Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 Dec;170(12):5718–5727. doi: 10.1128/jb.170.12.5718-5727.1988

Interference between Rhizobium meliloti and Rhizobium trifolii nodulation genes: genetic basis of R. meliloti dominance.

F Debellé 1, F Maillet 1, J Vasse 1, C Rosenberg 1, F de Billy 1, G Truchet 1, J Dénarié 1, F M Ausubel 1
PMCID: PMC211674  PMID: 2848012

Abstract

Transfer of an IncP plasmid carrying the Rhizobium meliloti nodFE, nodG, and nodH genes to Rhizobium trifolii enabled R. trifolii to nodulate alfalfa (Medicago sativa), the normal host of R. meliloti. Using transposon Tn5-linked mutations and in vitro-constructed deletions of the R. meliloti nodFE, nodG, and nodH genes, we showed that R. meliloti nodH was required for R. trifolii to elicit both root hair curling and nodule initiation on alfalfa and that nodH, nodFE, and nodG were required for R. trifolii to elicit infection threads in alfalfa root hairs. Interestingly, the transfer of the R. meliloti nodFE, nodG, and nodH genes to R. trifolii prevented R. trifolii from infecting and nodulating its normal host, white clover (Trifolium repens). Experiments with the mutated R. meliloti nodH, nodF, nodE, and nodG genes demonstrated that nodH, nodF, nodE, and possibly nodG have an additive effect in blocking infection and nodulation of clover.

Full text

PDF
5718

Images in this article

5721Image
on p.5721
5722Image
on p.5722
5724Image
on p.5724

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bánfalvi Z., Sakanyan V., Koncz C., Kiss A., Dusha I., Kondorosi A. Location of nodulation and nitrogen fixation genes on a high molecular weight plasmid of R. meliloti. Mol Gen Genet. 1981;184(2):318–325. doi: 10.1007/BF00272925. [DOI] [PubMed] [Google Scholar]
  2. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  3. Datta N., Hedges R. W., Shaw E. J., Sykes R. B., Richmond M. H. Properties of an R factor from Pseudomonas aeruginosa. J Bacteriol. 1971 Dec;108(3):1244–1249. doi: 10.1128/jb.108.3.1244-1249.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Debellé F., Rosenberg C., Vasse J., Maillet F., Martinez E., Dénarié J., Truchet G. Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J Bacteriol. 1986 Dec;168(3):1075–1086. doi: 10.1128/jb.168.3.1075-1086.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Debellé F., Sharma S. B. Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation. Nucleic Acids Res. 1986 Sep 25;14(18):7453–7472. doi: 10.1093/nar/14.18.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ditta G., Stanfield S., Corbin D., Helinski D. R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. doi: 10.1073/pnas.77.12.7347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Djordjevic M. A., Zurkowski W., Shine J., Rolfe B. G. Sym plasmid transfer to various symbiotic mutants of Rhizobium trifolii, R. leguminosarum, and R. meliloti. J Bacteriol. 1983 Dec;156(3):1035–1045. doi: 10.1128/jb.156.3.1035-1045.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Figurski D. H., Meyer R. J., Helinski D. R. Suppression of Co1E1 replication properties by the Inc P-1 plasmid RK2 in hybrid plasmids constructed in vitro. J Mol Biol. 1979 Sep 25;133(3):295–318. doi: 10.1016/0022-2836(79)90395-4. [DOI] [PubMed] [Google Scholar]
  9. Fisher R. F., Swanson J. A., Mulligan J. T., Long S. R. Extended Region of Nodulation Genes in Rhizobium meliloti 1021. II. Nucleotide Sequence, Transcription Start Sites and Protein Products. Genetics. 1987 Oct;117(2):191–201. doi: 10.1093/genetics/117.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gabriel D. W., Burges A., Lazo G. R. Gene-for-gene interactions of five cloned avirulence genes from Xanthomonas campestris pv. malvacearum with specific resistance genes in cotton. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6415–6419. doi: 10.1073/pnas.83.17.6415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Honma M. A., Ausubel F. M. Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory gene. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8558–8562. doi: 10.1073/pnas.84.23.8558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Horvath B., Bachem C. W., Schell J., Kondorosi A. Host-specific regulation of nodulation genes in Rhizobium is mediated by a plant-signal, interacting with the nodD gene product. EMBO J. 1987 Apr;6(4):841–848. doi: 10.1002/j.1460-2075.1987.tb04829.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horvath B., Kondorosi E., John M., Schmidt J., Török I., Györgypal Z., Barabas I., Wieneke U., Schell J., Kondorosi A. Organization, structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa. Cell. 1986 Aug 1;46(3):335–343. doi: 10.1016/0092-8674(86)90654-9. [DOI] [PubMed] [Google Scholar]
  14. Leigh J. A., Signer E. R., Walker G. C. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6231–6235. doi: 10.1073/pnas.82.18.6231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Martin M. O., Long S. R. Generalized transduction in Rhizobium meliloti. J Bacteriol. 1984 Jul;159(1):125–129. doi: 10.1128/jb.159.1.125-129.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol. 1982 Jan;149(1):114–122. doi: 10.1128/jb.149.1.114-122.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mulligan J. T., Long S. R. Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6609–6613. doi: 10.1073/pnas.82.19.6609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Putnoky P., Kondorosi A. Two gene clusters of Rhizobium meliloti code for early essential nodulation functions and a third influences nodulation efficiency. J Bacteriol. 1986 Sep;167(3):881–887. doi: 10.1128/jb.167.3.881-887.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Putnoky P., Kondorosi A. Two gene clusters of Rhizobium meliloti code for early essential nodulation functions and a third influences nodulation efficiency. J Bacteriol. 1986 Sep;167(3):881–887. doi: 10.1128/jb.167.3.881-887.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rosenberg C., Boistard P., Dénarié J., Casse-Delbart F. Genes controlling early and late functions in symbiosis are located on a megaplasmid in Rhizobium meliloti. Mol Gen Genet. 1981;184(2):326–333. doi: 10.1007/BF00272926. [DOI] [PubMed] [Google Scholar]
  21. Ruvkun G. B., Ausubel F. M. A general method for site-directed mutagenesis in prokaryotes. Nature. 1981 Jan 1;289(5793):85–88. doi: 10.1038/289085a0. [DOI] [PubMed] [Google Scholar]
  22. Schmidhauser T. J., Helinski D. R. Regions of broad-host-range plasmid RK2 involved in replication and stable maintenance in nine species of gram-negative bacteria. J Bacteriol. 1985 Oct;164(1):446–455. doi: 10.1128/jb.164.1.446-455.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Staskawicz B. J., Dahlbeck D., Keen N. T. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6024–6028. doi: 10.1073/pnas.81.19.6024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Swanson J. A., Tu J. K., Ogawa J., Sanga R., Fisher R. F., Long S. R. Extended Region of Nodulation Genes in Rhizobium meliloti 1021. I. Phenotypes of Tn5 Insertion Mutants. Genetics. 1987 Oct;117(2):181–189. doi: 10.1093/genetics/117.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thomas C. M., Smith C. A. Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. Annu Rev Microbiol. 1987;41:77–101. doi: 10.1146/annurev.mi.41.100187.000453. [DOI] [PubMed] [Google Scholar]
  26. Truchet G., Debellé F., Vasse J., Terzaghi B., Garnerone A. M., Rosenberg C., Batut J., Maillet F., Dénarié J. Identification of a Rhizobium meliloti pSym2011 region controlling the host specificity of root hair curling and nodulation. J Bacteriol. 1985 Dec;164(3):1200–1210. doi: 10.1128/jb.164.3.1200-1210.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Truchet G., Rosenberg C., Vasse J., Julliot J. S., Camut S., Denarie J. Transfer of Rhizobium meliloti pSym genes into Agrobacterium tumefaciens: host-specific nodulation by atypical infection. J Bacteriol. 1984 Jan;157(1):134–142. doi: 10.1128/jb.157.1.134-142.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES