Overexpression of (At)NPR1 in rice leads to a BTH- and environment-induced lesion-mimic/cell death phenotype

Molecular Plant-Microbe Interactions

Volumn 17, Issue 2, 2004, Pages 140-151

  Fitzgerald, Heather A ^a   Chern, Maw Sheng ^a   Navarre, Roy ^b   Ronald, Pamela C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EUKARYOTA; RHIZOBIUM; XANTHOMONAS; XANTHOMONAS ORYZAE; XANTHOMONAS ORYZAE PV. ORYZAE;

EID: 1642382760     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2004.17.2.140     Document Type: Article

References (64)

1. Agrawal, G. K., Rakwal, R., and Jwa, N. S. 2000. Rice (Oryza sativa L.) OxPR1b gene is phytohormonally regulated in close interaction with light signals. Biochem Biophys. Res Commun. 278:290-298.
2. Alvarez, M. 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol. Biol. 44:429-442.
3. Arase, S., Fujita, K., Uehara, T., Honda, Y., and Isota, J. 2000. Light-enhanced resistance to Magnaporthe grisea infection in the rice Sekiguchi lesion mutants. J. Phytopathol. 148:197-203.
4. Bowling, S. A., Guo, A., Cao, H., Gordon, A. S., Klessig, D. F., and Dong, X. 1994. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6:1845-1857.
5. Buschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., van Daelen, R., van der Lee, T., Dicrgaarde, P., Groenendijk, J., Topsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-705.
6. Cao, H., Bowling, S. A., Gordon, S. A., and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583-1592.
7. Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57-63.
8. Cao, H., Li, X., and Dong, X. 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. U.S.A. 11:6531-6536.
9. Century, K. S., Lagman, R. A., Adkisson, M., Morlan, J., Tobias, R., Schwartz, K., Smith, A., Lov, J., Ronald, P. C., and Whalen, M. C. 1999. Short communication: developmental control of Xa21-mediated disease resistance in rice. Plant J. 20:231-236.
10. Chen, Z., Iye, S., Caplan, A., Klessig, D., and Fan, B. 1997. Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol. 114:193-201.
11. Chern, M. S., Fitzgerald, H. A., Yadav, R. C., Canlas, P. E., Dong, X., and Ronald, P. C. 2001. Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J. 27:101-113.
12. 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.
13. Dietrich, R. A., Delaney T. P., Uknes, S. J., Ward, E. R., Ryals, J. A., and Dangl, J. L. 1994. Arabidopsis mutants simulating disease resistance response. Cell 77:565-577.
14. Delaney, T. P., Friedrich, L., and Ryals, J. A. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. U.S.A. 92:6602-6606.
15. Delaney, T. P., Uknes, S., Vernooij, B., Friedrick, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessman, H., Ward, E., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250.
16. Dellaporta, S. L., Wood, J., and Hicks, J. B. 1984. Maize DNA miniprep. Pages 36-37 in: Molecular Biology of Plants: A Laboratory Course Manual. R. Maimberg, ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, U.S.A.
17. Delledonne, M., Zeier, J., Marocco, A., and Lamb, C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. U.S.A. 98:13454-13459.
18. Fan, W., and Dong, X. 2002. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14:1377-1389.
19. Friedrich, L., Lawton, K., Dietrich, R., Willits, M., Cade, R., and Ryals, J. 2001. NIM1 overexpression in Arabidopsis potentiates plant disease resistance and results in enhanced effectiveness of fungicides. Mol. Plant-Microbe Interact. 9:1114-1124.
20. Friedrich, L., Lawton, K., Ruess, W., Masner, P, Speckner, N., Gut Rella, M., Meier, B., Dinsher, S., Staub, T., Uknes, S., Metraux, J.-P., Kessman, H., and Ryals, J. 1996. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 9:61-70.
21. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754-756.
22. Genoud, T., Buchala, A. J., Chua, N. H., and Metraux, J. P. 2002. Phytochrome signaling modulates the SA-perceptive pathway in Arabidopsis. Plant J. 31:87-95.
23. Gorlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove U., Kogel, K. H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H., and Ryals, J. 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 4:629-643.
24. Gray, J., Close, P. S., Briggs, S. P., and Johal, G. S. 1997. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89:25-31.
25. Gray, J., Janick-Buckner, D., Buckner, B., Close, P. S., and Johal, G. S. 2002. Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 130:1894-1907.
26. Greenberg, J. T., Silverman, F. P., and Liang, H. 2000. Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics 156:341-350.
27. Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol. 57:231-245.
28. Jabs, T., Deitrich, R. A., and Dangle J. L. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853-1856.
29. Jambunathan, N., Siani, J. M., and McNellis, T. W. 2001. A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell 13:2225-2240.
30. 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.
31. Kiyosawa, S. 1970. Inheritance of a particular sensitivity of the rice variety Sekiguchi Asahi, to pathogens and chemicals, and linkage relationship with blast resistance. Bull. Nat. Agric. Sci. (Jpn.) Ser. D. Physiol. Genet. 21:61-71.
32. Kohler, A., Schwindling, S., and Conrath, U. 2002. Benzothiadiazole- induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol. 128:1046-1056.
33. Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T., and Ryals, J. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 1:71-82.
34. Lee, M. W., Qi, M., and Yang, Y. 2001. A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Mol. Plant-Microbe Interact. 14:527-535.
35. Lorrain, S., Valileau, F., Balague, C., and Roby, D. 2003. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants. Trends Plant Sci. 8:263-271.
36. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I. 1990. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002-1004.
37. 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. 4:403-410.
38. McGee, J. D., Hamer, J. E., and Hodges, T. K. 2001. Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol. Plant-Microbe Interact. 14:877-886.
39. Metraux, J.-P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inveradi, B. 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004-1006.
40. Midoh, N., and Iwata, M. 1996. Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol. 37:9-18.
41. Morris, K., MacKerness, S. A., Page, T., John, C. F., Murphy, A. M., Carr, J. P., and Buchanan-Wollaston, V. 2000. Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23:677-685.
42. Morris, S. W., Vernooij, B., Titatarn, S., Starrett, M., Thomas, S., Wiltse, C. C., Frederiksen, R. A., Bhandhufalck, A., Hulbert, S., and Uknes, S. 1998. Induced resistance responses in maize. Mol. Plant-Microbe Interact. 11:643-658.
43. Mou, Z., Fan, W., and Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944.
44. Nishizawa, Y., Saruta, M., Nakazono, K., Nishio, Z., Soma, M., Yoshida, T., Nakajima, E., and Hibi, T. 2003. Characterization of transgenic rice plants over-expressing the stress-inducible beta-glucanase gene Gns1. Plant Mol. Biol. 51:143-152.
45. Oostendorp, M., Kunz, W., Dietrich, B., and Staub, T. 2001. Induced disease resistance in plants by chemicals. Eur. J. Plant Pathol. 107:19-28
46. Pieterse, C. M., van Wees, S. C., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., and van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.
47. Pilloff, R. K., Devadas, S. K., Enyedi, A., and Raina, R. 2002. The Arabidopsis gain-of-function mutant dll1 spontaneously develops lesions mimicking cell death associated with disease. Plant J. 30:61-70.
48. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steinen H-Y., and Hunt, M. D. 1996. Systemic acquired resistance. Plant Cell 8:1809-1819.
49. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H-Y., Johnson, J., Delaney, T. P., Jesse, T., Vos, P., and Uknes, S. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9:425-439.
50. Sambrook , J., Fritsch, E. F., and Maniatas, T. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
51. Schweizer, P., Schlagenhauf, E., Schaffrath, U., and Dudler, R. 1999. Different patterns of host genes are induced in rice by Pseudomonas svringae, a biological inducer of resistance, and the chemical inducer benzothiadiazole (BTH). Eur. J. Plant Pathol. 105:659-665.
52. Shah, J., Kachroo, P., and Klessig, D. F. 1999. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11:191-206.
53. Shah, J., Kachroo, P., Nandi, A., and Klessig, D. F. 2001. A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 25:563-574.
54. 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
55. Shirano, Y., Kachroo, P., Shah, J., and Klessig, D. F. 2002. A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 4:3149-3162.
56. Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J-P., and Raskin, I. 1995. Salicylic acid in rice: biosynthesis, conjugation and possible role. Plant Physiol. 108:633-639.
57. Smith, J. A., and Metraux, J.-P. 1991. Pseudomonas syringae pathovar syringae induces systemic resistance to Pyricularia oryzae in rice. Physiol. Mol. Plant Pathol. 39:451-461.
58. 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.
59. Subramaniam, R., Desveaux, D., Spickler, C., Michnick, S. W., and Brisson, N. 2001. Direct visualization of protein interactions in plant cells. Nat. Biotechnol. 19:769-772.
60. Takahashi, A., Kawasaki, T., Henmi, K., Shii, K., Kodama, O., Satoh, H., and Shimamoto, K. 1999. Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J. 17:535-545.
61. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessman, H., and Ryals, J. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959-965.
62. Ward, E. R., Uknes, S. J., Williams, S. C., Dinsher, S. S., Wiederhold, D. L., Alexander, D. C., Ahl-Goy, P., Metraux J.-P., and Ryals, J. A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094.
63. Yin, Z., Chen, J., Zeng, L., Goh, M., Leung, H., Khush, G., and Wang, G.-L. W. 2000. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant-Microbe Interact. 13:869-876.
64. Zhang, Y., Fan, W., Kinkema, 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. U.S.A. 96:6523-6528.