Brassinosteroids

Abstract

Brassinosteroids (BRs) are specific phytosteroids necessary for ordinary plant growth and development. BRs share similar chemical structures with animal steroidal hormones, but show a distinctive signal perception mechanism. The importance of BRs is illustrated by the typical phenotypes of mutants with lesions in key biosynthetic or signalling proteins. These mutants show severe dwarfism, curled and round leaves, considerably delayed senescence, reduced male fertility, altered light‐regulated developmental programs, changed responses to abiotic and biotic stresses and modified gene expression profiles. Extensive studies in the last four decades have resulted in a comprehensive picture of BRs, from their nearly completed biosynthesis and physiological functions to their mechanisms of action.

Key Concepts

  • Brassinosteroids (BRs) are essential plant hormones regulating various developmental processes.
  • BRs show structures similar to animal steroidal hormones.
  • Brassinolide is the final product of the BR biosynthetic pathway and the most active BR.
  • BRs are perceived by transmembrane receptor complexes including the receptor BRI1 and co‐receptor BAK1.
  • BRs cannot be transported in a long distant manner.
  • BES1 and BZR1 are the critical downstream transcription factors regulating the expression of thousands of BR response genes.

Keywords: brassinosteroids; brassinosteroid; brassinolide; biosynthesis; catabolism; receptor‐like kinase; signal transduction; BRI1; BAK1

Figure 1. BL chemical structure and phenotypes of representative BR signalling and biosynthetic mutants. Brassinolide, the most active and widespread BR, is a C28 steroidal lactone. The carbons are numbered and the rings are labelled by letters. There are over 70 BRs identified in plant kingdom. They can be grouped as C28, C29 and C30 BRs. The variations are basically found in rings A and B, as well as in the side‐chain. BR mutants, either signal transduction mutants (such as bri1‐701) or biosynthetic mutants (such as cpd), show similar defective phenotypes under both dark and light growing conditions.
Figure 2. A simplified BR biosynthetic pathway. BRs are biosynthesised from primary metabolic products, acetyl‐CoA, to form mevalonate. C6 mevalonate is then converted to C5 isopentenyl pyrophosphate (IPP), which is the building unit for various terpenoids including BRs. Steps from campesterol to BL are considered as the BR‐specific biosynthesis pathway. There are two coexisting pathways converting campestanol to CS; one is called later C‐6 oxidation pathway and the other is called early C‐6 oxidation pathway. Red arrows represent the predominant eight‐step BR biosynthetic route consisting of the CN‐independent and the late C‐6 oxidation pathways. Blue arrows represent a 10‐step CN‐dependent BR biosynthetic pathway. The enzymes indicated are all from Arabidopsis. The dashed arrow represents the unconfirmed step.
Figure 3. Representatives of BR inactivation reactions. From feeding experiments, it was predicted that many reactions can turn an active BR to an inactive form. The red parts represent modifications of the related substrates. The question mark represents a hypothetical reaction, which has not been confirmed in plants.
Figure 4. Structures of BRI1 and BAK1. BRs are perceived by a cell surface LRR‐RLK, BRI1. The second LRR‐RLK, BAK1, is also critical in regulating BR signal perception via its dimerisation with BRI1. BL interacts with the extracellular portion of BRI1, including the 70‐aa ‘island’ and the 22nd LRR, which can trigger the formation of a BRI1‐BL‐BAK1 complex. Formation of the BRI1‐BL‐BAK1 complex activates the downstream BR signalling cascade.
Figure 5. A proposed BR signal transduction pathway based on updated information as discussed in the text. In this model, the inactive form of BRI1 forms a dimer. BKI1 interacts with the kinase domain of BRI1, which blocks its association with BAK1. There may be an inhibitory protein or peptide that can block the binding of BL to its receptor. BRS1 may be involved in degrading this unidentified inhibitory protein. Binding BL with BRI1 extracellular domain can trigger BRI1 autophosphorylation, and subsequently induce its heterodimerisation with BAK1. Structural analysis indicated that BL is sandwiched by BRI1 and BAK1. Sequential transphosphorylation between BRI1 and BAK1 activates BRI1, which then phosphorylates BSKs and CDG1. The active BSKs and CDG1 then activate BSU1 by phosphorylation. Activated BSU1 dephosphorylates and inactivates BIN2. Unphosphorylated BZR1 and BES1 move into the nucleus to regulate expression of their target genes. PP2A is involved in dephosphorylation of phosphorylated BES1 and BZR1.
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References

Asami T, Mizutani M, Fujioka S, et al. (2001) Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in Planta. Journal of Biological Chemistry 276: 25687–25691.

Bajguz A and Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62: 1027–1046.

Bajguz A (2007) Metabolism of brassinosteroids in plants. Plant Physiology and Biochemistry 45: 95–107.

Bishop GJ, Harrison K and Jones JD (1996) The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8: 959–969.

Choe SW, Dilkes BP, Fujioka S, et al. (1998) The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22 alpha‐hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10: 231–243.

Choe S, Fujioka S, Noguchi T, et al. (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant Journal 26: 573–582.

Choi S, Cho YH, Kim K, et al. (2013) BAT1, a putative acyltransferase, modulates brassinosteroid levels in Arabidopsis. Plant Journal 73: 380–391.

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

Clouse SD and Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49: 427–451.

Ehsan H, Ray WK, Phinney B, et al. (2005) Interaction of Arabidopsis BRASSINOSTEROID‐INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF‐beta receptor interacting protein. Plant Journal 43: 251–261.

Fujioka S, Li JM, Choi YH, et al. (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9: 1951–1962.

Fujioka S, Takatsuto S and Yoshida S (2002) An early C‐22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiology 130: 930–939.

Fujioka S and Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annual Review of Plant Biology 54: 137–164.

Gampala SS, Kim TW, He JX, et al. (2007) An essential role for 14‐3‐3 proteins in brassinosteroid signal transduction in Arabidopsis. Developmental Cell 13: 177–189.

Gao Y, Zhang D and Li J (2015) TCP1 modulates DWF4 expression via directly interacting with the GGNCCC motifs in the promoter region of DWF4 in Arabidopsis thaliana. Journal of Genetics and Genomics 42: 383–392.

Gou XP, Yin HJ, He K, et al. (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genetics 8: e1002452.

Grove MD, Spencer GF, Rohwedder WK, et al. (1979) Brassinolide, a plant growth‐promoting steroid isolated from Brassica napus pollen. Nature 281: 216–217.

Guo Z, Fujioka S, Blancaflor EB, et al. (2010) TCP1 modulates brassinosteroid biosynthesis by regulating the expression of thekey biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 22: 1161–1173.

He K, Gou X, Yuan T, et al. (2007) BAK1 and BKK1 regulate brassinosteroid‐dependent growth and brassinosteroid‐independent cell‐death pathways. Current Biology 17: 1109–1115.

Hecht V, Vielle‐Calzada JP, Hartog MV, et al. (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology 127: 803–816.

Hong Z, Ueguchi‐Tanaka M, Shimizu‐Sato S, 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 Journal 32: 495–508.

Hothorn M, Belkhadir Y, Dreux M, et al. (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474: 467–471.

Kim TW, Guan S, Sun Y, et al. (2009) Brassinosteroid signal transduction from cell‐surface receptor kinases to nuclear transcription factors. Nature Cell Biology 11: 1254–1260.

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

Kinoshita T, Caño‐Delgado AC, Seto H, et al. (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167–171.

Li J, Nagpal P, Vitart V, et al. (1996) A role for brassinosteroids in light‐dependent development of Arabidopsis. Science 272: 398–401.

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

Li J, Lease KA, Tax FE and Walker JC (2001a) BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 98: 5916–5921.

Li J, Nam KH, Vafeados D and Chory J (2001b) BIN2, a new brassinosteroid‐insensitive locus in Arabidopsis. Plant Physiology 127: 14–22.

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

Li J, Wen J, Lease KA, et al. (2002) BAK1, an Arabidopsis LRR receptor‐like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213–222.

Mitchell JW, Mandava N, Worley JF, et al. (1970) Brassins – a new family of plant hormones from rape pollen. Nature 225: 1065–1066.

Mora‐García S, Vert G, Yin Y, et al. (2004) Nuclear protein phosphatases with Kelch‐repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes & Development 18: 448–460.

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

Nam KH and Li J (2004) The Arabidopsis transthyretin‐like protein is a potential substrate of BRASSINOSTEROID‐INSENSITIVE 1. Plant Cell 16: 2406–2417.

Neff MM, Nguyen SM, Malancharuvil EJ, et al. (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 96: 15316–15323.

Nomura T, Kushiro T, Yokota T, et al. (2005) The last reaction producing brassinolide is catalyzed by cytochrome P‐450s, CYP85A3 in tomato and CYP85A2 in Arabidopsis. Journal of Biological Chemistry 280: 17873–17879.

Ohnishi T, Szatmari AM, Watanabe B, et al. (2006) C‐23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 18: 3275–3288.

Ohnishi T, Godza B, Watanabe B, et al. (2012) CYP90A1/CPD, a brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C‐3 oxidation. Journal of Biological Chemistry 287: 31551–31560.

Poppenberger B, Fujioka S, Soeno K, et al. (2005) The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. Proceedings of the National Academy of Sciences of the United States of America 102: 15253–15258.

Poppenberger B, Rozhon W, Khan M, et al. (2011) CESTA, a positive regulator of brassinosteroid biosynthesis. EMBO Journal 30: 1149–1161.

Roh H, Jeong CW, Fujioka S, et al. (2012) Genetic evidence for the reduction of brassinosteroid levels by a BAHD acyltransferase‐like protein in Arabidopsis. Plant Physiology 159: 696–709.

Rouleau M, Marsolais F, Richard M, et al. (1999) Inactivation of brassinosteroid biological activity by a salicylate‐inducible steroid sulfotransferase from Brassica napus. Journal of Biological Chemistry 274: 20925–20930.

Santiago J, Henzler C and Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co‐receptor kinases. Science 341: 889–892.

She J, Han Z, Kim TW, et al. (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474: 472–476.

Shimada Y, Fujioka S, Miyauchi N, et al. (2001) Brassinosteroid‐6‐oxidases from arabidopsis and tomato catalyze multiple C‐6 oxidations in brassinosteroid biosynthesis. Plant Physiology 126: 770–779.

Shimada Y, Goda H, Nakamura A, et al. (2003) Organ‐specific expression of brassinosteroid‐biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiology 131: 287–297.

Sun Y, Fan XY, Cao DM, et al. (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19: 765–777.

Sun YD, Han ZF, Tang J, et al. (2013) Structure reveals that BAK1 as a co‐receptor recognizes the BRI1‐bound brassinolide. Cell Research 23: 1326–1329.

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

Szekeres M, Németh K, Koncz‐Kálmán Z, et al. (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de‐etiolation in Arabidopsis. Cell 85: 171–182.

Tanaka K, Asami T, Yoshida S, et al. (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138: 1117–1125.

Tang WQ, Kim TW, Oses‐Prieto JA, et al. (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321: 557–560.

Tang W, Yuan M, Wang R, et al. (2011) PP2A activates brassinosteroid‐responsive gene expression and plant growth by dephosphorylating BZR1. Nature Cell Biology 13: 124–131.

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

Wang ZY, Seto H, Fujioka S, et al. (2001) BRI1 is a critical component of a plasma‐membrane receptor for plant steroids. Nature 410: 380–383.

Wang ZY, Nakano T, Gendron J, et al. (2002) Nuclear‐localized BZR1 mediates brassinosteroid‐induced growth and feedback suppression of brassinosteroid biosynthesis. Developmental Cell 2: 505–513.

Wang XF, Goshe MB, Soderblom EJ, et al. (2005) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID‐INSENSITIVE1 receptor kinase. Plant Cell 17: 1685–1703.

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

Wang H, Yang C, Zhang C, et al. (2011) Dual role of BKI1 and 14‐3‐3 s in brassinosteroid signaling to link receptor with transcription factors. Developmental Cell 21: 825–834.

Wu G, Wang X, Li X, et al. (2011) Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Science Signaling 4: ra29.

Yang XH, Xu ZH and Xue HW (2005) Arabidopsis membrane steroid binding protein 1 is involved in inhibition of cell elongation. Plant Cell 17: 116–131.

Yin YH, Wang ZY, Mora‐Garcia S, et al. (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181–191.

Yokota T, Arima M and Takahashi N (1982) Castasterone, a new phytosterol with plant‐hormone potency, from chestnut insect gall. Tetrahedron Letters 23: 1275–1278.

Yu XF, Li L, Zola J, et al. (2011) A brassinosteroid transcriptional network revealed by genome‐wide identification of BESI target genes in Arabidopsis thaliana. Plant Journal 65: 634–646.

Yuan T, Fujioka S, Takatsuto S, et al. (2007) BEN1, a gene encoding a dihydroflavonol 4‐reductase (DFR)‐like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant Journal 51: 220–233.

Zhu W, Wang H, Fujioka S, et al. (2013) Homeostasis of brassinosteroids regulated by DRL1, a putative acyltransferase in Arabidopsis. Molecular Plant 6: 546–558.

Further Reading

Caño‐Delgado A, Yin YH, Yu C, et al. (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341–5351.

Friedrichsen DM, Joazeiro CA, Li J, et al. (2000) Brassinosteroid‐insensitive‐1 is a ubiquitously expressed leucine‐rich repeat receptor serine/threonine kinase. Plant Physiology 123: 1247–1256.

Kim GT, Fujioka S, Kozuka T, et al. (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant Journal 41: 710–721.

Kim HB, Kwon M, Ryu H, et al. (2006) The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiology 140: 548–557.

Noguchi T, Fujioka S, Takatsuto S, et al. (1999) Arabidopsis det2 is defective in the conversion of (24R)‐24‐methylcholest‐4‐En‐3‐one to (24R)‐24‐methyl‐5alpha‐cholestan‐3‐one in brassinosteroid biosynthesis. Plant Physiology 120: 833–839.

Sekimata K, Ohnishi T, Mizutani M, et al. (2008) Brz220 interacts with DWF4, a cytochrome P450 monooxygenase in brassinosteroid biosynthesis, and exerts biological activity. Bioscience, Biotechnology, and Biochemistry 72: 7–12.

Turk EM, Fujioka S, Seto H, et al. (2005) BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant Journal 42: 23–34.

Wang XF, Kota U, He K, et al. (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Developmental Cell 15: 220–235.

Wang R, Liu M, Yuan M, et al. (2015) The brassinosteroid‐activated BRI1 receptor kinase is switched off by dephosphorylation mediated by cytoplasm‐localized PP2A B' subunits. Molecular Plant 9 (1): 148–157.

Zhou A, Wang HC, Walker JC and Li J (2004) BRL1, a leucine‐rich repeat receptor‐like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant Journal 40: 399–409.

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Wei, Zhuoyun, Gou, Xiaoping, and Li, Jia(Jun 2016) Brassinosteroids. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020092.pub2]