Plant Molecular Biology

, Volume 60, Issue 1, pp 51–68 | Cite as

Transcriptional Regulation of ABI3- and ABA-responsive Genes Including RD29B and RD29A in Seeds, Germinating Embryos, and Seedlings of Arabidopsis

  • Kazuo Nakashima
  • Yasunari Fujita
  • Koji Katsura
  • Kyonoshin Maruyama
  • Yoshihiro Narusaka
  • Motoaki Seki
  • Kazuo Shinozaki
  • Kazuko Yamaguchi-ShinozakiEmail author


ABA-responsive elements (ABREs) are cis-acting elements and basic leucine zipper (bZIP)-type ABRE-binding proteins (AREBs) are transcriptional activators that function in the expression of RD29B in vegetative tissue of Arabidopsis in response to abscisic acid (ABA) treatment. Dehydration-responsive elements (DREs) function as coupling elements of ABRE in the expression of RD29A in response to ABA. Expression analysis using abi3 and abi5 mutants showed that ABI3 and ABI5 play important roles in the expression of RD29B in seeds. Base-substitution analysis showed that two ABREs function strongly and one ABRE coupled with DRE functions weakly in the expression of RD29A in embryos. In a transient transactivation experiment, ABI3, ABI5 and AREB1 activated transcription of a GUS reporter gene driven by the RD29B promoter strongly but these proteins activated the transcription driven by the RD29A promoter weakly. In 35S::ABI3 Arabidopsis plants, the expression of RD29B was up-regulated strongly, but that of RD29A was up-regulated weakly. These results indicate that the expression of RD29B having ABREs in the promoter is up-regulated strongly by ABI3, whereas that of RD29A having one ABRE coupled with DREs in the promoter is up-regulated weakly by ABI3. We compared the expression of 7000 Arabidopsis genes in response to ABA treatment during germination and in the vegetative growth stage, and that in 35S::ABI3 plants using a full-length cDNA microarray. The expression of ABI3- and/or ABA-responsive genes and cis-elements in the promoters are discussed.


Arabidopsis ABA ABI3 ABRE DRE germinating embryo 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

Supp.pdf (246 kb)
Supplementary material


  1. Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K. 2003Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signalingPlant Cell.156378CrossRefPubMedGoogle Scholar
  2. Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., Giraudat, J., Parcy, F. 2002The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesisPlant Cell.1413911403CrossRefPubMedGoogle Scholar
  3. Brocard, I.M., Lynch, T. J., Finkelstein, R.R. 2002Regulation and role of the Arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress responsePlant Physiol.12915331543CrossRefPubMedGoogle Scholar
  4. Brocard-Gifford, I.M., Lynch, T.J., Finkelstein, R.R. 2003Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signalingPlant Physiol.1317892CrossRefPubMedGoogle Scholar
  5. Carles, C., Bies-Etheve, N., Aspart, L., Léon-Kloosterziel, K.M., Koornneef, M., Echeverria, M., Delseny, M. 2002Regulation of Arabidopsis thaliana Em genes: role of ABI5Plant J.3037383CrossRefPubMedGoogle Scholar
  6. Chinnusamy, V., Schumaker, K., Zhu, J.-K. 2004Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plantsJ. Exp. Bot.55225236PubMedGoogle Scholar
  7. Choi, H., Hong, J., Ha, J., Kang, J., Kim, S.Y. 2000ABFs, a family of ABA-responsive element binding factorsJ. Biol. Chem.2117231730Google Scholar
  8. Finkelstein, R.R., Gampala, S.S.L., Rock, C.D. 2002Abscisic acid signaling in seeds and seedlingsPlant Cell14S15S45PubMedGoogle Scholar
  9. Finkelstein, R., Lynch, T. 2000The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factorPlant Cell12599609CrossRefPubMedGoogle Scholar
  10. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., Tran, L.-S.P., Yamaguchi-Shinozaki, K., Shinozaki, K. 2004A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathwayPlant J.39863876CrossRefPubMedGoogle Scholar
  11. Gallie, D.R., Sleat, D.E., Watts, J.W., Turner, P.C., Wilson, T.M. 1988Mutational analysis of the tobacco mosaic virus 5′-leader for altered ability to enhance translationNucl. Acids Res.16883893PubMedGoogle Scholar
  12. Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F., Goodman, H.M. 1992Isolation of the Arabidopsis ABI3 gene by positional cloningPlant Cell412511261CrossRefPubMedGoogle Scholar
  13. Hattori, T., Totsuka, M., Hobo, T., Kagaya, Y., Yamamoto-Toyoda, A. 2002Experimentally determined sequence requirement of ACGT-containing abscisic acid response elementPlant Cell Physiol.43136140PubMedGoogle Scholar
  14. Hattori, T., Vasil, V., Rosenkrans, L., Hannah, L.C., McCarty, D.R., Vasil, I.K. 1992The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maizeGenes Dev.6609618PubMedGoogle Scholar
  15. Hobo, T., Asada, M., Kowyama, Y., Hattori, T. 1999ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalentPlant J.19679689CrossRefPubMedGoogle Scholar
  16. Jakoby, M. Weisshaar, B. Droge-Laser, W. Vicente-Carbajosa, J. Tiedemann, J. Kroj, T. Parcy, F. The bZIP Research Group 2002bZIP transcription factors in ArabidopsisTrends Plant Sci.7106111CrossRefPubMedGoogle Scholar
  17. Kagaya, Y., Okuda, R., Ban, A., Toyoshima, R., Tsutsumida, K., Usui, H., Yamamoto, A., Hattori, T. 2005Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in ArabidopsisPlant Cell Physiol.46300311PubMedGoogle Scholar
  18. Kang, J., Choi, H., Im, M., Kim, S.Y. 2002Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signalingPlant Cell14343357CrossRefPubMedGoogle Scholar
  19. Kao, C.-Y., Cocciolone, S.M., Vasil, I.K., McCarty, D.R. 1996Localization and interaction of the cis-acting elements for abscisic acid, VIVIPAROUS1, and light activation of the C1 gene of maizePlant Cell811711179CrossRefPubMedGoogle Scholar
  20. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K. 1998Two 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 ArabidopsisPlant Cell.1013911406PubMedGoogle Scholar
  21. Lopez-Molina, L., Chua, N.-H. 2000A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thalianaPlant Cell Physiol.41541547PubMedGoogle Scholar
  22. Lopez-Molina, L., Mongrand, S., Chua, N.-H. 2001A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in ArabidopsisProc. Natl. Acad. Sci. U.S.A.9847824787CrossRefPubMedGoogle Scholar
  23. Lopez-Molina, L., Mongrand, S., McLachlin, D.T., Chait, B.T., Chua, N.-H. 2002ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germinationPlant J.32317328CrossRefPubMedGoogle Scholar
  24. Maruyama, K., Sakuma, Y., Kasuga, M., Ito, Y., Seki, M., Goda, H., Shimada, Y., Yoshida, S., Shinozaki, K., Yamaguchi-Shinozaki, K. 2004Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systemsPlant J.38982993CrossRefPubMedGoogle Scholar
  25. McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M., Vasil, I.K. 1991The Viviparous-1developmental gene of maize encodes a novel transcriptional activatorCell66895905CrossRefPubMedGoogle Scholar
  26. Mitsuhara, I., Ugaki, M., Hirochika, H., Ohshima, M., Murakami, T., Gotoh, Y., Katayose, Y., Nakamura, S., Honkura, R., Nishimiya, S., Ueno, K., Mochizuki, A., Tanimoto, H., Tsugawa, H., Otsuki, Y., Ohashi, Y. 1996Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plantsPlant Cell Physiol.374959PubMedGoogle Scholar
  27. Monke, G., Altschmied, L., Tewes, A., Reidt, W., Mock, H.-P., Baumlein, H., Conrad, U. 2004Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNAPlanta219158166PubMedGoogle Scholar
  28. Nakamura, S., Lynch, T.J., Finkelstein, R.R. 2001Physical interactions between ABA response loci of ArabidopsisPlant J.26627635CrossRefPubMedGoogle Scholar
  29. Nakashima, K., Yamaguchi-Shinozaki, K. 2002Use of β-glucuronidase to show dehydration and high-salt gene expressionJackson, J.F.Linskens, H.F. eds. Molecular Methods of Plant Analysis, Vol.22: Testing for Genetic Manipulation in PlantsSpringer-VerlagHeidelberg3761Google Scholar
  30. Nakashima, K., Yamaguchi-Shinozaki, K. 2005Molecular studies on stress-responsive gene expression in Arabidopsis and improvement of stress tolerance in crop plants by regulon biotechnologyJARQ39221229Google Scholar
  31. Nambara, E., Keith, K., McCourt, P., Naito, S. 1994Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 genePlant Cell Physiol.35509513PubMedGoogle Scholar
  32. Narusaka, Y., Nakashima, K., Shinwari, Z.K., Sakuma, Y., Furihata, T., Abe, H., Narusaka, M., Shinozaki, K., Yamaguchi-Shinozaki, K. 2003Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stressesPlant J.34137148CrossRefPubMedGoogle Scholar
  33. Parcy, F., Valon, C., Raynal, M., Gaubier-Comella, P., Delseny, M., Giraudat, J. 1994Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acidPlant Cell615671582CrossRefPubMedGoogle Scholar
  34. Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., Yamaguchi-Shinozaki, K. 2002DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expressionBiochem Biophys Res Commun.2909981009CrossRefPubMedGoogle Scholar
  35. Satoh, R., Fujita, Y., Nakashima, K., Shinozaki, K., Yamaguchi-Shinozaki, K. 2004A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in ArabidopsisPlant Cell Physiol.45309317PubMedGoogle Scholar
  36. 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. 2002aMonitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarrayFunct. Integr. Genomics2282291Google Scholar
  37. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y., Shinozaki, K. 2002bMonitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarrayPlant J.31279292CrossRefGoogle Scholar
  38. Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., Muramatsu, M., Hayashizaki, Y., Kawai, J., Carninci, P., Itoh, M., Ishii, Y., Arakawa, T., Shibata, K., Shinagawa, A., Shinozaki, K. 2002cFunctional annotation of a full-length Arabidopsis cDNA collectionScience296141145CrossRefGoogle Scholar
  39. Shen, Q., Ho, T.-H.D. 1995Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting elementPlant Cell7295307CrossRefPubMedGoogle Scholar
  40. Shen, Q., Zhang, P., Ho, T.-H.D. 1996Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barleyPlant Cell811071119CrossRefPubMedGoogle Scholar
  41. Shen, Q.J., Casaretto, J.A., Zhang, P., Ho, T.-H.D. 2004Functional definition of ABA-response complexes: the promoter units necessary and sufficient for ABA induction of gene expression in barley (Hordeum vulgare L.)Plant Mol. Biol.54111124CrossRefPubMedGoogle Scholar
  42. Shinozaki, K., Yamaguchi-Shinozaki, K., Seki, M. 2003Regulatory network of gene expression in the drought and cold stress responsesCurr. Opin. Plant Biol.6410417PubMedGoogle Scholar
  43. Suzuki, M., Ketterling, M.G., Li, Q.-B., McCarty, D.R. 2003Viviparous1 alters global gene expression patterns through regulation of abscisic acid signalingPlant Physiol.13216641677CrossRefPubMedGoogle Scholar
  44. Tran, L.-S.P., Nakashima, K., Sakuma, Y., Simpson, S.D., Fujita, Y., Maruyama, K., Fujita, M., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K. 2004Isolation 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 promoterPlant Cell.1624812498CrossRefPubMedGoogle Scholar
  45. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., Yamaguchi-Shinozaki, K. 2000Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditionsProc. Natl. Acad. Sci. U.S.A.971163211637CrossRefPubMedGoogle Scholar
  46. Yamaguchi-Shinozaki, K., Shinozaki, K. 1993Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plantsMol. Gen. Genet.236331340CrossRefPubMedGoogle Scholar
  47. Yamaguchi-Shinozaki, K., Shinozaki, K. 1994A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stressPlant Cell6251264CrossRefPubMedGoogle Scholar
  48. Yamaguchi-Shinozaki, K., Shinozaki, K. 2005Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promotersTrends Plant Sci.108894PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Kazuo Nakashima
    • 1
  • Yasunari Fujita
    • 1
  • Koji Katsura
    • 1
  • Kyonoshin Maruyama
    • 1
  • Yoshihiro Narusaka
    • 1
  • Motoaki Seki
    • 2
    • 3
  • Kazuo Shinozaki
    • 2
    • 3
    • 4
  • Kazuko Yamaguchi-Shinozaki
    • 1
    • 4
    • 5
    • 6
    Email author
  1. 1.Biological Resources DivisionJapan International Research Center for Agricultural Sciences (JIRCAS)TsukubaJapan
  2. 2.Laboratory of Plant Molecular BiologyRIKEN Tsukuba InstituteTsukubaJapan
  3. 3.Plant Functional Genomics GroupRIKEN Genomic Science CenterYokohamaJapan
  4. 4.Core Research for Evolutional Science and Technology (CREST)Japan Science and Technology AgencyKawaguchiJapan
  5. 5.Laboratory of Plant Molecular Physiology, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  6. 6.Department of BiologyTokyo Gakugei UniversityTokyoJapan

Personalised recommendations