Skip to main content
Log in

Brassinosteroid signaling network: implications on yield and stress tolerance

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

The steroidal hormone brassinosteroids (BRs) play important roles in plant growth and development. Genetic, genomic and proteomic studies in Arabidopsis have identified major BR signaling components and elucidated the signal transduction pathway from the cell surface receptor kinase BRI1 to the BES1/BZR1 family of transcription factors. BRs interact with other plant hormones in coordinating gene expression and plant growth and development. In this review, we provide an update on the latest progress in characterizing the BR signaling network and discuss its interactions with other hormone pathways in determining yield component traits and in regulating stress responses.

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.

Fig. 1

Similar content being viewed by others

References

  • Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, De Vries SC, Zipfel C (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci USA 109:303–308

    Article  CAS  PubMed  Google Scholar 

  • Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14–3–3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104:13839–13844

    Article  CAS  PubMed  Google Scholar 

  • Bai MY, Fan M, Oh E, Wang ZY (2012a) A triple helix–loop–helix/basic helix–loop–helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24:4917–4929

    Article  PubMed  CAS  Google Scholar 

  • Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012b) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817

    Article  CAS  PubMed  Google Scholar 

  • 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 134:1624–1631

    Article  CAS  PubMed  Google Scholar 

  • Belkhadir Y, Jaillais Y, Epple P, Balsemao-Pires E, Dangl JL, Chory J (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci USA 109:297–302

    Article  CAS  PubMed  Google Scholar 

  • Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS (2012) Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci USA 109:21146–21151

    Article  CAS  PubMed  Google Scholar 

  • Cheon J, Park SY, Schulz B, Choe S (2010) Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC Plant Biol 10:270

    Article  CAS  PubMed  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defense. Nature 448:497–500

    Article  CAS  PubMed  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 10:231–243

    CAS  PubMed  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 130:1506–1515

    Article  CAS  PubMed  Google Scholar 

  • Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D, Takeda K, Takatsuto S, Hoshino T, Watanabe Y (2003) A semi-dwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol 133:1209–1219

    Article  CAS  PubMed  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LSP (2012a) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One 7:e33210

    Article  CAS  PubMed  Google Scholar 

  • Choudhary SP, Yu JQ, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2012b) Benefits of brassinosteroid crosstalk. Trends Plant Sci 17:594–605

    Article  CAS  PubMed  Google Scholar 

  • Chung Y, Maharjan PM, Lee O, Fujioka S, Jang S, Kim B, Takatsuto S, Tsujimoto M, Kim H, Cho S et al (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J 66:564–578

    Article  CAS  PubMed  Google Scholar 

  • Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219–1230

    Article  CAS  PubMed  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 111:671–678

    Article  CAS  PubMed  Google Scholar 

  • Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q (2012) Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 24:233–244

    Article  CAS  PubMed  Google Scholar 

  • D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340

    Article  PubMed  CAS  Google Scholar 

  • De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, Vera-Cruz C, Kikuchi S, Hofte M (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846

    Article  PubMed  CAS  Google Scholar 

  • de Vries SC (2007) 14–3–3 proteins in plant brassinosteroid signaling. Dev Cell 13:162–164

    Article  PubMed  CAS  Google Scholar 

  • Deng Z, Zhang X, Tang W, Oses-Prieto JA, Suzuki N, Gendron JM, Chen H, Guan S, Chalkley RJ, Peterman TK, Burlingame AL, Wang ZY (2007) A proteomics study of brassinosteroid response in Arabidopsis. Mol Cell Proteomics 6:2058–2071

    Article  CAS  PubMed  Google Scholar 

  • Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. Nature Biotechnol 26:131–136

    CAS  Google Scholar 

  • Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gallego-Bartolome J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadi D, Blazquez MA (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109:13446–13451

    Article  CAS  PubMed  Google Scholar 

  • Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Wang ZY et al (2007) An essential role for 14–3–3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13:177–189

    Article  CAS  PubMed  Google Scholar 

  • Gendron JM, Liu J, Fan M, Bai M, Wenkel S, Springer PS (2012) Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc Natl Acad Sci USA 109:21152–21157

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, Cano-Delgado AI (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138:849–859

    Article  CAS  PubMed  Google Scholar 

  • Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, Clouse SD, Li J (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet 8:e1002452

    Article  CAS  PubMed  Google Scholar 

  • Gudesblat GE, Betti C, Russinova E (2012a) Brassinosteroids tailor stomatal production to different environments. Trends Plant Sci 17:685–687

    Article  CAS  PubMed  Google Scholar 

  • Gudesblat GE, Schneider-Pizon J, Betti C, Mayerhofer J, Vanhoutte I, Van Dongen W, Boeren S, Zhiponova M, De Vries S, Jonak C et al (2012b) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nature Cell Biol 14:548–554

    Article  CAS  PubMed  Google Scholar 

  • Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848

    Article  CAS  PubMed  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Hartwig T, Chuck GS, Fujioka S, Klempien A, Weizbauer R, Potluri DPV, Choee S, Johal GS, Schulz B (2011) Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci USA 108:19814–19819

    Article  CAS  PubMed  Google Scholar 

  • Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451

    Article  CAS  PubMed  Google Scholar 

  • Hategan L, Godza B, Szekeres M (2011) Regulation of brassinosteroid metabolism. In: Hayat S, Ahmad A (eds) Brassinosteroids: a class of plant hormone. Springer, Berlin, pp 775–781

  • Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Hayat Q, Ahmad A (2010) Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239:3–14

    Article  CAS  PubMed  Google Scholar 

  • Hayat S, Maheshwari P, Wani AS, Irfan M, Alyemeni MN, Ahmad A (2012) Comparative effect of 28 homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol Biochem 53:61–68

    Article  CAS  PubMed  Google Scholar 

  • He Z, Wang ZY, Li J, Zhu Q, Lamb C, Ronald P, Chory J (2000) Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360–2363

    Article  CAS  PubMed  Google Scholar 

  • He JX, Gendron JM, Yang Y, Li J, Wang ZY (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 

  • 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 307:1634–1638

    Article  CAS  PubMed  Google Scholar 

  • Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Sci Signal 104:12217

    CAS  Google Scholar 

  • Hong Z, Ueguchi-Tanaka M, Shimizu-Sato S, Inukai Y, Fujioka S, Shimada Y, Takatsuto S, Agetsuma M, Yoshida S, Matsuoka M et al (2002) Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. Plant J 32:495–508

    Article  CAS  PubMed  Google Scholar 

  • Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, Matsuoka M (2003) A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15:2900–2910

    Article  CAS  PubMed  Google Scholar 

  • Hong Z, Ueguchi-Tanaka M, Fujioka S, Takatsuto S, Yoshida S (2005) The Rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell 17:2243–2254

    Article  CAS  PubMed  Google Scholar 

  • Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467–471

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222:107–117

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Jiang W, Hu Y, Wu P, Zhu J, Liang W, Wang ZY, Lin W (2012) BR signal influences Arabidopsis ovule and seed number through regulating related genes expression by BZR1. Mol Plant. doi:10.1093/mp/sss070

    Google Scholar 

  • Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider-Pizon J, Hnilikova J, Sisa M, Buyst D, Vilarrasa-Blasi J, Szatmari AM et al (2012) Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat Chem Biol 8:583–589

    Article  CAS  PubMed  Google Scholar 

  • Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL (2011) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev 25:232–237

    Article  CAS  PubMed  Google Scholar 

  • Je BI, Piao HL, Park SJ, Park SH, Kim CM, Xuan YH, Park SH, Huang J, Do Choi Y, Han CD (2010) RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 22:1777–1791

    Article  CAS  PubMed  Google Scholar 

  • Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364

    Article  CAS  PubMed  Google Scholar 

  • Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704

    Article  CAS  PubMed  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 41:710–721

    Article  CAS  PubMed  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 140:548–557

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim TW, Guan S, Burlingame AL, Wang ZY (2011) The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol Cell 43:561–571

    Article  CAS  PubMed  Google Scholar 

  • Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–422

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171

    Article  CAS  PubMed  Google Scholar 

  • Koh S, Lee SC, Kim MK, Koh JH, Lee S, An G, Choe S, Kim SR (2007) T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol Biol 65:453–466

    Article  CAS  PubMed  Google Scholar 

  • Koka CV, Cerny RE, Gardner RG, Noguchi T, Fujioka S, Takatsuto S, Yoshida S, Clouse SD (2000) A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol 122:85–98

    Article  CAS  PubMed  Google Scholar 

  • Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297

    Article  CAS  PubMed  Google Scholar 

  • Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116

    Article  CAS  PubMed  Google Scholar 

  • Lanza M, Garcia-Ponce B, Castrillo G, Catarecha P, Sauer M, Rodriguez-Serrano M, Paez-Garcia A, Sanchez-Bermejo E, Leo del Puerto Y, TCM et al (2012) Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev Cell 22:1275–1285

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Lee S, Yang KY, Kim YM, Park SY, Kim SY, Soh MS (2006) Overexpression of PRE1 and its homologous genes activates gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol 47:591–600

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li J, Chory J (1999) Brassinosteroid actions in plants. J Exp Bot 50:275–282

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 110:213–222

    Article  CAS  PubMed  Google Scholar 

  • Li L, Xu J, Xu ZH, Xue HW (2005) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17:2738–2753

    Article  CAS  PubMed  Google Scholar 

  • Li D, Wang L, Wang M, Xu YY, Luo W, Liu YJ, Xu Z, Li J, Chong K (2009a) Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol J 7:791–806

    Article  CAS  PubMed  Google Scholar 

  • Li L, Yu X, Thompson A, Guo M, Yoshida S, Asami T, Chory J, Yin Y (2009b) Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J 58:275–286

    Article  CAS  PubMed  Google Scholar 

  • Li L, Ye H, Guo H, Yin Y (2010) Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 107:3918–3923

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Cui F, Li Q, Yin B, Zhang H, Lin B, Wu Y, Xia R, Tang S, Xie Q (2011) The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res 21:957–969

    Article  CAS  PubMed  Google Scholar 

  • MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–540

    Article  CAS  PubMed  Google Scholar 

  • Makarevitch I, Thompson A, Muehlbauer GJ, Springer NM (2012) Brd1 gene in maize encodes a brassinosteroid C-6 oxidase. PLoS One 7:e30798

    Article  CAS  PubMed  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  CAS  PubMed  Google Scholar 

  • Mathur J, Molnar G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Szekeres M et al (1998) Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J 14:593–602

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ (2002) Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14:3163–3176

    Article  CAS  PubMed  Google Scholar 

  • Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feed-back between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–461

    Article  CAS  PubMed  Google Scholar 

  • Mussig C, Fischer S, Altmann T (2002) Brassinosteroid-regulated gene expression. Plant Physiol 129:1241–1251

    Article  CAS  PubMed  Google Scholar 

  • Nahar K, Kyndt T, Hause B, Hofte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant Microbe Interact 26:106–115

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa H, Tanaka A, Tanabata T, Ohtake M, Fujioka S, Nakamura H, Ichikawa H, Mori M (2012) SHORT GRAIN 1 decreases organ elongation and brassinosteroid response in rice. Plant Physiol 158:1208–1219

    Article  CAS  PubMed  Google Scholar 

  • Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) 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, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S (2006) Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type. Plant J 45:193–205

    Article  CAS  PubMed  Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Chory J (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 JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:e258

    Article  PubMed  CAS  Google Scholar 

  • Nie WF, Wang MM, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2012) Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance. Plant Cell Environ 36:789–803

    Article  PubMed  CAS  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 121:743–752

    Article  CAS  PubMed  Google Scholar 

  • Nomura T, Bishop GJ, Kaneta T, Reid JB, Chory J, Yokota T (2003) The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea. Plant J 36:291–300

    Article  CAS  PubMed  Google Scholar 

  • Oh E, Zhu JY, Wang ZY (2012a) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809

    Article  CAS  PubMed  Google Scholar 

  • Oh M-H, Kim HS, Wu X, Clouse SD, Zielinski RE, Huber SC (2012b) Calcium/calmodulin inhibition of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase provides a possible link between calcium and brassinosteroid signalling. Biochem J 443:515–523

    Article  CAS  PubMed  Google Scholar 

  • Oh M-H, Wang X, Clouse SD, Huber SC (2012c) Deactivation of the Arabidopsis BRASSINOSTEROID INSENSITIVE 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop. Proc Natl Acad Sci USA 109:327–332

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signaling networks in plant defense. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  • Polko JK, Pierik R, van Zanten M, Tarkowska D, Strnad M, Voesenek LACJ, Peeters AJM (2013) Ethylene promotes hyponastic growth through interaction with ROTUNDIFOLIA3/CYP90C1 in Arabidopsis. J Exp Bot 64:613–624

    Article  CAS  PubMed  Google Scholar 

  • Ren C, Han C, Peng W, Huang Y, Peng Z, Xiong X, Zhu Q, Gao B, Xie D (2009) A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiol 151:1412–1420

    Article  CAS  PubMed  Google Scholar 

  • Roh H, Jeong CW, Fujioka S, Kim YK, Lee S, Ahn JH, Choi YD, Lee JS (2012) Genetic evidence for the reduction of brassinosteroid levels by a BAHD acyltransferase-like protein in Arabidopsis. Plant Physiol 159:696–709

    Article  CAS  PubMed  Google Scholar 

  • Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tor M, de Vries S, Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455

    Article  CAS  PubMed  Google Scholar 

  • Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–3229

    Article  CAS  PubMed  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 19:2749–2762

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Cho H, Kim K, Hwang I (2010) Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol Cells 29:283–290

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T (2006) Phytohormones and rice crop yield: strategies and opportunities for genetic improvement. Transgenic Res 15:399–404

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Matsuoka M et al (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Morinaka Y, Inukai Y, Kitano H, Fujioka S (2013) Auxin signal transcription factor regulates expression of brassinosteroid receptor gene in rice. Plant J 73:676–688

    Google Scholar 

  • Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7:e1002046

    Article  CAS  PubMed  Google Scholar 

  • She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, Shi S, Wang J, Yang M, Wang ZY, Chai J (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474:472–476

    Article  CAS  PubMed  Google Scholar 

  • Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S (2001) Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol 126:770–779

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Wang ZY et al (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777

    Article  CAS  PubMed  Google Scholar 

  • Symons GM, Reid JB (2004) Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol 135:2196–2206

    Article  CAS  PubMed  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 85:171–182

    Article  CAS  PubMed  Google Scholar 

  • Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S, Yano M, Yoshimura A, Kitano H, Matsuoka M, Iwasaki Y et al (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17:776–790

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Deng Z, Oses-Prieto JA, Suzuki N, Zhu S, Zhang X, Burlingame AL, Wang ZY (2008a) Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional DIGE. Mol Cell Proteomics 7:728–738

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Wang ZY et al (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13:124–131

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    CAS  PubMed  Google Scholar 

  • Tong H, Chu C (2009) Roles of DLT in fine modulation on brassinosteroid response in rice. Plant Signal Behav 4:438–439

    Article  CAS  PubMed  Google Scholar 

  • Tong H, Chu C (2012) Brassinosteroid signaling and application in rice. J Genet Genomics 39:3–9

    Article  CAS  PubMed  Google Scholar 

  • Tong H, Liu L, Jin Y, Du L, Yin Y, Qian Q, Zhu L, Chu C (2012) DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24:2562–2577

    Article  CAS  PubMed  Google Scholar 

  • Trupkin SA, Mora-Garcia S, Casal JJ (2012) The cyclophilin ROC1 links phytochrome and cryptochrome to brassinosteroid sensitivity. Plant J 71:712–723

    Article  CAS  PubMed  Google Scholar 

  • Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Neff MM (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 

  • van Esse GW, Van Mourik S, Stigter H, Colette A, Molenaar J, de Vries SC (2012) A mathematical model for BRASSINOSTEROID INSENSITIVE1-mediated signaling in root growth and hypocotyl elongation. Plant Physiol 160:523–532

    Article  PubMed  CAS  Google Scholar 

  • van Zanten M, Snoek LB, Proveniers MC, Peeters AJ (2009) The many functions of ERECTA. Trends Plant Sci 14:214–218

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche F, Callebert P, Zadnikova P, Benkova E, Van Der Straeten D (2012) Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. Am J Bot 100:1–11

    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 105:9829–9834

    Article  CAS  PubMed  Google Scholar 

  • Villiers F, Jourdain A, Bastien O, Leonhardt N, Fujioka S, Tichtincky G, Parcy F, Bourguignon J, Hugouvieux V (2012) Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J Exp Bot 63:1185–1200

    Article  CAS  PubMed  Google Scholar 

  • Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24:842–857

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383

    Article  CAS  PubMed  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 2:505–513

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 17:1685–1703

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Xu Y, Zhang C, Ma Q, Joo SH, Kim SK, Xu Z, Chong K (2008a) OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling. PLoS One 3:e3521

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008b) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220–235

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhu Y, Fujioka S, Asami T, Li JY, Li JM (2009) Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix–loop–helix proteins. Plant Cell 21:3781–3791

    Google Scholar 

  • Wang F, Bai MY, Deng Z, Oses-Prieto JA, Burlingame AL, Lu T, Chong K, Wang ZY (2010) Proteomic study identifies proteins involved in brassinosteroid regulation of rice growth. J Integr Plant Biol 52:1075–1085

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Yang C, Zhang C, Wang N, Lu D, Wang J, Zhang S, Wang ZX, Ma H, Wang X (2011) Dual role of BKI1 and 14–3–3s in brassinosteroid signaling to link receptor with transcription factors. Dev Cell 21:825–834

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Liu X, Wang R, Li W, Rodermel S, Yu F (2012a) Overexpression of a putative Arabidopsis BAHD acyltransferase causes dwarfism that can be rescued by brassinosteroid. J Exp Bot 63:5787–5801

    Google Scholar 

  • Wang X, Zhang J, Yuan M, Mao T (2012b) Arabidopsis MICROTUBULE DESTABILIZING PROTEIN40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24:4012–4025

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Bai MY, Oh E, Zhu JY (2012c) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724

    Article  CAS  PubMed  Google Scholar 

  • Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Zhai H, Takatsuto S, Pennell RI et al (2008) Brassinosteroids regulate grain filling in rice. Plant Cell 20:2130–2145

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Wang X, Li X, Kamiya Y, Otegui MS, Chory J (2011) Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci Signal 4:ra29

    Article  PubMed  CAS  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  CAS  PubMed  Google Scholar 

  • Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12:1591–1606

    CAS  PubMed  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 150:710–721

    Article  CAS  PubMed  Google Scholar 

  • Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600

    Article  CAS  PubMed  Google Scholar 

  • Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107:6100–6105

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Li L, Yin Y (2011) Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J Integr Plant Biol 53:455–468

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Li L, Guo H, Yin Y (2012) MYBL2 is a substrate of GSK3-like kinase BIN2 and acts as a corepressor of BES1 in brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 109:20142–20147

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, 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, Yokoda T, Asami T, Chory J (2005) A new class of transcription factors mediate brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259

    Article  CAS  PubMed  Google Scholar 

  • Yokota T, Higuchi K, Kosaka Y, Takahashi N (1992) Transport and metabolism of brassinosteroids in rice. In: Karssen CM, Loon LCV, Vreugdenhil D (eds) Progress in plant growth regulation. Kluwer, Dordrecht, pp 298–305

    Chapter  Google Scholar 

  • Yoshimitsu Y, Tanaka K, Fukuda W, Asami T, Yoshida S, Hayashi K-I, Kamiya Y, Jikumaru Y, Shigeta T, Nakamura Y et al (2011) Transcription of DWARF4 plays a crucial role in auxin-regulated root elongation in addition to brassinosteroid homeostasis in Arabidopsis thaliana. PLoS One 6:e23851

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Li L, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105:7618–7623

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65:634–646

    Article  CAS  PubMed  Google Scholar 

  • Yuldashev R, Avalbaev A, Bezrukova M, Vysotskaya L, Khripach V, Shakirova F (2012) Cytokinin oxidase is involved in the regulation of cytokinin content by 24-epibrassinolide in wheat seedlings. Plant Physiol Bioch 55:1–6

    Article  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2011) Protective response of 28-homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60:68–76

    Article  CAS  PubMed  Google Scholar 

  • Zhang LY, Bai MY, Wu J, Zhu JY, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Wang ZY et al (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21:3767–3780

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012) Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8:e1002686

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Li J (2012) Regulation of brassinosteroid biosynthesis and inactivation. J Integr Plant Biol 54:746–759

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Peng P, Schmitz RJ, Decker AD, Tax FE, Li J (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol 130:1221–1229

    Article  CAS  PubMed  Google Scholar 

  • Zhiponova MK, Vanhoutte I, Boudolf V, Betti C, Dhondt S, Coppens F, Mylle E, Maes S, Gonzalez-Garcia MP, Russinova E (2013) Brassinosteroid production and signaling differentially control cell division and expansion in the leaf. New Phytol 197:490–502

    Article  CAS  PubMed  Google Scholar 

  • Zhou XY, Song L, Xue HW (2012) Brassinosteroids regulate the differential growth of Arabidopsis hypocotyls through auxin signaling components IAA19 and ARF7. Mol Plant. doi:10.1093/mp/sss123

    Google Scholar 

Download references

Acknowledgments

The research in the authors’ lab is supported by The Consortium for Plant Biotechnology Research, Inc to S.F & Y.Y (GO12026-322) and NSF (IOS-1122166) to Y.Y. We thank Dr. Mark Widrelechner for his assistance in improving the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shui-zhang Fei.

Additional information

Communicated by A. Feher.

A contribution to the Special Issue: Plant Hormone Signaling.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hao, J., Yin, Y. & Fei, Sz. Brassinosteroid signaling network: implications on yield and stress tolerance. Plant Cell Rep 32, 1017–1030 (2013). https://doi.org/10.1007/s00299-013-1438-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1438-x

Keywords

Navigation