Russian Journal of Plant Physiology

, Volume 66, Issue 4, pp 521–529 | Cite as

The ABA- and Stress-Induced Expression of the ArabidopsisthalianaAt4g0180 Gene Is Determined by the Cis-Elements Responsible for Binding the ABA-Dependent Trans-Factors

  • N. V. Vinogradov
  • A. A. Andreeva
  • M. N. Danilova
  • A. S. Doroshenko
  • N. V. KudryakovaEmail author
  • V. V. Kusnetsov


In silico analysis of the promoter region of the At4g01870 gene of Arabidopsis thaliana (L.) Heynh. showed the presence of ABRE, W-box, RAV1-A, MYB, and LFY cis-elements in the sequence. These regulatory motifs bind the transcription factors involved in responses to abscisic acid (ABA) and stresses. Stable transgenic plants carrying the β-glucuronidase gene under the control of the 5'-deletion fragments of the At4g01870 promoter were obtained. According to the results of histochemical staining of transformants, gene expression was induced by abiotic stress and was most significant in the conductive tissues of the root, leaves, and sepals as well as in flowers. The study of At4g01870 gene expression by RT-PCR confirmed that the gene transcript content increased after the exposure of plants to a solution of NaCl or at 37°C and after ABA treatment; however, hypothermia almost unchanged the level of accumulation of the transcripts. Along with ABA, expression of the At4g01870 gene was induced by indolylacetic and salicylic acids and ethylene precursor 1-aminocyclopropane-1-carboxylic acid; it was hardly regulated by methyl jasmonate and inhibited by cytokinin. The TolB-like protein, encoded by the At4g01870 gene, functions as a type of platform, based on which protein complexes are assembled. Given the previously identified ABA-binding properties of the protein At4g01870 and the presence of the ABA-dependent cis-elements in the promoter of its coding gene, it can be assumed that the protein encoded by the At4g01870 gene allows to control the hormonal signals in the cell, providing a structural platform for the interaction of specific effector proteins, trans-factors and ion channels.


Arabidopsis thaliana abscisic acid cis-elements regulation of gene expression At4g01870 gene 



This study was supported by the Russian Science Foundation (project no. 14-14-00584).


The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.


  1. 1.
    Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R.K., Kumar, V., Verma, R., Upadhyay, R.G., Pandey, M., and Sharma, S., Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects, Front. Plant Sci., 2017, vol. 8: 161.Google Scholar
  2. 2.
    Hubbard, K.E., Nishimura, N., Hitomi, K., Getzoff, E.D., and Schroeder, J.I., Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions, Genes Dev., 2010, vol. 24, pp. 1695–1708.CrossRefGoogle Scholar
  3. 3.
    Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., and Zhu, J.K., In vitro reconstitution of an abscisic signalling pathway, Nature, 2009, vol. 462, pp. 660–664.CrossRefGoogle Scholar
  4. 4.
    Fujita, Y., Yoshida, T., and Yamaquchi-Shinozaki, K., Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants, Physiol. Plant., 2013, vol. 147, pp. 15–27.CrossRefGoogle Scholar
  5. 5.
    Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., and Lepiniec, L., MYB transcription factors in Arabidopsis, Trends Plant Sci., 2010, vol. 15, pp. 573–581.CrossRefGoogle Scholar
  6. 6.
    Bakshi, M. and Oelmüller, R., WRKY transcription factors: Jack of many trades in plants, Plant Signal. Behav., 2014, vol. 9: e27700.CrossRefGoogle Scholar
  7. 7.
    Demidenko, A.V., Kudryakova, N.V., Karavaiko, N.N., Kazakov, A.S., Cherepneva, G.N., Shevchenko, G.V., Permyakov, S.E., Kulaeva, O.N., Oelmüller, R., and Kusnetsov, V.V., The ABA-binding protein AA1 of Lu-pinus luteus is involved in ABA-mediated responses, Russ. J. Plant Physiol., 2015, vol. 62, pp. 161–170.CrossRefGoogle Scholar
  8. 8.
    Bonsor, D.A., Hecht, O., Vankemmelbeke, M., Sharma, A., Krachler, A.M., Housden, N.G., Lilly, K.J., Moore, G.R., and Kleanthous, C., Allosteric β-propeller signaling in TolB and its manipulation by translocating colicins, EMBO J., 2009, vol. 28, pp. 2846–2857.CrossRefGoogle Scholar
  9. 9.
    Bartashevich, D.A., Karavaiko, N.N., and Kusnetsov, V.V., The novel ABA-binding protein encoded by At4g01870 gene in A. thaliana is able to interact with RNA in vitro, Dokl. Biochem. Biophys., 2014, vol. 457, pp. 128–131.CrossRefGoogle Scholar
  10. 10.
    Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D’Angelo, C., Bornberg-Bauer, E., Kudla, J., and Harter, K., The AtGenE-xpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses, Plant J., 2007, vol. 50, pp. 347–363.CrossRefGoogle Scholar
  11. 11.
    Clough, S.J. and Bent, A.F., Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana, Plant J., 1988, vol. 16, pp. 735–743.CrossRefGoogle Scholar
  12. 12.
    Jefferson, R.A., Kavanagh, T.A., and Bevan, M.V., GUS-fusions: beta-glucuronidase as a sensitive and versalite gene fusion marker in higher plants, EMBO J., 1987, vol. 6, pp. 3901–3907.CrossRefGoogle Scholar
  13. 13.
    Vitha, S., Benes, K., Phillips, J.P., and Gartland, K.M.A., Histochemical GUS analysis, Methods Mol. Biol., 1995, vol. 44, pp. 185–193.Google Scholar
  14. 14.
    Danilova, M.N., Kudryakova, N.V., Voronin, P.Yu., Oelmüller, R., Kusnetsov, V.V., and Kulaeva, O.N., Membrane receptors of cytokinin and their regulatory role in Arabidopsis thaliana plant response to photooxidative stress under conditions of water deficit, Russ. J. Plant Physiol., 2014, vol. 61, pp. 434–442.CrossRefGoogle Scholar
  15. 15.
    Yilmaz, A., Mejia-Guerra, M.K., Kurz, K., Liang, X., Welch, L., and Grotewold, E., AGRIS: Arabidopsis Gene Regulatory Information Server, an update, Nucleic Acids Res., 2011, vol. 39, database issue, pp. 1118–1122.Google Scholar
  16. 16.
    Kim, J.B., Kang, J.Y., and Kim, S.Y., Over-expression of a transcription factor regulating ABA responsive gene expression confers multiple stress tolerance, Plant Biotech. J., 2004, vol. 2, pp. 459–466.CrossRefGoogle Scholar
  17. 17.
    Tuteja, N., Abscisic acid and abiotic stress, Plant Signal. Behav., 2007, vol. 2, pp. 135–138.CrossRefGoogle Scholar
  18. 18.
    Roy, S., Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome, Plant Signal. Behav., 2016, vol. 11: e1117723.CrossRefGoogle Scholar
  19. 19.
    Shinozaki, K. and Yamaguchi-Shinozaki, K., Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 217–223.CrossRefGoogle Scholar
  20. 20.
    Lamb, R.S., Hill, T.A., Tan, Q.K.G., and Irish, V.F., Regulation of APETALA3 floral homeotic gene expression by meristem identity genes, Development, 2002, vol. 129, pp. 2079–2086.Google Scholar
  21. 21.
    Weigel, D., Alvarez, J., Smyth, D.R., Yanofsky, M.F., and Meyerowitz, E.M., LEAFY controls floral meristem identity in Arabidopsis, Cell, 1992, vol. 69, pp. 643–659.CrossRefGoogle Scholar
  22. 22.
    Feng, C.Z., Chen, Y., Wang, C., Kong, Y.H., Wu, W.H., and Chen, Y.F., Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development, Plant J., 2014, vol. 80, pp. 654–668.CrossRefGoogle Scholar
  23. 23.
    Fu, M., Kang, H.K., Son, S.H., Kim, S.K., and Nam, K.H., A subset of Arabidopsis RAV transcription factors modulates drought and salt stress responses independent of ABA, Plant Cell Physiol., 2014, vol. 55, pp. 1892–1904.CrossRefGoogle Scholar
  24. 24.
    Hu, Y.X., Wang, Y.H., Liu, X.F., and Li, J.Y., Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development, Cell Res., 2004, vol. 14, pp. 8–15.CrossRefGoogle Scholar
  25. 25.
    Woo, H.R., Kim, J.H., Kim, J.Y., Kim, J.G., Lee, U., Song, I.J., Kim, J.H., Lee, H.Y., Nam, H.G., and Lim, P.O., The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis, J. Exp. Bot., 2010, vol. 61, pp. 3947–3957.CrossRefGoogle Scholar
  26. 26.
    Mueller, S., Hilbert, B., Dueckershoff, K., Roitsch, T., Krischke, M., Mueller, M.J., and Berger, S., General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in A-rabidopsis, Plant Cell, 2008, vol. 20, pp. 68–85.CrossRefGoogle Scholar
  27. 27.
    Shang, Y., Yan, L., Liu, Z.Q., Cao, Z., Mei, C., Xin, Q., Wu, F.Q., Wang, X.F., Du, S.Y., Jiang, T., Zhang, X.F., Zhao, R., Sun, H.L., Liu, R., Yu, Y.T., et al., The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition, Plant Cell, 2010, vol. 22, pp. 1909–1935.CrossRefGoogle Scholar
  28. 28.
    Vinogradov, N.V., Danilova, M.V., Kudryakova, N.V., Kusnetsov, V.V., and Kulaeva, O.N., ABA-dependent regulation of the expression of AA1 homologs (abscisic acid activated 1) in A. thaliana mutants with impaired synthesis or transduction of ABA signal, Mater. Mezhd. nauch. konf. “Fiziologiya rastenii—teoreticheskaya osnova innovatsionnykh agro- i fitobiotekhnologii” (Proc. Int. Sci. Conf. “Plant Physiology—Theoretical Basis for Innovative Agro- and Phytobiotechnologies”), Kaliningrad, 2014, pp. 33–35.Google Scholar
  29. 29.
    Skubacz, A., Daszkowska-Golec, A., and Szarejko, I., The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk, Front. Plant Sci., 2016, vol. 7: 1884.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • N. V. Vinogradov
    • 1
  • A. A. Andreeva
    • 1
  • M. N. Danilova
    • 1
  • A. S. Doroshenko
    • 1
  • N. V. Kudryakova
    • 1
    Email author
  • V. V. Kusnetsov
    • 1
  1. 1.Timiryazev Institute of Plant Physiology, Russian Academy of SciencesMoscowRussia

Personalised recommendations