The Post-transcriptional Regulator rsmA/csrA Activates T3SS by Stabilizing the 5′ UTR of hrpG, the Master Regulator of hrp/hrc Genes, in Xanthomonas

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Andrade, Maxuel O ^a   Farah, Chuck S ^b   Wang, Nian ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; CHLORAMPHENICOL; CIPROFLOXACIN; CSRA PROTEIN; GENTAMICIN; KANAMYCIN; REGULATOR PROTEIN; RIFAMPICIN; RSMA PROTEIN; SPECTINOMYCIN; STREPTOMYCIN; TETRACYCLINE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ALLERGIC REACTION; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GUS GENE; HRC GENE; HRP D; HRP G; HRP GENE; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; TRANSCRIPTION REGULATION; TYPE III SECRETION SYSTEM; WESTERN BLOTTING; XANTHOMONAS CITRI;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; XANTHOMONAS;

EID: 84895748284     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003945     Document Type: Article

References (114)

1. Buttner D, Bonas U, (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS microbiology reviews 34: 107-133.
2. Kay S, Bonas U, (2009) How Xanthomonas type III effectors manipulate the host plant. Current opinion in microbiology 12: 37-43.
3. Laia ML, Moreira LM, Dezajacomo J, Brigati JB, Ferreira CB, et al. (2009) New genes of Xanthomonas citri subsp. citri involved in pathogenesis and adaptation revealed by a transposon-based mutant library. BMC microbiology 9: 12.
4. Koebnik R, Kruger A, Thieme F, Urban A, Bonas U, (2006) Specific binding of the Xanthomonas campestris pv. vesicatoria AraC-type transcriptional activator HrpX to plant-inducible promoter boxes. Journal of bacteriology 188: 7652-7660.
5. Boch J, Bonas U, (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual review of phytopathology 48: 419-436.
6. Akimoto-Tomiyama C, Furutani A, Tsuge S, Washington EJ, Nishizawa Y, et al. (2012) XopR, a type III effector secreted by Xanthomonas oryzae pv. oryzae, suppresses Microbe-Associated Molecular Pattern-triggered immunity in Arabidopsis thaliana. Molecular plant-microbe interactions 25: 505-514.
7. Mole BM, Baltrus DA, Dangl JL, Grant SR, (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends in microbiology 15: 363-371.
8. Bonas U, (1994) hrp genes of phytopathogenic bacteria. Current topics in microbiology and immunology 192: 79-98.
9. Guo Y, Figueiredo F, Jones J, Wang N, (2011) HrpG and HrpX play global roles in coordinating different virulence traits of Xanthomonas axonopodis pv. citri. Molecular plant-microbe interactions 24: 649-661.
10. Wengelnik K, Van den Ackerveken G, Bonas U, (1996) HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Molecular plant-microbe interactions 9: 704-712.
11. Wengelnik K, Rossier O, Bonas U, (1999) Mutations in the regulatory gene hrpG of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. Journal of bacteriology 181: 6828-6831.
12. Li RF, Lu GT, Li L, Su HZ, Feng GF, et al. (2013) Identification of a putative cognate sensor kinase for the two-component response regulator HrpG, a key regulator controlling the expression of the hrp genes in Xanthomonas campestris pv. campestris. Environ Microbiol [epub ahead of print].
13. Furutani A, Nakayama T, Ochiai H, Kaku H, Kubo Y, et al. (2006) Identification of novel HrpXo regulons preceded by two cis-acting elements, a plant-inducible promoter box and a -10 box-like sequence, from the genome database of Xanthomonas oryzae pv. oryzae. FEMS microbiology letters 259: 133-141.
14. Jiang W, Jiang BL, Xu RQ, Huang JD, Wei HY, et al. (2009) Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv. campestris and five of them contribute individually to full pathogenicity. Molecular plant-microbe interactions 22: 1401-1411.
15. Lipscomb L, Schell MA, (2011) Elucidation of the regulon and cis-acting regulatory element of HrpB, the AraC-type regulator of a plant pathogen-like type III secretion system in Burkholderia pseudomallei. J Bacteriol 193: 1991-2001.
16. Cunnac S, Boucher C, Genin S, (2004) Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the type III secretion system and effector genes in Ralstonia solanacearum. Journal of bacteriology 186: 2309-2318.
17. Tang X, Xiao Y, Zhou JM, (2006) Regulation of the type III secretion system in phytopathogenic bacteria. Mol Plant Microbe Interact 19: 1159-1166.
18. Schmidtke C, Findeiss S, Sharma CM, Kuhfuss J, Hoffmann S, et al. (2012) Genome-wide transcriptome analysis of the plant pathogen Xanthomonas iden Nucleic acids research40: 2020-2031.
19. Chao NX, Wei K, Chen Q, Meng QL, Tang DJ, et al. (2008) The rsmA-like gene rsmA(Xcc) of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Molecular plant-microbe interactions 21: 411-423.
20. Zhu PL, Zhao S, Tang JL, Feng JX, (2011) The rsmA-like gene rsmA(Xoo) of Xanthomonas oryzae pv. oryzae regulates bacterial virulence and production of diffusible signal factor. Molecular plant pathology 12: 227-237.
21. Lapouge K, Schubert M, Allain FH, Haas D, (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Molecular microbiology 67: 241-253.
22. Romeo T, Vakulskas CA, Babitzke P, (2012) Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environmental microbiology 15 (2) (): 313-24.
23. White D, Hart ME, Romeo T, (1996) Phylogenetic distribution of the global regulatory gene csrA among eubacteria. Gene 182: 221-223.
24. Romeo T, (1998) Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Molecular microbiology 29: 1321-1330.
25. Babitzke P, Romeo T, (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Current opinion in microbiology 10: 156-163.
26. Jonas K, Edwards AN, Simm R, Romeo T, Romling U, et al. (2008) The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Molecular microbiology 70: 236-257.
27. Lu XH, An SQ, Tang DJ, McCarthy Y, Tang JL, et al. (2012) RsmA regulates biofilm formation in Xanthomonas campestris through a regulatory network involving cyclic di-GMP and the Clp transcription factor. PloS one 7: e52646.
28. Altier C, Suyemoto M, Lawhon SD, (2000) Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infection and immunity 68: 6790-6797.
29. Mulcahy H, O'Callaghan J, O'Grady EP, Adams C, O'Gara F, (2006) The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect Immun 74: 3012-3015.
30. Cui Y, Chatterjee A, Liu Y, Dumenyo CK, Chatterjee AK, (1995) Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. Journal of bacteriology 177: 5108-5115.
31. Liu Y, Cui Y, Mukherjee A, Chatterjee AK, (1998) Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Molecular microbiology 29: 219-234.
32. Zou L, Zeng Q, Lin H, Gyaneshwar P, Chen G, et al. (2012) SlyA regulates type III secretion system (T3SS) genes in parallel with the T3SS master regulator HrpL in Dickeya dadantii 3937. Appl Environ Microbiol 78: 2888-2895.
33. Schubert M, Lapouge K, Duss O, Oberstrass FC, Jelesarov I, et al. (2007) Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nature structural & molecular biology 14: 807-813.
34. Mercante J, Suzuki K, Cheng X, Babitzke P, Romeo T, (2006) Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. The Journal of biological chemistry 281: 31832-31842.
35. Dubey AK, Baker CS, Romeo T, Babitzke P, (2005) RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11: 1579-1587.
36. Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T, (2009) Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. Journal of molecular biology 392: 511-528.
37. Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P, et al. (2005) CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Molecular microbiology 56: 1648-1663.
38. Kerrinnes T, Zelas ZB, Streckel W, Faber F, Tietze E, et al. (2009) CsrA and CsrB are required for the post-transcriptional control of the virulence-associated effector protein AvrA of Salmonella enterica. International journal of medical microbiology: IJMM 299: 333-341.
39. Liu MY, Gui G, Wei B, Preston JF 3rd, Oakford L, et al. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. The Journal of biological chemistry 272: 17502-17510.
40. Burrowes E, Baysse C, Adams C, O'Gara F, (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152: 405-418.
41. Chatterjee A, Cui Y, Chatterjee AK, (2002) RsmA and the quorum-sensing signal, N-[3-oxohexanoyl]-L-homoserine lactone, control the levels of rsmB RNA in Erwinia carotovora subsp. carotovora by affecting its stability. Journal of bacteriology 184: 4089-4095.
42. Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, et al. (2007) Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Molecular microbiology 66: 341-356.
43. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, et al. (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Molecular microbiology 40: 245-256.
44. Yakhnin AV, Baker CS, Vakulskas CA, Yakhnin H, Berezin I, et al. (2013) CsrA activates flhDC expression by protecting flhDC mRNA from RNase E-mediated cleavage. Mol Microbiol 87: 851-866.
45. Gottwald TR, Sun X, Riley T, Graham JH, Ferrandino F, et al. (2002) Geo-referenced spatiotemporal analysis of the urban citrus canker epidemic in Florida. Phytopathology 92: 361-377.
46. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, et al. (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: 459-463.
47. Rife C, Schwarzenbacher R, McMullan D, Abdubek P, Ambing E, et al. (2005) Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 A resolution reveals a new fold. Proteins 61: 449-453.
48. Gutierrez P, Li Y, Osborne MJ, Pomerantseva E, Liu Q, et al. (2005) Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. Journal of bacteriology 187: 3496-3501.
49. Agaras B, Sobrero P, Valverde C, (2013) A CsrA/RsmA translational regulator gene encoded in the replication region of a Sinorhizobium meliloti cryptic plasmid complements Pseudomonas fluorescens rsmA/E mutants. Microbiology 159: 230-242.
50. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
51. Marden JN, Diaz MR, Walton WG, Gode CJ, Betts L, et al. (2013) An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 110: 15055-15060.
52. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, et al. (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4: 1-13.
53. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
54. Schwede T, Kopp J, Guex N, Peitsch MC, (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
55. Ordog R, (2008) PyDeT, a PyMOL plug-in for visualizing geometric concepts around proteins. Bioinformation 2: 346-347.
56. Astua-Monge G, Freitas-Astua J, Bacocina G, Roncoletta J, Carvalho SA, et al. (2005) Expression profiling of virulence and pathogenicity genes of Xanthomonas axonopodis pv. citri. Journal of bacteriology 187: 1201-1205.
57. Wengelnik K, Bonas U, (1996) HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. Journal of bacteriology 178: 3462-3469.
58. Lorenz C, Buttner D, (2011) Secretion of early and late substrates of the type III secretion system from Xanthomonas is controlled by HpaC and the C-terminal domain of HrcU. Molecular microbiology 79: 447-467.
59. Cappelletti PA, dos Santos RF, do Amaral AM, Homem RA, Souza Tdos S, et al. (2011) Structure-function analysis of the HrpB2-HrcU interaction in the Xanthomonas citri type III secretion system. PloS one 6: e17614.
60. Jefferson RA, (1989) The GUS reporter gene system. Nature 342: 837-838.
61. Atanassov II, Etchells JP, Turner SR, (2009) A simple, flexible and efficient PCR-fusion/Gateway cloning procedure for gene fusion, site-directed mutagenesis, short sequence insertion and domain deletions and swaps. Plant Methods 5: 14.
62. Heroven AK, Bohme K, Dersch P, (2012) The Csr/Rsm system of Yersinia and related pathogens: A post-transcriptional strategy for managing virulence. RNA biology 9: 379-391.
63. Weber E, Berger C, Bonas U, Koebnik R, (2007) Refinement of the Xanthomonas campestris pv. vesicatoria hrpD and hrpE operon structure. Molecular plant-microbe interactions 20: 559-567.
64. Kogenaru S, Qing Y, Guo Y, Wang N, (2012) RNA-seq and microarray complement each other in transcriptome profiling. BMC genomics 13: 629.
65. Furutani A, Nakayama T, Ochiai H, Kaku H, Kubo Y, et al. (2006) Identification of novel HrpXo regulons preceded by two cis-acting elements, a plant-inducible promoter box and a -10 box-like sequence, from the genome database of Xanthomonas oryzae pv. oryzae. FEMS Microbiol Lett 259: 133-141.
66. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
67. Yakhnin AV, Yakhnin H, Babitzke P, (2012) Gel mobility shift assays to detect protein-RNA interactions. Methods Mol Biol 905: 201-211.
68. Girish V, Vijayalakshmi A, (2004) Affordable image analysis using NIH Image/ImageJ. Indian J Cancer 41: 47.
69. Hartig SM, (2013) Basic image analysis and manipulation in ImageJ. Curr Protoc Mol Biol Chapter 14: Unit14 15.
70. Dubey AK, Baker CS, Suzuki K, Jones AD, Pandit P, et al. (2003) CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. Journal of bacteriology 185: 4450-4460.
71. Goldsborough AS, Kornberg TB, (1994) Allele-specific quantification of Drosophila engrailed and invected transcripts. Proc Natl Acad Sci U S A 91: 12696-12700.
72. Baker CS, Eory LA, Yakhnin H, Mercante J, Romeo T, et al. (2007) CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine-Dalgarno sequence. Journal of bacteriology 189: 5472-5481.
73. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, et al. (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40: 245-256.
74. Mackie GA, (1998) Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395: 720-723.
75. Liu MY, Yang H, Romeo T, (1995) The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. Journal of bacteriology 177: 2663-2672.
76. Drlica K, Zhao X, (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61: 377-392.
77. Drlica K, Hiasa H, Kerns R, Malik M, Mustaev A, et al. (2009) Quinolones: action and resistance updated. Curr Top Med Chem 9: 981-998.
78. Xu Y, Luo QQ, Zhou MG, (2013) Identification and characterization of integron-mediated antibiotic resistance in the phytopathogen Xanthomonas oryzae pv. oryzae. PLoS One 8: e55962.
79. Cheng CM, Tu J, Yang CC, Kuo TT, (1996) Rifampicin: an inhibitor of Xp12-specific protein phosphorylation in Xanthomonas oryzae pv. oryzae. FEMS Microbiol Lett 143: 141-149.
80. Lorenz C, Hausner J, Buttner D, (2012) HrcQ provides a docking site for early and late type III secretion substrates from Xanthomonas. PLoS One 7: e51063.
81. Martins PM, Lau IF, Bacci M, Belasque J, do Amaral AM, et al. (2010) Subcellular localization of proteins labeled with GFP in Xanthomonas citri ssp. citri: targeting the division septum. FEMS Microbiol Lett 310: 76-83.
82. Kondo H, Nakagawa A, Nishihira J, Nishimura Y, Mizuno T, et al. (1997) Escherichia coli positive regulator OmpR has a large loop structure at the putative RNA polymerase interaction site. Nat Struct Biol 4: 28-31.
83. Ingle CA, Kushner SR, (1996) Development of an in vitro mRNA decay system for Escherichia coli: poly(A) polymerase I is necessary to trigger degradation. Proc Natl Acad Sci U S A 93: 12926-12931.
84. Mohanty BK, Giladi H, Maples VF, Kushner SR, (2008) Analysis of RNA decay, processing, and polyadenylation in Escherichia coli and other prokaryotes. Methods Enzymol 447: 3-29.
85. Kushner SR, (2002) mRNA decay in Escherichia coli comes of age. J Bacteriol 184: 4658-4665 discussion 4657.
86. Martinez LC, Yakhnin H, Camacho MI, Georgellis D, Babitzke P, et al. (2011) Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol Microbiol 80: 1637-1656.
87. Kerrinnes T, Zelas ZB, Streckel W, Faber F, Tietze E, et al. (2009) CsrA and CsrB are required for the post-transcriptional control of the virulence-associated effector protein AvrA of Salmonella enterica. Int J Med Microbiol 299: 333-341.
88. Fortune DR, Suyemoto M, Altier C, (2006) Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 74: 331-339.
89. Chatterjee A, Cui Y, Chakrabarty P, Chatterjee AK, (2010) Regulation of motility in Erwinia carotovora subsp. carotovora: quorum-sensing signal controls FlhDC, the global regulator of flagellar and exoprotein genes, by modulating the production of RsmA, an RNA-binding protein. Molecular plant-microbe interactions 23: 1316-1323.
90. Liu Y, Cui Y, Mukherjee A, Chatterjee AK, (1998) Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 29: 219-234.
91. O'Grady EP, Mulcahy H, O'Callaghan J, Adams C, O'Gara F, (2006) Pseudomonas aeruginosa infection of airway epithelial cells modulates expression of Kruppel-like factors 2 and 6 via RsmA-mediated regulation of type III exoenzymes S and Y. Infection and immunity 74: 5893-5902.
92. Jorgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G, (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27: 1132-1145.
93. De Lay N, Gottesman S, (2012) A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86: 524-538.
94. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM, (2000) A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38: 986-1003.
95. Ryan RP, McCarthy Y, Andrade M, Farah CS, Armitage JP, et al. (2010) Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc Natl Acad Sci U S A 107: 5989-5994.
96. White TJ, Gonzalez CF, (1995) Electroporation of Xanthomonas. Methods Mol Biol 47: 135-141.
97. Souza DP, Andrade MO, Alvarez-Martinez CE, Arantes GM, Farah CS, et al. (2011) A component of the Xanthomonadaceae type IV secretion system combines a VirB7 motif with a N0 domain found in outer membrane transport proteins. PLoS Pathog 7: e1002031.
98. Sambrook J, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y. Cold Spring Harbor Laboratory Press.
99. De Feyter R, Yang Y, Gabriel DW, (1993) Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Mol Plant Microbe Interact 6: 225-237.
100. Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, et al. (2010) Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. The New phytologist 187: 983-1002.
101. Rybak M, Minsavage GV, Stall RE, Jones JB, (2009) Identification of Xanthomonas citri ssp. citri host specificity genes in a heterologous expression host. Mol Plant Pathol 10: 249-262.
102. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
103. Guo Y, Zhang Y, Li JL, Wang N, (2012) Diffusible signal factor-mediated quorum sensing plays a central role in coordinating gene expression of Xanthomonas citri subsp. citri. Molecular plant-microbe interactions 25: 165-179.
104. Smyth GK, Michaud J, Scott HS, (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075.
105. Hochberg Y, Benjamini Y, (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811-818.
106. Boulanger A, Chen Q, Hinton DM, Stibitz S, (2013) In vivo phosphorylation dynamics of the Bordetella pertussis virulence-controlling response regulator BvgA. Mol Microbiol 88: 156-172.
107. Barbieri CM, Stock AM, (2008) Universally applicable methods for monitoring response regulator aspartate phosphorylation both in vitro and in vivo using Phos-tag-based reagents. Anal Biochem 376: 73-82.
108. Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, et al. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37: 49-59.
109. Staskawicz B, Dahlbeck D, Keen N, Napoli C, (1987) Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol 169: 5789-5794.
110. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, et al. (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2: 443-448.
111. Tsuge S, Furutani A, Fukunaka R, Oku T, Tsuno K, et al. (2002) Expression of Xanthomonas oryzae pv. oryzae hrp Genes in XOM2, a Novel Synthetic Medium J Gen Plant Pathol 68: 363-371.
112. Jensen EC, (2013) Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec (Hoboken) 296: 378-381.
113. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
114. Bramucci E, Paiardini A, Bossa F, Pascarella S, (2012) PyMod: sequence similarity searches, multiple sequence-structure alignments, and homology modeling within PyMOL. BMC Bioinformatics 13 Suppl 4: S2.