Skip to main content
SpringerLink
Log in

BIN2/DWF12 Antagonistically Transduces Brassinosteroid and Auxin Signals in the Roots of Arabidopsis

  • Original Research
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Plant growth-stimulating hormones brassinosteroids (BRs) function via interactions with other hormones. However, the mechanism of these interactions remains to be elucidated. The unique phenotypes of brassinosteroid insensitive2/dwarf12-D (bin2/dwf12-D) mutants, such as twisted inflorescences and leaves, suggested that BIN2, a negative regulator of BR signaling, may be involved in auxin signaling. Furthermore, previously, we showed that auxin stimulates DWF4 expression. To determine the possible role of BIN2/DWF12 in Auxin signaling, we measured DWARF4pro:GUS activity through both GUS histochemical staining and in vivo GUS assay. We found that the GUS activity in the bin2/dwarf12-1D background dramatically increased relative to control. In addition, the number of lateral roots (LR) in bin2/dwf12-1D was greater than wild type, and the optimal concentration for auxin-mediated lateral root induction was lower in bin2/dwf12-1D; these findings suggest that BIN2 plays a positive role in auxin signaling. In contrast, ABA repressed both DWF4pro:GUS expression and lateral root development. However, the degree of repression was lower in bin2/dwf12-1D background, suggesting that BIN2 plays a role in ABA-mediated DWF4pro:GUS expression and subsequently in lateral root development, too. Therefore, it is likely that BIN2 plays a role of signal integrator for multiple hormones, such as BRs, auxin, and ABA.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134(4):1624–1631

    Article  PubMed  CAS  Google Scholar 

  • Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10(5):791–800

    Article  PubMed  CAS  Google Scholar 

  • Choe S (2004) Brassinosteroid biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic Publishers, Dordrecht, pp 156–178

    Google Scholar 

  • Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA (1998) The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10(2):231–243

    Article  PubMed  CAS  Google Scholar 

  • Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999a) The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119(3):897–907

    Article  PubMed  CAS  Google Scholar 

  • Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999b) The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11(2):207–221

    Article  PubMed  CAS  Google Scholar 

  • Choe S, Tanaka A, Noguchi T, Fujioka S, Takatsuto S, Ross AS, Tax FE, Yoshida S, Feldmann KA (2000) Lesions in the sterol Δ7 reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J 21(5):431–443

    Article  PubMed  CAS  Google Scholar 

  • Choe S, Schmitz RJ, Fujioka S, Takatsuto S, Lee MO, Yoshida S, Feldmann KA, Tax FE (2002) Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3β-like kinase. Plant Physiol 130(3):1506–1515

    Article  PubMed  CAS  Google Scholar 

  • Claisse G, Charrier B, Kreis M (2007) The Arabidopsis thaliana GSK3/Shaggy like kinase AtSK3-2 modulates floral cell expansion. Plant Mol Biol 64(1–2):113–124

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111(3):671–678

    Article  PubMed  CAS  Google Scholar 

  • Forde JE, Dale TC (2007) Glycogen synthase kinase 3: a key regulator of cellular fate. Cell Mol Life Sci 64(15):1930–1944

    Article  PubMed  CAS  Google Scholar 

  • Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM, Chen H, Shibagaki N, Ferl RJ, Ehrhardt D, Chong K, Burlingame AL, Wang ZY (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13(2):177–189

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Wang S, Asami T, Chen JG (2008) Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein alpha subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. Plant Cell Physiol 49(7):1013–1024

    Article  PubMed  CAS  Google Scholar 

  • Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu UH, Schulz B, Martinoia E (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15(7):3393–3405

    Article  PubMed  CAS  Google Scholar 

  • He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307(5715):1634–1638

    Article  PubMed  CAS  Google Scholar 

  • Ibanes M, Fabregas N, Chory J, Cano-Delgado AI (2009) Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc Natl Acad Sci USA 106(32):13630–13635

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907

    PubMed  CAS  Google Scholar 

  • Jonak C, Hirt H (2002) Glycogen synthase kinase 3/SHAGGY-like kinases in plants: an emerging family with novel functions. Trends Plant Sci 7(10):457–461

    Article  PubMed  CAS  Google Scholar 

  • Jope RS, Johnson GV (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29(2):95–102

    Article  PubMed  CAS  Google Scholar 

  • Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41(5):710–721

    Article  PubMed  CAS  Google Scholar 

  • Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, Yoshida S, An CS, Lee I, Hwang I, Choe S (2006) The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol 140(2):548–557

    Article  PubMed  CAS  Google Scholar 

  • Kim BK, Fujioka S, Takatsuto S, Tsujimoto M, Choe S (2008) Castasterone is a likely end product of brassinosteroid biosynthetic pathway in rice. Biochem Biophys Res Commun 374(4):614–619

    Article  PubMed  CAS  Google Scholar 

  • Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Burlingame AL, Wang ZY (2009a) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11(10):1254–1260

    Article  PubMed  CAS  Google Scholar 

  • Kim WY, Wang X, Wu Y, Doble BW, Patel S, Woodgett JR, Snider WD (2009b) GSK-3 is a master regulator of neural progenitor homeostasis. Nat Neurosci 12(11):1390–1397

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Lee YI, Seo M, Kim SY, Lee JE, Youn HD, Kim YS, Juhnn YS (2009c) Calcineurin dephosphorylates glycogen synthase kinase-3 beta at serine-9 in neuroblast-derived cells. J Neurochem 111(2):344–354

    Article  PubMed  CAS  Google Scholar 

  • Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90(5):929–938

    Article  PubMed  CAS  Google Scholar 

  • Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295(5558):1299–1301

    PubMed  CAS  Google Scholar 

  • Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272(5260):398–401

    Article  PubMed  CAS  Google Scholar 

  • Li J, Nam KH, Vafeados D, Chory J (2001) BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol 127(1):14–22

    Article  PubMed  CAS  Google Scholar 

  • Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110(2):213–222

    Article  PubMed  CAS  Google Scholar 

  • Meijer L, Flajolet M, Greengard P (2004) Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol Sci 25(9):471–480

    Article  PubMed  CAS  Google Scholar 

  • Mora-Garcia S, Vert G, Yin Y, Cano-Delgado A, Cheong H, Chory J (2004) Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 18(4):448–460

    Article  PubMed  CAS  Google Scholar 

  • Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110(2):203–212

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2(9):E258

    Article  PubMed  Google Scholar 

  • Noguchi T, Fujioka S, Choe S, Takatsuto S, Yoshida S, Yuan H, Feldmann KA, Tax FE (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol 121(3):743–752

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi T, Szatmari AM, Watanabe B, Fujita S, Bancos S, Koncz C, Lafos M, Shibata K, Yokota T, Sakata K, Szekeres M, Mizutani M (2006) C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 18(11):3275–3288

    Article  PubMed  CAS  Google Scholar 

  • Peng P, Yan Z, Zhu Y, Li J (2008) Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation. Mol Plant 1(2):338–346

    Article  PubMed  CAS  Google Scholar 

  • Perez-Perez JM, Ponce MR, Micol JL (2002) The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev Biol 242(2):161–173

    Article  PubMed  CAS  Google Scholar 

  • Piao HL, Pih KT, Lim JH, Kang SG, Jin JB, Kim SH, Hwang I (1999) An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. Plant Physiol 119(4):1527–1534

    Article  PubMed  CAS  Google Scholar 

  • Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 17:2749–2762

    Article  Google Scholar 

  • Stavang JA, Gallego-Bartolome J, Gomez MD, Yoshida S, Asami T, Olsen JE, Garcia-Martinez JL, Alabadi D, Blazquez MA (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60(4):589–601

    Article  PubMed  CAS  Google Scholar 

  • Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 125(2):763–769

    Article  PubMed  CAS  Google Scholar 

  • Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85(2):171–182

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138(2):1117–1125

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, Zhu S, Wang R, Burlingame AL, Wang ZY (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321(5888):557–560

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441(7089):96–100

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 105(28):9829–9834

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313(5790):1118–1122

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, Chory J (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2(4):505–513

    Article  PubMed  CAS  Google Scholar 

  • Xue LW, Du JB, Yang H, Xu F, Yuan S, Lin HH (2009) Brassinosteroids counteract abscisic acid in germination and growth of Arabidopsis. Z Naturforsch C 64(3–4):225–230

    PubMed  CAS  Google Scholar 

  • Yan Z, Zhao J, Peng P, Chihara RK, Li J (2009) BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol 150(2):710–721

    Article  PubMed  CAS  Google Scholar 

  • Yoo MJ, Albert VA, Soltis PS, Soltis DE (2006) Phylogenetic diversification of glycogen synthase kinase 3/SHAGGY-like kinase genes in plants. BMC Plant Biol 6:3

    Article  PubMed  Google Scholar 

  • Zhang S, Cai Z, Wang X (2009) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Natl Acad Sci USA 106(11):4543–4548

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported, in part, by Technology Development Program (110033-5) for Agriculture and Forestry, Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea, BK21 Research Fellowships (to P.M.), and Basic Science Research Program (2010-0012736) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology. S.D.G.

Author information

Authors and Affiliations

  1. School of Biological Sciences, College of Natural Sciences, Seoul National University, Seoul, 151-747, South Korea

    Puna Maya Maharjan & Sunghwa Choe

  2. Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, 47907, USA

    Burkhard Schulz

  3. Plant Genomics and Breeding Institute, Seoul National University, Seoul, 151-921, South Korea

    Sunghwa Choe

Authors
  1. Puna Maya Maharjan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Burkhard Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sunghwa Choe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sunghwa Choe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maharjan, P.M., Schulz, B. & Choe, S. BIN2/DWF12 Antagonistically Transduces Brassinosteroid and Auxin Signals in the Roots of Arabidopsis . J. Plant Biol. 54, 126–134 (2011). https://doi.org/10.1007/s12374-010-9138-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-010-9138-3

Keywords

Search

Navigation