The differential spatial distribution of secondary metabolites in Arabidopsis leaves reacting hypersensitively to Pseudomonas syringae pv. tomato is dependent on the oxidative burst

Journal of Experimental Botany

Volumn 61, Issue 12, 2010, Pages 3355-3370

  Simon, Clara ^a   Langlois Meurinne, Mathilde ^a   Bellvert, Floriant ^a,b,c   Garmier, Marie ^a   Didierlaurent, Laure ^a   Massoud, Kamal ^a   Chaouch, Sejir ^a   Marie, Arul ^d   Bodo, Bernard ^d   Kauffmann, Serge ^a   Noctor, Graham ^a   Saindrenan, Patrick ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE LYON   (France)

^c University of Lyon   (France)

^d MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Arabidopsis thaliana; Metabolite profiling; Oxidative burst; Plant defence; Pseudomonas syringae pv. tomato; Secondary metabolites

Indexed keywords

CAMALEXIN; COUMARIN DERIVATIVE; GLUCOSIDE; INDOLE DERIVATIVE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; SCOPOLIN; THIAZOLE DERIVATIVE;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS SYRINGAE; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

ARABIDOPSIS; COUMARINS; GENE EXPRESSION REGULATION, PLANT; GLUCOSIDES; INDOLES; METABOLOME; PLANT DISEASES; PLANT LEAVES; PSEUDOMONAS SYRINGAE; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SALICYLIC ACID; SIGNAL TRANSDUCTION; THIAZOLES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 77954768809     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq157     Document Type: Article

References (67)

1. Alvarez ME. 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Molecular Biology 44, 429-442.
2. Anterola AM, Lewis NG. 2002. Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61, 221-294.
3. Baillieul F, Genetet I, Kopp M, Saindrenan P, Fritig B, Kauffmann S. 1995. A new elicitor of the hypersensitive response in tobacco: a fungal glycoprotein elicits cell death, expression of defence genes, production of salicylic acid, and induction of systemic acquired resistance. The Plant Journal 8, 551-560.
4. Baker CJ, O'Neill NR, Deahl K, Lydon J. 2002. Continuous production of extracellular antioxidants in suspension cells attenuates the oxidative burst detected in plant microbe interactions. Plant Physiology and Biochemistry 40, 641-644.
5. Bednarek P, Piślewska-Bednarek M, Svatos A, et al. 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106.
6. Bednarek P, Schneider B, Svatos A, Oldham NJ, Hahlbrock K. 2005. Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiology 138, 1058-1070.
7. Bednarek P, Schulze-Lefert P. 2009. Role of plant secondary metabolites at the host-pathogen interface. In: Parker J, ed. Molecular aspect of plant disease resistance, Vol. 34. Hoboken, USA: Annual Plant Reviews, 220-260.
8. Bednarek P, Winter J, Hamberger B, Oldham NJ, Schneider B, Tan J, Hahlbrock K. 2004. Induction of 3#-O-b-d-ribofuranosyl adenosine during compatible, but not during incompatible, interactions of Arabidopsis thaliana or Lycopersicon esculentum with Pseudomonas syringae pathovar tomato. Planta 218, 668-672.
9. Bö ttcher C, von Roepenack-Lahaye E, Schmidt J, Schmotz C, Neumann S, Scheel D, Clemens S. 2008. Metabolome analysis of biosynthetic mutants reveals a diversity of metabolic changes and allows identification of a large number of new compounds in Arabidopsis. Plant Physiology. 138. 1058-1070.
10. Bö ttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E. 2009. The multifunctional enzyme CYP71B15 (PHYTOALAXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of. Arabidopsis thaliana. The Plant Cell 21, 1830-1845.
11. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X. 1997. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. The Plant Cell 9, 1573-1584.
12. Cano A, Alcaraz O, Arnao MB. 2003. Free radical-scavenging activity of indolic compounds in aquaeous and ethanolic media. Analytical and Bioanalytical Chemistry 376, 33-37.
13. Chaouch S, Queval G, Vanderauwera S, Vandorpe M, Langlois-Meurinne M, Van Breusegem F, Saindrenan P, Noctor G. 2010. Genetic reversion of cell death in the Arabidopsis cat2 knockout mutant shows that peroxisomal hydrogen peroxide is coupled to biotic defense responses by isochorismate synthase 1 in a daylength-related manner. Plant Physiology (in press).
14. 2 metabolism. FEBS Letters 458, 204-208.
15. Chong J, Baltz R, Schmitt C, Beffa R, Fritig B, Saindrenan P. 2002. Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin accumulation, enhances oxidative stress, and weakens virus resistance. The Plant Cell 14, 1093-1107.
16. Clausen S, Olsen O, Sö rensen H. 1982. 4-hydroxybenzoylcholine: a natural product present in Sinapis alba. Phytochemistry 21, 917-922.
17. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323, 95-101.
18. Coleman HD, Park J-Y, Nair R, Chapple C, Mansfield SD. 2008. RNAi-mediated suppression of p-coumaroyl-CoA 3#-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proceedings of the National Academy of Sciences, USA 105, 4501-4506.
19. Costet L, Cordelier S, Dorey S, Bailleuil F, Fritig B, Kauffmann S. 1999. Relationship between localized acquired resistance (LAR) and the hypersensitive response (HR): HR is necessary for LAR to occur and salicylic acid is not sufficient to trigger LAR. Molecular Plant-Microbe Interactions 12, 655-662.
20. Costet L, Fritig B, Kauffmann S. 2002. Scopoletin expression in elicitor-treated and tobacco mosaic virus-infected tobacco plants. Physiologia Plantarum 115, 228-235.
21. D'Auria JC, Gershenzon J. 2005. The secondary metabolism of Arabidopsis thaliana: growing like a weed. Current Opinion in Plant Biology 8, 308-316.
22. Desikan R, Mackerness SAH, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159-172.
23. Dixon RA. 2001. Natural products and plant disease resistance. Nature 411, 843-847.
24. Dorey S, Baillieul F, Pierrel MA, Saindrenan P, Fritig B, Kauffmann S. 1997. Spatial and temporal induction of cell death, defense genes, and accumulation of salicylic acid in tobacco leaves reacting hypersensitively to a fungal glycoprotein elicitor. Molecular Plant-Microbe Interactions 10, 646-655.
25. Dorey S, Baillieul F, Saindrenan P, Fritig B, Kauffmann S. 1998. Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Molecular Plant-Microbe Interactions 11, 1102-1109.
26. Dutilleul C, Garmier M, Noctor G, Mathieu C, Ché trit P, Foyer CH, de Paepe R. 2003. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. The Plant Cell 15, 1212-1226.
27. Enyedi AJ, Yalpani N, Silverman P, Raskin I. 1992. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proceedings of the National Academy of Sciences, USA 89, 2480-2484.
28. Foyer CH, Bloom AJ, Queval G, Noctor G. 2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology 60, 455-484.
29. Gachon CMM, Baltz R, Saindrenan P. 2004. Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance. Plant Molecular Biology 54, 137-146.
30. Gachon CMM, Langlois-Meurinne M, Henry Y, Saindrenan P. 2005. Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Molecular Biology 58, 229-245.
31. Glawischnig E. 2007. Camalexin. Phytochemistry 68, 401-406.
32. Glazebrook J, Ausubel FM. 1994. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proceedings of the National Academy of Sciences, USA 91, 8955-8959.
33. Hagemeier J, Schneider B, Oldham NJ, Hahlbrock K. 2001. Accumulation of soluble and wall-bound indolic metabolites in Arabidopsis thaliana leaves infected with virulent and avirulent Pseudomonas syringae pathovar tomato strains. Proceedings of the National Academy of Sciences, USA 98, 753-758.
34. Hahn MG, Bonhoff A, Grisebach H. 1985. Quantitative localization of the phytoalexin glyceollin I in relation to fungal hyphae in soybean roots infected with Phytophthora megasperma f. sp. glycinea. Plant Physiology 77, 591-601.
35. Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57, 303-333.
36. Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF. 1993. Interconversion of the salicylic acid signal and its glucoside in tobacco. The Plant Journal 4, 593-600.
37. Kai K, Mizutani M, Kawamura N, Yamamoto R, Tamai M, Yamaguchi H, Sakata K, Shimizu B. 2008. Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. The Plant Journal 55, 989-999.
38. Kai K, Shimizu B, Mizutani M, Watanabe K, Sakata K. 2006. Accumulation of coumarins in Arabidopsis thaliana. Phytochemistry 67, 379-386.
39. Kliebenstein DJ, Rowe HC, Denby KJ. 2005. Secondary metabolites infuence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. The Plant Journal 44, 25-36.
40. Kuc J. 1995. Phytoalexins, stress metabolism, and disease resistance in plants. Annual Review of Phytopathology 33, 275-297.
41. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251-275.
42. Langlois-Meurinne M, Gachon CMM, Saindrenan P. 2005. Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv. tomato in Arabidopsis. Plant Physiology 139, 1890-1901.
43. Loake G, Grant M. 2007. Salicylic acid in plant defence: the players and protagonists. Current Opinion in Plant Biology 10, 466-472.
44. Loreto F, Pinelli P, Manes F, Kollist H. 2004. Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiology 24, 361-367.
45. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
46. Mur LAJ, Kenton P, Lloyd AJ, Ougham H, Prats E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? Journal of Experimental Botany 59, 501-520.
47. Mur LAJ, Naylor G, Warner SAJ, Sugars JM, White RF, Draper J. 1996. Salicylic acid potentiates defense gene expression in tissue exhibiting acquired resistance to pathogen attack. The Plant Journal 9, 559-571.
48. 2-induced cell death. The Plant Journal 52, 640-657.
49. Rohde A, Morreel K, Ralph J, et al. 2004. Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. The Plant Cell 16, 2749-2771.
50. Saeed A, Sharov V, White J, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 24, 374-378.
51. Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. The Plant Journal 39, 790-818.
52. Schuhegger R, Rauhut T, Glawischnig E. 2007. Regulatory variability of camalexin biosynthesis. Journal of Plant Physiology 164, 636-644.
53. Seo S, Seto H, Koshino H, Yoshida S, Ohashi Y. 2003. A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco. The Plant Cell 15, 863-873.
54. Shah J. 2003. The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6, 365-371.
55. Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. The Plant Cell 9, 261-270.
56. Shroff R, Vergara F, Muck A, Svatos A, Gershenzon J. 2008. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proceedings of the National Academy of Sciences, USA 99, 517-522.
57. Song CJ, Steinebrunner I, Wang X, Stout SC, Roux SJ. 2006. Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiology 140, 1222-1232.
58. Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D. 2004. Plant eR genes that encode photorespiratory enzymes confer resistance against disease. The Plant Cell 16, 172-184.
59. Tan J, Bednarek P, Liu J, Schneider B, Svatos A, Hahlbrock K. 2003. Universally occuring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves. Phytochemistry 65, 691-699.
60. Thomma BPHJ, Nelissen I, Eggermont K, Broekaert WF. 1999. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. The Plant Journal 19, 163-171.
61. Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences, USA 99, 517-522.
62. Van Breusegem F, Dat JF. 2006. Reactive oxygen species in plant cell death. Plant Physiology 141, 384-390.
63. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 417, 562-565.
64. Wink M. 1999. Introduction: biochemistry, role and biotechnology of secondary metabolites. In: Wink M, ed. Functions of plant secondary metabolites and their exploitation in biotechnology, Vol. 3. Sheffield, UK: Annual Plant Reviews, 1-17.
65. Winkel-Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218-223.
66. Yang Y, Qi M, Mei C. 2004. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. The Plant Journal 40, 909-919.
67. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, Watanabe-Takahashi A, Inoue E, Saito K. 2008. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. The Plant Cell 20, 2160-2176.