Thermo-Regulation of Genes Mediating Motility and Plant Interactions in Pseudomonas syringae

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Hockett, Kevin L ^a,b   Burch, Adrien Y ^a   Lindow, Steven E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSURFACTANT; CHAPERONE; COMPLEMENTARY DNA; FLAGELLIN; HEAT SHOCK PROTEIN; PLANT TOXIN; POLYSACCHARIDE; QUATERNARY AMMONIUM DERIVATIVE; SYRINGAFACTIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SURVIVAL; BACTERIOPHAGE; BIOSYNTHESIS; CELL VIABILITY; CHEMOTAXIS; CONTROLLED STUDY; FLGM GENE; FLIC GENE; GENE; GENE DELETION; GENE FUNCTION; GENE INSERTION SEQUENCE; GENE REPRESSION; INCUBATION TEMPERATURE; NONHUMAN; PLANT PATHOGEN INTERACTION; PSEUDOMONAS SYRINGAE; RNA SEQUENCE; RNA TRANSLATION; SALA GENE; SWARMING MOTILITY; SWIMMING MOTILITY; SYFA GENE; SYRF GENE; SYRG GENE; TEMPERATURE SENSITIVITY; THERMOREGULATION; TRANSCRIPTION REGULATION; TYPE IV SECRETION SYSTEM;

FLAGELLA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MOVEMENT; PLANT LEAVES; PSEUDOMONAS SYRINGAE; QUATERNARY AMMONIUM COMPOUNDS; REAL-TIME POLYMERASE CHAIN REACTION; TEMPERATURE;

EID: 84875120369     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059850     Document Type: Article

References (77)

1. Rouse DI, Nordheim EV, Hirano SS, Upper CD, (1985) A Model relating the probability of foliar disease incidence to the population frequencies of bacterial plant-pathogens. Phytopathology 75: 505-509.
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. Lindow SE, Brandl MT, (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69: 1875-1883.
4. Monier JM, Lindow SE, (2004) Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl Environ Microbiol 70: 346-355.
5. Schonherr J, (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J Exp Bot 57: 2471-2491.
6. Haefele DM, Lindow SE, (1987) Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl Environ Microbiol 53: 2528-2533.
7. Hattermann DR, Ries SM, (1989) Motility of Pseudomonas syringae pv. glycinea and its role in infection. Phytopathology 79: 284-289.
8. Panopoulos NJ, Schroth MN, (1974) Role of flagellar motility in the invasion of bean leaves by Pseudomonas phaseolicola. Phytopathology 64: 1389-1397.
9. Schreiber KJ, Desveaux D, (2011) AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol Microbiol 80: 364-377.
10. Quinones B, Dulla G, Lindow SE, (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18: 682-693.
11. Dechesne A, Wang G, Gulez G, Or D, Smets BF, (2010) Hydration-controlled bacterial motility and dispersal on surfaces. Proc Natl Acad Sci USA 107: 14369-14372.
12. Macnab RM (1996) Flagella and Motility. In: Neidhardt FC, editor. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd ed. Washington, D.C.: ASM Press. 123-145.
13. Soscia C, Hachani A, Bernadac A, Filloux A, Bleves S, (2007) Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J Bacteriol 189: 3124-3132.
14. Tart AH, Blanks MJ, Wozniak DJ, (2006) The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J Bacteriol 188: 6483-6489.
15. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA, (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 3603-3612.
16. Lindeberg M, Cunnac S, Collmer A, (2009) The evolution of Pseudomonas syringae host specificity and type III effector repertoires. Mol Plant Pathol 10: 767-775.
17. Danhorn T, Fuqua C, (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61: 401-422.
18. Smirnova A, Li HQ, Weingart H, Aufhammer S, Burse A, et al. (2001) Thermoregulated expression of virulence factors in plant-associated bacteria. Arch Microbiol 176: 393-399.
19. Kearns DB, (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8: 634-644.
20. Burch AY, Shimada BK, Browne PJ, Lindow SE, (2010) Novel High-Throughput Detection Method To Assess Bacterial Surfactant Production. Appl Environ Microbiol 76: 5363-5372.
21. Berti AD, Greve NJ, Christensen QH, Thomas MG, (2007) Identification of a biosynthetic gene cluster and the six associated lipopeptides involved in swarming motility of Pseudomonas syringae pv. tomato DC3000. J Bacteriol 189: 6312-6323.
22. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50: 809-824.
23. Choy W-K, Zhou L, Syn CK-C, Zhang L-H, Swarup S, (2004) MorA defines a new class of regulators affecting flagellar development and biofilm formation in diverse Pseudomonas species. J Bacteriol 186: 7221-7228.
24. Aldridge P, Hughes KT, (2002) Regulation of flagellar assembly. Curr Opin Microbiol 5: 160-165.
25. Kitten T, Kinscherf TG, McEvoy JL, Willis DK, (1998) A newly identified regulator is required for virulence and toxin production in Pseudomonas syringae. Mol Microbiol 28: 917-929.
26. Leplae R, Lima-Mendez G, Toussaint A, (2010) ACLAME: A CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res 38: D57-D61.
27. Records AR, Gross DC, (2010) Sensor Kinases RetS and LadS Regulate Pseudomonas syringae Type VI Secretion and Virulence Factors. J Bacteriol 192: 3584-3596.
28. Chen CL, Beattie GA, (2007) Characterization of the osmoprotectant transporter OpuC from Pseudomonas syringae and demonstration that cystathionine-beta-synthase domains are required for its osmoregulatory function. J Bacteriol 189: 6901-6912.
29. Chen CL, Malek AA, Wargo MJ, Hogan DA, Beattie GA, (2010) The ATP-binding cassette transporter Cbc (choline/betaine/carnitine) recruits multiple substrate-binding proteins with strong specificity for distinct quaternary ammonium compounds. Mol Microbiol 75: 29-45.
30. Chen C, Beattie GA, (2008) Pseudomonas syringae BetT is a low-affinity choline transporter that is responsible for superior osmoprotection by choline over glycine betaine. J Bacteriol 190: 2717-2725.
31. Wargo MJ, Szwergold BS, Hogan DA, (2008) Identification of two gene clusters and a transcriptional regulator required for Pseudomonas aeruginosa glycine betaine catabolism. J Bacteriol 190: 2690-2699.
32. Matilla MA, Ramos JL, Duque E, Alche JD, Espinosa-Urgel M, et al. (2007) Temperature and pyoverdine-mediated iron acquisition control surface motility of Pseudomonas putida. Environ Microbiol 9: 1842-1850.
33. Kuiper I, Lagendijk EL, Pickford R, Derrick JP, Lamers GEM, et al. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51: 97-113.
34. Dubern JF, Bloemberg GV, (2006) Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445. FEMS Microbiol Lett 263: 169-175.
35. Dubern JF, Lagendijk EL, Lugtenberg BJJ, Bloemberg GV, (2005) The heat shock genes dnaK, dnaJ, and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J Bacteriol 187: 5967-5976.
36. Soutourina OA, Bertin PN, (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27: 505-523.
37. Horne SM, Pruss BM, (2006) Global gene regulation in Yersinia enterocolitica: effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch Microbiol 185: 115-126.
38. Rohde JR, Fox JM, Minnich SA, (1994) Thermoregulation in Yersinia enterocolitica is coincident with changes in DNA supercoiling. Mol Microbiol 12: 187-199.
39. Kapatral V, Olson JW, Pepe JC, Miller VL, Minnich SA, (1996) Temperature-dependent regulation of Yersinia enterocolitica class III flagellar genes. Mol Microbiol 19: 1061-1071.
40. Kapatral V, Campbell JW, Minnich SA, Thomson NR, Matsumura P, et al. (2004) Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150: 2289-2300.
41. Wosten M, van Dijk L, Veenendaal AKJ, de Zoete MR, Bleumink-Pluijm NMC, et al. (2010) Temperature-dependent FlgM/FliA complex formation regulates Campylobacter jejuni flagella length. Mol Microbiol 75: 1577-1591.
42. Alm RA, Guerry P, Trust TJ, (1993) The Campylobacter sigma 54 flaB flagellin promoter is subject to environmental regulation. J Bacteriol 175: 4448-4455.
43. Sinden SL, Devay JE, Backman PA (1971) Properties of syringomycin, a wide spectrum antibiotic and phytotoxin produced by Pseudomonas syringae, and its role in bacterial canker disease of peach trees. Physiological Plant Pathology 1: 199-&.
44. Lu SE, Wang N, Wang JL, Chen ZJ, Gross DC, (2005) Oligonucleotide microarray analysis of the salA regulon controlling phytotoxin production by Pseudomonas syringae pv. syringae. Mol Plant Microbe Interact 18: 324-333.
45. Lu SE, Scholz-Schroeder BK, Gross DC, (2002) Characterization of the salA, syrF, and syrG regulatory genes located at the right border of the syringomycin gene cluster of Pseudomonas syringae pv. syringae. Mol Plant Microbe Interact 15: 43-53.
46. Li HQ, Schenk A, Srivastava A, Zhurina D, Ullrich MS, (2006) Thermo-responsive expression and differential secretion of the extracellular enzyme levansucrase in the plant pathogenic bacterium Pseudomonas syringae pv. glycinea. FEMS Microbiol Lett 265: 178-185.
47. Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ, (2004) Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186: 4466-4475.
48. Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ, (2006) Analysis of Pseudomonas aeruginosa conditional Psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188: 8213-8221.
49. Lindeberg M, Myers CR, Collmer A, Schneider DJ, (2008) Roadmap to new virulence determinants in Pseudomonas syringae: Insights from comparative genomics and genome organization. Mol Plant Microbe Interact 21: 685-700.
50. Laue H, Schenk A, Li H, Lambertsen L, Neu TR, et al. (2006) Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152: 2909-2918.
51. Karatan E, Watnick P, (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73: 310-347.
52. Jacques MA, Josi K, Darrasse A, Samson R, (2005) Xanthomonas axonopodis pv. phaseoli var. fuscans is aggregated in stable biofilm population sizes in the phyllosphere of field-grown beans. Appl Environ Microbiol 71: 2008-2015.
53. Monier JM, Lindow SE, (2003) Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc Natl Acad Sci USA 100: 15977-15982.
54. Rivero RM, Ruiz JM, Romero LM, (2004) Importance of N source on heat stress tolerance due to the accumulation of proline and quaternary ammonium compounds in tomato plants. Plant Biol (Stuttg) 6: 702-707.
55. Fitzsimmons LF, Hampel KJ, Wargo MJ, (2012) Cellular choline and glycine betaine pools impact osmoprotection and phospholipase C production in Pseudomonas aeruginosa. J Bacteriol 194: 4718-4726.
56. Raymundo AK, Ries SM, (1981) Motility of Erwinia amylovora. Phytopathology 71: 45-49.
57. Wei ZM, Sneath BJ, Beer SV, (1992) EXPRESSION OF ERWINIA-AMYLOVORA HRP GENES IN RESPONSE TO ENVIRONMENTAL STIMULI. J Bacteriol 174: 1875-1882.
58. Gaudriault S, Malandrin L, Paulin JP, Barny MA, (1997) DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol 26: 1057-1069.
59. Kelm O, Kiecker C, Geider K, Bernhard F, (1997) Interaction of the regulator proteins RcsA and RcsB with the promoter of the operon for amylovoran biosynthesis in Erwinia amylovora. Mol Gen Genet 256: 72-83.
60. Bereswill S, Jock S, Aldridge P, Janse JD, Geider K, (1997) Molecular characterization of natural Erwinia amylovora strains deficient in levan synthesis. Physiological and Molecular Plant Pathology 51: 215-225.
61. Young JM, (1991) Pathogenicity and identification of the lilac pathogen, Pseudomonas syringae pv. syringae Van Hall 1902. Ann Appl Biol 118: 283-298.
62. Budde IP, Ullrich MS, (2000) Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. Mol Plant Microbe Interact 13: 951-961.
63. Loper JE, Lindow SE, (1987) Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77: 1449-1454.
64. King EO, Ward MK, Raney DE, (1954) 2 simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301-307.
65. Simon R, Priefer U, Puhler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio-Technology 1: 784-791.
66. Burch AY, Shimada BK, Mullin SWA, Dunlap CA, Bowman MJ, et al. (2012) Pseudomonas syringae coordinates production of a motility-enabling surfactant with flagellar assembly. J Bacteriol 194: 1287-1298.
67. Rutledge RG, Stewart D, (2008) A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biotechnol 8: 28.
68. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
69. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
70. Robinson MD, Oshlack A, (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: 9.
71. Dulla G (2007) Bacterial babel: breaking down quorum sensing cross-talk in the phyllosphere; analysis of the contributions of abiotic and biotic factors on AHL-mediated quorum sensing to epiphytic growth and virulence in Pseudomonas syringae. Berkeley: University of California, Berkeley, CA.
72. Marco ML, Legac J, Lindow SE, (2005) Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ Microbiol 7: 1379-1391.
73. Choi KH, Schweizer HP, (2005) An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol 5: 11.
74. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
75. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP, (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
76. Abramoff MD, Magalhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
77. Castillo-Davis CI, Hartl DL, (2003) GeneMerge- post-genomic analysis, data mining, and hypothesis testing. Bioinformatics 19: 891-892.