Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis

Plant Journal

Volumn 62, Issue 4, 2010, Pages 628-640

  Straus, Marco R ^a,b   Rietz, Steffen ^a   Ver Loren Van Themaat, Emiel ^a   Bartsch, Michael ^a,c   Parker, Jane E ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

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

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Flg22; Nudix hydrolase; Paraquat; Reactive oxygen species

Indexed keywords

ABIOTIC STRESS; ARABIDOPSIS; GENE EXPRESSION PROFILES; NADPH OXIDASE; NUDIX HYDROLASE; OXIDATIVE STRESS RESPONSE; PHOTO-OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SALICYLIC ACIDS;

ACID RESISTANCE; ACIDS; CHLOROPHYLL; DATA FLOW ANALYSIS; GENE EXPRESSION; HERBICIDES; OXIDATIVE STRESS; OXYGEN;

CELL DEATH;

ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; EDS1 PROTEIN, ARABIDOPSIS; HYDROGEN PEROXIDE; INORGANIC PYROPHOSPHATASE; NUDIX HYDROLASES; PLANT RNA; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PYROPHOSPHATASES; REACTIVE OXYGEN SPECIES; RNA, PLANT; SALICYLIC ACID; SEQUENCE ANALYSIS, DNA; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS;

EID: 77952191124     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04178.x     Document Type: Article

References (64)

1. Adams-Phillips, L., Wan, J.R., Tan, X.P., Dunning, F.M., Meyers, B.C., Michelmore, R.W. Bent, A.F. (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol. Plant Microbe Interact. 21, 646 657.
2. Apel, K. Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399.
3. Asada, K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391 396.
4. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977 983.
5. Attaran, E., Zeier, T.E., Griebel, T. Zeier, J. (2009) Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell, 21, 954 971.
6. Aviv, D.H., Rusterucci, C., Holt, B.F., Dietrich, R.A., Parker, J.E. Dangl, J.L. (2002) Runaway cell death, but not basal disease resistance, in Isd1 is SA- and NIM1/NPR1-dependent. Plant J. 29, 381 391.
7. Bartsch, M., Gobbato, E., Bednarek, P., Debey, S., Schultze, J.L., Bautor, J. Parker, J.E. (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell, 18, 1038 1051.
8. Birker, D., Heidrich, K., Takahara, H., Narusaka, M., Deslandes, L., Narusaka, Y., Reymond, M., Parker, J.E. O'Connell, R. (2009) A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60, 602 613.
9. Boller, T. Felix, G. (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379 406.
10. Brodersen, P., Malinovsky, F.G., Hematy, K., Newman, M.A. Mundy, J. (2005) The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol. 138, 1037 1045.
11. Delledonne, M., Zeier, J., Marocco, A. Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl Acad. Sci. USA, 98, 13454 13459.
12. Eulgem, T., Weigman, V.J., Chang, H.S., McDowell, J.M., Holub, E.B., Glazebrook, J., Zhu, T. Dangl, J.L. (2004) Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance. Plant Physiol. 135, 1129 1144.
13. Felix, G., Duran, J.D., Volko, S. Boller, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265 276.
14. Feys, B.J., Moisan, L.J., Newman, M.A. Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400 5411.
15. Feys, B.J., Wiermer, M., Bhat, R.A., Moisan, L.J., Medina-Escobar, N., Neu, C., Cabral, A. Parker, J.E. (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell, 17, 2601 2613.
16. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R. Van Breusegem, F. (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436 445.
17. Ge, X.C., Li, G.J., Wang, S.B., Zhu, H.F., Zhu, T., Wang, X. Xia, Y.J. (2007) AtNUDT7, a negative regulator of basal immunity in arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol. 145, 204 215.
18. Gomez-Gomez, L., Felix, G. Boller, T. (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277 284.
19. Grant, M.R. Jones, J.D.G. (2009) Hormone (dis)harmony moulds plant health and disease. Science, 324, 750 752.
20. He, P., Shan, L., Lin, N.C., Martin, G.B., Kemmerling, B., Nurnberger, T. Sheen, J. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell, 125, 563 575.
21. Innes, R.W., Bisgrove, S.R., Smith, N.M., Bent, A.F., Staskawicz, B.J. Liu, Y.C. (1993) Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the Rpg1 locus of soybean. Plant J. 4, 813 820.
22. Ishikawa, K., Ogawa, T., Hirosue, E., Nakayama, Y., Harada, K., Fukusaki, E., Yoshimura, K. Shigeoka, S. (2009) Modulation of the poly(ADP-ribosyl)ation reaction via the Arabidopsis ADP-ribose/NADH pyrophosphohydrolase, AtNUDX7, is involved in the response to oxidative stress. Plant Physiol. 151, 741 754.
23. Jabs, T., Dietrich, R.A. Dangl, J.L. (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science, 273, 1853 1856.
24. Jones, J.D.G. Dangl, J.L. (2006) The plant immune system. Nature, 444, 323 329.
25. Joo, J.H., Wang, S.Y., Chen, J.G., Jones, A.M. Fedoroff, N.V. (2005) Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell, 17, 957 970.
26. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. Dangl, J.L. (1999) LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12, 1022 1026.
27. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I. Apel, K. (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 672 677.
28. Lipka, V., Dittgen, J., Bednarek, P. et al. (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science, 310, 1180 1183.
29. Lorrain, S., Vailleau, F., Balaque, C. Roby, D. (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263 271.
30. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R. Dangl, J.L. (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112, 379 389.
31. Mateo, A., Muhlenbock, P., Rusterucci, C., Chang, C.C.C., Miszalski, Z., Karpinska, B., Parker, J.E., Mullineaux, P.M. Karpinski, S. (2004) Lesion simulating disease 1- is required for acclimation to conditions that promote excess excitation energy. Plant Physiol. 136, 2818 2830.
32. Mateo, A., Funck, D., Muhlenbock, P., Kular, B., Mullineaux, P.M. Karpinski, S. (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J. Exp. Bot. 57, 1795 1807.
33. McLennan, A.G. (2006) The Nudix hydrolase superfamily. Cell. Mol. Life Sci. 63, 123 143.
34. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., Dangl, J.L. Mittler, R. (2009) The plant NADPH oxidase RbohD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45.
35. Mishina, T.E. Zeier, J. (2007) Bacterial non-host resistance: interactions of Arabidopsis with non-adapted Pseudomonas syringae strains. Physiol. Plant. 131, 448 461.
36. Muhlenbock, P., Szechynska-Hebda, M., Plaszczyca, M., Baudo, M., Mullineaux, P.M., Parker, J.E., Karpinska, B. Karpinski, S. (2008) Chloroplast signaling and Lesion simulating disease1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell, 20, 2339 2356.
37. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T. Jones, J.D.G. (2004) The transcriptional innate immune response to flg22. interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113 1128.
38. Nuhse, T.S., Peck, S.C., Hirt, H. Boller, T. (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK6. J. Biol. Chem. 275, 7521 7526.
39. Ochsenbein, C., Przybyla, D., Danon, A., Landgraf, F., Gobel, C., Imboden, A., Feussner, I. Apel, K. (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J. 47, 445 456.
40. Ogawa, T., Ueda, Y., Yoshimura, K. Shigeoka, S. (2005) Comprehensive analysis of cytosolic nudix hydrolases in Arabidopsis thaliana. J. Biol. Chem. 280, 25277 25283.
41. Olejnik, K. Kraszewska, E. (2005) Cloning and characterization of an Arabidopsis thaliana Nudix hydrolase homologous to the mammalian GFG protein. Biochim. Biophys. Acta 1752, 133 141.
42. Peck, S.C., Nuhse, T.S., Hess, D., Iglesias, A., Meins, F. Boller, T. (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell, 13, 1467 1475.
43. Qin, X.J., Hudson, L.G., Liu, W., Timmins, G.S. Liu, K.J. (2008) Low concentration of arsenite exacerbates UVR-induced DNA strand breaks by inhibiting PARP-1 activity. Toxicol. Appl. Pharmacol. 232, 41 50.
44. Rajjou, L., Belghazi, M., Huguet, R., Robin, C., Moreau, A., Job, C. Job, D. (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol. 141, 910 923.
45. Rosebrock, T.R., Zeng, L.R., Brady, J.J., Abramovitch, R.B., Xiao, F.M. Martin, G.B. (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature, 448, 370 374.
46. Rusterucci, C., Aviv, D.H., Holt, B.F., Dangl, J.L. Parker, J.E. (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.
47. Shen, Q.H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ulker, B., Somssich, I.E. Schulze-Lefert, P. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science, 315, 1098 1103.
48. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A. Lamb, C. (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell, 9, 261 270.
49. Tao, Y., Xie, Z.Y., Chen, W.Q., Glazebrook, J., Chang, H.S., Han, B., Zhu, T., Zou, G.Z. Katagiri, F. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317 330.
50. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187 1194.
51. Torres, M.A., Dangl, J.L. Jones, J.D.G. (2002) Arabidopsis gp91(phox) homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA, 99, 517 522.
52. Torres, M.A., Jones, J.D.G. Dangl, J.L. (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130 1134.
53. Tsuda, K., Sato, M., Glazebrook, J., Cohen, J.D. Katagiri, F. (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J. 53, 763 775.
54. Van Breusegem, F., Bailey-Serres, J. Mittler, R. (2008) Unraveling the tapestry of networks involving Reactive Oxygen Species in plants. Plant Physiol. 147, 978 984. (Pubitemid 352844254) (Pubitemid 352844254) (Pubitemid 352844254)
55. Vlot, A.C., Liu, P.P., Cameron, R.K. et al. (2008) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J. 56, 445 456.
56. Wiermer, M., Feys, B.J. Parker, J.E. (2005) Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8, 383 389.
57. Wildermuth, M.C., Dewdney, J., Wu, G. Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562 565.
58. Wirthmueller, L., Zhang, Y., Jones, J.D.G. Parker, J.E. (2007) Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17, 2023 2029.
59. Wrzaczek, M., Brosche, M., Kollist, H. Kangasjarvi, J. (2009) Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS. Proc. Natl Acad. Sci. USA, 106, 5412 5417.
60. Xiang, T.T., Zong, N., Zou, Y. et al. (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18, 74 80.
61. Yun, B.W., Atkinson, H.A., Gaborit, C., Greenland, A., Read, N.D., Pallas, J.A. Loake, G.J. (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J. 34, 768 777.
62. Zeier, J., Delledonne, M., Mishina, T., Severi, E., Sonoda, M. Lamb, C. (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol. 136, 2875 2886.
63. Zhang, J., Shao, F., Cui, H. et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-Induced immunity in plants. Cell Host Microbe, 1, 175 185.
64. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D.G., Felix, G. Boller, T. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428, 764 767.