Advertisement

Brassinosteroid Signaling in Plant Immune System

  • P. Vidhyasekaran
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 2)

Abstract

Brassinosteroids (BRs) are growth-promoting steroidal hormones in plants; they are also involved in plant innate immunity. BR signals are perceived by the plasma membrane receptors BRI1 and co-receptor BAK1. Several positive (BSK1, BSU1, PP2A, CDG1) and negative (BKI1, BIN2, MSBP1, and 14-3-3) regulators of BR signaling control the activities of BZR1 and BES1 family of transcription factors, which regulate the expression of hundreds to thousands of genes for various BR responses. BRs either positively or negatively regulate plant innate immunity. Pathogen infection results in elevation of BR signal processing. BR triggers disease resistance against some pathogens. BAK1 is a key component in BR signaling pathway. It may be involved in triggering plant disease resistance by modulating JA signaling system. BR may also induce susceptibility. BR negates disease conferred by the SA synthetic analog benzothiadiazole, suggesting negative crosstalk between BR and SA signaling pathways. BR-mediated suppression of SA defenses occurs downstream of SA biosynthesis, but upstream of NPR1 and OsWRKY45 in the SA signaling pathway. BR triggers the expression of GA repressor proteins and suppresses GA-induced defense responses. BR signaling may also negatively regulate PAMP-triggered immunity. Enhanced BR signaling resulting from either a gain-of-function mutation in BAK1, ectopic expression of BRI1, or application of BR impedes immunity triggered by the PAMP. Crosstalk between PAMP–PRR signaling and BR synthesis pathway has been reported. BRI1–BAK signaling modulates PAMP–PRR signaling pathway. Increased BR signaling triggered by BRI1 overexpression antagonized the activities of the PAMPs/MAMPs flg22, elf18, and PGN that increased BR signaling. The bHLH transcription factor HBI1 is a positive regulator of BR-triggered resistance. HBI1 has been found to be a negative regulator of PAMP-triggered immunity (PTI). HBI1 overexpression led to reduced PAMP-triggered responses. This inhibition was found to be correlated with reduced steady-state expression of immune marker genes, leading to increased susceptibility to Pseudomonas syringae in Arabidopsis thaliana. Activation of the BRI1 pathway leads to inhibition of PAMP-triggered immunity (PTI). Pathogens may exploit BRs as virulence factors and hijack the plant BR machinery to cause disease. An oomycete pathogen has been shown to co-opt the plant BR machinery as a decoy strategy to tap into the immune signaling circuitry and interfere with effectual SA- and GA-controlled defenses.

Keywords

Brassinosteroid Signaling Plant Innate Immunity Gibberellic Acid Signaling BRI1 Plant Pythium Graminicola 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 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 U S A 109:303–308PubMedCentralGoogle Scholar
  2. Bach TJ, Boronat A, Campos N, Ferrer A, Vollack KU (1999) Mevalonate biosynthesis in plants. Crit Rev Biochem Mol Biol 34:107–122PubMedGoogle Scholar
  3. 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 U S A 104:13839–13844PubMedPubMedCentralGoogle Scholar
  4. Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8PubMedGoogle Scholar
  5. Bak S, Beisson F, Bishop G, Hamberger B, Hȍfer R, Paquette S, Werck-Reichhart D (2011) Cytochrome p450. Arabidopsis Book 9:e0144. doi: 10.1199/tab.0144 PubMedPubMedCentralGoogle Scholar
  6. Bancos S, Nomura T, Sato T, Molnar G, Bishop GJ, Koncz C, Yokota T, Nagy F, Szekeres M (2002) Regulation of transcript levels of the Arabidopsis cytochrome p450 genes involved in brassinosteroid biosynthesis. Plant Physiol 130:504–513PubMedPubMedCentralGoogle Scholar
  7. Belkhadir Y, Chory J (2006) Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314:1410–1411PubMedGoogle Scholar
  8. Belkhadir Y, Wang X, Chory J (2006) Arabidopsis brassinosteroid signaling pathway. Sci STKE. 2006:cm5Google Scholar
  9. Belkhadir Y, Jaillais Y, Epple P, Balsemäo-Pires E, Dangl JL, Chory J (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci U S A 109:297–302PubMedPubMedCentralGoogle Scholar
  10. Bishop GJ (2007) Refining the plant steroid hormone biosynthesis pathway. Trends Plant Sci 12:377–380PubMedGoogle Scholar
  11. Bishop GJ, Koncz C (2002) Brassinosteroids and plant steroid hormone signaling. Plant Cell 14(Suppl):S97–S110PubMedPubMedCentralGoogle Scholar
  12. Bishop G, Nomura T, Yokota T, Harrison K, Noguchi T, Fujioka S, Takatsuto S, Jones JD, Kamiya Y (1999) The tomato DWARF enzyme catalyzes C-6 oxidation in brassinosteroid biosynthesis. Proc Natl Acad Sci U S A 96:1761–1766PubMedPubMedCentralGoogle Scholar
  13. Bochar DA, Freisen JA, Stauffacher CV, Rodwell VW (1999) Biosynthesis of mevalonic acid from acetyl-CoA. In: Barton D, Nakanishi K (eds) Comprehensive natural products chemistry, vol 2. Elsevier Science Ltd, Amsterdam, pp 15–44Google Scholar
  14. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–422PubMedPubMedCentralGoogle Scholar
  15. Bridges D, Moorhead BG (2005) 14-3-3 proteins: a number of functions for a numbered protein. Sci STKE 2005:re10PubMedGoogle Scholar
  16. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351PubMedGoogle Scholar
  17. Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S (2011) The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One 6(1):e16608PubMedPubMedCentralGoogle Scholar
  18. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500PubMedGoogle Scholar
  19. Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009) One for all: the receptor-associated kinase BAK1. Trends Plant Sci 14:535–541PubMedGoogle Scholar
  20. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedGoogle Scholar
  21. Dai C, Xue H-W (2010) Rice early flowering1, a CK1, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signaling. EMBO J 29:1916–1927PubMedPubMedCentralGoogle Scholar
  22. De Vleeschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi I-R, Vera-Cruz C, Kikuchi S, Höfte M (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846Google Scholar
  23. Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. N Biotechnol 26:131–136PubMedGoogle Scholar
  24. Divi UK, Krishna P (2010) Overexpression of the brassinosteroid biosynthetic gene AtDWF4 in Arabidopsis seeds overcomes abscisic acid-induced inhibition of germination and increases cold tolerance in transgenic seedlings. J Plant Growth Regul 29:385–393Google Scholar
  25. 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 10:151PubMedPubMedCentralGoogle Scholar
  26. Duan K, Li L, Hu P, Xu S-P, Xu Z-H, Xue H-W (2006) A brassinolide-suppressed rice MADS-box transcription factor, OsMDP1, has a negative regulatory role in BR signaling. Plant J 47:519–531PubMedGoogle Scholar
  27. Friedrichsen DM, Nemhauser J, Muramitsu T, Maloof JN, Alonso J, Ecker JR, Furuya M, Chory J (2002) Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 162:1445–1456PubMedPubMedCentralGoogle Scholar
  28. Fujioka S (1999) Natural occurrence of brassinosteroids in the plant kingdom. In: Sakurai A, Yokota T, Clouse SD (eds) Brassinosteroids: steroidal plant hormones. Springer, Tokyo, pp 21–45Google Scholar
  29. Fujioka S, Sakurai A (1997) Biosynthesis and metabolism of brassinosteroids. Physiol Plant 100:710–715Google Scholar
  30. Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164Google Scholar
  31. Fujioka S, Takatsuto S, Yoshida S (2002) An early C-22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiol 130:930–939PubMedPubMedCentralGoogle Scholar
  32. 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 13:177–189PubMedPubMedCentralGoogle Scholar
  33. Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng YT, Chen S, Li X, Zhang Y (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 23:34–44Google Scholar
  34. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602PubMedPubMedCentralGoogle Scholar
  35. Gendron JM, Wang ZY (2007) Multiple mechanisms modulate brassinosteroid signaling. Curr Opin Plant Biol 10:436–441PubMedCentralGoogle Scholar
  36. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334PubMedPubMedCentralGoogle Scholar
  37. 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 134:1555–1573PubMedPubMedCentralGoogle Scholar
  38. Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD, Steffens GL, Flippenanderson JL, Cook JC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217Google Scholar
  39. Hansen M, Chae H, Kieber J (2009) Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J 57:606–614PubMedPubMedCentralGoogle Scholar
  40. Hauvermale AL, Ariizumi T, Steber CM (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160:83–92PubMedPubMedCentralGoogle Scholar
  41. 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 U S A 99:10185–10190PubMedPubMedCentralGoogle Scholar
  42. He J-X, Gendron MJ, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang Z-Y (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid biosynthesis and growth responses. Science 307:1634–1638PubMedPubMedCentralGoogle Scholar
  43. He P, Shan L, Sheen J (2007) Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 9:1385–1396PubMedGoogle Scholar
  44. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, 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. Proc Natl Acad Sci U S A 104:12217–12222PubMedPubMedCentralGoogle Scholar
  45. Hwang IS, Hwang BK (2011) The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiol 155:447–463PubMedPubMedCentralGoogle Scholar
  46. Iriti M, Faoro F (2009) Chitosan as a MAMP, searching for a PRR. Plant Signal Behav 4:66–68PubMedPubMedCentralGoogle Scholar
  47. Jaillais Y, Belkhadir Y, Balsemäo-Pires E, Dangl JL, Chory J (2011a) Extracellular leucine-rich repeats as a platform for receptor/co-receptor complex formation. Proc Natl Acad Sci U S A 108:8503–8507PubMedCentralGoogle Scholar
  48. Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL, Meyerowitz EM, Chory J (2011b) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev 25:232–237PubMedPubMedCentralGoogle Scholar
  49. Jaspert N, Throm C, Oecking C (2011) Arabidopsis 14-3-3 proteins: fascinating and less fascinating aspects. Front Plant Sci 2:96. doi: 10.3389/fpls.00096 PubMedPubMedCentralGoogle Scholar
  50. Je BI, Piao HL, Park SJ, Park SH, Kim CM, Xuan YH, Park SH, Huang J, Choi YD, An G, Wong HL, Fujioka S, Kim MC, Shimamoto K, Han C-D (2010) RAV1-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 22:1777–1791PubMedPubMedCentralGoogle Scholar
  51. 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 225:353–364PubMedGoogle Scholar
  52. Kanzaki H, Saitoh H, Takahashi Y, Berberich T, Ito A, Kamoun S, Terauchi R (2008) NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta 228:977–987PubMedGoogle Scholar
  53. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Müssig C, Thomma BPHJ, Albrecht C, de Vries SC, Hirt H, Nürnberger T (2007) The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr Biol 17:1116–1122PubMedGoogle Scholar
  54. Khripach V, Zhabinskii V, Groot AD (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for XX1 century. Ann Bot 86:441–447Google Scholar
  55. Kim T-W, Wang Z-Y (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704PubMedGoogle Scholar
  56. Kim G-T, 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 41:710–721PubMedGoogle Scholar
  57. Kim T-W, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Sun Y, Burlingame AL, Wang ZY (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11:1254–1260PubMedPubMedCentralGoogle Scholar
  58. Kim T-W, Guan S, Burlingame AL, Wang Z-Y (2011) The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol Cell 19(43):561–571Google Scholar
  59. Kinoshita T, Caño-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 433:167–171PubMedGoogle Scholar
  60. Lee S, Choi SC, An G (2008) Rice SVP-group MADS-box proteins, OsMAD22 and OsMAD55, are negative regulators of brassinosteroid responses. Plant J 54:93–105PubMedGoogle Scholar
  61. Li J, Chory JA (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938PubMedGoogle Scholar
  62. Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295:1299–1301PubMedGoogle Scholar
  63. 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 110:213–222PubMedGoogle Scholar
  64. Li J, Yu X, Thompson A, Guo M, Yoshida S, Asami T, Chory J, Yin Y (2009) Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene. Plant J 58:275–286PubMedPubMedCentralGoogle Scholar
  65. 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 U S A 107:3918–3923PubMedPubMedCentralGoogle Scholar
  66. Li Q-F, Wang C, Jiang L, Li S, Sun SS, He J-X (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5:ra72PubMedGoogle Scholar
  67. Lisso J, Steinhauser D, Altmann T, Kopka J, Mussig C (2005) Identification of brassinosteroid-related genes by means of transcript co-response analyses. Nucleic Acids Res 33:2685–2696PubMedPubMedCentralGoogle Scholar
  68. Lohmann GV, Shimoda Y, Nielsen W, Jørgensen FG, Grossmann C, Sandal N, Sørensen K, Thirup S, Madsen LH, Tabata S, Sato S, Stougaard J, Radutoiu S (2010) Evolution and regulation of the Lotus japonica LysM receptor gene family. Mol Plant Microbe Interact 23:510–521PubMedGoogle Scholar
  69. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci U S A 107:495–501Google Scholar
  70. Lu D, Lin W, Gao X, Wu S, Cheng C, Avita J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 17:1439–1442Google Scholar
  71. Malinovsky FG, Batoux M, Schwessinger B, Youn JH, Stransfeld L, Win J, Kim SK, Zipfel C (2014) Antagonistic regulation of growth and immunity by the Arabidopsis basic helix-loop-helix transcription factor homolog of brassinosteroid enhanced expression2 interacting with increased leaf inclination1 binding bHLH1. Plant Physiol 164:1443–1455PubMedPubMedCentralGoogle Scholar
  72. Mathur J, Molnar G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, Adam G, Voigt B, Nagy F, Maas C, Schell J, Koncz C, Szekeres M (1998) Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J 14:593–602PubMedGoogle Scholar
  73. Mersmann S, Bourdais G, Rietz S, Robatzek S (2010) Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400PubMedPubMedCentralGoogle Scholar
  74. 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 18:448–460PubMedPubMedCentralGoogle Scholar
  75. Müssig C, Biesgen C, Lisso J, Uwer U, Weiler EW, Altmann T (2000) A novel stress-inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between brassinosteroid-action and jasmonic acid synthesis. J Plant Physiol 157:143–152Google Scholar
  76. Müssig C, Fischer S, Altmann T (2002) Brassinosteroid-regulated gene expression. Plant Physiol 129:1241–1251PubMedPubMedCentralGoogle Scholar
  77. Muto H, Yabe N, Asami T, Hasunuma K, Yamamoto KT (2004) Overexpression of constitutive differential growth 1 gene, which encodes a RLCK VII-subfamily protein kinase, causes abnormal differential and elongation growth after organ differentiation in Arabidopsis. Plant Physiol 136:3124–3133PubMedPubMedCentralGoogle Scholar
  78. Nahar K, Kyndt T, Hause B, Höfte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with jasmonate pathway. Mol Plant Microbe Interact 26:106–115PubMedGoogle Scholar
  79. Nakamura M, Satoh T, Tanaka S, Mochizuki N, Yokota T, Nagatani A (2005) Activation of the cytochrome P450 gene, CYP72C1, reduces the levels of active brassinosteroids in vivo. J Exp Bot 56:833–840Google Scholar
  80. 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 33:887–898PubMedGoogle Scholar
  81. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212PubMedGoogle Scholar
  82. Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647PubMedPubMedCentralGoogle Scholar
  83. 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 121:743–752PubMedPubMedCentralGoogle Scholar
  84. Noguchi T, Fujioka S, Choe S, Takatsuto S, Tax FE, Feldmann KA (2000) Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol 124:201–209PubMedPubMedCentralGoogle Scholar
  85. Nomura T, Sato T, Bishop GJ, Kamiya Y, Takatsuto S, Yokota T (2001) Accumulation of 6-deoxocathasterone and 6-deoxocastasterone in Arabidopsis, pea and tomato is suggestive of common rate-limiting steps in brassinosteroid biosynthesis. Phytochemistry 57:171–178PubMedGoogle Scholar
  86. Oh MH, Wang X, Kota U, Goshe MB, Clouse SD, Huber SC (2009) Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc Natl Acad Sci U S A 107:17827–17832Google Scholar
  87. Oh MH, Wang X, Wu X, Zhao Y, Clouse SD, Huber SC (2010) Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signaling and basal defense gene expression. Proc Natl Acad Sci U S A 107:17827–17832PubMedPubMedCentralGoogle Scholar
  88. Oh MH, Wu X, Clouse SD, Huber SC (2011) Functional importance of BAK1 tyrosine phosphorylation in vivo. Plant Signal Behav 6:400–405PubMedPubMedCentralGoogle Scholar
  89. Oh MH, Wang X, Clouse SD, Huber SC (2012) Deactivation of the Arabidopsis BRASSINOSTEROID INSENSITIVE 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop. Proc Natl Acad Sci U S A 109:327–332PubMedPubMedCentralGoogle Scholar
  90. Ohnishi T, Godza B, Watanabe B, Fujioka S, Hategan L, Ide K, Shibata K, Yokota T, Szekeres M, Mizutani M (2012) CYP90A1/CPD, a brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C-3 oxidation. J Biol Chem 287:31551–31560PubMedPubMedCentralGoogle Scholar
  91. Owens RA, Tech KB, Shao JY, Sano T, Baker CJ (2012) Global analysis of tomato gene expression during Potato spindle tuber viroid infection reveals a complex array of changes affecting hormone signaling. Mol Plant Microbe Interact 25:582–598PubMedGoogle Scholar
  92. 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 1:338–346PubMedPubMedCentralGoogle Scholar
  93. Peng P, Zhao J, Zhu Y, Asami T, Li J (2010) A direct docking mechanism for a plant GSK3-like kinase to phosphorylate its substrates. J Biol Chem 285:24646–24653PubMedCentralGoogle Scholar
  94. Poppenberger B, Rozhon W, Khan M, Husar S, Adam G, Luschnig C, Fujioka S, Sieberer T (2011) CESTA, a positive regulator of brassinosteroid synthesis. EMBO J 30:1149–1161PubMedPubMedCentralGoogle Scholar
  95. Postel S, Kufner I, Beueter C, Mazzotta S, Schwedt A, Borlotti A, Halter T, Kemmerling B, Nürnberger T (2010) The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol 89:169–174PubMedGoogle Scholar
  96. Qin X, Liu JH, Zhao WS, Chen XJ, Guo ZJ, Peng YL (2013) Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice. Mol Plant Microbe Interact 26:227–239PubMedGoogle Scholar
  97. Qutob D, Kemmerling B, Brunner F, Küfner I, Engelhardt S, Gust AA, Luberacki B, Seitz HU, Stahl D, Rauhut T, Glawischnig E, Schween G, Lacombe B, Watanabe N, Lam E, Schlichting R, Scheel D, Nau K, Dodt G, Hubert D, Gijzen M, Nürnberger T (2006) Phytotoxicity and innate immune responses induced by NEP1-like proteins. Plant Cell 18:3721–3744PubMedPubMedCentralGoogle Scholar
  98. Rozhon W, Mayerhofer J, Petuschnig E, Fujioka S, Jonak C (2010) Arabidopsis GSK3, functions in the brassinosteroid signalling pathway. Plant J 62:215–223PubMedPubMedCentralGoogle Scholar
  99. Ryan CA, Huffaker A, Yamaguchi Y (2007) New insights into innate immunity in Arabidopsis. Cell Microbiol 9:1902–1908PubMedGoogle Scholar
  100. 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 19:2749–2762PubMedPubMedCentralGoogle Scholar
  101. Ryu H, Cho H, Kim K, Hwang I (2010a) Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol Cell 29:283–290Google Scholar
  102. Ryu H, Kim K, Cho H, Hwang I (2010b) Predominant actions of cytosolic BSU1 and nuclear BIN2 regulate subcellular localization of BES1 in brassinosteroid signaling. Mol Cells 29:291–296PubMedGoogle Scholar
  103. Saijo Y (2010) ER quality control of immune receptors and regulators in plants. Cell Microbiol 12:716–724Google Scholar
  104. Sakamoto T, Morinka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109PubMedGoogle Scholar
  105. Schulze B, Mentzel T, Jehle A, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451PubMedPubMedCentralGoogle Scholar
  106. Schweizer P, Buchala A, Dudler RA, Metraux JP (1998) Induced systemic resistance in wounded rice plants. Plant J 14:475–481Google Scholar
  107. 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(4):e1002046PubMedPubMedCentralGoogle Scholar
  108. Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61PubMedGoogle Scholar
  109. Sehnke PC, DeLille JM, Ferl RJ (2002) Consummating signal transduction: the role of 14-3-3 proteins in the completion of signal-induced transitions in protein activity. Plant Cell 14(Suppl):S339–S354PubMedPubMedCentralGoogle Scholar
  110. Shan L, He P, Li J, Heese A, Peck SC, Nümberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27PubMedPubMedCentralGoogle Scholar
  111. 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 474:472–476PubMedPubMedCentralGoogle Scholar
  112. Shi Y, Zhu S, Mao X, Feng J, Qin Y, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664PubMedPubMedCentralGoogle Scholar
  113. 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 126:770–779PubMedPubMedCentralGoogle Scholar
  114. Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:837–842Google Scholar
  115. Shimada A, Ueguchi-Tanaka M, Sakamoto T, Fujioka S, Takatsuto S, Yoshida S, Sazuka T, Ashikari M, Matsuoka M (2006) The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J 48:390–402PubMedGoogle Scholar
  116. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KE, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234PubMedPubMedCentralGoogle Scholar
  117. Song L, Shi QM, Yang XH, Xu ZH, Xue HW (2009) Membrane steroid-binding protein 1 (MSBP1) negatively regulates brassinosteroid signaling by enhancing the endocytosis of BAK1. Cell Res 19:864–876PubMedGoogle Scholar
  118. Sun Y, Fan X-Y, Cao D-M, He K, Tang W, Zhu J-Y, He J-X, Bai M-Y, Zhu S, Oh E, Patil S, Kim T-W, Ji H, Wong WH, Rhee SY, Wang Z-Y (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777PubMedPubMedCentralGoogle Scholar
  119. 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 138:1117–1125PubMedPubMedCentralGoogle Scholar
  120. Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, Zhu S, Wang R, Burlingame AL, Wang Z-Y (2008) Brassinosteroid-signaling kinases (BSKs) mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321:557–560PubMedPubMedCentralGoogle Scholar
  121. Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, Gendron JM, Jonassen EM, Lillo C, DeLong A, Burlingame AL, Sun Y, Wang ZY (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13:124–131PubMedPubMedCentralGoogle Scholar
  122. Tsuda K, Katagiri P (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465PubMedGoogle Scholar
  123. van Verk MC, Pappaaioannou D, Neeleman L, Bol JF, Linthorst HJM (2008) A novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol 140:1983–1995Google Scholar
  124. Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signaling. Nature 441:96–100PubMedGoogle Scholar
  125. Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci U S A 105:9829–9834PubMedPubMedCentralGoogle Scholar
  126. Vidhyasekaran P (2007) Fungal pathogenesis in plants and crops: molecular biology and host defense mechanisms, 2nd edn. CRC Press, Taylor Francis Group, Boca Raton, pp 510Google Scholar
  127. Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24:842–857PubMedPubMedCentralGoogle Scholar
  128. Wan J, Zhang X-C, Stacey G (2008) Chitin signaling and plant disease resistance. Plant Signal Behav 3:831–833PubMedCentralGoogle Scholar
  129. Wang Z-Y (2012) Brassinosteroids modulate plant innate immunity at multiple levels. Proc Natl Acad Sci U S A 109:7–8PubMedPubMedCentralGoogle Scholar
  130. Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1, from the plasma membrane. Science 313:1118–1122Google Scholar
  131. Wang Z-Y, He J-X (2004) Brassinosteroid signal transduction – choices of signals and receptors. Trends Plant Sci 9:91–96Google Scholar
  132. 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 410:380–383PubMedGoogle Scholar
  133. 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 2:505–513PubMedGoogle Scholar
  134. Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005a) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase. Plant Cell 17:1685–1703PubMedPubMedCentralGoogle Scholar
  135. Wang X, Li X, Meisenhelder J, Hunter T, Yoshida S, Asami T, Chory J (2005b) Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev Cell 8:855–865PubMedGoogle Scholar
  136. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Clouse SD (2008) Sequential transphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220–235PubMedGoogle Scholar
  137. Xia X-J, Wang Y-J, Zhou Y-H, Tao Y, Mao W-H, Shi K, Asami T, Chen Z, Yu J-Q (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–804PubMedPubMedCentralGoogle Scholar
  138. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou J-M (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedGoogle Scholar
  139. Yang DH, Hettenhausen C, Baldwin IT, Wu J (2011a) BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata’s responses to herbivory. J Exp Bot 62:641–652PubMedPubMedCentralGoogle Scholar
  140. Yang DH, Hettenhausen C, Baldwin IT, Wu J (2011b) The multifaceted function of BAK1/SERK3: plant immunity to pathogens and responses to insect herbivores. Plant Signal Behav 6:1322–1324PubMedPubMedCentralGoogle Scholar
  141. Ye H, Li L, Yin Y (2011) Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J Integr Plant Biol 53:455–468PubMedGoogle Scholar
  142. 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 109:181–191PubMedGoogle Scholar
  143. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259PubMedGoogle Scholar
  144. Yokota T, Nomura T, Nakayama M (1997) Identification of brassinosteroids that appear to be derived from campesterol and cholesterol in tomato shoots. Plant Cell Physiol 38:1291–1294Google Scholar
  145. Yu X, 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 BES1 target genes in Arabidopsis thaliana. Plant J 65:634–646PubMedGoogle Scholar
  146. Yun HS, Bae YH, Lee YJ, Chang SC, Kim SK, Li J, Nam KH (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 27:183–190PubMedGoogle Scholar
  147. Zhang J, Zhou J-M (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793PubMedGoogle Scholar
  148. Zhang S, Cai Z, Wang X (2009a) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Natl Acad Sci U S A 106:4543–4548PubMedPubMedCentralGoogle Scholar
  149. Zhang S, Wei Y, Lu Y, Wang X (2009b) Mechanisms of brassinosteroids interacting with multiple hormones. Plant Signal Behav 4:1117–1120PubMedPubMedCentralGoogle Scholar
  150. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou JM (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301PubMedGoogle Scholar
  151. Zhou A, Wang H, Walker JC, Li J (2004) BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BR1 in regulating Arabidopsis brassinosteroid signaling. Plant J 40:399–409PubMedGoogle Scholar
  152. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16PubMedGoogle Scholar
  153. Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • P. Vidhyasekaran
    • 1
  1. 1.Plant PathologyTamil Nadu Agricultural UniversityCoimbatoreIndia

Personalised recommendations