Skip to main content
Log in

A transcriptional feedback loop modulating signaling crosstalks between auxin and brassinosteroid in Arabidopsis

  • Published:
Molecules and Cells

Abstract

Auxin and brassinosteroid (BR) play essential roles in diverse aspects of growth and developmental processes in plants mainly through coordinate regulation of cell division, elongation, and differentiation. Consistent with the overlapped roles, accumulating evidence indicates that the two growth hormones act in a synergistic as well as in an interdependent manner in many cases, although the underlying molecular mechanisms are not fully understood. Here, we demonstrate that auxin and BR signaling pathways are interconnected at the transcriptional level via a negative feedback loop. An Arabidopsis activating tagging mutant dlf-1D exhibited dwarfed growth with small, dark-green leaves and reduced fertility. Hormone feeding assays revealed that the mutant phenotype is caused by the reduction of endogenous BR level. Consistent with this, a gene encoding the CYP72C1 enzyme that catabolizes BR was up-regulated. Notably, the transcript level of the ARF8 transcription factor gene, which modulates the expression of auxin-responsive genes, was significantly elevated in the mutant. In addition, the ARF8 gene expression was significantly reduced by BR but induced by brassinazole, a BR biosynthetic inhibitor. On the other hand, two BR catabolic pathway genes, DLF (CYP72C1) and BAS1, were induced by auxin. Our observations indicate that at least part of auxin and BR signaling pathways are unified through a transcriptional feedback control of the DLF and ARF8 genes.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Asami, T., Nakano, T., and Fujioka, S. (2005). Plant brassinosteroid hormones. Vitam. Horm. 72, 479–504.

    Article  CAS  PubMed  Google Scholar 

  • Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T., and Yang, Z. (2004). Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134, 1624–1631.

    Article  CAS  PubMed  Google Scholar 

  • Belkhadir, Y., and Chory, J. (2006). Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314, 1410–1411.

    Article  CAS  PubMed  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.

    Article  CAS  PubMed  Google Scholar 

  • Clouse, S.D. (1996). Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J. 10, 1–8.

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Hobbie, L., Ehrismann, J.S., Jürgens, G., and Estelle, M. (2005). Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109–119.

    Article  CAS  PubMed  Google Scholar 

  • Fujioka, S., and Yokota, T. (2003). Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137–164.

    Article  CAS  PubMed  Google Scholar 

  • Goda, H., Shimada, Y., Asami, T., Fujioka, S., and Yoshida, S. (2002). Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 13, 1319–1334.

    Article  Google Scholar 

  • Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y., and Yoshida, S. (2004). Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 134, 1555–1573.

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle, T.J., and Hagen, G. (2007). Auxin response factors. Curr. Opin. Plant Biol. 10, 453–460.

    Article  CAS  PubMed  Google Scholar 

  • He, J.X., Gendron, J.M., Yang, Y., Li, J., and Wang, Z.Y. (2002). The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 10185–10190.

    Article  CAS  PubMed  Google Scholar 

  • Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.

    Article  CAS  PubMed  Google Scholar 

  • Kim, T.W., Lee, S.M., Joo, S.H., Yun, H.S., Lee, Y., Kaufman, P.B., Kirakosyan, A., Kim, S.H., Nam, K.H., Lee, J.S., et al. (2007). Elongation and gravitropic responses of Arabidopsis roots are regulated by brassinolide and IAA. Plant Cell Environ. 30, 679–689.

    Article  CAS  PubMed  Google Scholar 

  • Leyser, H.M., Pickett, F.B., Dharmasiri, S., and Estelle, M. (1996). Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAURAC1 promoter. Plant J. 10, 403–413.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y.G., Mitsukawa, N., Oosumi, T., and Whittier, R.F. (1995). Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457–463.

    Article  CAS  PubMed  Google Scholar 

  • Mallory, A.C., Bartel, D.P., and Bartel, B. (2005). MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17, 1360–1375.

    Article  CAS  PubMed  Google Scholar 

  • Mora-García, S., Vert, G., Yin, Y., Caño-Delgado, A., Cheong, H., and Chory, J. (2004). Nuclear protein phosphatases with Kelchrepeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448–460.

    Article  PubMed  Google Scholar 

  • Nakamoto, D., Ikeura, A., Asami, T., and Yamamoto, K.T. (2006). Inhibition of brassinosteroid biosynthesis by either a dwarf4 mutation or a brassinosteroid biosynthesis inhibitor rescues defects in tropic responses of hypocotyls in the Arabidopsis mutant nonphototropic hypocotyl 4. Plant Physiol. 141, 456–464.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, A., Higuchi, K., Goda, H., Fujiwara, MT., Sawa, S., Koshiba, T., Shimada, Y., and Yoshida, S. (2003a). Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol. 133, 1843–1853.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, A., Shimada, Y., Goda, H, Fujiwara, M.T., Asami, T., and Yoshida, S. (2003b). AXR1 is involved in BR-mediated elongation and SAUR-AC1 gene expression in Arabidopsis. FEBS Lett. 553, 28–32.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, M., Satoh, T., Tanaka, S., Mochizuki, N., Yokota, T., and Nagatani, A. (2005). Activation of the cytochrome P450 gene, CYP72C1, reduces the levels of active brassinosteroids in vivo. J. Exp. Bot. 56, 833–840.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, A., Nakajima, N., Goda, H., Shimada, Y., Hayashi, K., Nozaki, H., Asami, T., Yoshida, S., and Fujioka, S. (2006). Arabidopsis Aux/IAA genes are involved in brassinosteroidmediated growth responses in a manner dependent on organ type. Plant J. 45, 193–205.

    Article  CAS  PubMed  Google Scholar 

  • Neff, M.M., Nguyen, S.M., Malancharuvil, E.J., Fujioka, S., Noguchi, T., Seto, H., Tsubuki, M., Honda, T., Takatsuto, S., Yoshida, S., et al. (1999). BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc. Natl. Acad. Sci. USA 96, 15316–15323.

    Article  CAS  PubMed  Google Scholar 

  • Nemhauser, J.L., Mockler, T.C., and Chory, J. (2004). Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2, E258.

    Article  PubMed  Google Scholar 

  • Park, J.E., Park, J.Y., Kim, Y.S., Staswick, P.E., Jeon, J., Yun, J., Kim, S.Y., Kim, J., Lee, Y.H., and Park, C.M. (2007). GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 10036–10046.

    Article  CAS  PubMed  Google Scholar 

  • Parry, G., and Estelle, M. (2006). Auxin receptors: a new role for F-box proteins. Curr. Opin. Cell Biol. 18, 152–156.

    Article  CAS  PubMed  Google Scholar 

  • Pfeffer, S., Lagos-Quintana, M., and Tuschl, T. (2003). Cloning of small RNA molecules. In current protocols in molecular biology. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidmann, J.A. Smith, and K. Struhl, eds. (New York: Wiley and Sons), pp. 26.

    Google Scholar 

  • Seo, P.J., Xiang, F., Qiao, M., Park, J.Y., Lee, Y.N., Kim, S.G., Lee, Y.H., Park, W.J., and Park, C.M. (2009). The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 151, 275–289.

    Article  CAS  PubMed  Google Scholar 

  • Staswick, P.E., Tiryaki, I., and Rowe, M.L. (2002). Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14, 1405–1415.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, N., Nakazawa, M., Shibata, K., Yokota, T., Ishikawa, A., Suzuki, K., Kawashima, M., Ichikawa, T., Shimada, H., and Matsui, M. (2005). shk1-D, a dwarf Arabidopsis mutant caused by activation of the CYP72C1 gene, has altered brassinosteroid levels. Plant J. 42, 13–22.

    Article  CAS  PubMed  Google Scholar 

  • Tan, X., Calderon-Villalobos, L.I., Sharon, M., Zheng, C., Robinson, C.V., Estelle, M., and Zheng, N. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–645.

    Article  CAS  PubMed  Google Scholar 

  • Tian, C.E., Muto, H., Higuchi, K., Matamura, T., Tatematsu, K., Koshiba, T., and Yamamoto, K.T. (2004). Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J. 40, 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Tiwari, S.B., Hagen, G., and Guilfoyle, T.J. (2004). Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16, 533–543.

    Article  CAS  PubMed  Google Scholar 

  • Turk, E.M., Fujioka, S., Seto, H., Shimada, Y., Takatsuto, S., Yoshida, S., Denzel, M.A., Torres, Q.I., and Neff, M.M. (2003). CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133, 1643–1653.

    Article  CAS  PubMed  Google Scholar 

  • Turk, E.M., Fujioka, S., Seto, H., Shimada, Y., Takatsuto, S., Yoshida, S., Wang, H., Torres, Q.I., Ward, J.M., Murthy, G., et al. (2005). BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J. 42, 23–34.

    Article  CAS  PubMed  Google Scholar 

  • Vanneste, S., and Friml, J. (2009) Auxin: a trigger for change in plant development. Cell 136, 1005–1016.

    Article  CAS  PubMed  Google Scholar 

  • Vert, G., and Chory, J. (2006). Downstream nuclear events in brassinosteroid signalling. Nature 441, 96–100.

    Article  CAS  PubMed  Google Scholar 

  • Vert, G., Walcher, C.L., Chory, J., and Nemhauser, J.L. (2008). Integration of auxin and brassinosteroid pathways by Auxin response factor 2. Proc. Natl. Acad. Sci. USA 105, 9829–9834.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Goshe, M.B., Soderblom, E.J., Phinney, B.S., Kuchar, J.A., Li, J., Asami, T., Yoshida, S., Huber, S.C., and Clouse, S.D. (2005a). Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROIDINSENSITIVE1 receptor kinase. Plant Cell 17, 1685–1703.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Li, X., Meisenhelder, J., Hunter, T., Yoshida, S., Asami, T., and Chory, J. (2005b). Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855–865.

    Article  CAS  PubMed  Google Scholar 

  • Weigel, D., Ahn, J.H., Blázquez, M.A., Borevitz, J.O., Christensen, S.K., Fankhauser, C., Ferrandiz, C., Kardailsky, I., Malancharuvil, E.J., Neff, M.M., et al. (2000). Activation tagging in Arabidopsis. Plant Physiol. 122, 1003–1013.

    Article  CAS  PubMed  Google Scholar 

  • Wu, M.F., Tian, Q., and Reed, J.W. (2006). Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211–4218.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J.H., Han, S.J., Yoon, E.K., and Lee, W.S. (2006). Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res. 34, 1892–1899.

    Article  CAS  PubMed  Google Scholar 

  • Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181–191.

    Article  CAS  PubMed  Google Scholar 

  • Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and Chory, J. (2005). A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120, 249–259.

    Article  CAS  PubMed  Google Scholar 

  • Yun, H.S., Bae, Y.H., Lee, Y.J., Chang, S.C., Kim, S.K., Li, J., and Nam, K.H. (2009). Analysis of phosphorylation of the BRI1/BAK1 complex in arabidopsis reveals amino acid residues critical for receptor formation and activation of BR signaling. Mol. Cells 27, 183–190.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chung-Mo Park.

About this article

Cite this article

Jung, JH., Lee, M. & Park, CM. A transcriptional feedback loop modulating signaling crosstalks between auxin and brassinosteroid in Arabidopsis . Mol Cells 29, 449–456 (2010). https://doi.org/10.1007/s10059-010-0055-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10059-010-0055-6

Keywords

Navigation