Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance

Plant Physiology

Volumn 135, Issue 2, 2004, Pages 1129-1144

  Eulgem, Thomas ^a,f   Weigman, Victor J ^a   Chang, Hur Song ^c,g   McDowell, John M ^d   Holub, Eric B ^e   Glazebrook, Jane ^c,h   Zhu, Tong ^c   Dangl, Jeffery L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c SYNGENTA BIOTECHNOLOGY INC   (United States)

^d Fralin Life Science Institute   (United States)

^e UNIVERSITY OF WARWICK   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g DIVERSA CORPORATION   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; DISEASES; GENES; MICROORGANISMS; PATHOLOGY; PROTEINS;

ARABIDOPSIS PROTEINS; SIGNALING PROTEINS;

PLANTS (BOTANY);

ARABIDOPSIS; EUKARYOTA; HYALOPERONOSPORA PARASITICA; PERONOSPORA; PERONOSPORA FARINOSA; PERONOSPORA PARASITICA; TEREBRANTIA;

EID: 3042537244     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.040444     Document Type: Article

References (76)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene mediated signalling pathways in Arabidopsis. Proc Natl Acad Sci USA 95: 10306-10311
2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-980
3. Austin MJ, Muskett PJ, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R-mediated plant defenses. Science 295: 2077-2080
4. Aviv DH, Rusterucci C, Holt III BF, Dietrich RA, Parker JE, Dangl JL (2002) Runaway cell death, but not basal disease resistance, in lsd1 is SA-and NIM1/NPR1-dependent. Plant J 29: 381-391
5. Azevedo C, Sadanandom A, Kitigawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1 is an essential component of R-gene triggered disease resistance. Science 295: 2073-2076
6. Bittner-Eddy PD, Beynon JL (2001) The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Mol Plant Microbe Interact 14: 416-421
7. Cao H, Bowling SA, Gordon S, Dong X (1994) Characterization of an Arabidopsis mutant that is non-responsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592
8. Cao H, Glazebrook J, Clark JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-64
9. Century KS, Holub EB, Staskawicz BJ (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
10. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963-1965
11. Chen W, Provart N, Glazebrook J, Katagiri F, Chang H-S, Eulgem T, Mauch F, Luan S, Zou G, Whitham S, et al (2002) Expression profile matrices of Arabidopsis transcription factor genes predict their putative functions in response to environmental stresses. Plant Cell 14: 559-574
12. Cooper B, Clarke JD, Budworth P, Kreps J, Hutchison D, Park S, Guimil S, Dunn M, Luginbuhl P, Ellero C, et al (2003) A network of rice genes associated with stress response and seed development. Proc Natl Acad Sci USA 100: 4945-4950
13. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833
14. Delaney T, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessman H, Ward E, et al (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250
15. Desveaux D, Allard J, Brisson N, Sygusch J (2002) A new family of plant transcription factors displays a novel ssDNA-binding surface. Nat Struct Biol 9: 512-517
16. Desveaux D, Subramaniam R, Després C, Mess J-N, Lévesque C, Fobert RR, Dangl JL, Brisson N (2004) A "Whirly" plant transcription factor is a component of the SA-signaling pathway and is required for maximal disease resistance. Dev Cell 6: 229-240
17. Dong X, Li X, Zhang Y, Fan W, Kinkema M, Clarke J (2001) Regulation of systemic acquired resistance by NPR1 and its partners. Novartis Found Symp 236: 165-173; discussion 173-175
18. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
19. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206
20. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signalling: rapid activation by WRKY transcription factors. EMBO J 18: 4689-4699
21. Falk A, Feys B, Frost LN, Jones JDG, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic Upases. Proc Natl Acad Sci USA 96: 3292-3297
22. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance proteins, EDS1 and PAD4. EMBO J 19: 5400-5411
23. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Ryals J (1993) Requirement for salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756
24. Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91: 8955-8959
25. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34: 217-228
26. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973-982
27. Glazebrook J, Rogers EE, Ausubel FM (1997a) Use of Arabidopsis for genetic dissection of plant defense responses. Annu Rev Genet 31: 547-569
28. Glazebrook J, Zook M, Mert F, Kagan I, Rogers EE, Crute IR, Holub EB, Ausubel FM (1997b) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146: 381-392
29. Gray WM, Muskett PR, Chuang HW, Parker JE (2003) Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15: 1310-1319
30. Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14: 177-193
31. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113
32. Heck S, Grau T, Buchala A, Metraux JP, 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 EB, Beynon JL (1996) Symbiology of Mouse Ear Cress (Arabidopsis thaliana) and oomycetes. Adv Bot Res 24: 228-273
34. Hughes JD, Estep PW, Tavazoie S, Church GM (2000) Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J Mol Biol 296: 1205-1214
35. Jabs T, Colling C, Tschöpe M, Hahlbrock K, Scheel D (1997) Elicitor-stimulated ion fluxes and reactive oxygen species from the oxidative burst signal defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 94: 4800-4805
36. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Farcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7: 106-111
37. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96: 13583-13588
38. Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416: 447-451
39. Kinkema M, Fan W, Dong X (2000) Nuclear localization of NRP1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350
40. Kirsch C, Logemann E, Lippok B, Schmelzer E, Hahlbrock K (2001) A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum. Plant J 26: 217-227
41. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, et al (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97: 8849-8855
42. Knudsen S (2002) A Biologist's Guide to Analysis of DNA Microarray Data. John Wiley & Sons, Hoboken, NJ
43. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141
44. Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6866-6871
45. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410
46. Marcotte EM, Thompson MJ, Yeates TO, Eisenberg D (1999) A combined algorithm for genome-wide prediction of protein function. Nature 402: 83-86
47. McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1, and salicylic acid accumulation. Plant J 22: 523-530
48. McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S, Holub EB, Dangl JL (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10: 1861-1874
49. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944
50. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-J, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110
51. Rogers EE, Glazebrook J, Ausubel FM (1996) Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol Plant Microbe Interact 9: 748-757
52. Rombauts S, Florquin K, Lescot M, Marchai K, Rouze P, van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132: 1162-1176
53. Rushton PJ, Reinstadler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14: 749-762
54. Rushton PJ, Somssich IE (1998) Transcriptional control of plant genes responsive to pathogens. Curr Opin Plant Biol 1: 311-315
55. Rushton PJ, Tovar Torres J, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15: 5690-5700
56. Rusterucci C, Aviv DH, Holt III BF, Dangl JL, Parker JE (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13: 2211-2224
57. Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner HY, Johnson J, Delaney TP, Jesse T, Vos P, et al (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor 1 kappa B. Plant Cell 9: 425-439
58. Schindler U, Beckmann H, Cashmore AR (1992) TGA1 and G-box binding factors: Two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. Plant Cell 4: 1309-1319
59. Schmelzer E, Krüger-Lebus S, Hahlbrock K (1989) Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1: 993-1001
60. Slusarenko AJS, Schlaich NL (2003) Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol Plant Pathol 4: 159-170
61. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, 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
62. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317-330
63. Tör M, Gordon P, Cuzick A, Eulgem T, Sinapidou E, Mert F, Can C, Dangl JL, Holub EB (2002) Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew (Peronospora parasitica) resistance genes. Plant Cell 14: 993-1003
64. van der Biezen EA, Freddie CT, Kahn K, Parker JE, Jones JDG (2002) Arabidopsis RPP4 is a member the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signaling components. Plant J 29: 439-451
65. van Wees SC, 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
66. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565
67. Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6: 520-527
68. Zhang Y, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15: 2647-2653
69. Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance of tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16: 3207-3218
70. Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camelexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419-2428
71. Zhou N, Tootle TL, Klessig DF, Glazebrook J (1998) PAD4 functions upstream of salicylic acid to control defense responses in Arabidopsis. Plant Cell 10: 1021-1030
72. Zhu T, Budworth P, Han B, Brown D, Chang HS, Zou G, Wang X (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8300 genes by high-density oligonucleotide probe array. Plant Physiol Biochem 39: 221-242
73. Zhu T, Wang X (2000) Large-scale profiling of the Arabidopsis transcriptome. Plant Physiol 124: 1472-1476
74. Zimmermann S, Nurnberger T, Frachisse JM, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca(2+)-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94: 2751-2755
75. Zook M, Hammerschmidt R (1997) Origin of the thiazole ring of camalexin, a phytoalexin from Arabidopsis thaliana. Plant Physiol 113: 463-468
76. Zook M, Leege L, Jacobson D, Hammerschmidt R (1998) Camalexin accumulation in Arabis lyrata. Phytochemistry 49: 2287-2289