Pseudomonas syringae pv. syringae Uses Proteasome Inhibitor Syringolin A to Colonize from Wound Infection Sites

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Misas Villamil, Johana C ^a   Kolodziejek, Izabella ^a   Crabill, Emerson ^b,c   Kaschani, Farnusch ^a,d   Niessen, Sherry ^e   Shindo, Takayuki ^a   Kaiser, Markus ^d   Alfano, James R ^b   van der Hoorn, Renier A L ^a  

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

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF NEBRASKA   (United States)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEASOME INHIBITOR; REACTIVE OXYGEN METABOLITE; STRESS HORMONE; SYRINGOLIN A; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL PLANT DISEASE; BIOSYNTHESIS; CELL DEATH; CONTROLLED STUDY; DNA ISOLATION; FLUORESCENCE MICROSCOPY; IMMUNE RESPONSE; NICOTIANA BENTHAMIANA; NONHUMAN; PEAR; PLANT GROWTH; PSEUDOMONAS SYRINGAE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WOUND INFECTION;

AMINO ACID SEQUENCE; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PLANT DISEASES; PLANT PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; TOBACCO; WOUND INFECTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. SYRINGAE; PUNCTUM BLANDIANUM; PYRUS;

EID: 84876004778     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003281     Document Type: Article

References (57)

1. Agrios GN (2005) Plant pathology. 5th edition. Burlington: Elsevier Academic Press. 952p.
2. Hirano SS, Upper CD, (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae- a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64: 624-653.
3. Lee J, Teitzel G, Munkvold K, del Pozo O, Martin GB, et al. (2012) Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiol 158: 1803-1818.
4. Greenberg JT, Yao N, (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6: 201-211.
5. Leben C, Schroth MN, Hildebrand DC, (1970) Colonization and movement of Pseudomonas syringae on healthy bean seedlings. Phytopathology 60: 677-680.
6. Hirano SS, Baker LS, Upper CD, (1996) Raindrop Momentum triggers growth of leaf-associated populations of Pseudomonas syringae on field-grown snap bean plants. Appl Environ Microbiol 62: 2560-2566.
7. Serfontein JJ, (1994) Occurrence of bacterial brown spot of dry beans in the Transvaal province of South Africa. Plant Pathol 43: 597-599.
8. Panagopoulos CG, Crosse JE, (1964) Frost injury as a predisposing factor in blossom blight of pear cause by Pseudomonas syringae van Hall. Nature 202: 1352.
9. Misas-Villamil JC, Kolodziejek I, van der Hoorn RAL, (2011) Pseudomonas syringae colonizes distant tissues in Nicotiana benthamiana through xylem vessels. Plant J 67: 774-782.
10. Goodin MM, Zaitlin D, Naidu RA, Lommel SA, (2008) Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant-Microbe Interact 21: 1015-1026.
11. Kvitko BH, Park DH, Velasuez AC, Wei CF, Russell AB, et al. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens 5: e100388.
12. Nguyen HP, Chakravarthy S, Velasquez AC, McLane HL, Zeng L, et al. (2010) Methods to study PAMP-triggred immunity using tomato and Nicotiana benthamiana. Mol Plant-Microbe Interact 23: 991-999.
13. Hann DR, Rathjen JP, (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J 49: 607-618.
14. Vinatzer BA, Teitzel GM, Lee MW, Jelenska J, Hotton S, et al. (2006) The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol Microbiol 62: 26-44.
15. 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.
16. Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, et al. (2012) Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24: 336-352.
17. Wäspi U, Blanc D, Winkler T, Rüedi P, Dudler R, (1998) Syringolin, a novel peptide elicitor from Pseudomonas syringae pv. syringae that induces resistance to Pyricularia oryzae in rice. Mol Plant-Microbe Interact 11: 727-733.
18. Groll M, Schellenberg B, Bachmann AS, Archer CR, Huber R, et al. (2008) A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 452: 755-758.
19. Schellenberg B, Ramel C, Dudler R, (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant-Microbe Interact 23: 1287-1293.
20. Kolodziejek I, Misas-Villamil JC, Kaschani F, Clerc J, Gu C, et al. (2011) Proteasome activity imaging and profiling characterizes bacterial effector Syringolin A. Plant Physiol 155: 477-489.
21. Jones JDG, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
22. Amrein H, Makart S, Granado J, Shakya R, Schneider-Pokorny J, et al. (2004) Functional analysis of genes involved in the synthesis of syringolin A by Pseudomonas syringae pv. syringae B301D-R. Mol Plant-Microbe Interact 17: 90-97.
23. Ramel C, Tobler M, Meyer M, Bigler L, Ebert MO, et al. (2009) Biosynthesis of the proteasome inhibitor syringolin A: the ureido group joining two amino acids originates from bicarbonate. BMC Biochemistry 10: 26.
24. Gu C, Kolodziejek I, Misas-Villamil J, Shindo T, Colby T, et al. (2010) Proteasome activity profiling: a simple, robust and versatile method revealing subunit-selective inhibitors and cytoplasmic, defence-induced proteasome activities. Plant J 62: 160-170.
25. Clerc J, Florea BI, Kraus M, Groll M, Huber R, et al. (2009) Syringolin A selectively labels the 20 S proteasome in murine EL4 and wild-type and bortezomib-adapted leukaemic cell lines. ChemBioChem 10: 2638-2643.
26. Vlot AC, Dempsey DA, Klessig DF, (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47: 177-206.
27. Kohler A, Schwindling S, Conrath U, (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128: 1046-1056.
28. He SY, Huang HS, Collmer A, (1993) Pseudomonas syringae pv. syringae HarpinPss: A protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73: 1255-1266.
29. Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, et al. (2007) A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J 51: 32-46.
30. Wulff BBH, Kruijt M, Collins PL, Thomas CM, Ludwig AA, et al. (2004) Gene shuffling-generated and natural variants of the tomato resistance gene Cf-9 exhibit different auto-necrosis-inducing activities in Nicotiana species. Plant J 40: 942-956.
31. Krzymowska M, Konopka-Postupolska D, Sobczak M, Macioszek V, Ellis BE, et al. (2007) Infection of tobacco with different Pseudomonas syringae pathovars leads to distinct morphotypes of programmed cell death. Plant J 50: 253-264.
32. Wang K, Uppalapati SR, Zhu X, Dinesh-Kumar SP, Mysore KS, (2010) SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol Plant Pathol 11: 597-611.
33. Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, et al. (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22: 5690-5699.
34. Monier JM, Lindow SE, (2003) Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc Natl Acad Sci U S A 100: 15977-15982.
35. Van Wees SCN, 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.
36. 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.
37. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, et al. (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23: 2496-2506.
38. Del Pozo O, Lam E, (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8: 1129-1132.
39. Meiners S, Ludwig A, Stangl V, Stangl K, (2008) Proteasome inhibitors: poisons and remedies. Med Res Rev 28: 309-327.
40. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, et al. (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220-223.
41. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, et al. (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448: 370-374.
42. Melotto M, Underwood W, Koczan J, Nomura K, He SH, (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
43. Sarkar SF, Gordon JS, Martin GB, Guttman DS, (2006) Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 174: 1041-1056.
44. Lin NC, Abramovitch RB, Kim YJ, Martin GB, (2006) Diverse AvrPtoB homologs from several Pseudomonas syringae pathovars elicit Pto-dependent resistance and have similar virulence activities. Appl Environm Microbiol 72: 702-712.
45. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, et al. (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860-872.
46. Khang CH, Berruyer R, Giraldo MC, Kankabala P, Park S, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388-1403.
47. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478: 395-398.
48. Uppalapati SR, Ihiga Y, Wangdi T, Kunkel BN, Anand A, et al. (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant-Microbe Interact 20: 955-965.
49. Zheng X, Spivey NW, Zeng W, Liu P, Fu ZQ, et al. (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signalling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11: 587-596.
50. Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, et al. (2005) Pseudomonas syringae manipulates systemic plant defences against pathogens and herbivores. Proc Natl Acad Sci U S A 102: 1791-1796.
51. Harper S, Zewdie N, Brown IR, Mansfield JW, (1987) Histological, physiological and genetical studies of the responses of leaves and pods of Phaseolus vulgaris to three races of Pseudomonas syringae pv. phaseolicola and to Pseudomonas syringae pv. coronafaciens. Physiol Mol Plant Pathology 31: 153-172.
52. Brown IR, Mansfield JW, (1988) An ultrascructural study, including cytochemistry and quantitative analysis, of the interactions between pseudomonads and leaves of Phaseolus vulgaris L. Physiol Mol Plant Pathol 33: 351-376.
53. Labes M, Pühler A, Simon R, (1990) A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria. Gene 89: 37-46.
54. Wilson M, Hirano SS, Lindow SE, (1999) Location and survival of leaf-associated bacteria in relation to pathogenicity and potential for growth within the leaf. App. Environ Microbiol 65: 1435-1443.
55. Clerc J, Groll M, Illich DJ, Bachmann AS, Huber R, et al. (2009) Synthetic and structural studies in syringolin A and B reveal critical determinants of selectivity and potency of proteasome inhibition. Proc Natl Acad Sci U S A 106: 6507-6512.
56. Straus MR, Rietz S, Ver Loren van Themaat E, Bartsch M, Parker JE, (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J 62: 628-640.
57. Adam L, Somerville SC, (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J 9: 341-356.