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PMID: 19386805 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber.

Plant physiology ·Vol. 150 ·No. 2 ·2009-06-00 ·Pages 801-14

Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ

Abstract

Brassinosteroids (BRs) induce plant tolerance to a wide spectrum of stresses. To study how BR induces stress tolerance, we manipulated the BR levels in cucumber (Cucumis sativus) through a chemical genetics approach and found that BR levels were positively correlated with the tolerance to photo-oxidative and cold stresses and resistance to Cucumber mosaic virus. We also showed that BR treatment enhanced NADPH oxidase activity and elevated H(2)O(2) levels in apoplast. H(2)O(2) levels were elevated as early as 3 h and returned to basal levels 3 d after BR treatment. BR-induced H(2)O(2) accumulation was accompanied by increased tolerance to oxidative stress. Inhibition of NADPH oxidase and chemical scavenging of H(2)O(2) reduced BR-induced oxidative and cold tolerance and defense gene expression. BR treatment induced expression of both regulatory genes, such as RBOH, MAPK1, and MAPK3, and genes involved in defense and antioxidant responses. These results strongly suggest that elevated H(2)O(2) levels resulting from enhanced NADPH oxidase activity are involved in the BR-induced stress tolerance.

MeSH Terms
Adaptation, Physiological/drug effects Antioxidants/metabolism Brassinosteroids Cholestanols/pharmacology Cold Temperature Cucumis sativus/drug effects,genetics,physiology,virology Cucumovirus/drug effects,physiology Gene Expression Regulation, Plant/drug effects Hydrogen Peroxide/metabolism Kinetics Models, Biological Molecular Sequence Data Paraquat/pharmacology RNA, Messenger/genetics,metabolism Reactive Oxygen Species/metabolism Steroids, Heterocyclic/pharmacology Stress, Physiological/drug effects Time Factors
Chemicals
Antioxidants Brassinosteroids Cholestanols RNA, Messenger Reactive Oxygen Species Steroids, Heterocyclic Hydrogen Peroxide Paraquat brassinolide
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Xia Xiao-Jian
Department of Horticulture, Zhejiang University, Hangzhou 310029, China.
Wang Yan-Jie
Zhou Yan-Hong
Tao Yuan
Mao Wei-Hua
Shi Kai
Asami Tadao
Chen Zhixiang
Yu Jing-Quan
References (67)
67 references, click to expand
  1. Hydrogen peroxide signalling.
    Curr Opin Plant Biol. 2002 Oct;5(5):388-95 PMID: 12183176
  2. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  3. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis.
    Plant Physiol. 2002 Nov;130(3):1319-34 PMID: 12427998
  4. Activation of Host Defense Mechanisms by Elevated Production of H2O2 in Transgenic Plants.
    Plant Physiol. 1997 Oct;115(2):427-435 PMID: 12223817
  5. Downstream nuclear events in brassinosteroid signalling.
    Nature. 2006 May 4;441(7089):96-100 PMID: 16672972
  6. 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. 2002 Dec;14(12):3163-76 PMID: 12468734
  7. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1.
    Nature. 2005 Jan 13;433(7022):167-71 PMID: 15650741
  8. Brassinosteroid-induced exaggerated growth in hydroponically grown Arabidopsis plants.
    Physiol Plant. 2001 May;112(1):104-112 PMID: 11319021
  9. Regulation of transcript levels of the Arabidopsis cytochrome p450 genes involved in brassinosteroid biosynthesis.
    Plant Physiol. 2002 Sep;130(1):504-13 PMID: 12226529
  10. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation.
    Cell. 2002 Apr 19;109(2):181-91 PMID: 12007405
  11. Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta.
    J Biol Chem. 2001 Jul 13;276(28):25687-91 PMID: 11319239
  12. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels.
    Plant J. 1997 May;11(5):993-1005 PMID: 9193071
  13. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis.
    Nature. 2004 Feb 26;427(6977):858-61 PMID: 14985766
  14. Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide.
    Plant Cell. 1994 Jan;6(1):65-74 PMID: 12244221
  15. A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus.
    J Exp Bot. 2004 May;55(399):1135-43 PMID: 15107450
  16. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction.
    Cell. 1997 Sep 5;90(5):929-38 PMID: 9298904
  17. A role of brassinosteroids in early fruit development in cucumber.
    J Exp Bot. 2008;59(9):2299-308 PMID: 18515830
  18. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide.
    Science. 1996 Sep 27;273(5283):1853-6 PMID: 8791589
  19. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses.
    Planta. 2007 Jan;225(2):353-64 PMID: 16906434
  20. Do brassinosteroids mediate the water stress response?
    Physiol Plant. 2008 Jun;133(2):417-25 PMID: 18282191
  21. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis.
    Cell. 1996 Apr 19;85(2):171-82 PMID: 8612270
  22. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor.
    Plant Physiol. 2000 May;123(1):93-100 PMID: 10806228
  23. The role of reactive oxygen species in hormonal responses.
    Plant Physiol. 2006 Jun;141(2):323-9 PMID: 16760482
  24. The role of abscisic acid in plant-pathogen interactions.
    Curr Opin Plant Biol. 2005 Aug;8(4):409-14 PMID: 15939661
  25. Molecular players regulating the jasmonate signalling network.
    Curr Opin Plant Biol. 2005 Oct;8(5):532-40 PMID: 16039901
  26. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.
    Plant Cell. 1997 Feb;9(2):209-21 PMID: 9061952
  27. Signaling of systemic acquired resistance in tobacco depends on ethylene perception.
    Plant J. 2003 Jul;35(1):27-32 PMID: 12834399
  28. Commentary to: "Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds" by Hodges et al., Planta (1999) 207:604-611.
    Planta. 2017 Jun;245(6):1067 PMID: 28456836
  29. Networks of WRKY transcription factors in defense signaling.
    Curr Opin Plant Biol. 2007 Aug;10(4):366-71 PMID: 17644023
  30. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling.
    Cell. 2002 Jul 26;110(2):213-22 PMID: 12150929
  31. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.
    Plant Physiol. 2001 Aug;126(4):1438-48 PMID: 11500543
  32. Signal crosstalk and induced resistance: straddling the line between cost and benefit.
    Annu Rev Phytopathol. 2005;43:545-80 PMID: 16078895
  33. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death.
    Bioessays. 2006 Nov;28(11):1091-101 PMID: 17041898
  34. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism.
    Planta. 1976 Jan;133(1):21-5 PMID: 24425174
  35. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.
    Science. 1999 Apr 23;284(5414):654-7 PMID: 10213690
  36. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling.
    Cell. 2002 Jul 26;110(2):203-12 PMID: 12150928
  37. Brassinosteroids and plant steroid hormone signaling.
    Plant Cell. 2002;14 Suppl:S97-110 PMID: 12045272
  38. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint.
    Plant Cell. 2000 Sep;12(9):1591-606 PMID: 11006334
  39. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis.
    Genes Dev. 2004 Feb 15;18(4):448-60 PMID: 14977918
  40. 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 Jul 23;99(15):10185-90 PMID: 12114546
  41. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways.
    Curr Biol. 2007 Jul 3;17(13):1109-15 PMID: 17600708
  42. Brassinosteroid-regulated gene expression.
    Plant Physiol. 2002 Jul;129(3):1241-51 PMID: 12114578
  43. A role for brassinosteroids in light-dependent development of Arabidopsis.
    Science. 1996 Apr 19;272(5260):398-401 PMID: 8602526
  44. Lipid peroxidation associated with accelerated aging of soybean axes.
    Plant Physiol. 1980 Feb;65(2):245-8 PMID: 16661168
  45. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.
    Annu Rev Plant Biol. 2004;55:373-99 PMID: 15377225
  46. Chlorophyll fluorescence--a practical guide.
    J Exp Bot. 2000 Apr;51(345):659-68 PMID: 10938857
  47. Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings.
    Plant Mol Biol. 1999 May;40(2):333-42 PMID: 10412911
  48. BRI1 is a critical component of a plasma-membrane receptor for plant steroids.
    Nature. 2001 Mar 15;410(6826):380-3 PMID: 11268216
  49. Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis.
    Plant J. 2000 Dec;24(5):693-701 PMID: 11123807
  50. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings
    Plant Physiol. 1998 Apr;116(4):1351-7 PMID: 9536052
  51. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance.
    J Biol Chem. 2006 Dec 8;281(49):37636-45 PMID: 17015446
  52. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control.
    Curr Biol. 2007 Jul 3;17(13):1116-22 PMID: 17583510
  53. Emerging MAP kinase pathways in plant stress signalling.
    Trends Plant Sci. 2005 Jul;10(7):339-46 PMID: 15953753
  54. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.
    Curr Opin Plant Biol. 2005 Aug;8(4):397-403 PMID: 15939662
  55. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  56. Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface.
    Science. 2006 Dec 1;314(5804):1410-1 PMID: 17138891
  57. Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress.
    Plant J. 2002 Mar;29(6):681-91 PMID: 12148527
  58. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2940-5 PMID: 10717008
  59. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase.
    Science. 2002 Feb 15;295(5558):1299-301 PMID: 11847343
  60. BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:427-451 PMID: 15012241
  61. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling.
    Plant Cell. 2003 Jan;15(1):63-78 PMID: 12509522
  62. The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea.
    Plant J. 2003 Nov;36(3):291-300 PMID: 14617087
  63. Brassinosteroid-Mediated Stress Responses.
    J Plant Growth Regul. 2003 Dec;22(4):289-297 PMID: 14676968
  64. Involvement of hydrogen peroxide in the regulation of senescence in pear.
    Plant Physiol. 1977 Mar;59(3):411-6 PMID: 16659863
  65. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.
    Curr Opin Plant Biol. 2006 Aug;9(4):436-42 PMID: 16759898
  66. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice.
    Plant J. 2003 Mar;33(5):887-98 PMID: 12609030
  67. Comparative biochemistry of the oxidative burst produced by rose and french bean cells reveals two distinct mechanisms
    Plant Physiol. 1998 Apr;116(4):1379-85 PMID: 9536055
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
DOI
10.1104/pp.109.138230
Published
2009-06-00
Epub
2009-00-22
Pages
801-14
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2689980
Subset
IM
Databases
GENBANK
AAZ74666, AF229811, AF475285, AJ249329, AY274258, D26392, D88649, DQ641122, EW968286, FJ036894, FJ036895, FJ036896, FJ036897, FJ036898, FJ036899, M91373, X67695
External Links
PubMed source DOI: 10.1104/pp.109.138230 PMC Full Text View journal details
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