The nucleoid-associated proteins H-NS and FIS modulate the DNA supercoiling response of the pel genes, the major virulence factors in the plant pathogen bacterium Dickeya dadantii

Nucleic Acids Research

Volumn 40, Issue 10, 2012, Pages 4306-4319

  Ouafa, Zghidi Abouzid ^a,b   Reverchon, Sylvie ^a,b   Lautier, Thomas ^a,b,d   Muskhelishvili, Georgi ^c   Nasser, William ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ DE LYON   (France)

^c JACOBS UNIVERSITY BREMEN   (Germany)

^d UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; FACTOR FOR INVERSION STIMULATION; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; PECTATE LYASE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL VIRULENCE; CONTROLLED STUDY; DICKEYA DADANTII; DNA SUPERCOILING; GENE ACTIVITY; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC TRANSCRIPTION; MODULATION; NONHUMAN; PECTOBACTERIUM CHRYSANTHEMI; PEL GENE; PLANT DISEASE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN LOCALIZATION;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; ENTEROBACTERIACEAE; FACTOR FOR INVERSION STIMULATION PROTEIN; GENE EXPRESSION REGULATION, BACTERIAL; POLYSACCHARIDE-LYASES; PROMOTER REGIONS, GENETIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); DICKEYA DADANTII;

EID: 84861556667     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks014     Document Type: Article

References (71)

1. Browning, D.F. and Busby, S.J. (2004) The regulation of bacterial transcription initiation. Nat. Rev. Microbiol., 2, 57-65.
2. Janga, S.C. and Collado-Vides, J. (2007) Structure and evolution of gene regulatory networks in microbial genomes. Res Microbiol., 158, 787-794.
3. Travers, A. and Muskhelishvili, G. (2005) DNA supercoiling-a global transcriptional regulator for enterobacterial growth? Nat. Rev. Microbiol., 3, 157-169.
4. Ishihama, A. (2010) Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol. Rev., 34, 628-645.
5. Muskhelishvili, G., Sobetzko, P., Geertz, M. and Berger, M. (2010) General organisational principles of the transcriptional regulation system: a tree or a circle? Mol. Biosyst., 6, 662-676.
6. Dillon, S.C. and Dorman, C.J. (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol., 8, 185-195.
7. Lebeau, A., Reverchon, S., Gaubert, S., Kraepiel, Y., Simond-Cote, E., Nasser, W. and Van Gijsegem, F. (2008) The GacA global regulator is required for the appropriate expression of Erwinia chrysanthemi 3937 pathogenicity genes during plant infection. Environ. Microbiol., 10, 545-559.
8. Hugouvieux-Cotte-Pattat, N., Condemine, G., Nasser, W. and Reverchon, S. (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu. Rev. Microbiol., 50, 213-257.
9. Sepulchre, J.A., Reverchon, S. and Nasser, W. (2007) Modeling the onset of virulence in a pectinolytic bacterium. J. Theor. Biol., 244, 239-257.
10. Kepseu, W.D., Sepulchre, J.A., Reverchon, S. and Nasser, W. (2010) Toward a quantitative modeling of the synthesis of the pectate lyases, essential virulence factors in Dickeya dadantii. J. Biol. Chem., 285, 28565-28576.
11. Reverchon, S., Nasser, W. and Robert-Baudouy, J. (1991) Characterization of kdgR, a gene of Erwinia chrysanthemi that regulates pectin degradation. Mol. Microbiol., 5, 2203-2216.
12. Reverchon, S., Van Gijsegem, F., Effantin, G., Zghidi-Abouzid, O. and Nasser, W. (2010) Systematic targeted mutagenesis of the MarR/SlyA family members of Dickeya dadantii 3937 reveals a role for MfbR in the modulation of virulence gene expression in response to acidic pH. Mol. Microbiol., 78, 1018-1037.
13. Hommais, F., Oger-Desfeux, C., Van Gijsegem, F., Castang, S., Ligori, S., Expert, D., Nasser, W. and Reverchon, S. (2008) PecS is a global regulator of the symptomatic phase in the phytopathogenic bacterium Erwinia chrysanthemi 3937. J. Bacteriol., 190, 7508-7522.
14. Castillo, A., Nasser, W., Condemine, G. and Reverchon, S. (1998) The PecT repressor interacts with regulatory regions of pectate lyase genes in Erwinia chrysanthemi. Biochim. Biophys. Acta, 1442, 148-160.
15. Nomura, K., Nasser, W. and Tsuyumu, S. (1999) Self-regulation of Pir, a regulatory protein responsible for hyperinduction of pectate lyase in Erwinia chrysanthemi EC16. Mol. Plant Microbe Interact., 12, 385-390.
16. Franza, T., Michaud-Soret, I., Piquerel, P. and Expert, D. (2002) Coupling of iron assimilation and pectinolysis in Erwinia chrysanthemi 3937. Mol. Plant Microbe Interact., 15, 1181-1191.
17. Nasser, W., Robert-Baudouy, J. and Reverchon, S. (1997) Antagonistic effect of CRP and KdgR in the transcription control of the Erwinia chrysanthemi pectinolysis genes. Mol. Microbiol., 26, 1071-1082.
18. Nasser, W., Faelen, M., Hugouvieux-Cotte-Pattat, N. and Reverchon, S. (2001) Role of the nucleoid-associated protein H-NS in the synthesis of virulence factors in the phytopathogenic bacterium Erwinia chrysanthemi. Mol. Plant Microbe Interact., 14, 10-20.
19. Nasser, W. and Reverchon, S. (2002) H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PecT repressor. Mol. Microbiol., 43, 733-748.
20. Lautier, T., Blot, N., Muskhelishvili, G. and Nasser, W. (2007) Integration of two essential virulence modulating signals at the Erwinia chrysanthemi pel gene promoters: a role for Fis in the growth-phase regulation. Mol. Microbiol., 66, 1491-1505.
21. Lautier, T. and Nasser, W. (2007) The DNA nucleoid-associated protein Fis co-ordinates the expression of the main virulence genes in the phytopathogenic bacterium Erwinia chrysanthemi. Mol. Microbiol., 66, 1474-1490.
22. Higgins, C.F., Dorman, C.J., Stirling, D.A., Waddell, L., Booth, I.R., May, G. and Bremer, E. (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell, 52, 569-584.
23. Dorman, C.J., Ni Bhriain, N. and Higgins, C.F. (1990) DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature, 344, 789-792.
24. Bouffartigues, E., Buckle, M., Badaut, C., Travers, A. and Rimsky, S. (2007) H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol., 14, 441-448.
25. Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C.O., Mavathur, R., Muskhelishvili, G., Pon, C.L., Rimsky, S. et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res., 35, 6330-6337.
26. Atlung, T. and Ingmer, H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol., 24, 7-17.
27. Falconi, M., Colonna, B., Prosseda, G., Micheli, G. and Gualerzi, C.O. (1998) Thermoregulation of Shigella and Escherichia coli EIEC pathogenicity. A temperature-dependent structural transition of DNA modulates accessibility of virF promoter to transcriptional repressor H-NS. EMBO J., 17, 7033-7043.
28. Prosseda, G., Fradiani, P.A., Di Lorenzo, M., Falconi, M., Micheli, G., Casalino, M., Nicoletti, M. and Colonna, B. (1998) A role for H-NS in the regulation of the virF gene of Shigella and enteroinvasive Escherichia coli. Res Microbiol., 149, 15-25.
29. Castang, S., McManus, H.R., Turner, K.H. and Dove, S.L. (2008) H-NS family members function coordinately in an opportunistic pathogen. Proc. Natl Acad. Sci. USA, 105, 18947-18952.
30. Tran, C.N., Giangrossi, M., Prosseda, G., Brandi, A., Di Martino, M.L., Colonna, B. and Falconi, M. (2011) A multifactor regulatory circuit involving H-NS, VirF and an antisense RNA modulates transcription of the virulence gene icsA of Shigella flexneri. Nucleic Acids Res., 39, 8122-8134.
31. Yu, R.R. and DiRita, V.J. (2002) Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol., 43, 119-134.
32. Ross, W., Thompson, J.F., Newlands, J.T. and Gourse, R.L. (1990) E. coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J., 9, 3733-3742.
33. Schneider, R., Travers, A., Kutateladze, T. and Muskhelishvili, G. (1999) A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol. Microbiol., 34, 953-964.
34. Weinstein-Fischer, D., Elgrably-Weiss, M. and Altuvia, S. (2000) Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol. Microbiol., 35, 1413-1420.
35. Schneider, R., Travers, A. and Muskhelishvili, G. (1997) FIS modulates growth phase-dependent topological transitions of DNA in Escherichia coli. Mol. Microbiol., 26, 519-530.
36. Blot, N., Mavathur, R., Geertz, M., Travers, A. and Muskhelishvili, G. (2006) Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep., 7, 710-715.
37. Ball, C.A., Osuna, R., Ferguson, K.C. and Johnson, R.C. (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol., 174, 8043-8056.
38. Goldberg, M.D., Johnson, M., Hinton, J.C. and Williams, P.H. (2001) Role of the nucleoid-associated protein Fis in the regulation of virulence properties of enteropathogenic Escherichia coli. Mol. Microbiol., 41, 549-559.
39. Falconi, M., Prosseda, G., Giangrossi, M., Beghetto, E. and Colonna, B. (2001) Involvement of FIS in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli. Mol. Microbiol., 42, 439-452.
40. Schechter, L.M., Jain, S., Akbar, S. and Lee, C.A. (2003) The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. Infect. Immun., 71, 5432-5435.
41. O. Croinin, T., Carroll, R.K., Kelly, A. and Dorman, C.J. (2006) Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol. Microbiol., 62, 869-882.
42. Lenz, D.H. and Bassler, B.L. (2007) The small nucleoid protein Fis is involved in Vibrio cholerae quorum sensing. Mol. Microbiol., 63, 859-871.
43. Rui, S. and Tse-Dinh, Y.C. (2003) Topoisomerase function during bacterial responses to environmental challenge. Front Biosci., 8, d256-d263.
44. Dorman, C.J. (1991) DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Infect. Immun., 59, 745-749.
45. Cameron, A.D., Stoebel, D.M. and Dorman, C.J. (2011) DNA supercoiling is differentially regulated by environmental factors and FIS in Escherichia coli and Salmonella enterica. Mol. Microbiol., 80, 85-101.
46. Keller, W. (1975) Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc. Natl Acad. Sci. USA, 72, 4876-4880.
47. Pfaffl, M.W., Horgan, G.W. and Dempfle, L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res., 30, e36.
48. Hommais, F., Zghidi-Abouzid, O., Oger-Desfeux, C., Pineau-Chapelle, E., Van Gijsegem, F., Nasser, W. and Reverchon, S. (2011) lpxC and yafS are the most suitable internal controls to normalize real time RT-qPCR expression in the phytopathogenic bacteria Dickeya dadantii. PLoS One, 6, e20269.
49. Balke, V.L. and Gralla, J.D. (1987) Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J. Bacteriol., 169, 4499-4506.
50. Maxwell, A. (1997) DNA gyrase as a drug target. Trends Microbiol., 5, 102-109.
51. Menzel, R. and Gellert, M. (1987) Modulation of transcription by DNA supercoiling: a deletion analysis of the Escherichia coli gyrA and gyrB promoters. Proc. Natl Acad. Sci. USA, 84, 4185-4189.
52. Khodursky, A.B., Zechiedrich, E.L. and Cozzarelli, N.R. (1995) Topoisomerase IV is a target of quinolones in Escherichia coli. Proc. Natl Acad. Sci. USA, 92, 11801-11805.
53. Zechiedrich, E.L., Khodursky, A.B. and Cozzarelli, N.R. (1997) Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev., 11, 2580-2592.
54. Nasser, W., Rochman, M. and Muskhelishvili, G. (2002) Transcriptional regulation of fis operon involves a module of multiple coupled promoters. EMBO J., 21, 715-724.
55. Dorman, C.J. and Corcoran, C.P. (2009) Bacterial DNA topology and infectious disease. Nucleic Acids Res., 37, 672-678.
56. Rimsky, S. and Travers, A. (2011) Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins. Curr. Opin. Microbiol., 14, 136-141.
57. Rochman, M., Aviv, M., Glaser, G. and Muskhelishvili, G. (2002) Promoter protection by a transcription factor acting as a local topological homeostat. EMBO Rep., 3, 355-360.
58. Auner, H., Buckle, M., Deufel, A., Kutateladze, T., Lazarus, L., Mavathur, R., Muskhelishvili, G., Pemberton, I., Schneider, R. and Travers, A. (2003) Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. J. Mol. Biol., 331, 331-344.
59. Muskhelishvili, G. and Travers, A. (2003) Transcription factor as a topological homeostat. Front Biosci., 8, d279-d285.
60. Ono, S., Goldberg, M.D., Olsson, T., Esposito, D., Hinton, J.C. and Ladbury, J.E. (2005) H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem. J., 391, 203-213.
61. Liu, Y., Chen, H., Kenney, L.J. and Yan, J. (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev., 24, 339-344.
62. Owen-Hughes, T.A., Pavitt, G.D., Santos, D.S., Sidebotham, J.M., Hulton, C.S., Hinton, J.C. and Higgins, C.F. (1992) The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell, 71, 255-265.
63. Zhang, W. and Baseman, J.B. (2011) Transcriptional regulation of MG-149, an osmoinducible lipoprotein gene from Mycoplasma genitalium. Mol. Microbiol., 81, 327-339.
64. Grignon, C. and Sentenac, H. (1991) pH and ionic conditions in the apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol., 42, 103-125.
65. D'Ovidio, R., Mattei, B., Roberti, S. and Bellincampi, D. (2004) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim. Biophys. Acta, 1696, 237-244.
66. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D., Felix, G. and Boller, T. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428, 764-767.
67. Nachin, L. and Barras, F. (2000) External pH: an environmental signal that helps to rationalize pel gene duplication in Erwinia chrysanthemi. Mol. Plant Microbe Interact., 13, 882-886.
68. Bardonnet, N. and Blanco, C. (1992) uidA-antibiotic-resistance cassettes for insertion mutagenesis, gene fusions and genetic constructions. FEMS Microbiol. Lett., 93, 243-248.
69. Castang, S., Reverchon, S., Gouet, P. and Nasser, W. (2006) Direct evidence for the modulation of the activity of the Erwinia chrysanthemi quorum-sensing regulator ExpR by acylhomoserine lactone pheromone. J. Biol. Chem., 281, 29972-29987.
70. Shao, Y., Feldman-Cohen, L.S. and Osuna, R. (2008) Functional characterization of the Escherichia coli Fis-DNA binding sequence. J. Mol. Biol., 376, 771-785.
71. Travers, A. and Muskhelishvili, G. (2007) A common topology for bacterial and eukaryotic transcription initiation? EMBO Rep., 8, 147-151.