Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance

Plant Journal

Volumn 47, Issue 6, 2006, Pages 851-863

  Bindschedler, Laurence V ^a,d   Dewdney, Julia ^b,c   Blee, Kris A ^a,e   Stone, Julie M ^b,c,f   Asai, Tsuneaki ^b,c,g   Plotnikov, Julia ^b,c   Denoux, Carine ^b,c   Hayes, Tezni ^a   Gerrish, Chris ^a   Davies, Dewi R ^a   Ausubel, Frederick M ^b,c   Bolwell, G Paul ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF READING   (United Kingdom)

^e CALIFORNIA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^g TOKAI UNIVERSITY   (Japan)

Author keywords

Apoplastic peroxidase; Arabidopsis; Oxidative burst; Reactive oxygen species

Indexed keywords

APOPLASTIC PEROXIDASE; ARABIDOPSIS; OXIDATIVE BURST; REACTIVE OXYGEN SPECIES;

DNA; GENETIC ENGINEERING; HYDROGEN PEROXIDE; PLANTS (BOTANY);

ENZYME KINETICS;

FUMONISIN; FUMONISIN B1; PEROXIDASE; REACTIVE OXYGEN METABOLITE;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; FUNGUS; GENE EXPRESSION PROFILING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; RESPIRATORY BURST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT;

ARABIDOPSIS; FUMONISINS; FUNGI; GENE EXPRESSION PROFILING; PEROXIDASES; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ENZYMES; HYDROGEN PEROXIDE; NUCLEIC ACIDS; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); FUSARIUM OXYSPORUM; PHASEOLUS VULGARIS;

EID: 33748297455     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02837.x     Document Type: Article

References (62)

1. Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B. and Martin, G.B. (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69.
2. Alvarez, M.E., Pennell, R.I., Meijer, P.-J., Ishikawa, A., Dixon, R.A. and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 93, 773-784.
3. Apel, K. and Hirt, H. (2004) reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
4. Bennett, M., Mehta, M. and Grant, M. (2005) Biophoton imaging; a non-destructive method for assaying R gene responses. Mol. Plant Microb. Interact. 18, 95-102.
5. Bestwick, C.S., Brown, I.R., Bennett, M.H.R. and Mansfield, J.W. (1997) Localisation of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell, 9, 209-221.
6. 2+. New Phytol. 151, 185-194.
7. Blee, K. A., Jupe, S.C., Richard, G., Zimmerlin, A., Davies, D.R. and Bolwell, G.P. (2001) Molecular identification and expression of the peroxidase responsible for the oxidative burst in French bean (Phaseolus vulgaris L.) and related members of the gene family. Plant Mol. Biol. 47, 607-620.
8. Blee, K.A., Choi, J.-W., O'Connell, A.P., Schuch, W., Lewis, N.G. and Bolwell, G.P. (2003) A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry, 64, 163-176.
9. Bolwell, G.P. (1999) Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 2, 287-294.
10. Bolwell, G.P. and Wojtaszek, P. (1997) Mechanisms for the generation of reactive oxygen species in plant defence - a broad perspective. Physiol. Mol. Plant Pathol. 51, 347-366.
11. Bolwell, G.P., Davies, D.R., Gerrish, C., Auh, C.K. and Murphy, T.M. (1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol. 116, 1379-1385.
12. Bolwell, G.P., Bindschedler, L.V., Blee, K.A., Butt, V.S., Davies, D.R., Gardner, S.L., Gerrish, C. and Minibayeva, F. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three component system. J. Exp. Bot. 53, 1367-1376.
13. Charmont, S., Jamet, E., Pont-Lezica, R. and Canut, H. (2005) Proteomic analysis of secreted proteins from Arabidopsis thaliana seedlings: improved recovery following removal of phenolic compounds. Phytochemistry, 66, 453-461.
14. Chen, Z., Kloek, A.P., Cuzick, A., Moeder, W., Tang, D., Innes, R.W., Klessig, D.F., McDowell, J.M. and Kunkel, B.N. (2004) The Pseudomonas syringae type III effector AvrRpt2 functions downstream or independently of SA to promote virulence on Arabidopsis thaliana. Plant J. 37, 494-504.
15. Chisholm, S.T., Dahlbeck, D., Krishnamurthy, N., Day, B., Sjolander, K. and Staskawicz, B.J. (2005) Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc. Natl Acad. Sci. USA, 102, 2087-2092.
16. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
17. Cuppels, D.A. (1986) Generation and characterisation of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl. Environ. Microbiol. 52, 323-327.
18. Debener, T., Lehnackers, H., Arnold, M. and Dangl, J.L. (1991) Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J. 1, 289-302.
19. Delledonne, M. (2005) NO news is good news for plants. Curr. Opin. Plant Biol. 8, 390-396.
20. Dewdney, J., Reuber, T.L., Wildermuth, M.C., Devoto, A., Cui, J., Stutius, L.M., Drummond, E.P. and Ausubel, F.M. (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24, 205-218.
21. Dong, X., Mindrinos, M., Davis, K.R. and Ausubel, F.M. (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell, 3, 61-72.
22. Duroux, L. and Welinder, K.G. (2003) The peroxidase gene family in plants: a phylogenetic overview. J. Mol. Evol. 57, 397-407.
23. Ferrari, S., Plotnikova, J.M., De Lorenzo, G. and Ausubel, F.M. (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35, 193-205.
24. 2-reducing activity of horseradish peroxidase by diphenyleneiodonium. Phytochemistry, 48, 223-227.
25. Gilchrist, D.G. (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu. Rev. Phytopathol. 36, 393-414.
26. Glazebrook, J., Rogers, E.E. and Ausubel, F.M. (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics, 143, 973-982.
27. Grant, J.J. and Loake, G.J. (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124, 21-29.
28. Grant, J.J., Yun, B.-W. and Loake, G.J. (2000a) Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J. 24, 569-582.
29. Grant, M., Brown, I., Adams, S., Knight, M., Ainslie, A. and Mansfield, J. (2000b) 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. 23, 441-450.
30. Greenberg, J.T. and Vinatzer, B.A. (2003) Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6, 20-28.
31. Hauck, P., Thilmony, R. and He, S.Y. (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl Acad. Sci. USA, 100, 8577-8582.
32. 2+ binding motifs. Plant Cell, 10, 255-266.
33. Kim, M.G., da Cunha, L., McFall, A.J., Belkhadir, Y., Debroy, S., Dangl, J.L. and Mackey, D. (2005) Two Pseudomonas syringae type III effectors Inhibit RIN4-regulated basal defense in Arabidopsis. Cell, 121, 749-759.
34. Kistler, H.C., Momol, E.A. and Benny, U. (1991) Repetitive genomic sequences for determining relatedness among strains of Fusarium-Oxysporum. Phytopathology, 81, 331-336.
35. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. and Dangl, J.L. (1999) LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12, 1022-1026.
36. Lamb, C. and Dixon, R.A. (1997) The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
37. Mach, J.M., Castillo, A.R., Hoogstraten, R. and Greenberg, J.T. (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl Acad. Sci. USA, 98, 771-776.
38. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410.
39. Martinez, C., Montillet, J.L., Bresson, E., Agnel, J.P., Daï, G.H., Daniel, J.F., Geiger, J.P. and Nicole, M. (1998) Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum race 18. Mol. Plant Microbe Interact. 11, 1038-1047.
40. Metz, M., Dahlbeck, D., Morales, C.Q., Al Sady, B., Clark, E.T. and Staskawicz, B.J. (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J. 41, 801-814.
41. Ostergaard, L., Pedersen, A.G., Jespersen, H.M., Brunak, S. and Welinder, K.G. (1998) Computational analyses and annotations of the Arabidopsis peroxidase gene family. FEBS Lett. 433, 98-102.
42. Ostergaard, L., Teilum, K., Mirza, O., Petersen, M., Welinder, K.G., Mundy, J., Gajhede, M. and Hendriksen, A. (2000) Arabidopsis ATPA2 peroxidase: expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Mol. Biol. 44, 231-243.
43. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
44. Plotnikova, J.M., Reuber, T.L., Ausubel, F.M. and Pfister, D.H. (1998) Powdery mildew pathogenesis of Arabidopsis thaliana. Mycologia, 90, 1009-1016.
45. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. (1998) Correlation of defence gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485.
46. Rogers, E.E. and Ausubel, F.M. (1997) Arabidopsis enhanced disease susceptibility mutants exhibit enhances susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell, 9, 305-316.
47. Scheideler, M., Schlaich, N.L., Fellenberg, K., Beissbarth, T., Hauser, N.C., Vingron, M., Slusarenko, A.J. and Hoheisel, J.D. (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J. Biol. Chem. 277, 10555-10561.
48. Semizarov, D., Frost, L., Sarthy, A., Kroeger, P., Halbert, D.N. and Fesik, S.W. (2003) Specificity of short interfering RNA determined through gene expression signatures. Proc. Natl Acad. Sci. USA, 100, 6347-6352.
49. Soylu, S., Brown, I. and Mansfield, J.W. (2005) Cellular reactions in Arabidopsis following challenge by strains of Pseudomonas syringae: from basal resistance to compatibility. Physiol. Mol. Plant Pathol. 66, 232-243.
50. Stone, J.M., Heard, J.E., Asai, T. and Ausubel, F.M. (2000) Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell, 12, 1811-1822.
51. Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H.-S., Han, B., Zhu, T., Zou, G. and Katagiri, F. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317-330.
52. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
53. Tognolli, M., Penel, C., Greppin, H. and Simon, P. (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene, 288, 129-138.
54. Torres, M. A. and Dangl, J.L. (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397-403.
55. phox). Plant J. 14, 365-370.
56. phox homologues, AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA, 99, 517-522.
57. Torres, M.A., Jones, J.D.G. and Dangl, J.L. (2005) Pathogen-induced NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130-1134.
58. Valério, L., de Meyer, M., Penel, C. and Dunand, C. (2004) Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry, 65, 1331-1342.
59. Waring, J.F., Jolly, R.A., Ciurlionis, R., Lum, P.Y., Praestgaard, J.T., Morfitt, D.C., Buratto, B., Roberts, C., Schadt, E. and Ulrich, R.G. (2001) Clustering of hepatotoxins based on mechanism of toxicity using gene expression profiles. Toxicol. Appl. Pharmacol. 175, 28-42.
60. Welinder, K.G., Justesen, A.F., Kjaersgard, I.V., Jensen, R.B., Rasmussen, S.K., Jespersen, H.M. and Duroux, L. (2002) Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur. J. Biochem. 269, 6063-6081.
61. Whalen, M.C., Innes, R.W., Bent, A.F. and Staskawicz, B.J. (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell, 3, 49-59.
62. Wojtaszek, P. (1997) The oxidative burst: a plant's early response against infection. Biochem. J. 322, 4158-4163.