Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas

FEMS Microbiology Letters

Volumn 327, Issue 1, 2012, Pages 1-8

  Fones, Helen ^a   Preston, Gail M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Catalase; Coronatine; Hydrogen peroxide; Polyhydroxyalkanoate; Superoxide; Superoxide dismutase

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL POLYSACCHARIDE; CATALASE; CHLOROPHYLL; COPPER ZINC SUPEROXIDE DISMUTASE; CORONATINE; OXIDATIVE SIGNAL INDUCIBLE 1; PEROXIDASE; POLYESTER; PROTEIN SERINE THREONINE KINASE; PYOCYANINE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; BACTERIAL COLONIZATION; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; NONHUMAN; OXIDATIVE STRESS; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE; RESPIRATORY BURST; SHORT SURVEY; TYPE III SECRETION SYSTEM;

HOST-PATHOGEN INTERACTIONS; OXIDATIVE STRESS; PLANT DISEASES; PLANTS; PSEUDOMONAS; REACTIVE OXYGEN SPECIES;

ANIMALIA; PSEUDOMONAS;

EID: 84855475719     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2011.02449.x     Document Type: Short Survey

References (73)

1. Albert FG, Benet LW & Anderson AJ (1986) Peroxidase associated with the root surface of Phaseols vulgaris. Can J Bot 64: 573-578.
2. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA & Lamb CJ (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773-784.
3. Ayub N, Tribelli P & López N (2009) Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14-3 during low temperature adaptation. Extremophiles 13: 59-66.
4. Bender CL, Stone HE, Sims JJ & Cooksey DA (1987) Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn5 mutants defective in coronatine production. Physiol Mol Plant Pathol 30: 272-283.
5. Bizzini A, Zhao C, Auffray Y & Hartke A (2009) The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J Antimicrob Chemother 64: 1196-1202.
6. Block A, Guo M, Li G, Elowsky C, Clemento TE & Alfano JR (2010) The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell Microbiol 12: 318-330.
7. Bradley DJ, Kjellbon P & Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell-wall protein: a novel, rapid defense response. Cell 70: 21-30.
8. Bretz JR & Hutcheson SW (2004) Role of type III effector secretion during bacterial pathogenesis in another kingdom. Infect Immun 72: 3697-3705.
9. Brown SM, Howell ML, Vasil ML, Anderson AJ & Hassett DJ (1995) Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J Bacteriol 177: 6536-6544.
10. Buell RC, Joardar V, Lindeberg M et al. (2003) The complete genome of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. P Natl Acad Sci USA 100: 10181-10186.
11. Castro-Sowinski S, Burdman S, Matan O & Okon Y (2010). Natural functions of bacterial polyhydroxyalkanoates. Plastics from Bacteria (Chen GG-Q, ed), pp. 39-61. Springer, Berlin/Heidelberg.
12. Chang W-S, van de Mortel M, Nielsen L, de Guzman GN, Li X & Halverson LJ (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189: 8290-8299.
13. Chen PR, Bae T, Williams WA, Duguid EM, Rice PA, Schneewind O & He C (2006) An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat Chem Biol 2: 591-595.
14. Chen H, Hu J, Chen PR, Lan L, Li Z, Hicks LM, Dinner AR & He C (2008) The Pseudomonas aeruginosa multidrug efflux regulator MexR uses an oxidation-sensing mechanism. P Natl Acad Sci USA 105: 13586-13591.
15. Cornelis P, Wei Q, Andrews SC & Vinckx T (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3: 540-549.
16. Cox CS (1989) Airbourne bacteria and viruses. Sci Prog 73: 469-500.
17. Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal cell wall components. Physiol Plant Pathol 23: 345-357.
18. Duffy B (2003) Pathogen self-defence: mechanisms to counteract microbial antagonism. Annu Rev Phytopathol 41: 501-538.
19. Fett WF & Dunn MF (1989) Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts. Plant Physiol 89: 5-9.
20. Fett WF, Osman SF & Dunn MF (1989) Characteristation of exopolysaccharides produced by plant-associated fluorescent pseudomonads. Appl Environ Microbiol 55: 579-583.
21. Finn RD, Mistry J, Tate J et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
22. Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, Dangl JL & Grant SR (2008) The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol Plant Microbe Interact 21: 361-370.
23. Goto S, Miyazaki S & Ohno A (1991) Virulence factors of Pseudomonas aeruginosa in mice. Jpn J Clin Med 2: 111-116.
24. Grant SR, Fisher EJ, Chang JH, Mole BM & Dangl JL (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60: 425-449.
25. Gusarov I, Shatalin K, Starodubtseva M & Nudler E (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325: 1380-1384.
26. Hasset DJ & Cohen MS (1989) Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. FASEB J 3: 2574-2582.
27. Howell ML, Alsabbagh E, Ma J-F et al. (2000) AnkB, a periplasmic ankyrin-like protein in Pseudomonas aeruginosa, is required for optimal catalase B (KatB) activity and resistance to hydrogen peroxide. J Bacteriol 182: 4545-4556.
28. Huisman GW, de Leeuw O, Eggink G & Witholt B (1989) Synthesis of poly-3-hydroxyalkanoates is a common feature of fluorescent pseudomonads. Applied and Environmental Microbiology 55: 1949-1954.
29. Iiyama K, Chieda Y, Lee JM, Kusakabe T, Yusunaga-Aoki C & Shimizu S (2007) Effect of superoxide gene inactivation on virulence of P. aeruginosa PA01 toward the silkworm, Bombyx mori. Appl Environ Microbiol 73: 1569-1575.
30. Imlay JA & Linn S (1988) DNA damage and oxygen radical toxicity. Science 240: 1302-1313.
31. Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B & Bender CL (2008) The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol 181: 147-160.
32. Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B & Bender CL (2009) Involvement of coronatine-inducible reactive oxygen species in bacterial speck disease of tomato. Plant Signal Behav 4: 237-239.
33. Katsuwon J & Anderson AJ (1989) Response of plant-colonising pseudomonads to hydrogen peroxide. Appl Environ Microbiol 55: 2985-2989.
34. Keith LMW & Bender CL (1999) AlgT (σ22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181: 7176-7184.
35. Keith RC, Keith LMW, Hernández-Guzmán G, Uppalapati SR & Bender CL (2003) Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and non-host plants. Microbiology 149: 1127-1138.
36. Kessler B & Palleroni NJ (2000) Taxonomic implications of synthesis of poly-beta-hydroxybutyrate and other poly-beta-hydroxyalkanoates by aerobic pseudomonads. Int J Syst Evol Microbiol 50: 711-713.
37. Kim YC, Miller CD & Anderson AJ (1999) Transcriptional regulation by iron and role during pathogenesis of genes encoding iron and manganese superoxide dismutases of Pseudomonas syringae pv. syringae. Physiol Mol Plant Pathol 55: 327-339.
38. Kim YC, Miller CD & Anderson AJ (2000) Superoxide dismutase activity in Pseudomonas putida affects utilization of sugars and growth on root surfaces. Appl Environ Microbiol 66: 1460-1467.
39. Klotz MG & Hutcheson SW (1992) Multiple periplasmic catalases in phytopathogenic strains of Pseudomonas syringae. Appl Environ Microbiol 58: 2468-2473.
40. Klotz MG, Kim YC, Katsuwon J & Anderson AJ (1995) Cloning, characterisation and phenotypic expression in Escherichia coli of catF, which encodes the catalytic subunit of catalase isozyme CatF of Pseudomonas syringae. Appl Microbiol Biotechnol 43: 656-666.
41. Kohanski MA, Dwyer DJ, Hayete B, Lawrence, CA & Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
42. Lamb CJ, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275.
43. Madison LL & Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63: 21-53.
44. Mahajan-Miklos S, Tan M-W, Rahme LG & Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
45. Marthi B, Shaffer BT, Lighthart B & Ganio L (1991) Resuscitation effects of catalase on airborne bacteria. Appl Environ Microbiol 57: 2775-2776.
46. Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105: 467-472.
47. Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D & Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27: 385-410.
48. Navarro L, Zepfel C, Rowland O, Keller I, Robatzek S, Boller T & Jones JDG (2004) Transcriptional innate immune response to flg22: interplay and overlap with Avr-gene-dependent defense responses and bacterial pathogens. Plant Physiol 135: 1113-1128.
49. Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K & Hassett DJ (2000) Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA Repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J Bacteriol 182: 4533-4544.
50. O'Malley YQ, Reszha KJ, Rasmussen GT, Abdulla MY, Denning GM & Britigan BE (2003) The Pseudomonas secretory product pyocyanin inhibits catalase in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 285: 1077-1086.
51. Panmanee W, Vattanaviboon P, Poole LB & Mongkolsuk S (2006) Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. J Bacteriol 188: 1389-1395.
52. Peng M & Kuc J (1992) Peroxide generated hydrogen peroxide as a source of toxicity in vitro and on tobacco leaf discs. Phytopathology 82: 696-699.
53. Petersen LN, Ingle RA, Knight MR & Denby KJ (2009) OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60: 3727-3735.
54. de Pinto MC, Lavermicocca P, Evidente A, Corsaro MM, Lazzaroni S & De Gara L (2003) Exopolysaccharides produced by plant pathogenic bacteria affect ascorbate metabolism in Nicotiana tabacum. Plant Cell Physiol 44: 803-810.
55. Quiñones B, Dulla G & Lindow SE (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18: 682-693.
56. Ran H, Hasset DJ & Lan GW (2003) Human targets of Pseudomonas aeruginosa pyocyanin. P Natl Acad Sci USA 100: 14315-14320.
57. Rico A, Bennett MH, Forcat S, Huang WE & Preston GM (2010) Agroinfiltration reduces ABA levels and suppresses Pseudomonas syringae-elicited salicylic acid production in Nicotiana tabacum. PLoS ONE 5: e8977.
58. Santos R, Franza T, Laporte ML, Sauvage C, Touati D & Expert D (2001) Essential role of superoxide dismutase on the pathogenicity of Erwinia chrysanthemi strain 3937. Mol Plant Microbe Interact 14: 758-767.
59. Scott MD, Meshnick SR & Eaton JW (1987) Superoxide dismutase-rich bacteria. Paradoxical effect on oxidant toxicity. J Biol Chem 262: 3640-3645.
60. Scott MD, Meshnick SR & Eaton JW (1989) Superoxide dismutase amplifies organismal sensitivity to ionising radiation. J Biol Chem 264: 2498-2501.
61. Shin D-H, Choi Y-S & Cho Y-H (2008) Unusual properties of catalase A (KatA) of Pseudomonas aeruginosa PA14 are associated with its biofilm peroxide resistance. J Bacteriol 190: 2663-2670.
62. Silipo A, Erbs G, Shinya T, Dow JM, Parrilli M, Lanzetta R, Shibuya N, Newman M-A & Molinaro A (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20: 406-419.
63. Soto MJ, Sanjuán J & Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiology 152: 3167-3174.
64. Tenhanken R, Levine A, Brisson LF, Dixon RA & Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. P Natl Acad Sci USA 92: 4158-4163.
65. Torres MA, Jones JDG & Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37: 1130-1134.
66. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bogre L & Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26: 1434-1443.
67. Touati D (2002) Investigating phenotypes resulting from a lack of superoxide dismutase in bacterial null mutants. Methods Enzymol 349: 145-154.
68. Uppalapati SR, Ishiga Y, Wangdi T, Urbanczyk-Wochniak E, Ishiga T, Mysore KS & Bender CL (2008) Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol Plant Microbe Interact 21: 383-395.
69. Vanacker H, Carver TLW & Foyer CH (1998) Pathogen induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117: 1103-1114.
70. Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681-692.
71. Yu JA, Peñaloza-Vázquez A, Chakrabarty AM & Bender CL (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33: 712-720.
72. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W & Wang X (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21: 2357-2377.
73. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY & Howe GA (2003) Virulence systems in Pseudomonas syringae pv. tomato promote bacterial speck disease by targeting the jasmonate signalling pathway. Plant J 36: 485-499.