattern of ca. 7000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291PubMedCrossRefGoogle Scholar
  86. Seki M, Kamei A, Satou M et al. (2003) Transcriptomeanalysis in abiotic stress conditions in higher plants. Topics Curr Genet 4:271–295Google Scholar
  87. Seki M, Satou M, Sakurai T et al. (2004) RIKEN Arabidopsis full-length (RAFL) cDNA and its applications for expression profiling under abiotic stress conditions. J Exp Bot 55:213–223PubMedCrossRefGoogle Scholar
  88. Seki M, Ishida J, Nakajima M et al. (2005) Genomic analysis of stress response. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress. Blackwell, Sheffield, pp 248–265CrossRefGoogle Scholar
  89. Seki M, Umezawa T, Kim JM et al. (2007) Transcriptome analysis of plant drought and salt stress response. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer Publishing, Dordrecht, pp 261–283CrossRefGoogle Scholar
  90. Shi H, Lee BH, Wu SJ et al. (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85PubMedCrossRefGoogle Scholar
  91. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223PubMedGoogle Scholar
  92. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417PubMedCrossRefGoogle Scholar
  93. Simpson SD, Nakashima K, Narusaka Y et al. (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270PubMedCrossRefGoogle Scholar
  94. Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic responses in Arabidopsis. Plant J 46:124–133PubMedCrossRefGoogle Scholar
  95. Stockinger EJ, Mao Y, Regier MK et al. (2001) Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res 29:1524–1533PubMedCrossRefGoogle Scholar
  96. Stolc V, Samanta MP, Tongprasit W et al. (2005) Identification of transcribed sequences in Arabidopsis thaliana by using high-resolution genome tiling arrays. Proc Natl Acad Sci U S A 102:4453–4458Google Scholar
  97. Sunkar R, Chinnusamy V, Zhu J et al. (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309PubMedCrossRefGoogle Scholar
  98. Taji T, Ohsumi C, Iuchi S et al. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  99. Taji T, Seki M, Satou M et al. (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using arabidopsis microarray. Plant Physiol 135:1697–1709PubMedCrossRefGoogle Scholar
  100. Teige M, Scheikl E, Eulgem T et al. (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152PubMedCrossRefGoogle Scholar
  101. Tokimatsu T, Sakurai N, Suzuki H et al. (2005) KaPPA-View. A web-based analysis tool for integration of transcript and metabolite data on plant metabolic pathway maps. Plant Physiol 138:1289–1300Google Scholar
  102. Tran LSP, Nakashima K, Sakuma Y et al. (2004) Functional analysis of Arabidopsis NAC transcription factors controlling expression of erd1 gene under drought stress. Plant Cell 16:2481–2498PubMedCrossRefGoogle Scholar
  103. Tran LSP, Nakashima K, Sakuma Y et al. (2007a) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49:46–63PubMedCrossRefGoogle Scholar
  104. Tran LSP, Urao T, Qin F et al. (2007b) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci U S A 104:20623–20628PubMedCrossRefGoogle Scholar
  105. Ulm R, Ichimura K, Mizoguchi T et al. (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21:6483–6493PubMedCrossRefGoogle Scholar
  106. Umezawa T, Yoshida R, Maruyama K et al. (2004) 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 101:17306–17311PubMedCrossRefGoogle Scholar
  107. Umezawa T, Fujita M, Fujita Y et al. (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122PubMedGoogle Scholar
  108. Uno Y, Furihata T, Abe H et al. (2000) Arabidopsis basic leucing zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 97:11632–11637PubMedCrossRefGoogle Scholar
  109. Urao T, Yakubov B, Satoh R et al. (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754PubMedCrossRefGoogle Scholar
  110. Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195PubMedCrossRefGoogle Scholar
  111. Vanderauwera S, De Block M, Van de Steene N et al. (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci U S A 104:15150–15155PubMedCrossRefGoogle Scholar
  112. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132PubMedCrossRefGoogle Scholar
  113. Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15:626–638PubMedCrossRefGoogle Scholar
  114. Vogel JT, Zarka DG, Van Buskirk HA et al. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211PubMedCrossRefGoogle Scholar
  115. Wang H, Miyazaki S, Kawai K et al. (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52:873–891PubMedCrossRefGoogle Scholar
  116. Watkinson JI, Sioson AA, Vasquez-Robinet C et al. (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133:1702–1716PubMedCrossRefGoogle Scholar
  117. Wong CE, Li Y, Labbe A et al. (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450PubMedCrossRefGoogle Scholar
  118. Xin Z, Browse J (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci U S A 95:7799–7804PubMedCrossRefGoogle Scholar
  119. Xin Z, Mandaokar A, Chen J et al. (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49:786–799PubMedCrossRefGoogle Scholar
  120. Xiong L, Gong Z, Rock CD et al. (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1:771–781PubMedCrossRefGoogle Scholar
  121. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell Suppl S165–183Google Scholar
  122. Yamada K, Lim J, Dale JM et al. (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846.PubMedCrossRefGoogle Scholar
  123. Yamada M, Morishita H, Urano K et al. (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981PubMedCrossRefGoogle Scholar
  124. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94PubMedCrossRefGoogle Scholar
  125. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803PubMedCrossRefGoogle Scholar
  126. Yu LX, Setter TL (2003) Comparative transcriptional profiling of placenta and endosperm in developing maize kernels in response to water defecit. Plant Physiol 131:568–582PubMedCrossRefGoogle Scholar
  127. Zhang JZ (2003) Overexpression analysis of plant transcription factors. Curr Opin Plant Biol 6:430–440PubMedCrossRefGoogle Scholar
  128. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  129. Zhu J, Shi H, Lee BH et al. (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci U S A 101:9873–9878PubMedCrossRefGoogle Scholar
  130. Zhu J, Verslues PE, Zheng X et al. (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci U S A 102:9966–9971PubMedCrossRefGoogle Scholar
  131. Zimmermann P, Hirsch-Hoffmann M, Hennig L et al. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Motoaki Seki
    • 1
    • 2
    Email author
  • Masanori Okamoto
    • 1
  • Akihiro Matsui
    • 1
  • Jong-Myong Kim
    • 1
  • Yukio Kurihara
    • 1
  • Junko Ishida
    • 1
  • Taeko Morosawa
    • 1
  • Makiko Kawashima
    • 1
  • Taiko Kim To
    • 1
  • Kazuo Shinozaki
    • 3
  1. 1.Plant Genomic Network Research Team, Plant Functional Genomics Research Group, RIKEN Plant Science Center (PSC), RIKEN Yokohama InstituteTsurumi-kuJapan
  2. 2.Kihara Institute for Biological Research, Yokohama City UniversityTotsuka-kuJapan
  3. 3.Gene Discovery Research Team, Gene Discovery Research Group, RIKEN Plant Science Center (PSC), RIKEN Tsukuba InstituteTsukubaJapan

Personalised recommendations