A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down-regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots

Planta

Volumn 226, Issue 2, 2007, Pages 283-297

  Rudrappa, Thimmaraju ^a   Quinn, William J ^b   Stanley Wall, Nicola R ^b   Bais, Harsh P ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Arabidopsis; Bacillus subtilis; Biofilm; Catechol; Reactive oxygen species (ROS); Roots

Indexed keywords

ASCORBIC ACID; CATECHOL; CATECHOL DERIVATIVE; MIXED FUNCTION OXIDASE; REACTIVE OXYGEN METABOLITE; SALICYLATE 1 MONOOXYGENASE; SALICYLATE 1-MONOOXYGENASE; SALICYLIC ACID; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BACILLUS SUBTILIS; BIOFILM; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PHYSIOLOGY; PLANT ROOT; TRANSGENIC PLANT;

ARABIDOPSIS; ASCORBIC ACID; BACILLUS SUBTILIS; BIOFILMS; CATECHOLS; IMMUNITY, NATURAL; MIXED FUNCTION OXYGENASES; OXIDATIVE STRESS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; SALICYLIC ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACILLUS SUBTILIS; RHIZOBIALES;

EID: 34250012624     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-007-0480-8     Document Type: Article

References (58)

1. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823-1835
2. Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani damping off of Tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081-4085
3. Bacon CW, Yates IE, Hinton DM, Meredith F (2001) Biological control of Fusarium moneliforme in maize. Environ Health Perspect 109:325-332
4. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:377-1380
5. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis root by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307-319
6. Bradley DJ, Kjellbom 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
7. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621-11626
8. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229-1238
9. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich SD, Losick R, Kolter R (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186:3970-3979
10. Cavaglieri L, Orlando J, Rodriguez MI, Chulze S, Etcheverry M (2005) Biocontrol of Bacillus subtilis against Fusarium verticilloides in vitro and at the maize root level. Res Microbiol 156:748-754
11. Chen Z, Gallie DR (2005) Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol 138:1673-1689
12. Chu F, Kearns DB, Branda SS, Kolter R, Losick R (2006) Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol Microbiol 59:1216-1228
13. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant associated bacteria. Crit Rev Microbiol 21:1-18
14. Dal-Soo K, Cook RJ, Weller DM (1997) Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. Biol Control 87:551-558
15. Davey ME, O'toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847-867
16. Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a gram positive perspective. FEMS Microbiol Lett 171:1-9
17. Estevez de Jensen C, Percich JA, Graham PH (2002) Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. Field Crops Res 74:107-115
18. Fall R, Kinsinger RF, Wheeler KA (2004) A simple method to isolate biofilm forming Bacillus subtilis and related species from plant roots. Syst Appl Microbiol 27:372-379
19. Fujishige NA, Kapadia NN, Hirsh AM (2006) A feeling for the micro-organism: structure on a small scale, biofilms on plant roots. Bot J London Soc 150:79-88
20. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95-108
21. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42:1199-1209
22. Hamon MA, Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2004) Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol Microbiol 52:847-860
23. Harwood CR, Cutting SM (1990) Molecular biological methods for Bacillus. John, Chichester, England
24. Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 97:2405-2407
25. Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739-749
26. Kerry BR (2000) Rhizosphere interaction and the exploitation of microbial agents for the biological control of plant pathogenic Fungi. Annu Rev Phytopathol 38:423-432
27. Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Kliester DL, Cregan PG (eds) The rhizosphere and plant growth. Kluwer Academic Press, Dordrecht, The Netherlands, pp 315-326
28. Laloi C, Apel K, Danon K (2004) Latest news in reactive oxygen species. Curr Opin Plant Biol 7:323-328
29. Lambeth JD, Cheng G, Arnold RS, Edens WA (2000) Novel homologs of gp91phox. Trends Biochem Sci 25:459-461
30. Lutenberg BJJ, De Weger LA, Bennett JW (1991) Microbial stimulation of plant growth and protection from disease. Curr Opin Microbiol 2:457-464
31. Mao W, Lumsden RD, Lewis JA, Hebbar PK (1998) Seed treatment using pre-infiltration and biocontrol agents to reduce damping-off caused by species of Pythium and Fusarium. Plant Dis 82:294-299
32. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tissue culture. Physiol Planta 15:473-497
33. Muzandu K, Shaban Z, Ishizuka M, Kazusaka A, Fujita S (2005) Nitric oxide enhances catechol estrogen-induced oxidative stress in LNCaP cells. Free Radic Res 39:389-398
34. Nacamulli C, Bevivino A, Dalmastri C, Tabacchioni S, Chiarini L (1997) Perturbation of maize rhizosphere microflora following seed bacterization with Burkholderia cepacia MCI7. FEMS Microbiol Ecol 23:183-193
35. Narula N, Deubel A, Gans W, Behl RK, Merbach W (2006) Paranodules and colonization of wheat roots by phytohormone producing bacteria in soil. Plant Soil Environ 52:119-129
36. O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol Microbiol 28:449-461
37. Perego M, Spiegelman GB, Hoch JA (1988) Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol Microbiol 2:689-699
38. Powell KA, Jutsum AR (1993) Technical and commercial aspects of biological control products. Pestic Sci 37:315-321
39. Ramey BE, Koutsoudis M, von Bodman S, Fuqua C (2004) Biofilm formation in plant-microbe associations. Curr Opin Microbiol 7:602-609
40. Roberts MFC (1995) Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution 49:1081-1094
41. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Pare P-W (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927-4932
42. Ryu C-M, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growth promoting rhizobacteria systematically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1 independent and jasmonic acid-dependent signaling pathway. Plant J 39:381-392
43. Schweigert N, Zehnder AJB, Eggen RIL (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3:81-91
44. Scott IM, Clarke SM, Wood JE, Mur LAJ (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040-1049
45. Shin R, Berg HR, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorous and potassium deficiency. Plant Cell Physiol 46:1350-1357
46. Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951-1957
47. Stanley NR, Lazazzera B (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-DL- glutamic acid production and biofilm formation. Mol Microbiol 57:1143-1158
48. Suh Y-A, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD (1999) Cell transformation by the superoxide- generating oxidase Mox1. Nature 401:79-82
49. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052-1066
50. Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227-235
51. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187-1194
52. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373-378
53. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153-S164
54. van Wees SC, de Swart EA, van Pelt JA, van Loon LC, Pieterse CM (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711-8716
55. van Wees SCM, Glazebrook J (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. Phaseolicola is due to degradation product of salicylic acid. Plant J 33:733-742
56. Warrior P, Konduru K, Vasudevan P (2002) Formulation of biological control agents for pest and disease management. In: Gnanamanickam SS (ed) Biological control of crop diseases. Marcel Dekker, New York, pp 421-442
57. Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909-919
58. Yuan G, Wong SL (1995) Regulation of groE expression in Bacillus subtilis: the involvement of the sigma A-like promoter and the roles of the inverted repeat sequence (CIRCE). J Bacteriol 177:5427-5433