Home LiteratureArticle Details
PMID: 17905862 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens.

Plant physiology ·Vol. 145 ·No. 3 ·2007-11-00 ·Pages 890-904

Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK

Abstract

Reactive oxygen species (ROS) are responsible for mediating cellular defense responses in plants. Controversy has existed over the origin of ROS in plant defense. We have isolated a novel extracellular peroxidase gene, CaPO2, from pepper (Capsicum annuum). Local or systemic expression of CaPO2 is induced in pepper by avirulent Xanthomonas campestris pv vesicatoria (Xcv) infection. We examined the function of the CaPO2 gene in plant defense using the virus-induced gene silencing technique and gain-of-function transgenic plants. CaPO2-silenced pepper plants were highly susceptible to Xcv infection. Virus-induced gene silencing of the CaPO2 gene also compromised hydrogen peroxide (H(2)O(2)) accumulation and hypersensitive cell death in leaves, both locally and systemically, during avirulent Xcv infection. In contrast, overexpression of CaPO2 in Arabidopsis (Arabidopsis thaliana) conferred enhanced disease resistance accompanied by cell death, H(2)O(2) accumulation, and PR gene induction. In CaPO2-overexpression Arabidopsis leaves infected by Pseudomonas syringae pv tomato, H(2)O(2) generation was sensitive to potassium cyanide (a peroxidase inhibitor) but insensitive to diphenylene iodonium (an NADPH oxidase inhibitor), suggesting that H(2)O(2) generation depends on peroxidase in Arabidopsis. Together, these results indicate that the CaPO2 peroxidase is involved in ROS generation, both locally and systemically, to activate cell death and PR gene induction during the defense response to pathogen invasion.

MeSH Terms
Arabidopsis/genetics,metabolism Capsicum/enzymology Cell Death/physiology Chlorates Gene Expression Regulation, Plant Gene Silencing Hydrogen Peroxide/metabolism Magnesium Compounds Peroxidases/metabolism Plant Diseases/microbiology Plant Leaves/metabolism,microbiology Respiratory Burst Transcriptional Activation
Chemicals
Chlorates Magnesium Compounds Hydrogen Peroxide Peroxidases magnesium chlorate
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Choi Hyong Woo
College of Life Sciences and Biotechnology, Korea University, Seoul 136-713, Republic of Korea.
Kim Young Jin
Lee Sung Chul
Hong Jeum Kyu
Hwang Byung Kook
References (48)
48 references, click to expand
  1. Vascular defense responses in rice: peroxidase accumulation in xylem parenchyma cells and xylem wall thickening.
    Mol Plant Microbe Interact. 2001 Dec;14(12):1411-9 PMID: 11768536
  2. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals.
    Biochem Pharmacol. 1999 Feb 1;57(3):231-45 PMID: 9890550
  3. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death.
    Plant J. 2000 Aug;23(4):441-50 PMID: 10972870
  4. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.
    Cell. 1998 Mar 20;92(6):773-84 PMID: 9529253
  5. Virus-induced gene silencing in tomato.
    Plant J. 2002 Sep;31(6):777-86 PMID: 12220268
  6. 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
  7. Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells.
    Free Radic Res. 1999 Dec;31 Suppl:S137-45 PMID: 10694052
  8. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  9. Isolation, partial sequencing, and expression of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria.
    Mol Plant Microbe Interact. 2000 Jan;13(1):136-42 PMID: 10656596
  10. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275 PMID: 15012264
  11. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):517-22 PMID: 11756663
  12. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response.
    Cell. 1992 Jul 10;70(1):21-30 PMID: 1623521
  13. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction.
    Plant Cell Rep. 2003 Jun;21(9):829-37 PMID: 12789499
  14. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox).
    Plant J. 1998 May;14(3):365-70 PMID: 9628030
  15. A method of high frequency virus-induced gene silencing in chili pepper (Capsicum annuum L. cv. Bukang).
    Mol Cells. 2004 Apr 30;17(2):377-80 PMID: 15179058
  16. Resistance gene-dependent plant defense responses.
    Plant Cell. 1996 Oct;8(10):1773-91 PMID: 8914325
  17. Reactive oxygen signalling: the latest news.
    Curr Opin Plant Biol. 2004 Jun;7(3):323-8 PMID: 15134754
  18. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance.
    Cell. 2003 Feb 7;112(3):379-89 PMID: 12581527
  19. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  20. The respiratory burst of phagocytes.
    J Clin Invest. 1984 Mar;73(3):599-601 PMID: 6323522
  21. Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum.
    Planta. 2005 Aug;221(6):790-800 PMID: 15729568
  22. Expression of peroxidase-like genes, H2O2 production, and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum.
    Mol Plant Microbe Interact. 2003 Mar;16(3):196-205 PMID: 12650451
  23. Fast forward genetics based on virus-induced gene silencing.
    Curr Opin Plant Biol. 1999 Apr;2(2):109-13 PMID: 10322199
  24. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?
    Trends Plant Sci. 2003 Jun;8(6):263-71 PMID: 12818660
  25. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.
    Plant Physiol. 2001 Aug;126(4):1438-48 PMID: 11500543
  26. Peroxidases have more functions than a Swiss army knife.
    Plant Cell Rep. 2005 Jul;24(5):255-65 PMID: 15856234
  27. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  28. A large family of class III plant peroxidases.
    Plant Cell Physiol. 2001 May;42(5):462-8 PMID: 11382811
  29. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene.
    Plant J. 1996 Sep;10(3):515-22 PMID: 8811865
  30. Properties, functions, and secretion of human myeloperoxidase.
    Biochemistry (Mosc). 2004 Jan;69(1):4-9 PMID: 14972011
  31. Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death.
    Plant J. 2004 Jun;38(6):940-53 PMID: 15165186
  32. Function of the oxidative burst in hypersensitive disease resistance.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4158-63 PMID: 11607542
  33. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.
    Plant Cell. 2001 Jan;13(1):179-91 PMID: 11158538
  34. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.
    Annu Rev Plant Biol. 2004;55:373-99 PMID: 15377225
  35. Hydroperoxide assay with the ferric-xylenol orange complex.
    Anal Biochem. 1999 Sep 10;273(2):149-55 PMID: 10469484
  36. Performing the paradoxical: how plant peroxidases modify the cell wall.
    Trends Plant Sci. 2004 Nov;9(11):534-40 PMID: 15501178
  37. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.
    Plant Cell. 2003 Mar;15(3):706-18 PMID: 12615943
  38. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance.
    Plant J. 2006 Sep;47(6):851-63 PMID: 16889645
  39. Active Oxygen Species in Plant Defense against Pathogens.
    Plant Physiol. 1994 Jun;105(2):467-472 PMID: 12232215
  40. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana.
    Nat Genet. 2005 Oct;37(10):1130-4 PMID: 16170317
  41. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
    Plant Cell. 1998 Feb;10(2):255-66 PMID: 9490748
  42. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana.
    Science. 2004 Nov 12;306(5699):1183-5 PMID: 15539603
  43. Short communication: subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells.
    Plant J. 1999 Nov;20(3):349-56 PMID: 10571895
  44. 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
  45. Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species.
    Plant Physiol. 2005 Oct;139(2):935-48 PMID: 16169957
  46. Arabidopsis is susceptible to infection by a downy mildew fungus.
    Plant Cell. 1990 May;2(5):437-45 PMID: 2152169
  47. Synthesis of dehydrogenation polymers of ferulic acid with high specificity by a purified cell-wall peroxidase from French bean (Phaseolus vulgaris L.).
    Biochem J. 1994 May 1;299 ( Pt 3):747-53 PMID: 8192663
  48. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2007-11-00
Epub
2007-00-28
Pages
890-904
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2048806
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]