Skip to main content
SpringerLink
Log in

The homeobox genes ATHB12 and ATHB7encode potential regulators of growth in response to water deficit in Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The Arabidopsis thaliana homeodomain leucine-zipper gene ATHB7, which is active specifically under water deficit conditions, is proposed to act as a negative regulator of growth (Söderman et al., 1996, Plant J. 10: 375 381; Hjellström et al., 2003, Plant Cell Environ 26: 1127 1136). In this report we demonstrate that the paralogous gene, ATHB12, has a similar expression pattern and function. ATHB12,like ATHB7,was up-regulated during water deficit conditions, the up-regulation being dependent on abscisic acid (ABA) and on the activity of the Ser/Thr phosphatases ABI1 and ABI2. Plants that are mutant for ATHB12, as a result of T-DNA insertions in the ATHB12 gene, showed a reduced sensitivity to ABA in root elongation assays, whereas transgenic Arabidopsis plants expressing ATHB12 and/orATHB7 as driven by the CaMV 35S promoter were hypersensitive in this response compared to wild-type. High-level expression of either gene also resulted in a delay in inflorescence stem elongation growth and caused plants to develop rosette leaves with a more rounded shape, shorter petioles, and increased branching of the inflorescence stem. Transgenic Arabidopsisplants expressing the reporter geneuidA under the control of the ATHB12promoter showed marker gene activity in axillary shoot primordia, lateral root primordia, inflorescence stems and in flower organs. Treatment of plants with ABA or water deficit conditions caused the activity of ATHB12to increase in the inflorescence stem, the flower organs and the leaves, and to expand into the vasculature of roots and the differentiation/elongation zone of root tips. Taken together, these results indicate that ATHB12 and ATHB7 act to mediate a growth response to water deficit by similar mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    Google Scholar 

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

    Google Scholar 

  • Aoyama, T., Dong, C.H., Wu, Y., Carabelli, M., Sessa, G., Ruberti, I., Morelli, G. and Chua, N.H. 1995. Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell 7: 1773–1785.

    Google Scholar 

  • The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Baima, S., Sessa, G., Ruberti, I. and Morelli, G. 1995. A cDNA encoding Arabidopsis thaliana cytoplasmic ribosomal protein L18. Gene 153: 171–174.

    Google Scholar 

  • Berleth, T. and Ju¨ rgens, G. 1993. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118: 575–587.

    Google Scholar 

  • Bertauche, N., Leung, J. and Giraudat, J. 1996. Protein phosphatase activity of abscisic acid insensitive 1 (ABI1) protein from Arabidopsis thaliana. Eur. J. Biochem. 241: 193–200.

    Google Scholar 

  • Carabelli, M., Morelli, G., Whitelam, G. and Ruberti, I. 1996. Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc. Natl. Acad. Sci. USA 93: 3530–3535.

    Google Scholar 

  • Chang, S., Purear, J. and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11: 113–116.

    Google Scholar 

  • Cheng, W.H., Endo, A., Zhou, L., Penney, J., Chen, H.C., Arroyo, A., Leon, P., Nambara, E., Asami, T., Seo, M., Koshiba, T. and Sheen, J. 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14: 2723–2743.

    Google Scholar 

  • Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B.H., Hong, X., Agarwal, M. and Zhu, J.K. 2003. ICE1: a regulator of coldinduced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17: 1043–1054.

    Google Scholar 

  • Choi, H., Hong, J., Ha, J., Kang, J. and Kim, S.Y. 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275: 1723–1730.

    Google Scholar 

  • Clough, S.J. and Bent, A.F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.

    Google Scholar 

  • Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A. and Benfey, P.N. 1996. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423–433.

    Google Scholar 

  • Elomaa, P., Honkanen, J., Puska, R., Seppa¨ nen, P., Helariutta, Y., Mehto, M., Kotilainen, M., Nevalainen, L. and Teeri, T.H. 1993. Agrobacterium-mediated transfer of antisense chalcone synthase cDNA to Gerbera hybrida inhibits flower pigmentation. Bio/Technology 11: 508–511.

    Google Scholar 

  • Fedoroff, N.V. 2002. Cross-talk in abscisic acid signaling. Sci. STKE 9: RE10.

    Google Scholar 

  • Ferrandiz, C., Pelaz, S. and Yanofsky, M.F. 1999. Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem. 68: 321–354.

    Google Scholar 

  • Finkelstein, R.R. 1994. Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J. 5: 765–771.

    Google Scholar 

  • Finkelstein, R.R., Gampala, S.S.L. and Rock, C.D. 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14: S15–S45.

    Google Scholar 

  • Finkelstein, R.R. and Sommerville, C.R. 1990. Three classes of abscisic acid (ABA) – insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol. 94: 1172–1179.

    Google Scholar 

  • Frank, W., Phillips, J., Salamini, F. and Bartels, D. 1998. Two dehydration–inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J. 15: 413–421.

    Google Scholar 

  • Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., M., H.J., F., T.M. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16: 433–442.

    Google Scholar 

  • Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A., Vartanian, N. and Giraudat, J. 1999. ABI1 protein phosphatase 2C Is a negative regulator of abscisic acid signaling. Plant Cell 11: 1897–1910.

    Google Scholar 

  • Hanson, J. 2000. Functional characterization of the pointed cotyledon subclass of HDZip genes in Arabidopsis thaliana. Comprehensive Summaries of Uppsala Dissertation from the Faculty of Science and Technology. 580 Uppsala, Acta Universitatis Upsaliensis.

    Google Scholar 

  • Hanson, J., Johannesson, H. and Engstro¨ m, P. 2001. Sugardependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol. Biol. 45: 247–262.

    Google Scholar 

  • Himmelbach, A., Hoffmann, T., Leube, M., Ho¨ hner, B. and 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.

    Google Scholar 

  • Himmelbach, A., Iten, M. and Grill, E. 1998. Signalling of abscisic acid to regulate plant growth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353: 1439–1444.

    Google Scholar 

  • Hjellstro¨ m, M., Olsson, A.S.B., Engstro¨ m, P. and So¨ derman, E. 2003. Constitutive expression of the water deficit-inducible homeobox gene ATHB7 in transgenic Arabidopsis causes a suppression of stem elongation growth. Plant Cell Environ. 26: 1127–1136.

    Google Scholar 

  • Izawa, T., Foster, R. and Chua, N.H. 1993. Plant bZIP protein DNA binding specificity. J. Mol. Biol. 230: 1131–1144.

    Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusions: beta–glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.

    Google Scholar 

  • Johannesson, H., Wang, Y. and Engstro¨ m, P. 2001. DNAbinding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. Plant Mol. Biol. 45: 63–73.

    Google Scholar 

  • Johannesson, H., Wang, Y., Hanson, J. and Engstro¨ m, 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.

    Google Scholar 

  • Kang, J.Y., Choi, H.I., Im, M.Y. and Kim, S.Y. 2002. Arabidopsis basic leucine zipper proteins that mediate stress–responsive abscisic acid signaling. Plant Cell 14: 343–357.

    Google Scholar 

  • Koornneef, M., Reuling, G. and Karssen, C.M. 1984. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Plant Physiol. 61: 377–383.

    Google Scholar 

  • Krysan, P.J., Young, J.C. and Sussman, M.R. 1999. T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283–2290.

    Google Scholar 

  • Lee, Y.H. and Chun, J.Y. 1998. A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol. Biol. 37: 377–384.

    Google Scholar 

  • Lee, Y.H., Oh, H.S., Cheon, C.I., Hwang, I.T., Kim, Y.J. and Chun, J.Y. 2001. Structure and expression of the Arabidopsis thaliana homeobox gene Athb-12. Biochem. Biophys. Res. Commun. 284: 133–141.

    Google Scholar 

  • Leung, J., Bouvier-Durand, M., Morris, P.C., Guerrier, D., Chefdor, F. and Giraudat, J. 1994. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448–1452.

    Google Scholar 

  • Leung, J., Merlot, S. and Giraudat, J. 1997. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759–771.

    Google Scholar 

  • Leung, J., Merlot, S., Gosti, F., Bertauche, N., Blatt, M.R. and Giraudat, J. 1998. The role of ABI1 in abscisic acid signal transduction: from gene to cell. Symp. Soc. Exp. Biol. 51: 65–71.

    Google Scholar 

  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and 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-temperatureresponsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391–1406.

    Google Scholar 

  • Mattsson, J., So¨ derman, E. Svensson., Borkird, C. and Engstro¨ m, P. 1992. A new homeobox-leucine zipper gene from Arabidopsis thaliana. Plant Mol. Biol. 18: 1019–1022.

    Google Scholar 

  • McCarty, D.R. 1995. Genetic control and integration of maturation and germination pathways in seed development. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 46: 71–93.

    Google Scholar 

  • Meijer, A.H., Scarpella, E., van Dijk, E.L., Qin, L., Taal, A.J., Rueb, S., Harrington, S.E., McCouch, S.R., Schilperoort, R.A. and Hoge, J.H. 1997. Transcriptional repression by Oshox1, a novel homeodomain leucine zipper protein from rice. Plant J. 11: 263–276.

    Google Scholar 

  • Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A. and Giraudat, J. 2001. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25: 295–303.

    Google Scholar 

  • Meyer, K., Leube, M.P. and Grill, E. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452–1455.

    Google Scholar 

  • Ohgishi, M., Oka, A., Morelli, G., Ruberti, I. and Aoyama, T. 2001. Negative autoregulation of the Arabidopsis homeobox gene ATHB–2. Plant J. 25: 389–98.

    Google Scholar 

  • Rodriguez, P.L., Benning, G. and Grill, E. 1998. ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett. 421: 185–190.

    Google Scholar 

  • Saab, I.N., Sharp, R.R., Pritchard, J. and Voetberg, G.S. 1990. Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol. 93: 1329–1336.

    Google Scholar 

  • Saez, A., Apostolova, N., Gonzalez-Guzman. M., Gonzalez-Garcia, M.P., Nicolas, C., Lorenzo, O. and Rodriguez, P.L. 2004. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 37: 354–369.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbour Laboratory Press, New York.

    Google Scholar 

  • 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. and Shinozaki, K. 2002a. 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.

    Google Scholar 

  • 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. and Shinozaki, K. 2002b. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31: 279–292.

    Google Scholar 

  • Sessa, G., Carabelli, M. and Ruberti, I. 1994. Identification of distinct families of HD-Zip proteins in Arabidopsis thaliana. In: Coruzzi, G.a.P., P. (Ed.), Plant Molecular Biology, Springer-Verlag, Berlin, pp. 412–426. (1994).

    Google Scholar 

  • Sessa, G., Morelli, G. and Ruberti, I. 1993. The Athb-1 and-2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. EMBO J. 12: 3507–3517.

    Google Scholar 

  • Sheen, J. 1998. Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc. Natl. Acad. Sci. USA. 95: 975–980.

    Google Scholar 

  • Shen, Q. and Ho, T.H. 1995. Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7: 295–307.

    Google Scholar 

  • Smyth, D.R., Bowman, J.L. and Meyerowitz, E.M. 1990. Early flower development in Arabidopsis. Plant Cell 2: 755–767.

    Google Scholar 

  • Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G. and Ruberti, I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 26: 4235–4245.

    Google Scholar 

  • Stockinger, E.J., Gilmour, S.J. and Thomashow, M.F. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA. 94: 1035–1040.

    Google Scholar 

  • So¨ derman, E., Hjellstrom, M., Fahleson, J. and Engstrom, 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.

    Google Scholar 

  • So¨ derman, E., Mattsson, J. and Engstrom, P. 1996. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J. 10: 375–381.

    Google Scholar 

  • Ta¨ htiharju, S. and Palva, T. 2001. Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J. 26: 461–470.

    Google Scholar 

  • Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic aciddependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. USA 97: 11632–116327.

    Google Scholar 

  • Verwoerd, T.C., Dekker, B.M. and Hoekema, A. 1989. A small scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17: 2362.

    Google Scholar 

  • Wang, Y., Henriksson, E., So¨ derman, E., Nordin Henriksson, K., Sundberg, E. and Engstro¨ m, P. 2003. The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev. Biol. 264: 228–239.

    Google Scholar 

  • Zeevaart, J.A.D. and Creelman, R.A. 1988. Metabolism and physiology of abscisic acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 439–473.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Villavägen 6, Sweden

    Anna Olsson, Peter Engström & Eva Söderman

Authors
  1. Anna Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Engström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Söderman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olsson, A., Engström, P. & Söderman, E. The homeobox genes ATHB12 and ATHB7encode potential regulators of growth in response to water deficit in Arabidopsis . Plant Mol Biol 55, 663–677 (2004). https://doi.org/10.1007/s11103-004-1581-4

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-1581-4

Search

Navigation