Negative regulation of defence signalling pathways by the EDR1 protein kinase

Molecular Plant Pathology

Volumn 12, Issue 8, 2011, Pages 746-758

  Christiansen, Katy M ^a,b   Gu, Yangnan ^a   Rodibaugh, Natalie ^a   Innes, Roger W ^a  

^a INDIANA UNIVERSITY   (United States)

^b JOINT BIOENERGY INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; EDR1 PROTEIN, ARABIDOPSIS; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; ASCOMYCETES; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL NUCLEUS; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); ERYSIPHALES; GOLOVINOMYCES CICHORACEARUM;

EID: 80052402892     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2011.00708.x     Document Type: Article

References (66)

1. Adam, L. and Somerville, S.C. (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341-356.
2. Adam, L., Ellwood, S., Wilson, I., Saenz, G., Xiao, S., Oliver, R.P., Turner, J.G. and Somerville, S. (1999) Comparison of Erysiphe cichoracearum and E. cruciferarum and a survey of 360 Arabidopsis thaliana accessions for resistance to these two powdery mildew pathogens. Mol. Plant-Microbe Interact. 12, 1031-1043.
3. Ade, J., DeYoung, B.J., Golstein, C. and Innes, R.W. (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc. Natl. Acad. Sci. USA 104, 2531-2536.
4. Allan, A.C. and Fluhr, R. (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9, 1559-1572.
5. Aoyama, T. and Chua, N.H. (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605-612.
6. Apel, K. and Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
7. Basha, E., Friedrich, K.L. and Vierling, E. (2006) The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J. Biol. Chem. 281, 39943-39952.
8. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 57, 289-300.
9. Bent, A.F. and Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436.
10. Berardini, T.Z., Mundodi, S., Reiser, L., Huala, E., Garcia-Hernandez, M., Zhang, P., Mueller, L.A., Yoon, J., Doyle, A., Lander, G., Moseyko, N., Yoo, D., Xu, I., Zoeckler, B., Montoya, M., Miller, N., Weems, D. and Rhee, S.Y. (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 135, 745-755.
11. Bhat, R.A., Borst, J.W., Riehl, M. and Thompson, R.D. (2004) Interaction of maize Opaque-2 and the transcriptional co-activators GCN5 and ADA2, in the modulation of transcriptional activity. Plant Mol. Biol. 55, 239-252.
12. Bhattarai, K.K., Atamian, H.S., Kaloshian, I. and Eulgem, T. (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J. 63, 229-240.
13. 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.
14. Buttner, M. and Singh, K.B. (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc. Natl. Acad. Sci. USA 94, 5961-5966.
15. Chakravarthy, S. (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell Online 15, 3033-3050.
16. Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T. and Luan, S. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129, 661-677.
17. Ciolkowski, I., Wanke, D., Birkenbihl, R.P. and Somssich, I.E. (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol. Biol. 68, 81-92.
18. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
19. Custers, J., Harrison, S., Sela-Buurlage, M., Van Deventer, E., Lageweg, W., Howe, P., Van Der Meijs, P., Ponstein, A., Simons, B., Melchers, L. and Stuiver, M. (2004) Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. Plant J. 39, 147-160.
20. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826-833.
21. Devaiah, B.N., Karthikeyan, A.S. and Raghothama, K.G. (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143, 1789-1801.
22. Du, L. and Chen, Z. (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J. 24, 837-847.
23. Epple, P., Apel, K. and Bohlmann, H. (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 109, 813-820.
24. Eulgem, T. and Somssich, I. (2007) Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366-371.
25. Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
26. Fabro, G., Di Rienzo, J.A., Voigt, C.A., Savchenko, T., Dehesh, K., Somerville, S. and Alvarez, M.E. (2008) Genome-wide expression profiling of Arabidopsis at the stage of Golovinomyces cichoracearum haustorium formation. Plant Physiol. 146, 1421-1439.
27. Frye, C.A. and Innes, R.W. (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10, 947-956.
28. Frye, C.A., Tang, D. and Innes, R.W. (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98, 373-378.
29. Gagne, J.M., Smalle, J., Gingerich, D.J., Walker, J.M., Yoo, S.D., Yanagisawa, S. and Vierstra, R.D. (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad. Sci. USA 101, 6803-6808.
30. Gao, Z., Chen, Y.F., Randlett, M.D., Zhao, X.C., Findell, J.L., Kieber, J.J. and Schaller, G.E. (2003) Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J. Biol. Chem. 278, 34725-34732.
31. 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.
32. Guo, H. and Ecker, J.R. (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115, 667-677.
33. Gutterson, N. and Reuber, T.L. (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr. Opin. Plant Biol. 7, 465-471.
34. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W. and Zimmermann, P. (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747.
35. Jing, H.C., Anderson, L., Sturre, M.J., Hille, J. and Dijkwel, P.P. (2007) Arabidopsis CPR5 is a senescence-regulatory gene with pleiotropic functions as predicted by the evolutionary theory of senescence. J. Exp. Bot. 58, 3885-3894.
36. Kremers, G.J., Goedhart, J., van Munster, E.B. and Gadella, T.W., Jr (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 45, 6570-6580.
37. Li, J., Brader, G. and Palva, E.T. (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16, 319-331.
38. McNellis, T.W., Mudgett, M.B., Li, K., Aoyama, T., Horvath, D., Chua, N.H. and Staskawicz, B.J. (1998) Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death. Plant J. 14, 247-257.
39. Mur, L.A., 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.
40. Nelson, B.K., Cai, X. and Nebenfuhr, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
41. Ning, J., Li, X., Hicks, L.M. and Xiong, L. (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 152, 876-890.
42. Nobuta, K., Okrent, R.A., Stoutemyer, M., Rodibaugh, N., Kempema, L., Wildermuth, M.C. and Innes, R.W. (2007) The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol. 144, 1144-1156.
43. Potter, S., Uknes, S., Lawton, K., Winter, A.M., Chandler, D., DiMaio, J., Novitzky, R., Ward, E. and Ryals, J. (1993) Regulation of a hevein-like gene in Arabidopsis. Mol. Plant-Microbe Interact. 6, 680-685.
44. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C. and Genschik, P. (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679-689.
45. Pre, M., Atallah, M., Champion, A., De Vos, M., Pieterse, C.M. and Memelink, J. (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347-1357.
46. Prelic, A., Bleuler, S., Zimmermann, P., Wille, A., Buhlmann, P., Gruissem, W., Hennig, L., Thiele, L. and Zitzler, E. (2006) A systematic comparison and evaluation of biclustering methods for gene expression data. Bioinformatics 22, 1122-1129.
47. Qi, Y. and Katagiri, F. (2009) Purification of low-abundance Arabidopsis plasma-membrane protein complexes and identification of candidate components. Plant J. 57, 932-944.
48. Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K. and Somssich, I.E. (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15, 5690-5700.
49. Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292-1309.
50. Shiu, S.H. and Bleecker, A.B. (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE 2001, RE22.
51. Silverstein, K.A., Graham, M.A., Paape, T.D. and VandenBosch, K.A. (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol. 138, 600-610.
52. Song, C.P., Agarwal, M., Ohta, M., Guo, Y., Halfter, U., Wang, P. and Zhu, J.K. (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384-2396.
53. Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D. and Callis, J. (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18, 3415-3428.
54. Tang, D. and Innes, R.W. (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J. 32, 975-983.
55. Tang, D., Christiansen, K.M. and Innes, R.W. (2005) Regulation of plant disease resistance, stress responses, cell death, and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol. 138, 1018-1026.
56. Torres, M.A., Jones, J.D. and Dangl, J. (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130-1134.
57. Vera-Estrella, R., Blumwald, E. and Higgins, V.J. (1992) Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells: evidence for the involvement of active oxygen species. Plant Physiol. 99, 1208-1215.
58. Verburg, J.G. and Huynh, Q.K. (1991) Purification and characterization of an antifungal chitinase from Arabidopsis thaliana. Plant Physiol. 95, 450-455.
59. Wagner, U., Edwards, R., Dixon, D.P. and Mauch, F. (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515-532.
60. Wang, D., Amornsiripanitch, N. and Dong, X. (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. Plos. Pathog. 2, e123.
61. Wawrzynska, A., Christiansen, K.M., Lan, Y., Rodibaugh, N.L. and Innes, R.W. (2008) Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol. 148, 1510-1522.
62. Yoo, S.D., Cho, Y.H., Tena, G., Xiong, Y. and Sheen, J. (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789-795.
63. Yoshida, K., Kaothien, P., Matsui, T., Kawaoka, A. and Shinmyo, A. (2003) Molecular biology and application of plant peroxidase genes. Appl. Microbiol. Biotechnol. 60, 665-670.
64. Yoshida, S., Ito, M., Nishida, I. and Watanabe, A. (2002) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defence responses in Arabidopsis thaliana. Plant J. 29, 427-437.
65. Zimmerli, L., Stein, M., Lipka, V., Schulze-Lefert, P. and Somerville, S. (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J. 40, 633-646.
66. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.