Abstract
The symbiotic pattern of expression of Rhizobium meliloti N2-fixation genes is tightly coupled with the histological organization of the alfalfa root nodule and thus is under developmental control. N2-fixation gene expression is induced very sharply at a particular zone of the nodule called interzone II-III that precedes the zone where N2 fixation takes place. We show here that this coupling can be disrupted, hereby resulting in ectopic expression of N2-fixation genes in the prefixing zone II of the nodule. Uncoupling was obtained either by using a R. meliloti strain in which a mutation rendered N2-fixation gene expression constitutive with respect to oxygen in free-living bacterial cultures or by placing nodules induced by a wild-type R. meliloti strain in a microoxic environment. These results implicate oxygen as a key determinant of the symbiotic pattern of N2-fixation gene expression.
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- Agron P. G., Ditta G. S., Helinski D. R. Oxygen regulation of nifA transcription in vitro. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3506–3510. doi: 10.1073/pnas.90.8.3506. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Batut J., Daveran-Mingot M. L., David M., Jacobs J., Garnerone A. M., Kahn D. fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBO J. 1989 Apr;8(4):1279–1286. doi: 10.1002/j.1460-2075.1989.tb03502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boivin C., Camut S., Malpica C. A., Truchet G., Rosenberg C. Rhizobium meliloti Genes Encoding Catabolism of Trigonelline Are Induced under Symbiotic Conditions. Plant Cell. 1990 Dec;2(12):1157–1170. doi: 10.1105/tpc.2.12.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- David M., Daveran M. L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell. 1988 Aug 26;54(5):671–683. doi: 10.1016/s0092-8674(88)80012-6. [DOI] [PubMed] [Google Scholar]
- Ditta G., Virts E., Palomares A., Kim C. H. The nifA gene of Rhizobium meliloti is oxygen regulated. J Bacteriol. 1987 Jul;169(7):3217–3223. doi: 10.1128/jb.169.7.3217-3223.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischer H. M. Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev. 1994 Sep;58(3):352–386. doi: 10.1128/mr.58.3.352-386.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franssen H. J., Vijn I., Yang W. C., Bisseling T. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol. 1992 May;19(1):89–107. doi: 10.1007/BF00015608. [DOI] [PubMed] [Google Scholar]
- Galinier A., Garnerone A. M., Reyrat J. M., Kahn D., Batut J., Boistard P. Phosphorylation of the Rhizobium meliloti FixJ protein induces its binding to a compound regulatory region at the fixK promoter. J Biol Chem. 1994 Sep 23;269(38):23784–23789. [PubMed] [Google Scholar]
- Gay P., Le Coq D., Steinmetz M., Berkelman T., Kado C. I. Positive selection procedure for entrapment of insertion sequence elements in gram-negative bacteria. J Bacteriol. 1985 Nov;164(2):918–921. doi: 10.1128/jb.164.2.918-921.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilles-Gonzalez M. A., Ditta G. S., Helinski D. R. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature. 1991 Mar 14;350(6314):170–172. doi: 10.1038/350170a0. [DOI] [PubMed] [Google Scholar]
- Gilles-Gonzalez M. A., Gonzalez G. Regulation of the kinase activity of heme protein FixL from the two-component system FixL/FixJ of Rhizobium meliloti. J Biol Chem. 1993 Aug 5;268(22):16293–16297. [PubMed] [Google Scholar]
- Green J. B., Smith J. C. Growth factors as morphogens: do gradients and thresholds establish body plan? Trends Genet. 1991 Aug;7(8):245–250. doi: 10.1016/0168-9525(91)90323-I. [DOI] [PubMed] [Google Scholar]
- Kahn D., Ditta G. Modular structure of FixJ: homology of the transcriptional activator domain with the -35 binding domain of sigma factors. Mol Microbiol. 1991 Apr;5(4):987–997. doi: 10.1111/j.1365-2958.1991.tb00774.x. [DOI] [PubMed] [Google Scholar]
- Kardailsky I., Yang W. C., Zalensky A., van Kammen A., Bisseling T. The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENOD3/14 and is expressed after the leghaemoglobin genes. Plant Mol Biol. 1993 Dec;23(5):1029–1037. doi: 10.1007/BF00021817. [DOI] [PubMed] [Google Scholar]
- Labes M., Rastogi V., Watson R., Finan T. M. Symbiotic nitrogen fixation by a nifA deletion mutant of Rhizobium meliloti: the role of an unusual ntrC allele. J Bacteriol. 1993 May;175(9):2662–2673. doi: 10.1128/jb.175.9.2662-2673.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Layzell D. B., Hunt S., Palmer G. R. Mechanism of Nitrogenase Inhibition in Soybean Nodules : Pulse-Modulated Spectroscopy Indicates that Nitrogenase Activity Is Limited by O(2). Plant Physiol. 1990 Apr;92(4):1101–1107. doi: 10.1104/pp.92.4.1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lois A. F., Weinstein M., Ditta G. S., Helinski D. R. Autophosphorylation and phosphatase activities of the oxygen-sensing protein FixL of Rhizobium meliloti are coordinately regulated by oxygen. J Biol Chem. 1993 Feb 25;268(6):4370–4375. [PubMed] [Google Scholar]
- Quandt J., Hynes M. F. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene. 1993 May 15;127(1):15–21. doi: 10.1016/0378-1119(93)90611-6. [DOI] [PubMed] [Google Scholar]
- Reyrat J. M., David M., Batut J., Boistard P. FixL of Rhizobium meliloti enhances the transcriptional activity of a mutant FixJD54N protein by phosphorylation of an alternate residue. J Bacteriol. 1994 Apr;176(7):1969–1976. doi: 10.1128/jb.176.7.1969-1976.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reyrat J. M., David M., Blonski C., Boistard P., Batut J. Oxygen-regulated in vitro transcription of Rhizobium meliloti nifA and fixK genes. J Bacteriol. 1993 Nov;175(21):6867–6872. doi: 10.1128/jb.175.21.6867-6872.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vasse J., de Billy F., Camut S., Truchet G. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol. 1990 Aug;172(8):4295–4306. doi: 10.1128/jb.172.8.4295-4306.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]