Expression of Pseudomonas syringae type III effectors in yeast under stress conditions reveals that HopX1 attenuates activation of the high osmolarity glycerol MAP kinase pathway

Microbiology (United Kingdom)

Volumn 158, Issue 11, 2012, Pages 2859-2869

  Salomon, Dor ^a   Bosis, Eran ^a   Dar, Daniel ^a   Nachman, Iftach ^a   Sessa, Guido ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; FUNGUS GROWTH; GROWTH INHIBITION; NONHUMAN; OSMOLARITY; OSMOTIC STRESS; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE; STRESS; YEAST;

BACTERIAL PROTEINS; GENE EXPRESSION; GLYCEROL; MITOGEN-ACTIVATED PROTEIN KINASES; OSMOLAR CONCENTRATION; PLANT DISEASES; PSEUDOMONAS SYRINGAE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

BACTERIA (MICROORGANISMS); EUKARYOTA; LYCOPERSICON ESCULENTUM; NEGIBACTERIA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 84868321735     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.062513-0     Document Type: Article

References (59)

1. 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.
2. Auesukaree, C., Damnernsawad, A., Kruatrachue, M., Pokethitiyook, P., Boonchird, C., Kaneko, Y. & Harashima, S. (2009). Genome-wide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. J Appl Genet 50, 301-310.
3. Block, A. & Alfano, J. R. (2011). Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr Opin Microbiol 14, 39-46.
4. Block, A., Guo, M., Li, G., Elowsky, C., Clemente, T. E. & Alfano, J. R. (2010). The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell Microbiol 12, 318-330.
5. Bosis, E., Salomon, D. & Sessa, G. (2011). A simple yeast-based strategy to identify host cellular processes targeted by bacterial effector proteins. PLoS ONE 6, e27698.
6. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S. & other authors (2003). The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100, 10181-10186.
7. Cox, J. S. & Walter, P. (1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404.
8. Cunnac, S., Lindeberg, M. & Collmer, A. (2009). Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr Opin Microbiol 12, 53-60.
9. Cunnac, S., Chakravarthy, S., Kvitko, B. H., Russell, A. B., Martin, G. B. & Collmer, A. (2011). Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108, 2975-2980.
10. Curak, J., Rohde, J. & Stagljar, I. (2009). Yeast as a tool to study bacterial effectors. Curr Opin Microbiol 12, 18-23.
11. del Pozo, O., Pedley, K. F. & Martin, G. B. (2004). MAPKKKa is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 23, 3072-3082.
12. Feng, F. & Zhou, J. M. (2012). Plant-bacterial pathogen interactions mediated by type III effectors. Curr Opin Plant Biol 15, 469-476.
13. Ferrigno, P., Posas, F., Koepp, D., Saito, H. & Silver, P. A. (1998). Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1. EMBO J 17, 5606-5614.
14. Fu, Z. Q., Guo, M., Jeong, B. R., Tian, F., Elthon, T. E., Cerny, R. L., Staiger, D. & Alfano, J. R. (2007). A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284-288.
15. García, R., Rodríguez-Peña, J. M., Bermejo, C., Nombela, C. & Arroyo, J. (2009). The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J Biol Chem 284, 10901-10911.
16. Gimenez-Ibanez, S., Hann, D. R., Ntoukakis, V., Petutschnig, E., Lipka, V. & Rathjen, J. P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19, 423-429.
17. Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J. W. & Robatzek, S. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18, 1824-1832.
18. Gustin, M. C., Albertyn, J., Alexander, M. & Davenport, K. (1998). MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62, 1264-1300.
19. Ham, J. H., Majerczak, D., Ewert, S., Sreerekha, M. V., Mackey, D. & Coplin, D. (2008). WtsE, an AvrE-family type III effector protein of Pantoea stewartii subsp. stewartii, causes cell death in non-host plants. Mol Plant Pathol 9, 633-643.
20. Hersen, P., McClean, M. N., Mahadevan, L. & Ramanathan, S. (2008). Signal processing by the HOG MAP kinase pathway. Proc Natl Acad Sci U S A 105, 7165-7170.
21. Hoffman, G. A., Garrison, T. R. & Dohlman, H. G. (2002). Analysis of RGS proteins in Saccharomyces cerevisiae. Methods Enzymol 344, 617-631.
22. Hohmann, S. (2002). Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66, 300-372.
23. Howson, R., Huh, W. K., Ghaemmaghami, S., Falvo, J. V., Bower, K., Belle, A., Dephoure, N., Wykoff, D. D., Weissman, J. S. & O'Shea, E. K. (2005). Construction, verification and experimental use of two epitope-tagged collections of budding yeast strains. Comp Funct Genomics 6, 2-16.
24. Jelenska, J., Yao, N., Vinatzer, B. A., Wright, C. M., Brodsky, J. L. & Greenberg, J. T. (2007). A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17, 499-508.
25. Jung, U. S., Sobering, A. K., Romeo, M. J. & Levin, D. E. (2002). Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol Microbiol 46, 781-789.
26. Kippert, F. (1995). A rapid permeabilization procedure for accurate quantitative determination of b-galactosidase activity in yeast cells. FEMS Microbiol Lett 128, 201-206.
27. Kuranda, K., Leberre, V., Sokol, S., Palamarczyk, G. & Franç ois, J. (2006). Investigating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the connection between TOR, PKC and Ras/cAMP signalling pathways. Mol Microbiol 61, 1147-1166.
28. Kvitko, B. H., Park, D. H., Velá squez, A. C., Wei, C. F., Russell, A. B., Martin, G. B., Schneider, D. J. & Collmer, A. (2009). Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5, e1000388.
29. Maayan, I. & Engelberg, D. (2009). The yeast MAPK Hog1 is not essential for immediate survival under osmostress. FEBS Lett 583, 2015-2020.
30. Martin, G. B., Bogdanove, A. J. & Sessa, G. (2003). Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54, 23-61.
31. Melech-Bonfil, S. & Sessa, G. (2010). Tomato MAPKKKe is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J 64, 379-391.
32. Munkvold, K. R., Martin, M. E., Bronstein, P. A. & Collmer, A. (2008). A survey of the Pseudomonas syringae pv. tomato DC3000 type III secretion system effector repertoire reveals several effectors that are deleterious when expressed in Saccharomyces cerevisiae. Mol Plant Microbe Interact 21, 490-502.
33. Mur, L. A., Kenton, P., Lloyd, A. J., Ougham, H. & Prats, E. (2008). The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59, 501-520.
34. Nachman, I., Regev, A. & Ramanathan, S. (2007). Dissecting timing variability in yeast meiosis. Cell 131, 544-556.
35. Nimchuk, Z. L., Fisher, E. J., Desveaux, D., Chang, J. H. & Dangl, J. L. (2007). The HopX (AvrPphE) family of Pseudomonas syringae type III effectors require a catalytic triad and a novel N-terminal domain for function. Mol Plant Microbe Interact 20, 346-357.
36. Nomura, K., Debroy, S., Lee, Y. H., Pumplin, N., Jones, J. & He, S. Y. (2006). A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313, 220-223.
37. Ntoukakis, V., Mucyn, T. S., Gimenez-Ibanez, S., Chapman, H. C., Gutierrez, J. R., Balmuth, A. L., Jones, A. M. & Rathjen, J. P. (2009). Host inhibition of a bacterial virulence effector triggers immunity to infection. Science 324, 784-787.
38. Parsons, A. B., Brost, R. L., Ding, H., Li, Z., Zhang, C., Sheikh, B., Brown, G. W., Kane, P. M., Hughes, T. R. & Boone, C. (2004). Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat Biotechnol 22, 62-69.
39. Patterson, J. C., Klimenko, E. S. & Thorner, J. (2010). Single-cell analysis reveals that insulation maintains signaling specificity between two yeast MAPK pathways with common components. Sci Signal 3, ra75.
40. Preston, G. M. (2000). Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1, 263-275.
41. Rodriguez, M. C., Petersen, M. & Mundy, J. (2010). Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61, 621-649.
42. Rodríguez-Herva, J. J., Gonzá lez-Melendi, P., Cuartas-Lanza, R., Antúnez-Lamas, M., Río-Alvarez, I., Li, Z., López-Torrejón, G., Díaz, I., Del Pozo, J. C. & other authors (2012). A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cell Microbiol 14, 669-681.
43. Rodríguez-Peña, J. M., García, R., Nombela, C. & Arroyo, J. (2010). The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast 27, 495-502.
44. Rosebrock, T. R., Zeng, L., Brady, J. J., Abramovitch, R. B., Xiao, F. & Martin, G. B. (2007). A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448, 370-374.
45. Salomon, D. & Sessa, G. (2010). Identification of growth inhibition phenotypes induced by expression of bacterial type III effectors in yeast. J Vis Exp (37).
46. Salomon, D., Dar, D., Sreeramulu, S. & Sessa, G. (2011). Expression of Xanthomonas campestris pv. vesicatoria type III effectors in yeast affects cell growth and viability. Mol Plant Microbe Interact 24, 305-314.
47. Schacherer, J., Ruderfer, D. M., Gresham, D., Dolinski, K., Botstein, D. & Kruglyak, L. (2007). Genome-wide analysis of nucleotide-level variation in commonly used Saccharomyces cerevisiae strains. PLoS ONE 2, e322.
48. Shan, L., He, P. & Sheen, J. (2007). Intercepting host MAPK signaling cascades by bacterial type III effectors. Cell Host Microbe 1, 167-174.
49. Siggers, K. A. & Lesser, C. F. (2008). The yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 4, 8-15.
50. Slagowski, N. L., Kramer, R. W., Morrison, M. F., LaBaer, J. & Lesser, C. F. (2008). A functional genomic yeast screen to identify pathogenic bacterial proteins. PLoS Pathog 4, e9.
51. Tatebayashi, K., Yamamoto, K., Tanaka, K., Tomida, T., Maruoka, T., Kasukawa, E. & Saito, H. (2006). Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. EMBO J 25, 3033-3044.
52. Tatebayashi, K., Tanaka, K., Yang, H. Y., Yamamoto, K., Matsushita, Y., Tomida, T., Imai, M. & Saito, H. (2007). Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26, 3521-3533.
53. Tena, G., Boudsocq, M. & Sheen, J. (2011). Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14, 519-529.
54. Valdivia, R. H. (2004). Modeling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot Cell 3, 827-834.
55. Wang, Y., Li, J., Hou, S., Wang, X., Li, Y., Ren, D., Chen, S., Tang, X. & Zhou, J. M. (2010). A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22, 2033-2044.
56. Wilton, M., Subramaniam, R., Elmore, J., Felsensteiner, C., Coaker, G. & Desveaux, D. (2010). The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc Natl Acad Sci U S A 107, 2349-2354.
57. Xiang, T., Zong, N., Zou, Y., Wu, Y., Zhang, J., Xing, W., Li, Y., Tang, X., Zhu, L. & other authors (2008). Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18, 74-80.
58. Yoon, S., Liu, Z., Eyobo, Y. & Orth, K. (2003). Yersinia effector YopJ inhibits yeast MAPK signaling pathways by an evolutionarily conserved mechanism. J Biol Chem 278, 2131-2135.
59. Zeng, L., Velá squez, A. C., Munkvold, K. R., Zhang, J. & Martin, G. B. (2012). A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 69, 92-103.