Transcriptional profile of P. syringae pv. phaseolicola NPS3121 at low temperature: Physiology of phytopathogenic bacteria

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Arvizu Gómez, Jackeline Lizzeta ^a   Hernández Morales, Alejandro ^b   Aguilar, Juan Ramiro Pacheco ^c   Álvarez Morales, Ariel ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DE QUERÉTARO   (Mexico)

Author keywords

Low temperature; P. syringae pv. phaseolicola; Physiology; Phytopathogen; Transcriptional profile

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; CELL MOTILITY; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; IRON METABOLISM; LOW TEMPERATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHASEOLICOLA; PSEUDOMONAS SYRINGAE; TYPE III SECRETION SYSTEM; UPREGULATION;

COLD TEMPERATURE; MICROARRAY ANALYSIS; PSEUDOMONAS SYRINGAE; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84877746572     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-81     Document Type: Article

References (73)

1. Agrios GN, Plant Pathology California: Academic Press 4 1997
2. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Hirano SS, Upper CD, Microbiol Mol Biol Rev 2000 64 624 653 10.1128/MMBR.64.3.624-653.2000 10974129
3. Effects of environmental factors on plant disease. Colhoun J, Ann Rev Phytopatol 1973 11 343 364 10.1146/annurev.py.11.090173.002015
4. Thermoregulated expression of virulence factors in plant associated bacteria. Smirnova A, Li H, Weingart H, Aufhammer S, Burse A, Finis K, Schenk A, Ullrich MS, Arch Microbiol 2001 176 393 399 10.1007/s002030100344 11734881
5. Bean halo-blight toxin. Mitchell RE, Nature 1976 260 75 76 10.1038/260075a0
6. Isolation and structure of a chlorosis inducing toxin of Pseudomonas phaseolicola. Mitchell RE, Phytochemistry 1976 15 1941 1947 10.1016/S0031- 9422(00)88851-2
7. Involvement of phaseolotoxin in Halo blight of beans. Mitchell RE, Bieleski RL, Plant Physiol 1977 60 723 729 10.1104/pp.60.5.723 16660172
8. The relation of temperature to common and halo blight of beans. Goss RW, Phytopathology 1970 30 258 264
9. Phaseolotoxin production by Pseudomonas syringae pv. phaseolicola: the influence of temperature. Nüske J, Fritsche W, J Basic Microbiol 1989 29 441 447 10.1002/jobm.3620290713 2600779
10. Phaseolotoxin: chlorosis, ornithine accumulation and inhibition of ornithine carbamoyltransferase in different plants. Ferguson AR, Johnston JS, Physiol Plant Pathol 1980 16 269 275 10.1016/0048-4059(80)90041-7
11. The inhibition of ornithine transcarbamoylase from Escherichia coli W by phaseolotoxin. Templeton MD, Sullivan PA, Shepherd MG, Biochem J 1984 224 379 388 6393952
12. Functional characterization of the gene cluster from Pseudomonas syringae pv. phaseolicola NPS3121 involved in synthesis of phaseolotoxin. Aguilera S, López-López K, Nieto Y, Garcidueñas-Piña R, Hernández-Guzmán G, Hernández-Flores JL, Murillo J, Álvarez-Morales A, J Bacteriol 2007 189 2834 2843 10.1128/JB.01845-06 17237165
13. Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Smoot LM, Smoot JC, Graham MR, Somerville GE, Sturdevant DE, LUx Migliaccio CA, Sylva GL, Musser JM, Proc Natl Acad Sci 2001 98 10416 10421 10.1073/pnas.191267598 11517341
14. Human body temperature (37°C) increases the expression of iron, carbohydrate and amino acid utilization genes in Escherichia coli K12. White-Zielger CA, Malhowski AJ, Young S, J Bacteriol 2007 189 5429 5440 10.1128/JB.01929-06 17526711
15. The effects on temperature on growth in vitro of Pseudomonas syringae and Xanthomonas pruni. Young JM, Luketina RC, J Appl Bacteriol 1977 42 345 354 10.1111/j.1365-2672.1977.tb00702.x 885818
16. Physical map of the chromosome of the phytopathogenic bacterium Pseudomonas syringae pv. phaseolicola. De Ita ME, Marsch-Moreno R, Guzman P, Álvarez-morales A, Microbiol 1998 144 493 501 10.1099/00221287-144-2-493
17. Integration Host Factor (IHF) binds to the promoter región of the phtD operon involved in phaseolotoxin synthesis in P. syringae pv. phaseolicola NPS3121. Arvizu-Gómez J, Hernández-Morales A, Pastor-Palacios G, Brieba L, Álvarez-Morales A, BMC Microbiol 2011 11 90 10.1186/1471-2180-11-90 21542933
18. Whole genome sequence analysis of Pseudomonas syringae pv phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, DeBoy R, Durkin AS, Giglio MG, Madupu R, Nelson WC, Rasovitz MJ, Sullivan S, Crabtree J, Creasy T, Davidsen T, Haft DH, Zafar N, Zhou L, Halpin R, Holley T, Khouri H, Feldblyum T, White O, Fraser CM, Chatterjee AK, Cartinhour S, Schneider DJ, Mansfield J, Collmer A, Buell R, J Bacteriol 2005 187 6488 6498 10.1128/JB.187.18.6488-6498.2005 16159782
19. Pseudomonas syringae Phytotoxins: Mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Bender CL, Alarcón-Chaidez F, Gross DC, Microbiol Mol Biol Rev 1999 63 266 292 10357851
20. Biosynthesis of nonribosomal peptides. Finking R, Marahiel MA, Annu Rev Microbiol 2004 58 453 488 10.1146/annurev.micro.58.030603.123615 15487945
21. Gene expression of Pht cluster genes and a putative non-ribosomal peptide synthetase required for phaseolotoxin production is regulated by GacS/GacA in Pseudomonas syringae pv. phaseolicola. De la Torre-Zavala S, Aguilera S, Ibarra-Laclette E, Hernández-Flores JL, Hernández-Morales A, Murillo J, Álvarez-Morales A, Res Microbiol 2011 20 1 11
22. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis what can be learned from available microbial genomic resources? Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I, BMC Genomics 2009 10 104 10.1186/1471-2164-10-104 19284603
23. The type VI secretion toolkit. Cascales E, EMBO Rep 2008 9 735 741 10.1038/embor.2008.131 18617888
24. In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Sarris PF, Skandalis N, Kokkinidis M, Panopoulos NJ, Mol Plant Pathol 2010 11 795 804 21091602
25. Tubules and donuts:a type VI secretion story. Bönemann G, Pietrosiuk A, Mogk A, Mol Microbiol 2010 76 815 821 10.1111/j.1365-2958.2010.07171.x 20444095
26. Type VI secretion: a beginneŕs guide. Bingle LEH, Bailey CM, Pallen MJ, Curr Opinion Microbiol 2008 11 3 8 10.1016/j.mib.2008.01.006
27. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Filloux A, Hachain A, Bleves S, Microbiol 2008 154 1570 1583 10.1099/mic.0.2008/016840-0
28. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. Records AR, Gross D, J Bacteriol 2010 192 3584 3596 10.1128/JB.00114-10 20472799
29. Nooks and crannies in type VI secretion regulation. Bernard CS, Brunet YR, Gueguen E, Cascales E, J Bacteriol 2010 192 3850 3860 10.1128/JB.00370-10 20511495
30. Cold Shock and adaptation. Thieringer HA, Jones PG, Inouye M, Bioessays 1998 20 49 57 10.1002/(SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0.CO;2-N 9504047
31. Ray MK, Cold stress response of low temperature adapted bacteria In: Amere S. Sreedhar and Usha K. Srinivas editors. Stress response A molecular biology approach 2006 1 23
32. Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Weber MHW, Klein W, Muller L, Niess UM, Marahiel MA, Mol Microbiol 2001 39 1321 1329 10.1111/j.1365-2958.2001.02322.x 11251847
33. Bacterial cold shock responses. Weber MHW, Marahiel MA, Sci Progress 2003 86 9 75 10.3184/003685003783238707
34. Molecular components of physiological stress responses in Escherichia coli. Wick LM, Egli T, Adv Biochem Engin/Biotechnol 2004 89 1 45 10.1007/b93957
35. Cold-induced gene expression profiles of Vibrio parahemolyticus: a time-course analysis. Yang L, Zhou D, Liu X, Han H, Zhan L, Gou Z, Zhang I, Qin C, Wong HC, Yang R, FEMS Microbiol Lett 2008 291 50 58 19054071
36. Bacterial Chemotaxis. Eisenbach M, Embryonic encyclopedia of life sciences London England: Ltd, Macmillan publisher 2001
37. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, Lory S, Ramphal R, Mol Microbiol 2003 50 809 824 10.1046/j.1365-2958.2003.03740.x 14617143
38. The causal agent of halo blight in bean Pseudomonas syringae pv. phaseolicola attaches to stomata via its pili. Romantschuk M, Bamford DH, Microb Pathog 1986 1 139 148 10.1016/0882-4010(86)90016-1 2907769
39. Formation of pilin in Pseudomonas aeruginosa requires the alternative σ factor (RpoN) of RNA polymerase. Ishimoto KS, Lory S, Proc Natl Acad Sci USA 1989 86 1954 1957 10.1073/pnas.86.6.1954 2564676
40. Microarray analysis of temperature induced transcriptome of Yersinia pestis. Hang Y, Zhou D, Pang X, Song Y, Zhang L, Bao J, Tong Z, Wang J, Guo Z, Zhai J, Du Z, Wang X, Zhang X, Wang J, Huang O, Yang R, Microbiol Inmmunol 2004 48 791 805
41. Pseudomonas syringae pv. Phaseolicola mutants compromised for type III secretion system gene induction. Deng X, Xiao Y, Lan L, Zhou JM, Tang X, Mol Plant Microbe Int 2009 22 964 976 10.1094/MPMI-22-8-0964
42. Pseudomonas syringae coordinates production of a motility-enabling surfactant with flagellar assembly. Burch AY, Shimada BK, Mullin SWA, Dunlap CA, Bowman MJ, Lindow SE, J Bacteriol 2012 194 1287 1298 10.1128/JB.06058-11 22194459
43. Effect of overexpressing rsmA from Pseudomonas aeruginosa on virulence of select phytotozin-producing strains of P. syringae. Kong HS, Roberts DP, Patterson CD, Kuehne SA, Heeb S, Lakshman DK, Lydon J, Phytopatol 2012 102 575 587 10.1094/PHYTO-09-11-0267
44. Bacterial iron transport:mechanisms, genetics and regulation. Braun V, Hantke K, Koster W, Metal Ions Biol Syst 1998 35 67 145
45. Pyoverdine siderophores:from biogenesis to biosignificance. Visca P, Imperi F, Lamont LL, Trends Microbiol 2006 10.1016/j.tim.2006.11.004
46. Characterization of the PvdS-regulated promoter motif in Pseudomonas syringae pv. tomato DC3000 reveals regulon members and insights regarding PvdS function in other pseudomonads. Swingle B, Thete D, Moll M, Myers CR, Schneider DJ, Cartinhour S, Mol Microbiol 2008 68 871 889 10.1111/j.1365-2958.2008.06209.x 18363796
47. How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. Vasil ML, Biometals 2007 20 587 601 10.1007/s10534-006-9067-2 17186376
48. Increase in oxidative stress at low temperature in an Antarctic bacterium. Chattopadhyay MK, Raghu G, Sharma YVRK, Rajasehharan MV, Shivaji S, Curr Microbiol 2011 62 544 546 10.1007/s00284-010-9742-y 20730433
49. The role of antioxidant systems in the cold stress response of Escherichia coli. Smirnova GV, Zakirova ON, Oktyabrskii ON, Microbiol 2001 70 45 50 10.1023/A:1004840720600
50. Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. Palma M, DeLuca D, Worgall S, Quadri LEN, J Bacteriol 2004 186 248 252 10.1128/JB.186.1.248-252.2004 14679246
51. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Outten FW, Djaman O, Storz G, Mol Microbiol 2004 52 861 872 10.1111/j.1365-2958.2004.04025.x 15101990
52. DNA microarray mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRosa RA, Storz G, J Bacteriol 2001 183 4562 4570 10.1128/JB.183.15.4562-4570. 2001 11443091
53. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP, Poole K, J Bacteriol 2008 190 662 671 10.1128/JB.01473-07 17993517
54. Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. May TB, Shinabarger D, Maharaj R, Kato J, Chu L, Devault JD, Roychoudhury S, Zielinski NA, Berry A, Rothmel RK, Misra TK, Chakrabarty AM, Clinical Microbiol Rev 1991 4 191 206
55. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Yu J, Peñaloza-Vazquez A, Chakrabarty AM, Bender CL, Mol Microbiol 1999 33 712 720 10.1046/j.1365-2958.1999.01516.x 10447881
56. Characterization of the alginate biosynthetic gene cluster in Pseudomonas syringae pv. syringae. Peñaloza-Vázquez A, Kidambi SP, Chakrabarty AM, Bender CL, J Bacteriol 1997 179 4464 4472 9226254
57. Dual regulation of mucoidy in Pseudomonas aeruginosa and sigma factor antagonism. Boucher JC, Schurr MJ, Deretic V, Mol Microbiol 2000 36 341 351 10.1046/j.1365-2958.2000.01846.x 10792721
58. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Hickman JW, Harwood CS, Mol Microbiol 2008 69 376 389 10.1111/j.1365-2958.2008.06281.x 18485075
59. Phytopathogen type III effector weaponry and their plant targets. Block A, Li G, Qing Fu Z, Alfano JR, Curr Opin Plant Biol 2008 11 396 403 10.1016/j.pbi.2008.06.007 18657470
60. Global transcriptional response of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. Bronstein PA, Filiatrault MJ, Myers CR, Rutzke M, Schneider DJ, Cartinhour SW, BMC Microbiol 2008 8 209 10.1186/1471-2180-8-209 19055731
61. Comparative genomic analysis of the pPT23A plasmid family of Pseudomonas syringae. Zhao Y, Ma X, Sundin GW, J Bacteriol 2005 187 2113 2126 10.1128/JB.187.6.2113-2126.2005 15743960
62. Type IV secretion systems:versatility and diversity in function. Wallden K, Rivera-Calzada A, Waksman G, Cell Microbiol 2010 12 1203 1212 10.1111/j.1462-5822.2010.01499.x 20642798
63. Regulation networks. Wagner R, Transcription regulation in prokaryotes USA: Oxford University Press 2000 264 335
64. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Kandror O, Golgberg AL, Proc Natl Acad Sci USA 1997 94 4978 4981 10.1073/pnas.94.10.4978 9144175
65. Growth of Pseudomonas putida at low temperature global transcriptomic and proteomic analyses. Fonseca P, Moreno R, Rojo F, Env. Microbiol Rep 2011 10.1111/j.1758-2229.2010.00229.x
66. Rapid and sensitive microbiological assay for phaseolotoxin. Staskawicz BB, Panopoulos NJ, Phytopatol 1979 69 663 666 10.1094/Phyto-69-663
67. Transcriptional profile of Pseudomonas syringae pv phaseolicola NPS3121 in response to tissue extracts from a susceptible Phaseolus vulgaris L. cultivar. Hernández-Morales A, De La Torre-Zavala S, Ibarra-Laclette E, Hernández- Flores JL, Jofre-Garfias AE, Martínez-Antonio A, Álvarez Morales A, BMC Microbiol 2009 9 257 10.1186/1471-2180-9-257 20003402
68. GenoMap a circular genome data viewer. Sato N, Ehira S, Bioinformatics 2003 19 1583 1584 10.1093/bioinformatics/btg195 12912843
69. Sambrook J, Fritsch EF, Maniatis T, Molecular cloning: a laboratory manual New York: Cold Spring Harbor 2 1989
70. A simple and rapid method for the preparation of gram negative bacterial genomic DNA. Chen WP, Kuo TT, Nucleic Acids Res 1993 21 2260 10.1093/nar/21.9.2260 8502576
71. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Alexander DB, Zuberer DA, Boil fertile soils 1991 12 39 45 10.1007/BF00369386
72. May TB, Chakghbarty AM, Isolation and assays of Pseudomonas aeruginosa alginate Methods in enzymology: Academis Press Inc 1994
73. A homologue of the 3 oxoacyl- (acyl carrier protein) synthase III gene located in the glycosylation island of Pseudomonas syringae pv. tabaci regulates virulence factors via N-acyl homoserine lactona and fatty acid synthesis. Taguchi F, Ogawa Y, Takeuchi K, Suzuki T, Toyoda K, Shiraishi T, Ichinose Y, J Bacteriol 2006 188 8376 8384 10.1128/JB.00763-06 17028280