Global analysis of the HrpL regulon in the plant pathogen Pseudomonas syringae pv. tomato DC3000 reveals new regulon members with diverse functions

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Lam, Hanh N ^a   Chakravarthy, Suma ^a   Wei, Hai Lei ^a   BuiNguyen, HoangChuong ^a   Stodghill, Paul V ^a,b   Collmer, Alan ^a   Swingle, Bryan M ^a,b   Cartinhour, Samuel W ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b United States Department of Agriculture Agricultural Research Service ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; SIGMA FACTOR HRPL; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HRPL PROTEIN, PSEUDOMONAS SYRINGAE; MESSENGER RNA; SIGMA FACTOR; TYPE III SECRETION SYSTEM;

ARTICLE; BACTERIAL GENE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HRP GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PSEUDOMONAS SYRINGAE PV. TOMATO; REGULON; RNA SEQUENCE; SEQUENCE ALIGNMENT; TYPE III SECRETION SYSTEM; GENETICS; MICROBIOLOGY; PROCEDURES; PSEUDOMONAS SYRINGAE; TOMATO; VIRULENCE;

BACTERIAL PROTEINS; BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LYCOPERSICON ESCULENTUM; PROMOTER REGIONS, GENETIC; PSEUDOMONAS SYRINGAE; REGULON; RNA, MESSENGER; SIGMA FACTOR; TYPE III SECRETION SYSTEMS; VIRULENCE;

EID: 84939218124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106115     Document Type: Article

References (81)

1. Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae Pathogens of Arabidopsis and a Bacterial Locus Determining Avirulence on Both Arabidopsis and Soybean Plant Cell 3: 49-59.
2. Cuppels DA, Ainsworth T (1995) Molecular and Physiological Characterization of Pseudomonas syringae pv. tomato and Pseudomonas yringae pv. maculicola Strains That Produce the Phytotoxin Coronatine. Appl Environ Microbiol 61: 3530-3536.
3. Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, et al. (2007) A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J 51: 32-46. (Pubitemid 46985556)
4. Jin QL, Thilmony R, Zwiesler-Vollick J, He SY (2003) Type III protein secretion in Pseudomonas syringae. Microbes and Infection 5: 301-310. (Pubitemid 36428719)
5. Alfano JR, Collmer A (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179: 5655-5662. (Pubitemid 27398261)
6. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, et al. (2005) Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact 18: 275-282. (Pubitemid 40383895)
7. Deslandes L, Rivas S (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17: 644-655.
8. Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56: 509-531.
9. Feng F, Zhou JM (2012) Plant-bacterial pathogen interactions mediated by type III effectors. Curr Opin Plant Biol 15: 469-476.
10. Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7: 601-611. (Pubitemid 44325351)
11. Kobayashi DY, Tamaki SJ, Keen NT (1989) Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc Natl Acad Sci U S A 86: 157-161.
12. Staskawicz BJ, Dahlbeck D, Keen NT (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci U S A 81: 6024-6028. (Pubitemid 15219589)
13. Kim JF, Alfano JR (2002) Pathogenicity islands and virulence plasmids of bacterial plant pathogens. Curr Top Microbiol Immunol 264: 127-147. (Pubitemid 34241996)
14. Yuan J, He SY (1996) The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J Bacteriol 178: 6399-6402. (Pubitemid 26365731)
15. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, et al. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726. (Pubitemid 34202909)
16. Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L, et al. (2002) Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 99: 7652-7657. (Pubitemid 34568746)
17. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176: 1025-1036. (Pubitemid 24060119)
18. Xiao Y, Hutcheson SW (1994) A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J Bacteriol 176: 3089-3091. (Pubitemid 24152960)
19. Shen H, Keen NT (1993) Characterization of the promoter of avirulence gene D from Pseudomonas syringae pv. tomato. J Bacteriol 175: 5916-5924. (Pubitemid 23277440)
20. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences of the United States of America 100: 10181-10186. (Pubitemid 37071853)
21. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci U S A 99: 2275-2280. (Pubitemid 34169051)
22. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, et al. (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci U S A 102: 2549-2554. (Pubitemid 40279414)
23. Ferreira AO, Myers CR, Gordon JS, Martin GB, Vencato M, et al. (2006) Whole-genome expression profiling defines the HrpL regulon of Pseudomonas syringae pv. tomato DC3000, allows de novo reconstruction of the Hrp cis clement, and identifies novel coregulated genes. Mol Plant Microbe Interact 19: 1167-1179. (Pubitemid 44607329)
24. Schechter LM, Vencato M, Jordan KL, Schneider SE, Schneider DJ, et al. (2006) Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Mol Plant Microbe Interact 19: 1180-1192. (Pubitemid 44607330)
25. Lindeberg M, Cartinhour S, Myers CR, Schechter LM, Schneider DJ, et al. (2006) Closing the Circle on the Discovery of Genes Encoding Hrp Regulon Members and Type III Secretion System Effectors in the Genomes of Three Model Pseudomonas syringae Strains MPMI 19: 8.
26. Mucyn TS, Yourstone S, Lind AL, Biswas S, Nishimura MT, et al. (2014) Variable suites of non-effector genes are co-regulated in the type III secretion virulence regulon across the Pseudomonas syringae phylogeny. PLoS Pathog 10: e1003807.
27. Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S, et al. (2006) Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol Plant Microbe In 19: 1193-1206. (Pubitemid 44607331)
28. Kvitko BH, Park DH, squez ACV, Wei C-F, Russell AB, et al. (2009) Deletions in the Repertoire of Pseudomonassyringae pv. tomato DC3000 Type III Secretion Effector Genes Reveal Functional Overlap among Effectors. PLoS Pathog. pp. 1-16.
29. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, et al. (2011) Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108: 2975-2980.
30. Filiatrault MJ, Stodghill PV, Bronstein PA, Moll S, Lindeberg M, et al. (2010) Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 192: 2359-2372.
31. Rhee HS, Pugh BF (2012) ChIP-exo method for identifying genomic location of DNA-binding proteins with near-single-nucleotide accuracy. Curr Protoc Mol Biol Chapter 21: Unit 21 24.
32. Lan L, Deng X, Zhou J, Tang X (2006) Genome-Wide Gene Expression Analysis of Pseudomonas syringae pv. tomato DC3000 Reveals Overlapping and Distinct Pathways Regulated by hrpL and hrpRS. MPMI 19: 10.
33. Bronstein PA, Filiatrault MJ, Myers CR, Rutzke M, Schneider DJ, et al. (2008) Global transcriptional responses of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. Bmc Microbiol 8: 209.
34. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301-307.
35. Huynh TV, Dahlbeck D, Staskawicz BJ (1989) Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
36. Hanahan D (1985) Techniques for transformation of E. coli. DNA cloning: a practical approach. Oxford, United Kingdom: IRL Press. p. 26.
37. Choi KH, Kumar A, Schweizer HP (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: Application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Meth 64: 391-397. (Pubitemid 43212814)
38. Kvitko BH, Ramos AR, Morello JE, Oh HS, Collmer A (2007) Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. Journal of Bacteriology 189: 8059-8072. (Pubitemid 350178917)
39. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68. (Pubitemid 19125654)
40. Swingle B, Thete D, Moll M, Myers CR, Schneider DJ, et al. (2008) Characterization of the PvdS-regulated promoter motif in Pseudomonas syringae pv. tomato DC3000 reveals regulon members and insights regarding PvdS function in other pseudomonads. Molecular Microbiology 68: 871-889. (Pubitemid 351581065)
41. DeLisa MP, Samuelson P, Palmer T, Georgiou G (2002) Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J Biol Chem 277: 29825-29831.
42. Markel E, Maciak C, Butcher BG, Myers CR, Stodghill P, et al. (2011) An extracytoplasmic function sigma factor-mediated cell surface signaling system in Pseudomonas syringae pv. tomato DC3000 regulates gene expression in response to heterologous siderophores. J Bacteriol 193: 5775-5783.
43. Oh HS, Kvitko BH, Morello JE, Collmer A (2007) Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells. J Bacteriol 189: 8277-8289. (Pubitemid 350178940)
44. Rhee HS, Pugh BF (2011) Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147: 1408-1419.
45. Butcher BG, Bronstein PA, Myers CR, Stodghill PV, Bolton JJ, et al. (2011) Characterization of the Fur regulon in Pseudomonas syringae pv. tomato DC3000. J Bacteriol 193: 4598-4611.
46. Filiatrault MJ, Stodghill PV, Myers CR, Bronstein PA, Butcher BG, et al. (2011) Genome-wide identification of transcriptional start sites in the plant pathogen Pseudomonas syringae pv. tomato str. DC3000. PLoS One 6: e29335.
47. Patel RK, Jain M (2012) NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data. Plos One 7.
48. Li RQ, Yu C, Li YR, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
49. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
50. Albert I, Wachi S, Jiang C, Pugh F (2008) GeneTrack-a genomic data processing and visualization framework. Bioinformatics 24: 1305-1306. (Pubitemid 351659629)
51. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
52. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
53. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, et al. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. Bmc Bioinformatics 11: 119.
54. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
55. Enz S, Mahren S, Menzel C, Braun V (2003) Analysis of the ferric citrate transport gene promoter of Escherichia coli. J Bacteriol 185: 2387-2391. (Pubitemid 36363203)
56. Lane WJ, Darst SA (2006) The structural basis for promoter 235 element recognition by the group IV sigma factors. PLoS Biol 4: e269.
57. (2005) The filA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for flagellin synthesis. pp. 1-12.
58. Potvin E, Sanschagrin F, Levesque RC (2008) Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev. pp. 38-55. (Pubitemid 350293915)
59. Ellinger T, Behnke D, Bujard H, Gralla JD (1994) Stalling of Escherichia-Coli Rna-Polymerase in the +6 to +12 Region in-Vivo Is Associated with Tight-Binding to Consensus Promoter Elements. J Mol Biol 239: 455-465. (Pubitemid 24210418)
60. Carpousis AJ, Stefano JE, Gralla JD (1982) 59 Nucleotide Heterogeneity and Altered Initiation of Transcription at Mutant Lac Promoters. J Mol Biol 157: 619-633. (Pubitemid 12055304)
61. Wagner R (2000) Transcription Regulation in Prokaryotes. Oxford University Press. p. 380.
62. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10: 462-469.
63. Cunnac S, Lindeberg M, Collmer A (2009) Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Current Opinion in Microbiology 12: 53-60.
64. Schechter LM, Valenta JC, Schneider DJ, Collmer A, Sakk E (2012) Functional and Computational Analysis of Amino Acid Patterns Predictive Type III Secretion System Substrates in Pseudomonas syringae. Plos One 7.
65. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, et al. (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7: e1002132.
66. Dong TG, Mekalanos JJ (2012) Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Res 40: 7766-7775.
67. Markel E, Butcher BG, Myers CR, Stodghill P, Cartinhour S, et al. (2013) Regulons of three Pseudomonas syringae pv. tomato DC3000 iron starvation sigma factors. Appl Environ Microbiol 79: 725-727.
68. Preiter K, Brooks DM, Penaloza-Vazquez A, Sreedharan A, Bender CL, et al. (2005) Novel virulence gene of Pseudomonas syringae pv. tomato strain DC3000. J Bacteriol 187: 7805-7814. (Pubitemid 41587717)
69. Bardoel BW, van der Ent S, Pel MJC, Tommassen J, Pieterse CMJ, et al. (2011) Pseudomonas Evades Immune Recognition of Flagellin in Both Mammals and Plants. PLoS Pathog 7.
70. Pel MJ, Van Dijken AJ, Bardoel BW, Seidl MF, Van der Ent S, et al. (2014) Pseudomonas syringae evades host immunity by degrading flagellin monomers with alkaline protease AprA. Mol Plant Microbe Interact.
71. Létoffé S, Delepelaire P, Wandersman C (1990) Protease secretion by Erwinia chrysanthemi: the specific secretion functions are analogous to those of Escherichia coli alpha-haemolysin. EMBO J 9: 8.
72. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A (2004) Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J Bacteriol 186: 543-555. (Pubitemid 38076444)
73. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10(1): 1-6.
74. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nature reviews Genetics 8: 206-216.
75. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190. (Pubitemid 38811555)
76. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548.
77. Jovanovic M, James EH, Burrows PC, Rego FG, Buck M, et al. (2011) Regulation of the co-evolved HrpR and HrpS AAA+ proteins required for Pseudomonas syringae pathogenicity. Nat Commun 2: 177.
78. Schaefer A, Tauch A, Jaeger W, Kalinowski J, Thierbach G, et al. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73. (Pubitemid 24224965)
79. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. PNAS. pp. 1-6.
80. Badel JL, Shimizu R, Oh HS, Collmer A (2006) A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol Plant Microbe In 19: 99-111. (Pubitemid 43172824)
81. Bronstein PA, Marrichi M, Cartinhour S, Schneider DJ, DeLisa MP (2005) Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J Bacteriol 187: 8450-8461. (Pubitemid 41780509)