Trade-off between growth and immunity: Role of brassinosteroids

Trends in Plant Science

Volumn 20, Issue 1, 2015, Pages 12-19

  Lozano Durán, Rosa ^a   Zipfel, Cyril ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

Author keywords

BZR1; Crosstalk; Growth; Immunity; Trade off; Transcriptional regulation

Indexed keywords

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; TRANSCRIPTION FACTOR;

ARABIDOPSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84920133713     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2014.09.003     Document Type: Review

References (85)

1. Vert G., Chory K. Crosstalk in cellular signaling: background noise or the real thing?. Dev. Cell 2011, 21:985-991.
2. Herms D.A., Mattson W.J. The dilemma of plants: to grow or defend. Q. Rev. Biol. 1992, 67:283-335.
3. Pieterse C.M., et al. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28:489-521.
4. Walters D., Heils M. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 2007, 71:3-17.
5. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60:379-406.
6. De Vleesschauwer D., et al. Hormone defense networking in rice: tales from a different world. Trends Plant Sci. 2013, 18:555-565.
7. Denance N., et al. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 2013, 4:155.
8. Huot B., et al. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 2014, 7:1267-1287.
9. Albrecht C., et al. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:303-308.
10. Belkhadir Y., et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:297-302.
11. Chandran D., et al. Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid. Cell Host Microbe 2014, 15:506-513.
12. Fan M., et al. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 2014, 26:828-841.
13. Lozano-Duran R., et al. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. Elife 2013, 2:e00983.
14. Malinovsky F.G., et al. 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. 2014, 164:1443-1455.
15. Navarro L., et al. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 2008, 18:650-655.
16. Yang D.L., et al. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E1192-E1200.
17. Clouse S.D. Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 2011, 23:1219-1230.
18. Zhu J.Y., et al. Brassinosteroid signalling. Development 2013, 140:1615-1620.
19. He Z., et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 2000, 288:2360-2363.
20. Hothorn M., et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 2011, 474:467-471.
21. Kinoshita T., et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 2005, 433:167-171.
22. She J., et al. Structural insight into brassinosteroid perception by BRI1. Nature 2011, 474:472-476.
23. Li J., et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 2002, 110:213-222.
24. Nam K.H., Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 2002, 110:203-212.
25. Jaillais Y., et al. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 2011, 25:232-237.
26. Wang X., Chory J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 2006, 313:1118-1122.
27. Wang X., et al. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 2005, 17:1685-1703.
28. Wang X., et al. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 2008, 15:220-235.
29. Wang H., et al. Dual role of BKI1 and 14-3-3s in brassinosteroid signaling to link receptor with transcription factors. Dev. Cell 2011, 21:825-834.
30. Lin W., et al. Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:12114-12119.
31. Kim T.W., et al. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 2011, 43:561-571.
32. Tang W., et al. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 2008, 321:557-560.
33. Kim T.W., et al. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 2009, 11:1254-1260.
34. Mora-Garcia S., et al. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 2004, 18:448-460.
35. Peng P., et al. Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation. Mol. Plant 2008, 1:338-346.
36. He J.X., et al. 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. 2002, 99:10185-10190.
37. Vert G., Chory J. Downstream nuclear events in brassinosteroid signalling. Nature 2006, 441:96-100.
38. Wang Z.Y., et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2002, 2:505-513.
39. Yin Y., et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 2002, 109:181-191.
40. Gampala S.S., et al. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 2007, 13:177-189.
41. Ryu H., et al. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 2007, 19:2749-2762.
42. Tang W., et al. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 2011, 13:124-131.
43. Sun Y., et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 2010, 19:765-777.
44. Yu X., et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 2011, 65:634-646.
45. Gomez-Gomez L., Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 2000, 5:1003-1011.
46. Chinchilla D., et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007, 448:497-500.
47. Heese A., et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12217-12222.
48. Schulze B., et al. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 2010, 285:9444-9451.
49. Kadota Y., et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 2014, 54:43-55.
50. Laluk K., et al. Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 2011, 23. 2831-49.
51. Lu D., et al. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:496-501.
52. Zhang J., et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 2010, 7:290-301.
53. Li L., et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 2014, 15:329-338.
54. Shi H., et al. BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 2013, 25:1143-1157.
55. 2+ sensor protein kinases. Nature 2010, 464:418-422.
56. Tena G., et al. Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 2011, 14:519-529.
57. Sun Y., et al. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res. 2013, 23:1326-1329.
58. Sun Y., et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 2013, 342:624-628.
59. Wang Z.Y. Brassinosteroids modulate plant immunity at multiple levels. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:7-8.
60. Gimenez-Ibanez S., et al. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 2009, 19:423-429.
61. Ranf S., et al. Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J. 2011, 68:100-113.
62. Shan L., et al. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 2008, 4:17-27.
63. Luna E., et al. Callose deposition: a multifaceted plant defense response. Mol. Plant Microbe Interact. 2011, 24:183-193.
64. Bucherl C.A., et al. Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol. 2013, 162:1911-1925.
65. Diévart A., et al. Brassinosteroid-independent function of BRI1/CLV1 chimeric receptors. Funct. Plant Biol. 2006, 33.
66. Santiago J., et al. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 2013, 341:889-892.
67. Bai M.Y., et al. 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 2012, 24:4917-4929.
68. Choudhary S.P., et al. Benefits of brassinosteroid crosstalk. Trends Plant Sci. 2012, 17:594-605.
69. Bai M.Y., et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat. Cell Biol. 2012, 14:810-817.
70. Gallego-Bartolome J., et al. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:13446-13451.
71. Li Q.F., et al. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci. Signal. 2012, 5:ra72.
72. Kim B., et al. Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in Arabidopsis. Plant J. 2014, 77:737-747.
73. Luo X.M., et al. Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev. Cell 2010, 19:872-883.
74. Oh E., et al. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 2012, 14:802-809.
75. Wang C., et al. Identification of BZR1-interacting proteins as potential components of the brassinosteroid signaling pathway in Arabidopsis through tandem affinity purification. Mol. Cell. Proteomics 2013, 12:3653-3665.
76. Kim B., et al. Arabidopsis brassinosteroid-overproducing gulliver3-D/dwarf4-D mutants exhibit altered responses to jasmonic acid and pathogen. Plant Cell Rep. 2013, 32:1139-1149.
77. Kemen E., et al. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol. 2011, 9:e1001094.
78. Nakashita H., et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 2003, 33:887-898.
79. De Vleesschauwer D., et al. Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol. 2012, 158:1833-1846.
80. Nahar K., et al. Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol. Plant Microbe Interact. 2013, 26:106-115.
81. Ali S.S., et al. Brassinosteroid enhances resistance to Fusarium diseases of barley. Phytopathology 2013, 103:1260-1267.
82. Chono M., et al. A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol. 2003, 133:1209-1219.
83. Chen G., et al. The non-gibberellic acid-responsive semi-dwarfing gene uzu affects Fusarium crown rot resistance in barley. BMC Plant Biol. 2014, 14:22.
84. Ali S.S., et al. Plant disease resistance is augmented in uzu barley lines modified in the brassinosteroid receptor BRI1. BMC Plant Biol. 2014, 14:227.
85. Goddard R., et al. Enhanced disease resistance caused by BRI1 mutation is conserved between Brachypodium distachyon and barley (Hordeum vulgare). Mol. Plant Microbe Interact. 2014, 27:1095-1106.