Enhanced defense responses in arabidopsis induced by the cell wall protein fractions from pythium oligandrum require SGT1, RAR1, NPR1 and JAR1

Plant and Cell Physiology

Volumn 50, Issue 5, 2009, Pages 924-934

  Kawamura, Yoko ^a   Takenaka, Shigehito ^b   Hase, Shu ^a   Kubota, Mayumi ^c   Ichinose, Yuki ^d   Kanayama, Yoshinori ^a   Nakaho, Kazuhiro ^e   Klessig, Daniel F ^f   Takahashi, Hideki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b NATIONAL AGRICULTURAL RESEARCH CENTER FOR HOKKAIDO REGION   (Japan)

^c GIFU UNIVERSITY   (Japan)

^d OKAYAMA UNIVERSITY   (Japan)

^e NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^f United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Elicitin; Ethylene; Induced resistance; Jasmonic acid; Pseudomonas syringae; Ralstonia solanaceraum

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; PYTHIUM; PYTHIUM OLIGANDRUM; RALSTONIA;

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; GLUCOSYLTRANSFERASE; JAR1 PROTEIN, ARABIDOPSIS; JASMONIC ACID; NPR1 PROTEIN, ARABIDOPSIS; NUCLEOTIDYLTRANSFERASE; OXYLIPIN; PBS2 PROTEIN, ARABIDOPSIS; PLANT RNA; SALICYLIC ACID; SGT1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CELL WALL; CHEMISTRY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; PLANT GENE; PSEUDOMONAS SYRINGAE; PYTHIUM; RALSTONIA; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL WALL; CYCLOPENTANES; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSYLTRANSFERASES; NUCLEOTIDYLTRANSFERASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYLIPINS; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; PYTHIUM; RALSTONIA; RNA, PLANT; SALICYLIC ACID; SIGNAL TRANSDUCTION;

EID: 66149154292     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp044     Document Type: Article

References (75)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl Acad. Sci. USA 95: 10306-10311.
2. Al-Rawahi, A.K. and Hancock, J.G. (1997) Rhizosphere competence of Pythium oligandrum. Phytopathology 87: 951-959.
3. Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D.G. and Parker, J.E. (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077-2080.
4. Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noel, L., Sadanandom, A., et al. (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J. 25: 2007-2016.
5. Belkhadir, Y., Subramaniam, R. and Dangl, J.L. (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7: 391-399.
6. Benhamou, N., Rey, P., Cherif, M., Hockenhull, J. and Tirilly, Y. (1997) Treatment with the mycoparasite Pythium oligandrum triggers induction of defense-related reactions in tomato roots when challenged with Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 87: 108-122.
7. Benhamou, N., Rey, P., Picard, K. and Tirilly, Y. (1999) Ultrastructural and cytochemical aspects of the interaction between the mycoparasite Pythium oligandrum and soilborne plant pathogens. Phytopathology 89: 506-517.
8. Bittel, P. and Robatzek, S. (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr. Opin. Plant Biol. 10: 335-341.
9. Brozova, J. (2002) Exploitation of the mycoparasitic fungus Pythium oligandrum in plant protection. Plant Prot. Sci. 38: 29-35.
10. Butt, T.M. and Copping, L.G. (2000) Fungal biological control agents. Pestic. Outlook 11: 186-191.
11. Cao, H., Bowling, S.A., Gordon, A.S.and Dong, X. (1994) Characterization of an Arabidopsis mutant that is non-responsive to inducers of systemic aquired resistance. Plant Cell 6: 1583-1592.
12. Century, K.S., Holub, E.B. and Staskawicz, B.J. (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl Acad. Sci. USA 92: 6597-6601.
13. Century, K.S., Shapiro, A.D., Repetti, P.P., Dahlbeck, D., Holub, E. and Staskawicz, B.J. (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963-1965.
14. Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262: 539-544.
15. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, T., Jones. J.D.G., et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
16. Chomczynski, P. and Sacci, N. (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform| extraction. Anal. Biochem. 162: 156-159.
17. Clarke, J.D., Volko, S.M., Ledford, H., Ausubel, F.M. and Dong, X. (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12: 2175-2190.
18. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al. (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250.
19. Despres, C., DeLong, C., Glaze, S., Liu, E. and Fobert, P.R. (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12: 279-290.
20. Dong, X. (2004) NPR1, all things considered. Curr. Opin. Plant Biol. 7: 547-552.
21. Durrant, WE. and Dong, X. (2004) Systemic acquired resistance. Annu. Rev. Phytopathol. 42: 185-209.
22. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D.G., Daniels, M.J. and Parker, J.E. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipase. Proc. Natl Acad. Sci. USA 96: 3292-3297.
23. Feys, B.J., Moisan, L.J., Newman, M.A. and Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20: 5400-5411.
24. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43: 205-227.
25. 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.
26. TIR1-mediated auxin response. Plant Cell 15: 1310-1319.
27. Guzman, P. and Ecker, J.R. (1990) Exploting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-523.
28. Hase, S., Shimizu, A., Nakaho, K., Takenaka, S. and Takahashi, H. (2006) Induction of transient ethylene and reduction in severity of tomato bacterial wilt by Pythium oligandrum. Plant Pathol. 55: 537-543.
29. Hase, S., Takahashi, S., Nakaho, K., Arie, T., Seo, S., Ohashi, Y., et al. (2008) Jasmonic acid signaling is required for bacterial wild disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol. 57: 870-876.
30. Hendrick, C. and Sequeira, L. (1984) Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl. Environ. Microbiol. 48: 94-101.
31. Hubert, D.A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shiraru, K., et al. (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22: 5679-5689.
32. Huitema, E., Vleeshouwers, V.G.A.A., Francis, D.M. and Kamoun, S. (2003) Active defense responses associated with non-host resistance of Arabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Mol. Plant Pathol. 4: 487-500.
33. Jirage, D., Tootle, T.L., Reuber, T.L., Frost, L.N., Feys, B.J., Parker, J.E., et al. (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl Acad. Sci. USA 96: 13583-13488.
34. Kawamura, Y., Hase, S., Takenaka, S., Kanayama, Y., Yoshioka, H., Kamoun, S., et al. (2008) INF1 elicitin activates jasmonic acid- and ethylene-mediated signaling pathways and induces resistance to bacterial wilt disease in tomato. J. Phytopathol. (in press).
35. Kinkema, M., Fan, W. and Dong, X. (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350.
36. Laurie-Berry, N., Joardar, V., Street, I.H. and Kunkel, B.N. (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol. Plant-Microbe Interact. 19: 789-800.
37. Lewis, K., Whipps, J.M. and Cooke, R.C. (1989) Mechanisms of biological disease control with special reference to the case study of Pythium oligandrum as an antagonist. In Biotechnology of Fungi for Improving Plant Growth. Edited by Whipps, J.M. and Lumdsen, R.D. pp. 191-217. Cambridge University Press, Cambridge, UK.
38. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. and Dinesh-Kumar, S.P. (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279: 2101-2108.
39. Lorenzo, O. and Solano, R. (2005) Molecular players regulating the jasmonate signaling network. Curr. Opin. Plant Biol. 8: 532-540.
40. Lu, R., Malcuit, I., Moffett, P., Ruiz, M.T., Peart, J., Wu, A.-J., et al. (2003) High throughput virus-induced gene silelncing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22: 5690-5699.
41. Martin, F.N. and Hancock, J.G. (1987) The use of Pythium oligandrum for biological control of preemergence damping-off caused by P. ultimum. Phytopathology 77: 1013-1020.
42. McDowell, J.M., Cuzick, A., Can, C., Beynon, J., Dangl, J.L. and Holub, E.B. (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 22: 523-529.
43. McDowell, J.M. and Dangl, J.L. (2000) Signal transduction in the plant immune response. Trends Biochem. Sci. 25: 79-82.
44. McQuilken, M.P., Whipps, J.M. and Cooke, R.C. (1990) Control of damping-off in cress and sugar-beet by commercial seed-coating with Pythium oligandrum. Plant Pathol. 39: 452-462.
45. Nakaho, K., Inoue, H., Takayama, T. and Miyagawa, H. (2004) Distribution and multiplication of Ralstonia solanacearum in tomato plants with resistance derived from different origins. J. Gen. Plant Pathol. 70: 115-119.
46. Nurnberger, T. and Kemmerling, B. (2006) Receptor protein kinases - pattern recognition receptors in plant immunity. Trends Plant Sci. 11: 519-522.
47. Parker, J.E., Holub, E.B., Frost, L.N., Falk, A., Gunn, N.D. and Daniels, M.J. (1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033-2046.
48. Peart, J.R., Lu, R., Sadanandom, A., Malcuit, I., Mofffett, P., Brice, D.C., et al. (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl Acad. Sci. USA 99: 10865-10869.
49. Picard, K., Ponchet, M., Blein, J.-P., Rey, P., Tirilly, Y. and Benhamou, N. (2000) Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrium induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol. 124: 379-395.
50. Pieterse, C.M.J., Van Pelt, J.A., Ton, J., Parchmann, S., Mueller, M.J., Buchala, A.J., et al. (2000) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol. Mol. Plant Pathol. 57: 123-134.
51. Pieterse, C.M.J., Van Wees, S.C.M., Van Pelt, JA., Knoester, M., Laan, R., Gerrits, H., et al. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580.
52. Ponchet, M., Panabieres, F., Milat, M.-L., Mikes, V., Montillet, J.-L., Suty, L., et al. (1999) Are elicitins cryptograms in plant-oomycete communications? Cell. Mol. Life Sci. 56: 1020-1047.
53. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning. A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Schwessinger, B. and Zipfel, C. (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11: 369-395.
55. Sekine, K.-T., Kawakami, S., Kubota, M., Ichinose, Y., Shah, J., Kang, H.-G. et al. (2008) High-level expression of a virus resistance gene, RCY1 confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21: 1398-1407.
56. Shah, J., Tsui, F. and Klessig, D.F. (1997) Characterization of a salicylic acid insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant-Microbe Interact. 10: 69-78.
57. Shirasu, K. and Schluz-Lefert, P. (2000) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci. 8: 252-258.
58. Spoel, S.H., Koornneef, A., Claessens, S.M.C., Korzelius, J.P., Van Pelt, J.A., Mueller, M.J., et al. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770.
59. Staswick, P.E., Su, W. and Howell, S.H. (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl Acad. Sci. USA 89: 6837-6840.
60. Takahashi, A., Casais, C., Ichimura, K. and Shirasu, K. (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA 100: 11777-11782.
61. Takahashi, H., Ishihara, T., Hase, S., Chiba, A., Nakaho, K., Arie, T., et al. (2006) Beta-cyanoalanine synthase as a molecular marker for induced resistance by fungal glycoprotein elicitor and commercial plant activators. Phytopathology 96: 908-916.
62. Takahashi, H., Kanayama, Y., Zheng, M.S., Kusano, T., Hase, S., Ikegami, M., et al. (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulated expression of defense genes and gene-for-gene resistance to Cucumber mosaic virus. Plant Cell Physiol. 45: 803-809.
63. Takenaka, S., Nakamura, Y., Kono, T., Sekiguchi, H., Masunaka, A. and Takahashi, H. (2006) Novel elicitin-like proteins isolated from cell wall of the biocontrol agent Pythium oligandrum induce defense-related genes in sugar beet. Mol. Plant Pathol. 7: 325-339.
64. Takenaka, S., Nishio, Z. and Nakamura, Y. (2003) Induction of defense reactions in sugar beet and wheat by treatment with cell wall protein fractions from the mycoparasite Pythium oligandrum. Phytopathology 93: 1228-1232.
65. Tameling, W.I.L. and Joosten M.H.A.J. (2007) The deverse roles of NB-LRR proteins in plants. Physiol. Mol. Plant Pathol. 71: 126-134.
66. Titarenko, E., Rojo, E., Leon, J. and Sanchez-Serrano, J.J. (1997) Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol. 115: 817-826.
67. Tör, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert-Tuck, F., et al. (2002) Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14: 993-1003.
68. Tornero, P., Merritt, P., Sadanandom, A., Shirasu, K., Innes, R.W. and Dangl, J.L. (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005-1015.
69. Wiermer, M., Feys, B.J. and Parker, J.E. (2005) Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8: 383-389.
70. Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M. and Turner, J.G. (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091 -1094.
71. COI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14: 1919-1935.
72. Xu, Y., Chang, P.L.C., Liu, D., Narasimhan, M.L., Kashchandra, G.R., Hasegawa, P.M., et al. (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077-1085.
73. Zhang, Y., Fan, W., Kinekema, M., Li, X. and Dong, X. (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl Acad. Sci. USA 96: 6523-6528.
74. Zhou, J.M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J., et al. (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant-Microbe Interact. 13: 191-202.
75. Zhou, F., Mosher, S., Tian, M., Sassi, C, Parker, J. and Klessig, D.F. (2008) The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol. Plant-Microbe Interact. 21: 40-49.