Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites

Molecular Microbiology

Volumn 29, Issue 1, 1998, Pages 219-234

  Liu, Yang ^a   Cui, Yaya ^a   Mukherjee, Asita ^a   Chatterjee, Arun K ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULASE; ENZYME; LACTONE DERIVATIVE; PECTATE LYASE; POLYGALACTURONASE; PROTEINASE; RECOMBINANT PROTEIN; RNA; RNA BINDING PROTEIN;

ARTICLE; GENE; GENE EXPRESSION; MUTATION; NONHUMAN; NORTHERN BLOTTING; PECTOBACTERIUM CAROTOVORUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, NORTHERN; CHROMOSOME MAPPING; DNA, BACTERIAL; ENZYMES; EXTRACELLULAR SPACE; GLYCOGEN; MOLECULAR SEQUENCE DATA; PECTOBACTERIUM CAROTOVORUM; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; TRANSCRIPTION FACTORS;

ENTEROBACTERIACEAE; ERWINIA; ESCHERICHIA COLI; PECTOBACTERIUM CAROTOVORUM; PROKARYOTA; SERRATIA MARCESCENS;

EID: 7344251897     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00924.x     Document Type: Article

References (64)

1. Aiba, H., Adhya, S., and de Crombrugghe, B. (1981) Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem 256: 11905-11910.
2. Ahmed, M., Majerczak, D.R., and Coplin, D.L. (1996) Harpin is not necessary for the pathogenicity of Erwinia stewartii on maize. Phytopathology 86: S77.
3. Alfano, J.R., and Collmer, A. (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8: 1684-1698.
4. Andersson, R.A., Eriksson, A.R.B., Pirhonen, M., and Palva, E.T. (1996) The EXPS sensory kinase controls virulence gene expression in Erwinia carotovora. In 8th International Congress of Biology of Plant-Microbe Interactions. Knoxville, TN. Abstract G15.
5. Bainton, N.J., Bycroft, B.W., Chhabra, S.R., Stead, P., Gledhill, L., Hill, P.J., et al. (1992) A general role for the lux autoinducer in bacterial cell signalling: Control of antibiotic biosynthesis in Erwinia. Gene 116: 87-91.
6. Barras, F., van Gijsegem, F., and Chatterjee, A.K. (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32: 201-234.
7. Bauer, D.W., Bogdanove, A.J., Beer, S.V., and Collmer, A. (1994) Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol Plant-Microbe Interact 7: 573-581.
8. Ech: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol Plant-Microbe Interact 8: 484-491.
9. Sensing, B.A., and Dunny, G.M. (1997) Pheromone-inducible expression of an aggregation protein in Enterococcus faecalis requires interaction of a plasmid-encoded RNA with components of the ribosome. Mol Microbiol 24: 295-308.
10. Chatterjee, A.K., Ross, L.M., McEvoy, J.M., and Thurn, K.K. (1985) pULB113, an RP4: mini-Mu plasmid, mediates chromosomal moblilization and R′ formation in Erwinia amylovora, Erwinia chrysanthemi, and subspecies of Erwinia carotovora. Appl Environ Microbiol 50: 1-9.
11. Chatterjee, A., Liu, Y., Murata, H., Souissi, T., and Chatterjee, A.K. (1993) Physiological and genetic regulation of a pectate lyase structural gene, pel-1 of Erwinia carotovora ssp. carotovora strain 71. In Advances in Molecular Genetics of Plant-Microbe Interactions. Nester, E.W., and Verma, D.P.S. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 241-251.
12. Chatterjee, A., Cui, Y., Liu, Y., Dumenyo, C.K., and Chatterjee, A.K. (1995) Inactiviation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora ssp. carotovora in the absence of the starvation/cell density sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol 61: 1959-67.
13. Chatterjee, A.K., Cui, Y., Liu, Y., Dumenyo, C.K., and Mukerjee, A. (1997) Identification of a new regulatory locus (rsmB) of Erwinia carotovora ssp. carotovora that controls extracellular enzymes, Harpin and RsmA. Phytopathology 87: S18.
14. Collmer, A., and Keen, N.T. (1986) The role of pectic enzymes in plant pathogenesis. Annu Rev Phytopathol 24: 383-409.
15. Court, D. (1993) RNA processing and degradation by RNase III. In Control of Messenger RNA Stability. Belasco, J.G., and Brawerman, G. (eds). San Diego: Academic Press, pp. 71-108.
16. Cui, Y., Chatterjee, A., Liu, Y., Dumenyo, C.K., and Chatterjee, A.K. (1995) Identification of a global repressor gene, rsmA, of Erwinia carotovora ssp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol 177: 5108-5115.
17. Ecc and elicit a hypersensitive reaction-like response in tobacco leaves. Mol Plant-Microbe Interact 9: 565-573.
18. Eriksson, A.R.B., Andersson, R.A., Pirhonen, M., and Palva, E.T. (1996) EXPA, a GACA-like response regulator involved in the global regulation of virulence in Erwinia carotovora ssp. carotovora. In 8th International Congress of Biology of Plant-Microbe Interactions. Knoxville, TN. Abstract G14.
19. Frederick, R.D., Chiu, J., Bennetzen, J.L., and Handa, A.K. (1997) Identification of a pathogenicity locus, rpfA, in Erwinia carotovora ssp. carotovora that encodes a two-component sensor-regulator protein. Mol Plant-Microbe Interact 10: 407-415.
20. Fuqua, W.C., Winans, S.C., and Greenberg, E.P. (1994) Quorum sensing in bacteria: the LuxR-Luxl family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
21. Fuqua, C., Winans, S.C., and Greenberg, E.P. (1996) Census and consensus in bacterial ecosystems: the LuxR-Luxl family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50: 727-751.
22. Gamper, M., and Haas, D. (1993) Processing of the Pseudomonas arcDABC mRNA requires functional RNase E in Escherichia coli. Gene 129: 119-122.
23. Govons, S., Vinopal, R., Ingraham, J., and Preiss, J. (1969) Isolation of mutants of Escherichia coli B altered in their ability to synthesize glycogen. J Bacteriol 97: 970-972.
24. Handa, A.K., Chiu, J., Rozycki, H., and Bennetzen, L. (1990) Evidence for global regulation of the expression of pathogenicity genes in soft-rot Erwinia. In Plant Pathogenic Bacteria. Klement, Z. (ed.). Budapest: Akademiai Kiado, pp. 707-712.
25. Jones, S., Yu, B., Bainton, N.J., Birdsall, M., Bycroft, B.W., Chhabra, S.R., et al. (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12: 2477-2482.
26. Keen, N.T., Tamaki, S., Kobayashi, D., and Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70: 191-197.
27. Keiler, K.C., Waller, P.R.H., and Sauer, R.T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990-993.
28. Laby, R.J., and Beer, S.V. (1992) Hybridization and functional complementation of the hrp gene cluster from Erwinia amylovora strain Ea321 with DNA of other bacteria. Mol Plant-Microbe Interact 5: 412-419.
29. Lerner, C.G., and Inouye, M. (1990) Low copy number plasmids for regulated low-level expression of cloned genes in Escherichia coli with blue/white insert screening capability Nucleic Acids Res 18: 4631.
30. Liu, Y., Murata, H., Chatterjee, A., and Chatterjee, A.K (1993) Characterization of a novel regulatory gene aepA that controls extracellular enzyme production in the phytopathogenic bacterium Erwinia carotovora ssp. carotovora. Mol Plant-Microbe Interact 6: 299-308.
31. Liu, Y., Chatterjee, A., and Chatterjee, A.K. (1994) Nucleotide sequence and expression of a novel pectate lyase gene (pel-3) and a closely linked endopolygalacturonase gene (peh-1) of Erwinia carotovora ssp. carotovora 71. Appl Environ Microbiol 60: 2545-2552.
32. Liu, M.Y., Yang, H., and Romeo, T. (1995) The product of the pleotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol 177: 2663-2672.
33. Liu, Y., Wang, X., Chatterjee, A., and Chatterjee, A.K. (1996) RecA relieves negative autoregulation of rdgA, which specifies a component of the RecA-Rdg regulatory circuit controlling pectin lyase production in Erwinia carotovora ssp. carotovora. Mol Microbiol 22: 909-918.
34. Liu, M.-Y., Gui, G., Wei, B., Preston, J.F., III, Oakford, L., Yüksel, Ü., et al. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 272: 17502-17510.
35. Mattheakis, L.C., and Nomura, M. (1988) Feedback regulation of the spc operon in Escherichia coli: translational coupling and mRNA processing. J Bacteriol 170: 4484-4492.
36. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press.
37. Mott, J.E., Galloway, J.L., and Platt, T. (1985) Maturation of Escherichia coli tryptophan operon mRNA: evidence for 3′ exonucleolytic processing after rho-dependent termination. EMBO J 4: 1887-1891.
38. Mudd, E.A., Prentki, P., Belin, D., and Krisch, H.M. (1988) Processing an unstable bacteriophage T4 gene 32 mRNAs into a stable species requires Escherichia coli ribonuclease E. EMBO J 7: 3601-3607.
39. Mukherjee, A., Cui, Y., Liu, Y., Dumenyo, C.K., and Chatterjee, A.K. (1996a) Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiology 142: 427-434.
40. Ecc and genes for other exoproteins in soft-rotting Erwinia carotovora by RsmA, a putative RNA-binding protein. In Biology of Plant-Microbe Interactions. Stacey, G., Mullins, B., and Gresshoff, P.M. (eds). St. Paul, MN: International Society for Molecular Plant-Microbe Interactions Press, pp. 187-190.
41. Ecc gene, which encodes an elicitor of the hypersensitive reaction. Mol Plant-Mircobe Interact 10: 462-471.
42. Ecc and extracellular proteins in Erwinia carotovora. J Bacteriol (in press).
43. Murata, H., Fons, M., Chatterjee, A., Collmer, A., and Chatterjee, A.K. (1990) Characterization of transposon insertion Out mutants of Erwinia carotovora ssp. carotovora defective in enzyme export and of a DNA segment that complements out mutations in E. carotovora ssp. carotovora, E. carotovora ssp. atroseptica, and Erwinia chrysanthemi. J Bacteriol 172: 2970-2978.
44. Murata, H., McEvoy, J.L., Chatterjee, A., Collmer, A., and Chatterjee, A.K. (1991) Molecular cloning of an aepA gene that activates production of extracellular pectolytic, cellulolytic, and proteolytic enzymes in Erwinia carotovora ssp. carotovora. Mol Plant-Mircobe Interact 4: 239-246.
45. Murata, H., Chatterjee, A., Liu, Y., and Chatterjee, A.K. (1994) Regulation of the production of extracellular pectinase, cellulase, and protease in the soft rot bacterium Erwinia carotovora ssp. carotovora: evidence that aepH of E. carotovora ssp. carotovora 71 activates gene expression in E. carotovora ssp. carotovora, E. carotovora ssp. atroseptica, and Escherichia coli. Appl Environ Microbiol 60: 3150-3159.
46. Nakamura, K., Imai, Y., Nakamura, A., and Yamane, K. (1992) Small cytoplasmic RNA of Bacillus subtilis: functional relationship with human signal recognition particle 7S RNA and Escherichia coli 4.5S RNA. J Bacteriol 174: 2185-2192.
47. Nasser, W., Reverchon, S., Condemine, G., and Robert-Baudouy, J. (1994) Specific interactions of Erwinia chrysanthemi kdgR represser with different operators of genes involved in pectinolysis. J Mol Biol 236: 427-440.
48. Naureckiene, S., and Uhlin, B.E. (1996) In vitro analysis of mRNA processing by RNase E in the pap operon of Escherichia coli. Mol Microbiol 21: 55-68.
49. Novick, R.P., Ross, H.F., Projan, S.J., Kornblum, J., Kreiswirth, B., and Moghazeh, S. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967-3975.
50. Paruchuri, D.K., and Harshey, R.M. (1987) Flagellar variation in Serratia marcescens is associated with color variation. J Bacteriol 169: 61-65.
51. Pirhonen, M., Flego, D., Heikinheimo, R., and Palva, E.T. (1993) A small diffusible signal molecular is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12: 2467-2476.
52. Romeo, T., Gong, M., Liu, M.-Y., and Brun-Zinkernagel, A.-M. (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175: 4744-4755.
53. Sabnis, N.A., Yang, H., and Romeo, T. (1995) Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA. J Biol Chem 270: 29096-29104.
54. Schell, M.A. (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47: 597-626.
55. Sledjeski, D., and Gottesman, S. (1995) A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci USA 92: 2003-2007.
56. Sledjeski, D.D., Gupta, A., and Gottesman, S. (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15: 3993-4000.
57. Spaink, H.P., Okker, R.J.H., Wijffelman, C.A., Pees, E., and Lugtenberg, B.J.J. (1987) Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9: 27-39.
58. Stromberg, V.K., Lacy, G.H., and Kyostio, S. (1994) Erwinia carotovora ssp. carotovora: protease in soft rot. Phytopathology 84: 1109.
59. Surgey, N., Robert-Baudouy, J., and Condemine, G. (1996) The Erwinia chrysanthemi pecT gene regulates pectinase gene expression. J Bacteriol 178: 1593-1599.
60. Thomson, N.R., Cox, A., Bycroft, B.W., Stewart, G.S.A.B., Williams, P., and Salmond, G.P.C. (1997) The Rap and Hor proteins of Erwinia, Serratia and Yersinia: a novel subgroup in a growing superfamily of proteins regulating diverse physiological processes in bacterial pathogens. Mol Microbiol 26: 531-544.
61. Walker, D.S., Reeves, P.J., and Salmond, G.P.C. (1994) The major secreted cellulase, CelV, of Erwinia carotovora ssp. carotovora is an important soft rot virulence factor. Mol Plant-Microbe Interact 7: 425-431.
62. Wharam, S.D., Mulholland, V., and Salmond, G.P.C. (1995) Conserved virulence factor regulation and secretion systems in bacterial pathogens of plants and animals. Eur J Plant Pathol 101: 1-13.
63. Zink, R.T., Kemble, R.J., and Chatterjee, A.K. (1984) Transposon Tn5 mutagenesis in Erwinia carotovora ssp. carotovora and Erwinia carotovora ssp. atroseptica. J Bacteriol 157: 809-814.
64. Zhao, X., and McEntee, K. (1990) DNA sequence analysis of the recA genes from Proteus vulgaris, Erwinia carotovora, Shigella flexneri and Escherichia coli B/r. Mol Gen Genet 222: 369-376.