The Rhizobium leguminosarum bv. trifolii RosR: Transcriptional regulator involved in exopolysaccharide production

Molecular Plant-Microbe Interactions

Volumn 20, Issue 7, 2007, Pages 867-881

  Janczarek, Monika ^a   Skorupska, Anna ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

Catabolic repression; Zinc finger protein

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; REPRESSOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; RHIZOBIUM LEGUMINOSARUM; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; CLONING, MOLECULAR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MUTATION; POLYSACCHARIDES, BACTERIAL; PROTEIN BINDING; REPRESSOR PROTEINS; RHIZOBIUM LEGUMINOSARUM; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM LEGUMINOSARUM BV. TRIFOLII; TRIFOLIUM;

EID: 34250668344     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-7-0867     Document Type: Article

References (62)

1. Araujo, R. S., Robleto, E. A., and Handelsman, J. 1994. A hydrophobic mutant of Rhizobium etli altered in nodulation competitiveness and growth in the rhizosphere. Appl. Environ. Microbiol. 60:1430-1436.
2. Barnett, M. J., and Long, S. R. 1997. Identification and characterization of a gene on Rhizobium meliloti pSymA, syrB, that negatively affects syrM expression. Mol. Plant-Microbe Interact. 10:550-559.
3. Becker, A., and Pühler, A. 1998. Production of exopolysaccharides. Pages 97-118 in: Rhizobiaceae. H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas, eds. Kluwer Academic Publishers, Dordrecht, London.
4. Becker, A., Rüberg, S., Küster, H., Roxlau, A. A., Keller, M., Ivashina, T., Cheng, H., Walker, G. C., and Pühler, A. 1997. The 32-kilobase exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: Genetic organization and properties of the encoded gene products. J. Bacteriol. 179:1375-1384.
5. Berg, J. M., and Shi, Y. 1996. The galvanization of biology: A growing appreciation for the roles of zinc. Science 271:1081-1085.
6. Bertram-Drogatz, P. A., Rüberg, S., and Becker, A. 1997. The regulatory protein MucR binds to a short DNA region located upstream of the mucR coding region in Rhizobium meliloti. Mol. Gen. Genet. 254:529-538.
7. Bertram-Drogatz, P. A., Quester, I., Becker, A., and Pühler, A. 1998. The Sinorhizobium meliloti MucR protein, which is essential for the production of high-molecular-weight succinoglycan exopolysaccharide, binds to short DNA regions upstream of exoH and exoY. Mol. Gen. Genet. 257:433-441.
8. Bittinger, M. A., and Handelsman, J. 2000. Identification of genes in the RosR regulon of Rhizobium etli. J. Bacteriol. 182:1706-1713.
9. Bittinger, M. A., Milner, J. L., Saville, B. J., and Handelsman J. 1997. rosR, a determinant of nodulation competitiveness in Rhizobium etli. Mol. Plant-Microbe Interact. 10:180-186.
10. Borthakur, D., and Johnston, A. W. B. 1987. Sequence of psi, a gene of the symbiotic plasmid of Rhizobium phaseoli which inhibits exopolysaccharide synthesis and nodulation and demonstration that its transcription is inhibited by psr, another gene on the symbiotic plasmid. Mol. Gen. Genet. 207:149-154.
11. Borthakur, D., Barker, R. F., Latchford, J. W., Rossen, L., and Johnston, A. W. B. 1988. Analysis of pss genes of Rhizobium leguminosarum required for exopolysaccharide synthesis and nodulation of peas: Their primary structure and their interaction with psi and other nodulation genes. Mol. Gen. Genet. 213:155-162.
12. Brightwell, G., Hussain, H., Tiburtius, K., Yeoman, K. H., and Johnston, A. W. B. 1995. Pleiotropic effects of regulatory ros mutants of Agrobacterium radiobacter and their interaction with Fe and glucose. Mol. Plant-Microbe Interact. 8:747-754.
13. Brown, C. M., and Dilworth, M. J. 1975. Ammonia assimilation by Rhizobium cultures and bacteroids. J. Gen. Microbiol. 86:39-48.
14. Casse, F., Boucher, C., Julliot, J. S., Michel, M., and Denarie, J. 1979. Identification and characterization of large plasmids in Rhizobium meliloti using agarose gel electrophoresis. J. Gen. Microbiol. 113:229-242.
15. Chakravorty, A. K., Zurkowski, W., Shine, J., and Rolfe, B. G. J. 1982. Symbiotic nitrogen fixation: Molecular cloning of Rhizobium genes involved in exopolysaccharide synthesis and effective nodulation. J. Mol. Appl. Genet. 1:585-596.
16. Chou, A. Y., Archdeacon, J., and Kado, C. I. 1998. Agrobacterium transcriptional regulator Ros is a prokaryotic zinc finger protein that regulates the plant oncogen ipt. Proc. Natl. Acad. Sci. U.S.A. 95:5293-5298.
17. Cooley, M. B., D'Souza, M. R., and Kado, C. I. 1991. The virC and virD operons of the Agrobacierium Ti plasmid are regulated by the ros chromosomal gene: Analysis of the cloned ros gene. J. Bacteriol. 173:2608-2616.
18. D'Souza-Ault, M. R., Cooley, M. B., and Kado, C. I. 1993. Analysis of the repressor of Agrobacierium virC and virD operons: molecular intercommunication between plasmid and chromosomal genes. J. Bacteriol. 175:3486-3490.
19. Dusha, I., Olah, B., Szegletes, Z., Erdei, L, and Kondorosi, A. 1999. syrM involved in the determination of the amount and ratio of the two forms of the acidic exopolysaccharide EPSI in Rhizobium meliloti. Mol. Plant-Microbe Interact. 12:755-765.
20. Ebright, R. H., Ebright, Y. W., and Gunasekera, A. 1989. Consensus DNA site for the Escherichia coli catabolite gene activator protein (CAP): CAP exhibits a 450-fold higher affinity for the consensus DNA site than for the E. coli iac DNA site. Nucleic Acids Res. 17(24):10295-10305.
21. Figurski, D. H., and Helinski, D. R. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76:1648-1652.
22. Gaal, T., Bartlett, M. S., Ross, W., Turnbough, C. L., Jr., and Gourse, R. L. 1997. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278:2092-2097.
23. Glazebrook, J., and Walker, G. C. 1989. A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 56:661-672.
24. González, V., Santamaría, R. I., Bustos, P., Hernández-González, I., Medrano-Soto, A., Moreno-Hagelsieb, G., Chandra Janga, S., Ramírez, M. A., Jiménez-Jacinto, V., Collado-Vides, J., and Dávila, G. 2006. The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons. Proc. Natl. Acad. Sci. U.S.A. 103:3834-3839.
25. Harman, J. G. 2001. Allosteric regulation of the cAMP receptor protein. Biochem. Biophys. Acta 1547:1-17.
26. Hollingsworth, R. I., Dazzo, F. B., Hallenga, K., and Musselman, B. 1988. The complete structure of the trifolim A lectin-binding capsular polysaccharide of Rhizobium trifolii 843. Carbohydr. Res. 172:97-112.
27. Janczarek, M., and Skorupska, A. 2004. Regulation of pssA and pssB gene expression in R. leguminosarum bv. trifolii in response to environmental factors. Antonie Leeuwenhook 85:217-227.
28. Katzen, F., Becker, A., Ielmini, M. V., Oddo, C. G., and Ielpi, L. 1999. New mobilizable vectors suitable for gene replacement in gram-negative bacteria and their use in mapping of the 3′ end of the Xanthomonas campestris pv. campestris gum operon. Appl. Environ. Microbiol. 65:278-282
29. Keller, M., Roxlau, A., Wenig, W. M., Schmidt, M., Quandt, J., Niehaus, K., Jording, D., Arnold, W., and Pühler A. 1995. Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan. Mol. Plant-Microbe Interact. 8:267-275.
30. Kolb, A., Busby, S., Buc, H., Garges, S., and Adhya, S. 1993. Transcriptional regulation by cAMP and its receptor protein. Annu. Rev. Biochem. 62:749-795.
31. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
32. Lai, E. M., and Kado, C. I. 1998. Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J. Bacteriol. 180:2711-2717.
33. Latchford, J. W., Borthakur, D., and Johnston, A. W. B. 1991. The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface. Mol. Microbiol. 5:2107-2114.
34. Lloyd, A. L., Marshall, B. J., and Mee, B. J. 2005. Identifying cloned Helicobacter pylori promoters by primer extension using a FAM-labelled primer and GeneScan analysis. J. Microbiol. Methods 60:291-298.
35. Loewus, F. A. 1952. Improvement in the anthrone method for determination of carbohydrates. Anal. Chem. 24:219.
36. Long, S. R. 2001. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol. 125:69-72.
37. Martin, M., Llorel, J., Sanchez-Contreras, M., Bonilla, I., and Rivilla, R. 2000. MucR is necessary for galacloglucan production in Sinorhizobium meliloti EFB1. Mol. Plant-Microbe Interact. 13:129-135.
38. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
39. Mimmack, M. L., Borthakur, D., Jones, M. A., Downie, J. A., and Johnston, A. W. B. 1994a. The psi operon of Rhizobium leguminosarum biovar phaseoli: Identification of two genes whose products are located at the bacterial cell surface. Microbiology 140:1223-1229.
40. Mimmack, M. L., Hong, G. F., and Johnston, A. W. B. 1994b. Sequence and regulation of psrA, a gene on the Sym plasmid of Rhizobium leguminosarum biovar phaseoli which inhibits transcription of the psi genes. Microbiology 140:455-461.
41. Noel, K. D., Sanchez, A., Fernandez, L., Leemans, J., and Cevallos, M. A. 1984. Rhizobium pliaseoli symbiotic mutants with transposon Tn5 insertions. J. Bacteriol. 158:148-155.
42. Pabo, C., and Sauer, R. T. 1992. Transcription factors: Structural families and principles of DNA recognition. Annu. Rev. Biochem. 61:1053-1095.
43. Perret, X., Staehelin, C., and Broughton, W. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180-201.
44. Pollock, T. J., van Workum, W. A. T., Thorne, L., Mikolajczak, M. J., Yamazaki, M., Kijne, J. W., and Armentrout, R. W. 1998. Assignment of biochemical functions to glycosyl transferase genes which are essential for biosynthesis of exopolysaccharides in Sphingomonas strain S88 and Rhizobium leguminosarum. J. Bacteriol. 180:586-593.
45. Quester, I., and Becker, A. 2004. Four promoters subject to regulation by ExoR and PhoB direct transcription of the Sinorhizobium meliloti exoYFQ operon involved in the biosynthesis of succinoglycan. J. Mol. Microbiol. Biotechnol. 7:115-132.
46. Reeve, W. G., Dilworth, M. J., Tiwari, R. P., and Glenn, A. R. 1997. Regulation of exopolysaccharide production in Rhizobium leguminosarum biovar viciae WSM710 involves exoR. Microbiology 143:1951-1958.
47. Rolfe, B. G., Carlson, R. W., Ridge, R. W., Dazzo, R. W., Mateos, F. B., and Pankhurst, C. E. 1996. Defective infection and nodulation of clovers by exopolysaccharide mutants of Rhizobium leguminosarum bv. trifolii. Aust. J. Plant Physiol. 23:285-303.
48. Rüberg, S., Pühler, A., and Becker, A. 1999. Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology 145:603-611.
49. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
50. Schell, M. A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597-626.
51. Sharypova, L., Yurgel, S., Keller, M., Simarov, B., Pühler, A., and Becker A. 1999. The eff-482 locus of Sinorhizobium meliloti CXMI-105 that influences symbiotic effectiveness consists of three genes encoding an endoglycanase, a transcriptional regulator and an adenylate cyclase. Mol. Gen. Genet. 261:1032-1044.
52. Skorupska, A., Białek, U., Urbanik-Sypniewska, T., and van Lammeren, A. 1995. Two types of nodules induced on Trifolium pratense by mutants of Rhizobium leguminosarum bv. trifolii deficient in exopolysaccharide production. J. Plant Physiol. 147:93-100.
53. Skorupska, A., Janczarek, M., Marczak, M., Mazur, A., and Krol, J. 2006. Rhizobial exopolysaccharides: Genetic control and symbiotic functions. Microb. Cell Fact. 16:7.
54. 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.
55. Stanley, J., Dowling, D. N., Stucker, M., and Broughton W. J. 1987. Screening costramid libraries for chromosomal genes: An alternative interspecific hybridization method. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 48:25-30.
56. Tellez-Sosa, J., Soberon, N., Vega-Segura, A., Torres-Marquez, M. E., and Cevallos, M. A. 2002. The Rhizobium etli cyaC product: Characterization of a novel adenylate cyclase class. J. Bacteriol. 184:3560-3568.
57. van Workum, W. A., Canter Cremers, H. C. J., Wijfjes, A. H. M., van der Kolk, C., Wijffelman, C. A., and Kijne, J. W. 1997. Cloning and characterization of four genes of Rhizobium leguminosarum bv. trifolii involved in exopolysaccharide production and nodulation. Mol. Plant-Microbe Interact. 10:290-301.
58. Vincent, J. M. 1970. A manual for the practical study of root nodule bacteria. International Biological Program Handbook No. 15. Blackwell Scientific Publications, Ltd., Oxford.
59. Wösten, M. M. 1998. Eubacterial sigma-factors. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 22:127-150.
60. Young, J. P., Crossman, L. C., Johnston, A. W., Thomson, N. R., Ghazoui, Z. F., Hull, K. H., Wexler, M., Curson, A. R., Todd, J. D., Poole, P. S., Mauchline, T. H., East, A. K., Quail, M. A., Churcher, C., Arrowsmith, C., Cherevach, I., Chillingworth, T., Clarke, K., Cronin, A., Davis, P., Praser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Mungall, K., Norbertczak, H., Rabbinowitsch, E., Sanders, M., Simmonds, M., Whitehead, S., and Parkhill, J. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7(4):R34.
61. Zevenhuizen, L. P. T. M. 1986. Selective synthesis of polysaccharides by Rhizobium trifolii. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 35:43-47.
62. Zhan, H. J., Levery, S. B., Lee, C. C., and Leigh J. A. 1989. A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion. Proc. Natl. Acad. Sci. U.S.A. 86:3055-3059.