A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum

Microbiology

Volumn 156, Issue 5, 2010, Pages 1323-1334

  Andresen, Liis ^a   Sala, Erki ^a   Kõiv, Viia ^a   Mäe, Andres ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; PROTEINASE; SIGMA FACTOR RPOS;

ARTICLE; BINDING SITE; CELL WALL; CONTROLLED STUDY; ENZYME DEGRADATION; ESCHERICHIA COLI; GENE; GENE ACTIVATION; GENE CONTROL; GENE FUSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; GUSA GENE; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PECTOBACTERIUM CAROTOVORUM; PLANT CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; RCS GENE; RCSB GENE; RPRA GENE; RSMB GENE; SIGNAL TRANSDUCTION; WILD TYPE;

BACTERIAL PROTEINS; CELL WALL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; OPERON; PECTOBACTERIUM CAROTOVORUM; PLANTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIRULENCE;

ESCHERICHIA COLI; PECTOBACTERIUM CAROTOVORUM SUBSP. CAROTOVORUM;

EID: 77952353247     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.033936-0     Document Type: Article

References (57)

1. Andersson, R. A., Kõiv, V., Norman-Setterblad, C. & Pirhonen, M. (1999). Role of RpoS in virulence and stress tolerance of the plant pathogen Erwinia carotovora subsp. carotovora. Microbiology 145, 3547-3556. (Pubitemid 30018798)
2. Andresen, L., Kõiv, V., Alamäe, T. & Mäe, A. (2007). The Rcs phosphorelay modulates the expression of plant cell wall degrading enzymes and virulence in Pectobacterium carotovorum ssp carotovorum. FEMS Microbiol Lett 273, 229-238. (Pubitemid 47084011)
3. Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J. & other authors (2004). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101, 11105-11110. (Pubitemid 38989591)
4. Burr, T., Barnard, A. M. L., Corbett, M. J., Pemberton, C. L., Simpson, N. J. L. & Salmond, G. P. C. (2006). Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol Microbiol 59, 113-125.
5. Carballes, F., Bertrand, C., Bouche, J. P. & Cam, K. (1999). Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 34, 442-450. (Pubitemid 29507305)
6. Chatterjee, A., Cui, Y., Liu, Y., Dumenyo, C. K. & Chatterjee, A. K. (1995). Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L- homoserine lactone. Appl Environ Microbiol 61, 1959-1967.
7. Chatterjee, A., Cui, Y. Y. & Chatterjee, A. K. (2009). RsmC of Erwinia carotovora subsp. carotovora negatively controls motility, extracellular protein production, and virulence by binding FlhD and modulating transcriptional activity of the master regulator, FlhDC. J Bacteriol 191, 4582-4593.
8. Cui, Y., Chatterjee, A., Liu, Y., Dumenyo, C. K. & Chatterjee, A. K. (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 softrotting Erwinia spp. J Bacteriol 177, 5108-5115.
9. Ecc production and virulence by modulating levels of regulatory RNA (rsmB) and RNA-binding protein (RsmA). J Bacteriol 181, 6042-6052.
10. Cui, Y., Chatterjee, A. & Chatterjee, A. K. (2001). Effects of the twocomponent system comprising GacA and GacS of Erwinia carotovora subsp. carotovora on the production of global regulatory rsmB RNA, extracellular enzymes, and harpinEcc. Mol Plant Microbe Interact 14, 516-526. (Pubitemid 32235584)
11. Cui, Y., Chatterjee, A., Hasegawa, H., Dixit, V., Leigh, N. & Chatterjee, A. K. (2005). ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J Bacteriol 187, 4792-4803. (Pubitemid 40962196)
12. Cui, Y., Chatterjee, A., Yang, H. & Chatterjee, A. K. (2008). Regulatory network controlling extracellular proteins in Erwinia carotovora subsp. carotovora: FlhDC, the master regulator of flagellar genes, activates rsmB regulatory RNA production by affecting gacA and hexA (lrhA) expression. J Bacteriol 190, 4610-4623. (Pubitemid 351898978)
13. Datsenko, K. A. & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
14. Davalos-Garcia, M., Conter, A., Toesca, I., Gutierrez, C. & Cam, K. (2001). Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli. J Bacteriol 183, 5870-5876. (Pubitemid 32917405)
15. de Lorenzo, V., Herrero, M., Jakubzik, U. & Timmis, K. N. (1990). Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172, 6568-6572. (Pubitemid 20372802)
16. Eriksson, A. R. B., Andersson, R. A., Pirhonen, M. & Palva, E. T. (1998). Two-component regulators involved in the global control of virulence in Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 11, 743-752. (Pubitemid 28338708)
17. Flego, D., Marits, R., Eriksson, A. R. B., Koiv, V., Karlsson, M. B., Heikinheimo, R. & Palva, E. T. (2000). A two-component regulatory system, pehR-pehS, controls endopolygalacturonase production and virulence in the plant pathogen Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 13, 447-455. (Pubitemid 30174528)
18. Francez-Charlot, A., Laugel, B., Van Gemert, A., Dubarry, N., Wiorowski, F., Castanie-Cornet, M. P., Gutierrez, C. & Cam, K. (2003). RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol Microbiol 49, 823-832. (Pubitemid 36918699)
19. Gervais, F. G., Phoenix, P. & Drapeau, G. R. (1992). The rcsB gene, a positive regulator of colanic acid biosynthesis in Escherichia coli, is also an activator of FtsZ expression. J Bacteriol 174, 3964-3971.
20. Gottesman, S., Trisler, P. & Torres-Cabassa, A. (1985). Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J Bacteriol 162, 1111-1119. (Pubitemid 15008161)
21. Gupte, G., Woodward, C. & Stout, V. (1997). Isolation and characterization of rcsB mutations that affect colanic acid capsule synthesis in Escherichia coli K-12. J Bacteriol 179, 4328-4335. (Pubitemid 27291066)
22. Harris, S. J., Shih, Y. L., Bentley, S. D. & Salmond, G. P. (1998). The hexA gene of Erwinia carotovora encodes a LysR homologue and regulates motility and the expression of multiple virulence determinants. Mol Microbiol 28, 705-717.
23. Heikinheimo, R., Flego, D., Pirhonen, M., Karlsson, M. B., Eriksson, A., Mäe, A., Kõiv, V. & Palva, E. T. (1995). Characterization of a novel pectate lyase from Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 8, 207-217.
24. Hinchliffe, S. J., Howard, S. L., Huang, Y. H., Clarke, D. J. & Wren, B. W. (2008). The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae. Microbiology 154, 1117-1131.
25. Hõrak, R., Ilves, H., Pruunsild, P., Kuljus, M. & Kivisaar, M. (2004). The ColR-ColS two-component signal transduction system is involved in regulation of Tn4652 transposition in Pseudomonas putida under starvation conditions. Mol Microbiol 54, 795-807. (Pubitemid 39457299)
26. Hossain, M. M., Shibata, S., Aizawa, S. I. & Tsuyumu, S. (2005). Motility is an important determinant for pathogenesis of Erwinia carotovora subsp. carotovora. Physiol Mol Plant Pathol 66, 134-143. (Pubitemid 41406046)
27. Hyytiäinen, H., Sjöblom, S., Palomäki, T., Tuikkala, A. & Palva, E. T. (2003). The PmrA-PmrB two-component system responding to acidic pH and iron controls virulence in the plant pathogen Erwinia carotovora ssp. carotovora. Mol Microbiol 50, 795-807. (Pubitemid 37372244)
28. Ilves, H., Hõrak, R., Teras, R. & Kivisaar, M. (2004). IHF is the limiting host factor in transposition of Pseudomonas putida transposon Tn4652 in stationary phase. Mol Microbiol 51, 1773-1785. (Pubitemid 38406548)
29. Jones, A. M., Goodwill, A. & Elliott, T. (2006). Limited role for the DsrA and RprA regulatory RNAs in rpoS regulation in Salmonella enterica. J Bacteriol 188, 5077-5088. (Pubitemid 44051474)
30. Kapatral, V., Campbell, J. W., Minnich, S. A., Thomson, N. R., Matsumura, P. & Pruss, B. M. (2004). Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150, 2289-2300. (Pubitemid 39117641)
31. Liu, Y., Cui, Y., Mukherjee, A. & Chatterjee, A. K. (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. (Pubitemid 28318576)
32. Liu, Y., Jiang, G., Cui, Y., Mukherjee, A., Ma, W. L. & Chatterjee, A. K. (1999). kdgREcc negatively regulates genes for pectinases, cellulase, protease, harpinEcc, and a global RNA regulator in Erwinia carotovora subsp. carotovora. J Bacteriol 181, 2411-2421. (Pubitemid 29181563)
33. -ΔΔCt method. Methods 25, 402-408.
34. Mäe, A., Heikinheimo, R. & Palva, E. T. (1995). Structure and regulation of the Erwinia carotovora subspecies carotovora Scc3193 cellulase gene Celv1 and the role of cellulase in phytopathogenicity. Mol Gen Genet 247, 17-26.
35. Majdalani, N., Chen, S., Murrow, J., St John, K. & Gottesman, S. (2001). Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 39, 1382-1394. (Pubitemid 32225146)
36. Majdalani, N., Hernandez, D. & Gottesman, S. (2002). Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46, 813-826. (Pubitemid 35365616)
37. Majdalani, N., Heck, M., Stout, V. & Gottesman, S. (2005). Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J Bacteriol 187, 6770-6778. (Pubitemid 41356251)
38. Marits, R., Kõiv, V., Laasik, E. & Mäe, A. (1999). Isolation of an extracellular protease gene of Erwinia carotovora subsp. carotovora strain SCC3193 by transposon mutagenesis and the role of protease in phytopathogenicity. Microbiology 145, 1959-1966. (Pubitemid 29396926)
39. Marits, R., Tshuikina, M., Pirhonen, M., Laasik, E. & Mäe, A. (2002). Regulation of the expression of prtW : gusA fusions in Erwinia carotovora subsp. carotovora. Microbiology 148, 835-842. (Pubitemid 34232868)
40. Miller, J. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
41. Mouslim, C., Delgado, M. & Groisman, E. A. (2004). Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol Microbiol 54, 386-395. (Pubitemid 39388283)
42. Münch, R., Hiller, K., Grote, A., Scheer, M., Klein, J., Schobert, M. & Jahn, D. (2005). Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21, 4187-4189.
43. Novel, G., Didier-Fichet, M. L. & Stoeber, F. (1974). Inducibility of beta-glucuronidase in wild-type and hexuronate-negative mutants of Escherichia coli K-12. J Bacteriol 120, 89-95.
44. Pavel, H., Forsman, M. & Shingler, V. (1994). An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols. J Bacteriol 176, 7550-7557. (Pubitemid 24382034)
45. Pérombelon, M. C. M. (2002). Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathol 51, 1-12.
46. Pirhonen, M., Heino, P., Helander, I., Harju, P. & Palva, E. T. (1988). Bacteriophage T4 resistant mutants of the plant pathogen Erwinia carotovora. Microb Pathog 4, 359-367.
47. Pirhonen, M., Saarilahti, H., Karlsson, M. B. & Palva, E. T. (1991). Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol Plant Microbe Interact 4, 276-283.
48. Prüß, B. M. (2000). FlhD, a transcriptional regulator in bacteria. Recent Res Dev Microbiol 4, 31-42.
49. Prüß, B. M., Liu, X., Hendrickson, W. & Matsumura, P. (2001). FlhD/FlhC-regulated promoters analyzed by gene array and lacZ gene fusions. FEMS Microbiol Lett 197, 91-97. (Pubitemid 32245757)
50. Prüß, B. M., Campbell, J. W., Van Dyk, T. K., Zhu, C., Kogan, Y. & Matsumura, P. (2003). FlhD/FlhC is a regulator of anaerobic respiration and the Entner-Doudoroff pathway through induction of the methyl-accepting chemotaxis protein Aer. J Bacteriol 185, 534-543. (Pubitemid 36070480)
51. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
52. Sjöblom, S., Brader, G., Koch, G. & Palva, T. E. (2006). Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60, 1474-1489. (Pubitemid 43801438)
53. Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113-130.
54. Takle, G. W., Toth, I. K. & Brurberg, M. B. (2007). Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. BMC Plant Biol 7, 50.
55. Wang, Q., Zhao, Y., McClelland, M. & Harshey, R. M. (2007). The RcsCDB signaling system and swarming motility in Salmonella enterica serovar Typhimurium: dual regulation of flagellar and SPI-2 virulence genes. J Bacteriol 189, 8447-8457.
56. Wang, D., Korban, S. S. & Zhao, Y. (2009). The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. Mol Plant Pathol 10, 277-290.
57. Wehland, M. & Bernhard, F. (2000). The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem 275, 7013-7020. (Pubitemid 30146246)