Mangotoxin production of Pseudomonas syringae pv. syringae is regulated by MgoA

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Carrión, Víctor J ^a,c,d   Van Der Voort, Menno ^c   Arrebola, Eva ^b   Gutiérrez Barranquero, José A ^a,e   De Vicente, Antonio ^a   Raaijmakers, Jos M ^c,d   Cazorla, Francisco M ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^e UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Antimetabolite toxin; GacS GacA; mgo operon; Plant microbe interaction

Indexed keywords

ANTIMETABOLITE; BACTERIAL RNA; BACTERIAL TOXIN; MANGOTOXIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL TRANSFORMATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; GENE FUSION; GENETIC TRANSCRIPTION; HETEROLOGOUS EXPRESSION; MGOA GENE; MUTANT; NEIGHBOR JOINING METHOD; NONHUMAN; OPERON; PATHOTYPE; PHYLOGENY; PLANT LEAF; POLYMERASE CHAIN REACTION; PROMOTER REGION; PSEUDOMONAS SYRINGAE PV. SYRINGAE; QUANTITATIVE ANALYSIS; TOMATO; TOXIN SYNTHESIS;

LYCOPERSICON ESCULENTUM; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. SYRINGAE;

ARTIFICIAL GENE FUSION; BACTERIAL TOXINS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; LYCOPERSICON ESCULENTUM; PEPTIDE SYNTHASES; PLANT LEAVES; PSEUDOMONAS SYRINGAE; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84896093415     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-46     Document Type: Article

References (57)

1. Pseudomonas syringae diseases of fruit trees: progress toward understanding and control. Kennelly MM, Cazorla FM, de Vicente A, Ramos C, Sundin GW, Plant Dis 2007 91 1 4 17 10.1094/PD-91-0004 (Pubitemid 46025697)
2. Mangotoxin: a novel antimetabolite toxin produced by Pseudomonas syringae inhibiting ornithine/arginine biosynthesis. Arrebola E, Cazorla FM, Durán VE, Rivera E, Olea F, Codina JC, Pérez-Garca A, de Vicente A, Physiol Mol Plant Path 2003 63 3 117 127 10.1016/j.pmpp.2003.11.003 (Pubitemid 38319077)
3. Bacterial apical necrosis of mango in southern Spain: a disease caused by Pseudomonas syringae pv. syringae. Cazorla FM, Torés JA, Olalla L, Pérez-García A, Farré JM, de Vicente A, Phytopathology 1998 88 7 614 620 10.1094/PHYTO.1998.88.7.614 18944933 (Pubitemid 28456090)
4. A nonribosomal peptide synthetase gene (mgoA) of Pseudomonas syringae pv. syringae is involved in mangotoxin biosynthesis and is required for full virulence. Arrebola E, Cazorla FM, Romero D, Pérez-García A, de Vicente A, Mol Plant-Microbe Interact 2007 20 5 500 509 10.1094/MPMI-20-5-0500 (Pubitemid 46641428)
5. Contribution of mangotoxin to the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Arrebola E, Cazorla FM, Codina JC, Gutiérrez-Barranquero JA, Pérez-García A, de Vicente A, Int Microbiol 2009 12 1139-6709 87 95 19784928
6. The mbo operon is specific and essential for biosynthesis of mangotoxin in Pseudomonas syringae. Carrión VJ, Arrebola E, Cazorla FM, Murillo J, de Vicente A, PLoS One 2012 7 5 36709 10.1371/journal.pone.0036709 22615797
7. Characterisation of the mgo operon in Pseudomonas syringae pv. syringae UMAF0158 that is required for mangotoxin production. Arrebola E, Carrión VJ, Cazorla FM, Pérez-García A, Murillo J, de Vicente A, BMC Microbiol 2012 12 1 10 10.1186/1471-2180-12-10 22251433
8. Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Heeb S, Haas D, Mol Plant-Microbe Interact 2001 14 12 1351 1363 10.1094/MPMI.2001.14.12.1351 (Pubitemid 34018322)
9. Two-component transcriptional regulation of N -acyl-homoserine lactone production in Pseudomonas aureofaciens. Chancey ST, Wood DW, Pierson LS, Appl Environ Microbiol 1999 65 6 2294 2299 10347004
10. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. Kay E, Humair B, Dénervaud V, Riedel K, Spahr S, Eberl L, Valverde C, Haas D, J Bacteriol 2006 188 16 6026 6033 10.1128/JB.00409-06 16885472 (Pubitemid 44384112)
11. A global regulator of secondary metabolite production in Pseudomonas fluorescens Pf-5. Corbell N, Loper JE, J Bacteriol 1995 177 21 6230 6236 7592389
12. Repression of phenazine antibiotic production in Pseudomonas aureofaciens strain 30-84 by RpeA. Whistler CA, Pierson LS III, J Bacteriol 2003 185 13 3718 3725 10.1128/JB.185.13.3718-3725.2003 12813064 (Pubitemid 36735921)
13. Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Hassan KA, Johnson A, Shaffer BT, Ren Q, Kidarsa TA, Elbourne LDH, Hartney S, Duboy R, Goebel NC, Zabriskie TM, Paulsen IT, Loper JE, Environ Microbiol 2010 12 4 899 915 10.1111/j.1462-2920.2009.02134.x 20089046
14. The Gac regulon of Pseudomonas fluorescens SBW25. Cheng X, de Bruijn I, van der Voort M, Loper JE, Raaijmakers JM, Environ Microbiol Rep 2013 5 4 608 619 10.1111/1758-2229.12061 23864577
15. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Parkins MD, Ceri H, Storey DG, Mol Microbiol 2001 40 5 1215 1226 10.1046/j.1365-2958.2001.02469.x 11401724 (Pubitemid 32574987)
16. The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. Petrova OE, Sauer K, J Bacteriol 2010 192 20 5275 5288 10.1128/JB.00387-10 20656909
17. The mxd operon in Shewanella oneidensis MR-1 is induced in response to starvation and regulated by ArcS/ArcA and BarA/UvrY. Muller J, Shukla S, Jost K, Spormann A, BMC Microbiol 2013 13 1 119 10.1186/1471-2180-13-119 23705927
18. Characterization of the salA, syrF, and syrG regulatory genes located at the right border of the syringomycin gene cluster of Pseudomonas syringae pv. syringae. Lu S-E, Scholz-Schroeder BK, Gross DC, Mol Plant-Microbe Interact 2002 15 1 43 53 10.1094/MPMI.2002.15.1.43 (Pubitemid 34096265)
19. The expression of genes encoding lipodepsipeptide phytotoxins by Pseudomonas syringae pv. syringae is coordinated in response to plant signal molecules. Wang N, Lu S-E, Wang J, Chen ZJ, Gross DC, Mol Plant-Microbe Interact 2006 19 3 257 269 10.1094/MPMI-19-0257 (Pubitemid 43271603)
20. Oligonucleotide microarray analysis of the SalA regulon controlling phytotoxin production by Pseudomonas syringae pv. syringae. Lu S-E, Wang N, Wang J, Chen ZJ, Gross DC, Mol Plant-Microbe Interact 2005 18 4 324 333 10.1094/MPMI-18-0324 (Pubitemid 40383900)
21. Regulation of tabtoxin production by the lemA gene in Pseudomonas syringae. Barta TM, Kinscherf TG, Willis DK, J Bacteriol 1992 174 9 3021 3029 1314808
22. 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 2 266 292 10357851 (Pubitemid 29264972)
23. 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, Hernandez-Flores JL, Hernández-Morales A, Murillo J, Alvarez-Morales A, Res Microbiol 2011 162 5 488 498 10.1016/j.resmic.2011.04.010 21527339
24. Isolation and characterization of a Pseudomonas syringae pv. syringae mutant deficient in lesion formation on bean. Willis DK, Hrabak EM, Rich JJ, Barta TM, Lindow SE, Panopoulos NJ, Mol Plant-Microbe Interact 1990 3 3 149 156 10.1094/MPMI-3-149
25. GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA, transcriptional activators, and alternate sigma factors. Chatterjee A, Cui Y, Yang H, Collmer A, Alfano JR, Chatterjee AK, Mol Plant-Microbe Interact 2003 16 12 1106 1117 10.1094/MPMI.2003.16.12.1106 (Pubitemid 37481656)
26. Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Lindeberg M, Myers CR, Collmer A, Schneider DJ, Mol Plant-Microbe Interact 2008 21 6 685 700 10.1094/MPMI-21-6-0685 (Pubitemid 351929163)
27. Comparative genomics of Plant-Associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. Loper JE, Hassan KA, Mavrodi DV, Davis EW II, Lim CK, Shaffer BT, Elbourne LDH, Stockwell VO, Hartney SL, Breakwell K, Henkels MD, Tetu SG, Rangel LI, Kidarsa TA, Wilson NL, van de Mortel JE, Song C, Blumhagen R, Radune D, Hostetler JB, Brinkac LM, Durkin AS, Kluepfel DA, Wechter WP, Anderson AJ, Kim YC, Pierson LS III, Pierson EA, Lindow SE, Kobayashi DY, et al. PLoS Genet 2012 8 7 1002784 10.1371/journal.pgen.1002784 22792073
28. A secondary metabolite acting as a signalling molecule controls Pseudomonas entomophila virulence. Vallet-Gely I, Opota O, Boniface A, Novikov A, Lemaitre B, Cell Microbiol 2010 12 11 1666 1679 10.1111/j.1462-5822.2010. 01501.x 20597908
29. The mangotoxin biosynthetic operon (mbo) is specifically distributed within Pseudomonas syringae Genomospecies 1 and was acquired only once during evolution. Carrión VJ, Gutiérrez-Barranquero JA, Arrebola E, Bardaji L, Codina JC, de Vicente A, Cazorla FM, Murillo J, Appl Environ Microbiol 2013 79 3 756 767 10.1128/AEM.03007-12 23144138
30. A Pseudomonas syringae diversity survey reveals a differentiated phylotype of the pathovar syringae associated with the mango host and mangotoxin production. Gutiérrez-Barranquero JA, Carrión VJ, Murillo J, Arrebola E, Arnold DL, Cazorla FM, de Vicente A, Phytopathology 2013 103 11 1115 1129 10.1094/PHYTO-04-13-0093-R 24102210
31. Two simple media for the demonstration of pyocyanin and fluorescin. King EO, Ward MK, Raney DE, J Lab Clin Med 1954 44 2 301 307 13184240
32. Indicator technique for antimetabolic toxin production by phytopathogenic species of Pseudomonas. Gasson MJ, Appl Environ Microbiol 1980 39 1 25 29 16345492 (Pubitemid 10099177)
33. Studies on transformation of Escherichia coli with plasmids. Hanahan D, J M Biol 1983 166 4 557 580 10.1016/S0022-2836(83)80284-8 (Pubitemid 13027898)
34. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E, Thiel J, Malfatti S, Loper JE, Lapidus A, Detter JC, Land M, Richardson PM, Kyrpides NC, Ivanova N, Lindow SE, Proc Natl Acad Sci USA 2005 102 31 11064 11069 10.1073/pnas.0504930102 16043691 (Pubitemid 41105993)
35. Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Howell CR, Stipanovic RD, Phytopathology 1980 70 712 715 10.1094/Phyto-70-712
36. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Kovach ME, Elzer PH, Steven Hill D, Robertson GT, Farris MA, Roop Ii RM, Peterson KM, Gene 1995 166 1 175 176 10.1016/0378-1119(95)00584-1 8529885
37. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ, Plant Mol Biol 1987 9 1 27 39 10.1007/BF00017984 24276795
38. Sambrook J, Russel DW, Molecular Cloning: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press 2001
39. Massetolide A biosynthesis in Pseudomonas fluorescens. de Bruijn I, de Kock MJD, de Waard P, van Beek TA, Raaijmakers JM, J Bacteriol 2008 190 8 2777 2789 10.1128/JB.01563-07 17993540 (Pubitemid 351508177)
40. Regulation of cyclic lipopeptide biosynthesis in Pseudomonas fluorescens by the ClpP protease. de Bruijn I, Raaijmakers JM, J Bacteriol 2009 191 6 1910 1923 10.1128/JB.01558-08 19114474
41. Miller JH, Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory 1972
42. Basic local alignment search tool. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, J Mol Biol 1990 215 3 403 410 2231712
43. Chapter 8 methods for in silico prediction of microbial polyketide and nonribosomal peptide biosynthetic pathways from DNA sequence data. Bachmann BO, Ravel J, Method Enzymol PA: Academic Press, David AH, 2009 181 217 vol. Volume 458
44. Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. de Bruijn I, de Kock MJD, Yang M, de Waard P, van Beek TA, Raaijmakers JM, Mol Microbiol 2007 63 2 417 428 10.1111/j.1365-2958.2006.05525.x 17241198 (Pubitemid 46058929)
45. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 10 2731 2739 10.1093/molbev/msr121 21546353
46. Artemis: sequence visualization and annotation. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B, Bioinformatics 2000 16 10 944 945 10.1093/bioinformatics/16.10.944 11120685
47. ACT: the Artemis comparison tool. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J, Bioinformatics 2005 21 16 3422 3423 10.1093/bioinformatics/bti553 15976072 (Pubitemid 41222448)
48. WebACT-an online companion for the Artemis Comparison Tool. Abbott JC, Aanensen DM, Rutherford K, Butcher S, Spratt BG, Bioinformatics 2005 21 18 3665 3666 10.1093/bioinformatics/bti601 16076890 (Pubitemid 41264103)
49. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Blumer C, Heeb S, Pessi G, Haas D, Proc Natl Acad Sci USA 1999 96 24 14073 14078 10.1073/pnas.96.24.14073 10570200
50. A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens. Valverde C, Lindell M, Wagner EGH, Haas D, J Biol Chem 2004 279 24 25066 25074 10.1074/jbc.M401870200 15031281 (Pubitemid 38756755)
51. CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. Dubey AK, Baker CS, Suzuki K, Jones AD, Pandit P, Romeo T, Babitzke P, J Bacteriol 2003 185 15 4450 4460 10.1128/JB.185.15.4450-4460.2003 12867454 (Pubitemid 36890492)
52. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Saitou N, Nei M, Mol Biol Evol 1987 4 4 406 425 3447015
53. The rapid generation of mutation data matrices from protein sequences. Jones DT, Taylor WR, Thornton JM, Comput Appl Biosci 1992 8 3 275 282 1633570
54. Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, Babitzke P, Haas D, Mol Microbiol 2007 66 2 341 356 10.1111/j.1365-2958.2007.05909.x 17850261 (Pubitemid 47482376)
55. Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Lapouge K, Schubert M, Allain FHT, Haas D, Mol Microbiol 2008 67 2 241 253 18047567 (Pubitemid 350295835)
56. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Kay E, Dubuis C, Haas D, Proc Natl Acad Sci USA 2005 102 47 17136 17141 10.1073/pnas.0505673102 16286659 (Pubitemid 41692696)
57. Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Vodovar N, Vallenet D, Cruveiller S, Rouy Z, Barbe V, Acosta C, Cattolico L, Jubin C, Lajus A, Segurens B, Vacherie B, Wincker P, Weissenbach J, Lemaitre B, Médigue C, Boccard F, Nat Biotechnol 2006 24 6 673 679 10.1038/nbt1212 16699499 (Pubitemid 43882118)