The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000

Molecular Plant-Microbe Interactions

Volumn 20, Issue 8, 2007, Pages 955-965

  Uppalapati, Srinivasa Rao ^a,b   Ishiga, Yasuhiro ^a   Wangdi, Tamding ^a   Kunkel, Barbara N ^c   Anand, Ajith ^b   Mysore, Kirankumar S ^b   Bender, Carol L ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b PLANT BIOLOGY DIVISION   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 AMINO 2 ETHYLCYCLOPROPANECARBOXYLIC ACID; 1-AMINO-2-ETHYLCYCLOPROPANE-1-CARBOXYLIC ACID; AMINO ACID; BACTERIAL TOXIN; CORONAFACIC ACID; CORONATINE; CYCLOPENTANE DERIVATIVE; INDENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; TOMATO;

AMINO ACIDS; BACTERIAL TOXINS; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; INDENES; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PSEUDOMONAS SYRINGAE; SALICYLIC ACID; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LYCOPERSICON; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; SOLANUM;

EID: 34547093636     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-8-0955     Document Type: Article

References (78)

1. Abramovitch, R. B., and Martin, G. B. 2004. Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 7:356-364.
2. An, G. 1987. Binary Ti vectors for plant transformation and promoter analysis. Methods Enzymol. 153:292-305.
3. Bender, C. L., Stone, H. E., Sims, J. J., and Cooksey, D. A. 1987. Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn5 insertions defective in coronatine production. Physiol. Mol. Plant Pathol. 30:273-283.
4. Bender, C. L., Alarcón-Chaidez, F., and Gross, D. C. 1999. Pseudomonas syringae phytotoxins: Mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266-292.
5. Block, A., Schmelz, E., Jones, J. J., and Klee. H. J. 2005. Coronatine and salicylic acid: The battle between Arabidopsis and Pseudomonas for phytohormone control. Mol. Plant Pathol. 6:79-83.
6. Boch, J., Joardar, V., Gao, L., Robertson, T. L., Lim, M., and Kunkel, B. N. 2002. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44:73-88.
7. Brading, P. A., Hammond-Kosack, K. E., Parr, A., and Jones, J. D. 2000. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J. 23:305-318.
8. Brooks, D. M., Guzman, G. H., Kloek, A. P., Alarcón-Chaidez, F., Sreedharan, A., Rangaswamy, V., Peñaloza-Vázquez, A., Bender, C. L., and Kunkel, B. N. 2004. Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pathovar tomato DC3000. Mol. Plant-Microbe Interact. 17:162-174.
9. Brooks, D. M., Bender, C. L., and Kunkel, B. N. 2005. The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol. Plant Pathol. 6:629-639.
10. Brown, N. P., Leroy, C., and Sander, C. 1998. MView: A web compatible database search or multiple alignment viewer. Bioinformatics 14:380-381.
11. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Liu, J., Yuan, Q., Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Vanaken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W.-L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186.
12. Cao, H., Bowling, S. A., Gordon, A. S., and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583-1592.
13. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weyman, K., Negrotto, D., Gaffney, T., Gut-Reila, M., Kessman, H., Ward, E., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250.
14. Dong, X. 1998. SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1:316-323.
15. Durner, J., Shah, J., and Klessig, D. F. 1997. Salicylic acid and disease resistance in plants. Crit. Rev. Plant. Sci. 18:547-575.
16. Ekengren, S. K., Liu, Y., Schiff, M., Dinesh-Kumar, S. P., and Martin, G. B. 2003. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36:905-917.
17. Elizabeth, S. V., and Bender, C. L. 2007. The phytotoxin coronatine from Pseudomonas syringae pv. tomato DC3000 functions as a virulence factor and influences defense pathways in edible Brassicas. Mol. Plant Pathol. 8:83-92.
18. Espinosa, A., Guo, M., Tam, V. C., Fu, Z. Q., and Alfano, J. R. 2003. The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49:377-387.
19. Eulgem, T. 2005. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10:71-78.
20. Feys, B. J. F., Benedetti, C. E., Penfold, C. N., and Turner, J. G. 1994. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751-759.
21. Fouts, D. E., Abramovitch, R. B., Alfano, J. R., Baldo, A. M., Buell, C. R., Cartinhour, S., Chatterjee, A. K., D'Ascenzo, M., Gwinn, M. L., Lazarowitz, S. G., Lin, N. C., Martin, G. B., Rehm, A. H., Schneider, D. J., van Dijk, K., Tang, X., and Collmer, A. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. U.S.A. 99:2275-2280.
22. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227.
23. 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.
24. Glazebrook, J., Chen, W., Estes, B., Chang, H. S., Nawrath, C., Metraux, J. P., Zhu, T., and Katagiri, F. 2003. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J. 34:217-228.
25. Gnanamanickam, S. S., Starratt, A. N., and Ward, E. W. B. 1982. Coronatine production in vitro and in vivo and its relation to symptom development in bacterial blight of soybean. Can. J. Bot. 60:645-650.
26. He, P., Chintamanani, S., Chen, Z., Zhu, L., Kunkel, B. N., Alfano, J. R., Tang, X., and Zhou, J. M. 2004. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J. 37:589-602.
27. Heck, S., Grau, T., Buchala, A., Metraux, J. P., and Nawrath, C. 2003. Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. Plant J. 36:342-352.
28. Heitz, T., Bergey, D. R., and Ryan, C. A. 1997. A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol. 114:1085-1093.
29. Huang, Z., Yeakley, J. M., Garcia, E. W., Holdridge, J. D., Fan, J. B., and Whitham, S. A. 2005. Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol. 137:1147-1159.
30. Imanishi, S., Nakakita, M., Yamashita, K., Furata, A., Utsuno, K., Muramoto, N., Kojima, H., and Nakamura, K. 2000. Aspirin and salicylic acid do not inhibit methyl jasmonate-inducible expression of a gene for ornithine decarboxylase in tobacco BY-2 cells. Biosci. Biotechnol. Biochem. 64:125-133.
31. Jakobek, J. L., Smith, J. A., and Lindgren, P. B. 1993. Suppression of bean defense responses by Pseudomonas syringae. Plant Cell 5:57-63.
32. Katagiri, F. 2004. A global view of defense gene expression regulation - A highly interconnected signaling network. Curr. Opin. Plant Biol. 7:506-511.
33. King, E. O., Ward, N. K., and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab Clin. Med. 44:301-307.
34. Kloek, A. P., Verbsky, M. L., Sharma, S. B., Schoelz, J. E., Vogel, J., Klessig, D. F., and Kunkel, B.N. 2001. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive coi1 mutation occurs through two distinct mechanisms. Plant J. 26:509-522.
35. Kunkel, B. N., and Brooks, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331.
36. Kunkel, B. N., and Chen, Z. 2005. Virulence strategies of plant pathogenic bacteria. In: The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, Release 3.20. M. Dworkin, ed. Springer-Verlag, New York.
37. Laurie-Berry, N., Joardar, V., Street, I. H., and Kunkel, B. N. 2006. The Arabidopsis thaliana Jasmonate Insensitive 1 gene defines a branch of the jasmonate signaling pathway required for suppression of salicylic acid-dependent defenses during infection by P. syringae. Mol. Plant-Microbe Interact. 19:789-800.
38. Leon, J., Rojo, E., and Sanchez-Serrano, J. J. 2001. Wound signaling in plants. J. Exp. Bot. 52:1-9.
39. Li, J., Shan, L., Zhou, J.-M., and Tang, X. 2002. Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol. Plant-Microbe Interact. 15:654-661.
40. Lim, M. T., and Kunkel, B. N. 2005. The Pseudomonas syringae avrRpt2 gene contributes to virulence on tomato. Mol. Plant-Microbe Interact. 18:626-633.
41. Liu, Y., Schiff, M., and Dinesh-Kumar, S. P. 2002. Virus-induced gene silencing in tomato. Plant J. 31:777-786.
42. Lund, S. T., Stall, R. E., and Klee, H. J. 1998. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371-382.
43. Ma, S.-W., Morris, V. L., and Cuppels, D. A. 1991. Characterization of a DNA region required for production of the phytotoxin coronatine by Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 4:69-74.
44. 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. U.S.A. 98:771-776.
45. Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S. Y. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-980.
46. Mitchell, R. E. 1984. A naturally-occurring structural analogue of the phytotoxin coronatine. Phytochemistry 23:791-793.
47. Mitchell, R. E., and Ford, K. L. 1998. Chlorosis-inducing products from Pseudomonas syringae pathovars: New N-coronafacoyl compounds. Phytochemistry 49:1579-1583.
48. Mittal, S. M., and Davis, K. R. 1995. Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 8:165-171.
49. Mudgett, M. B. 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu. Rev. Plant Biol. 56:509-531.
50. Mur, L. A. J., Kenton, P., Atzorn, R., Miersch, O., and Wasternack, C. 2006. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140:249-262.
51. Mysore, K. S., Crasta, O. R., Tuori, R. P., Folkerts, O., Swirsky, P. B., and Martin, G. B. 2002. Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J. 32:299-315.
52. Nawrath, C., and Metraux, J. P. 1999. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393-1404.
53. O'Donnell, P. J., Schmelz, E., Block, A., Miersch, O., Wasternack, C., Jones, J. B., and Klee, H. J. 2003. Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol. 133:1181-1189.
54. Oldroyd, G. E. D., and Staskawicz, B. J. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. U.S.A. 95:10300-10305.
55. Palmer, D. A., and Bender, C. L. 1995. Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Mol. Plant-Microbe Interact. 8:683-692.
56. Pena-Cortes, H., Fisahn, J., and Willmitzer, L. 1995. Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. U.S.A. 92:4106-4113.
57. Peñaloza-Vázquez, A., Preston, G. M., Collmer, A., and Bender, C. L. 2000. Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. Microbiology 146:2447-2456.
58. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y., and Hunt, M. D. 1996. Systemic acquired resistance. Plant Cell 8:1809-1819.
59. Ryu, C. M., Anand, A., Kang, L., and Mysore, K. S. 2004. Agrodrench: A novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse solanaceous species. Plant J. 40:322-331.
60. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
61. Schmelz, E. A., Engelberth, J., Alborn, H. T., O'Donnell, P., Sammons, M., Toshima, H., and Tumlinson, J. H. 2003. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Natl. Acad. Sci. U.S.A. 100:10552-10557.
62. Shah, J. 2003. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6:365-371.
63. Spoel, S.H., Koornneef, A., Claessens, S.M., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., Buchala, A. J., Metraux, J. P., Brown, R., Kazan, K., Van Loon, L. C., Dong, X., and Pieterse, C. M. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760-770.
64. Sreedharan, A., Peñaloza-Vazquez, A., Kunkel, B. N., and Bender. C. L. 2006. CorR regulates multiple components of virulence in Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 19:768-779.
65. Staswick, P. E., and Tiryaki, I. 2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117-2127.
66. Sugimoto, M., Toyoda, K., Ichinosae, Y., Yamada, T., and Shiraishi, T. 2000. Cytochalasin A inhibits the binding of phenylalanine ammonia-lyase mRNA to ribosomes during induction of phytoalexin in pea seedlings. Plant Cell Physiol. 41:234-238.
67. Thaler, J. S., Fidantsef, A. L, and Bostock, R. M. 2002. Antagonism between jasmonate- and salicylate-mediated induced plant resistance: Effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J. Chem. Ecol. 28:1131-1159.
68. Thilmony, R., Underwood, W., and He, S. Y. 2006. Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J. 46:34-53.
69. Thomma, B. P., Penninckx, I. A., Broekaert, W. F., and Cammue, B. P. 2001. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13:63-68.
70. Truman, W., Bennett, M. H., Kubigsteltig, I., Turnbull, C., and Grant, M. 2007. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. U.S.A. 104:1075-1080.
71. Uppalapati S. R., Yasuhiro, I., Toyoda, K., Ichinose, Y., and Shiraishi, T. 2004. Differential regulation of MBP kinases by a glycoproptein elicitor and a polypeptide suppressor from Mycosphaerella pinodes in pea. Physiol. Mol. Plant Pathol. 64:17-25.
72. Uppalapati, S. R., Patricia A., Weng, H., P., Palmer, D. A., Mitchell, R.E., Jones, W., and Bender, C. L. 2005. The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J. 42:201-217.
73. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:0034.1-0034.11
74. van Wees, S. C., and Glazebrook, J. 2003. Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J. 33:733-742.
75. Vidya, C. S. S., Manoharan, M., and Sita, G. L. 1999. Cloning and characterization of salicylic acid-induced, intracellular pathogenesis related gene from tomato Lycopersicon esculentum. J. Biosci. 24:287-293.
76. Weiler, E. W., Kutchan, T. M., Gorba, T., Brodschelm, W., Neisel, U., and Bublitz, F. 1994. The Pseudomonas phytotoxin coronatine mimics octadecanoid signaling molecules of higher plants. FEBS (Fed. Eur. Biol. Soc.) Lett. 345:9-13.
77. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565.
78. Zhao, Y., Thilmony, R., Bender, C. L., Schaller, A., He, S. Y., and Howe, G. A. 2003. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J. 36:485-499.