An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance

Plant Journal

Volumn 41, Issue 2, 2005, Pages 304-318

  Liu, Guosheng ^a   Holub, Eric B ^b   Alonso, Jose M ^c,d   Ecker, Joseph R ^c   Fobert, Pierre R ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Cross talk; Gene family; PR genes; Reverse genetics; Salicylic acid; Signaling

Indexed keywords

BACTERIA; DISEASES; MUTAGENESIS; ORGANIC ACIDS; PROTEINS; YEAST;

HYBRID ASSAYS; JASMONIC ACID (JA); PATHWAY MARKERS; TRANSCRIPTION FACTORS;

GENES;

ARABIDOPSIS PROTEIN; BACTERIAL DNA; NPR1 PROTEIN, ARABIDOPSIS; NPR4 PROTEIN, ARABIDOPSIS; T DNA; T-DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; INNATE IMMUNITY; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PLANT DISEASE; PSEUDOMONAS SYRINGAE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; IMMUNITY, NATURAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PHYLOGENY; PLANT DISEASES; PSEUDOMONAS SYRINGAE;

BACTERIA; DISEASES; GENES; MUTATION; PROTEINS; SALICYLIC ACID; YEASTS;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); ERYSIPHE; GOLOVINOMYCES CICHORACEARUM; HYALOPERONOSPORA PARASITICA; INSERTION SEQUENCES; LYCOPERSICON ESCULENTUM; PERONOSPORA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; TEREBRANTIA;

EID: 12844264294     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02296.x     Document Type: Article

References (79)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
3. Berger, S., Bell, E., Sadka, A. and Mullet, J.E. (1995) Arabidopsis thaliana AtVsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27, 933-942.
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. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell, 9, 1573-1584.
6. 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.
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. USA, 95, 6531-6536.
9. 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.
10. Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557-569.
11. 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.
12. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation in Arabidopsis thaliana. Plant J. 16, 735-743.
13. Conrath, U., Pieterse, C.M.J. and Mauch-Mani, B. (2002) Priming in plant-pathogen interactions. Trends Plant Sci. 7, 210-216.
14. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S. and Somerville, C.R. (2000) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl Acad. Sci. USA, 97, 3718-3723.
15. Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
16. 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. USA, 92, 6602-6606.
17. Després, C., DeLong, C., Glaze, S., Liu, E. and Robert, 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.
18. Després, C., Chubak, C., Rochon, A., Clark, R., Bethune, T., Desveaux, D. and Fobert, P.R. (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell, 15, 2181-2191.
19. Dong, X. (2001) Genetic dissection of systemic acquired resistance. Curr. Opin. Plant Biol. 4, 309-314.
20. Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell, 13, 1025-1030.
21. 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 lipases. Proc. Natl Acad. Sci. USA, 96, 3292-3297.
22. 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.
23. Feys, B.J. and Parker, J.E. (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449-455.
24. Foster, E., Hattori, J., Labbe, H., Ouellet, T., Fobert, P.R., James, L.E., Iyer, V.N. and Miki, B.L. (1999) A tobacco cryptic constitutive promoter, tCUP, revealed by T-DNA tagging. Plant Mol. Biol. 41, 45-55.
25. Franklin, K.A., Davis, S.J., Stoddart, W.M., Vierstra, R.D. and Whitelam, G.C. (2003) Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell, 15, 1981-1989.
26. Friedrich, L., Lawson, 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. 14, 1114-1124.
27. Glazebrook, J. (2001) Genes controlling expression of defense responses in Arabidopsis - 2001 status. Curr. Opin. Plant Biol. 4, 301-308.
28. 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.
29. 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.
30. Hammond-Kosack, K.E. and Jones, J.D. (1996) Resistance gene-dependent plant defense responses. Plant Cell, 8, 1773-1791.
31. Hammond-Kosack, K.E. and Parker, J.E. (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14, 177-193.
32. Heck, S., Grau, T., Buchala, A., Métraux, 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.
33. Holub, E.B. (2001) The arms race is ancient history in Arabidopsis and the wildflower. Nat. Rev. Genet. 2, 516-527.
34. Hood, E.E., Gelvin, S.B., Melchers, L.S. and Hoekema, A. (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2, 208-218.
35. Jirage, D., Tootle, T.L., Reuber, T.L., Frost, L.N., Feys, B.J., Parker, J.E. and Ausubel, P.M. (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl Acad. Sci. USA, 96, 13583-13588.
36. Johnson, C., Boden, E. and Arias, J. (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell, 15, 1846-1858.
37. Jupin, I. and Chua, N.H. (1996) Activation of the CaMV as-1 cis-element by salicylic acid: differential DNA-binding of a factor related to TGA1a. EMBO J. 15, 5679-5689.
38. Kim, H.S. and Delaney, T.P. (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/ NPR1, confers SAP-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J. 32, 151-163.
39. 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.
40. Kohalmi, S.E., Nowak, J. and Crosby, W.L. (1997) The yeast two-hybrid system. In Differentially Expressed Genes in Plants: A Bench Manual (Hansen, E. and Harper, G., eds). London: Taylor and Francis, pp. 63-82.
41. Kunkel, B.N. and Brooks, D.M. (2002) Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331.
42. Lam, E., Benfey, P.M., Gilmartin, P.M., Fang, R.X. and Chua, N.H. (1989) Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc. Natl Acad. Sci. USA, 86, 7890-7894.
43. Li, X., Zhang, Y., Clarke, J.D., Li, Y. and Dong, X. (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell, 98, 329-339.
44. Liu, G., Sánchez-Fernández, R., Li, Z.-S. and Rea, P.A. (2001) Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J. Biol. Chem. 276, 8648-8656.
45. Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J. and Cameron, R.K. (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature, 419, 399-403.
46. 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.
47. Manners, J.M., Penninckx, I.A.M.A., Vermaere, K., Kazan, K., Brown, R.L., Morgan, A., Maclean, D.J., Curtis, M.D., Cammue, B.P.A. and Broekaert, W.F. (1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid. Plant Mol. Biol. 38, 1071-1080.
48. 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.
49. Monte, E., Alonso, J.M., Ecker, J.R., Zhang, Y., Li, X., Young, J., Austin-Phillips, S. and Quail, P.H. (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell, 15, 1962-1980.
50. Mou, Z., Fan, W. and Dong, X. (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113, 935-944.
51. Nawrath, C. and Métraux, 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.
52. Nawrath, C., Heck, S., Parinthawong, N. and Métraux, J.-P. (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14, 275-286.
53. Niggeweg, R., Thurow, C., Kegler, C. and Gatz, C. (2000) Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters. J. Biol. Chem. 275, 19897-19905.
54. Penninckx, I.A.M.A., Eggermont, K., Terras, F.R.G., Thomma, B.P.H.J., De Samblanx, G.W., Buchala, A., Métraux, J.-P., Manners, J.M. and Broekaert, W.F. (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 8, 2309-2323.
55. Pieterse, C.M.J., van Wees, S.C.M., Hoffland, E., van Pelt, J.A. and van Loon, L.C. (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell, 8, 1225-1237.
56. Polowick, P.L., Quandt, J. and Mahon, J.D. (2000) The ability of pea transformation technology to transfer genes into peas adapted to western Canadian growing conditions. Plant Sci. 153, 161-170.
57. Pontier, D., Miao, Z.H. and Lam, E. (2001) Trans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses. Plant J. 27, 529-538.
58. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485.
59. Ryals, J.A., Neuenschwander, D.H., Willits, M.G., Molina, A., Steiner, H.-Y. and Hunt, M.D. (1996) Systemic acquired resistance. Plant Cell, 8, 1808-1819.
60. Ryals, J., Weymann, K., Lawton, K. et al. (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell, 9, 425-439.
61. Sánchez-Fernández, R., Emyr Davies, T.G., Coleman, J.O.D. and Rea, P.A. (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J. Biol. Chem. 276, 30231-30244.
62. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl Acad. Sci. USA, 97, 11655-11660.
63. 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.
64. Sharma, K.G., Mason, D.L., Liu, G., Rea, P.A., Bachhawat, A.K. and Michaelis, S. (2002) Localization, regulation and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot. Cell, 1, 391-400.
65. Slusarenko, A.J. and Schlaich, N.L. (2003) Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol. Plant Pathol. 4, 159-170.
66. Spoel, S.H., Koornneef, A., Claessens, S.M.C. 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.
67. 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.
68. Thomma, B.P.H.J., Penninckx, I.A.M.A., Cammue, B.P.A. and Broekaert, W.F. (2001) The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13, 63-68.
69. Tör, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert-Türk, F., Can, C., Dangl, J.L. and Holub, E.B. (2002) Arabidopsis SGT1b is required for defense signalling conferred by several downy mildew resistance genes. Plant Cell, 14, 993-1003.
70. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E. and Ryals, J. (1992) Acquired resistance in Arabidopsis. Plant Cell, 4, 645-656.
71. Varagona, M.J., Schmidt, R.J. and Raikhel, N.V. (1992) Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell, 4, 1213-1227.
72. van Wees, S.C.M. 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.
73. Weigel, R.F., Bauscher, C., Pfitzner, A.J.P. and Pfitzner, U.M. (2001) NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants. Plant Mol. Biol. 46, 143-160.
74. Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature, 414, 562-565.
75. Witte, R.S. (1989) Statistics, 3rd edn. New York: Holt, Rinehart and Winston, Inc., The Dryden Press.
76. Xiang, C., Miao, Z.H. and Lam, E. (1996) Coordinated activation of as-1-type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide. Plant Mol. Biol. 32, 415-426.
77. 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. USA, 96, 6523-6528.
78. Zhang, Y., Tessaro, M.J., Lassner, M. and Li, X. (2003) Knockout analysis of Arabidopsis TGA2, TGA5 and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell, 15, 2647-2653.
79. Zhou, J.M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J. and Klessig, D.F. (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.