Skip to main content
SpringerLink
Log in

Rhizobium nod genes are involved in the induction of two early nodulin genes in Vicia sativa root nodules

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Nodulin gene expresison was studied in Vicia sativa (common vetch) root nodules induced by several Rhizobium and Agrobacterium strains. An Agrobacterium transconjugant containing a R. leguminosarum symplasmid instead of its Ti-plasmid, that was previously shown to form “empty” nodules on pea, induced nodules on Vicia roots in which nodule cells were infected with bacteria. In the Vicia nodules induced by this transconjugant, two so-called early nodulin genes were found to be expressed, whereas in the nodules formed on pea the expression of only one early nodulin gene was detected. In both cases the majority of the nodulin genes was not expressed.

Apparently, an intracellular location of the bacteria is not sufficient for the induction of the majority of the nodulin genes. All nodulin genes were expressed in nodules induced by cured Rhizobium strains containing cosmid clones that have a 10 kb nod region of the sym-plasmid in common. Since in tumours no nodulin gene expression was found at all, the Agrobacterium chromosome does not contribute to the induction of nodulin genes. Therefore it is concluded that the signal for the induction of the expression of the two Vicia early nodulin genes is encoded by the nod-region, and the signal involved in the induction of all other nodulin genes has to be located outside the sym-plasmid, on the Rhizobium chromosome. The apparent difference in early nodulin gene expression between pea and Vicia is discussed in the light of the usefulness of Agrobacterium transconjugants in the study of nodulin gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bhuvaneswari TV, Turgeon BG, Bauer WD: Early events in the infection of soybean (Glycine max L. Merr) by Rhizobium japonicum. Plant Physiol 66: 1027–1031, 1980.

    Google Scholar 

  2. Bisseling T, van denBos RC, vanKammen A: The effect of ammonium nitrate on the synthesis of nitrogenase and the concentration of leghemoglobin in pea root nodules induced by Rhizobium leguminosarum. Biochim Biophys Acta 539: 1–11, 1978.

    Google Scholar 

  3. Bisseling T, Govers F, Wyndale R, Nap JP, Taanman JW, vanKammen A: Expression of nodulin genes during nodule development from effective and ineffective root nodules. In: Veeger C, Newton WE (eds) Advances in Nitrogen Fixation Research, Nijhoff/Junk, The Hague, 1984, pp 579–586.

    Google Scholar 

  4. Djordjevic MA, Innes RW, Wijffelman CA, Schofield PR, Rolfe BG: Nodulation of specific legumes is controlled by several distinct loci in Rhizobium trifolii. Plant Mol Biol 6: 389–401, 1986.

    Google Scholar 

  5. Downie JA, Hombrecher G, Ma Q-S, Knight CD, Wells B, Johnston AWB: Cloned nodulation genes of R. leguminosarum determine host-specificity. Mol Gen Genet 190: 359–365, 1983.

    Google Scholar 

  6. Firmin JL, Wilson KE, Rossen L, Johnston AWB: Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324: 90–92, 1986.

    Google Scholar 

  7. Franssen HJ, Nap JP, Gloudemans T, Stiekema W, van Dam H, Govers F, Louwerse J, van Kammen A, Bisseling T: Characterization of cDNA for nodulin-75 of soybean: a gene product involved in early stages of root nodule development. Proc Natl Acad Sci USA, in press.

  8. Füller F, Verma DPS: Appearance and accumulation of nodulin mRNAs and their relationship to the effectiveness of root nodules. Plant Mol Biol 3: 21–28, 1984.

    Google Scholar 

  9. Govers F, Gloudemans T, Moerman M, vanKammen A, Bisseling T: Expression of plant genes during the development of pea root nodules. EMBO J 4: 861–867, 1985.

    Google Scholar 

  10. Govers F, Moerman M, Downie JA, Hooykaas P, Franssen HJ, Louwerse J, vanKammen A, Bisseling T: Rhizobium nod genes are involved in inducing an early nodulin gene. Nature 323: 564–566, 1986.

    Google Scholar 

  11. Govers F, Nap JP, van Kammen A, Bisseling T: Nodulins in the developing root nodule. Plant Physiol Biochem, in press.

  12. Hirsch AM, Wilson KJ, Jones JDG, Bang M, Walker VV, Ausubel FM: Rhizobium meliloti nodulation genes allow Agrobacterium tumefaciens and Escherichia coli to form pseudonodules on alfalfa. J Bacteriol 158: 1133–1143, 1984.

    Google Scholar 

  13. Hooykaas PJJ, vanBrussel AAN, denDulk-Ras H, vanSlogteren GMS, Schilperoort RA: Sym-plasmid of Rhizobium trifolii expressed in different rhizobial species and in Agrobacterium tumefaciens. Nature 291: 351–353, 1981.

    Google Scholar 

  14. Hooykaas PJJ, Snijdewint FGM, Schilperoort RA: Identification of the sym-plasmid of Rhizobium leguminosarum strain 1001 and its transfer to and expression in other rhizobia and Agrobacterium tumefaciens. Plasmid 8: 73–82, 1982.

    Google Scholar 

  15. Hooykaas PJJ, Hofker M, denDulk-Ras H, Schilperoort RA: A comparison of virulence determinants in an octopine Ti-plasmid, a nopaline Ti-plasmid, and an Ri-plasmid by complementation analysis of Agrobacterium tumefaciens mutants. Plasmid 11: 195–205, 1984.

    Google Scholar 

  16. Hooykaas PJJ, vanBrussel AAN, vanVeen RJM, Wijffelman CA: The expression of sym-plasmids and Ti-plasmids in rhizobia and agrobacteria. In: Veeger C, Newton WE (eds) Advances in Nitrogen Fixation Research, Nijhoff/Junk, The Hague, 1984, pp 661–666.

    Google Scholar 

  17. 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 46: 335–343, 1986.

    Google Scholar 

  18. Lang-Unnasch N, Dunn K, Ausubel F: Symbiotic nitrogen fixation: developmental genetics of nodule formation. In: Molecular Biology of Development, Cold Spring Harbor Symposia on Quantitative Biology L: 555–563, 1985.

  19. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning, a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1982.

    Google Scholar 

  20. Mulligan JT, Long SR: Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc Natl Acad Sci USA 20: 6609–6613, 1985.

    Google Scholar 

  21. O'Farrell PH: High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007–4021, 1975.

    Google Scholar 

  22. Pelham HRB, Jackson RJ: An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem 67: 247–256, 1976.

    Google Scholar 

  23. Rossen L, Shearman CA, Johnston AWB, Downie JA: The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodA, B, C genes. EMBO J 4: 3369–3373, 1985.

    Google Scholar 

  24. Sengupta-Gopalan C, Pitas JW, Thompson DV, Hoffman LM: Expression of host genes during root nodule development in soybeans. Mol Gen Genet 203: 410–420, 1986.

    Google Scholar 

  25. Stachel SE, Messens E, vanMontagu M, Zambryski P: Identification of the signal molecules produced by wounded plant cells that activate T-DNAs transfer in Agrobacterium tumefaciens. Nature 318: 624–629, 1985.

    Google Scholar 

  26. Stachel SE, Nester EW, Zambryski P: A plant cell factor induces Agrobacterium tumefaciens vir gene expression. Proc Natl Acad Sci USA 83: 379–383, 1986.

    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 157: 134–142, 1984.

    Google Scholar 

  28. vanBrussel AAN, Zaat SAJ, Canter-Cremers HCJ, Wijffelman CA, Pees E, Tak T, Lugtenberg BJJ: Role of plant root exudate and sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch. J Bacteriol 165: 517–522, 1986.

    Google Scholar 

  29. vanKammen A: Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol Biol Rep 2: 43–45, 1984.

    Google Scholar 

  30. Vincent JM: Factors controlling the legume-Rhizobium symbiosis. In: Newton WE, Orme-Johnson WH (eds) Nitrogen Fixation II, University Park Press, Baltimore, 1980, pp 103–129.

    Google Scholar 

  31. Wong CH, Pankhurst E, Kondorosi A, Broughton WJ: Morphology of root nodules and nodule-like structures formed by Rhizobium and Agrobacterium strains containing a Rhizobium meliloti megaplasmid. J Cell Biol 97: 787–794, 1983.

    Google Scholar 

  32. Yanofsky M, Lowe B, Montoya A, Rubin R, Krul W, Gordon M, Nester E: Molecular and genetic analysis of factors controlling host-range in Agrobacterium tumefaciens. Mol Gen Genet 201: 237–246, 1985.

    Google Scholar 

  33. Zaat SAJ, Wijffelman C, Spaink H, van Brussel AAN, Okker RHJ, Lugtenberg BJJ: Induction of the nodA promotor of the R. leguminosarum sym-plasmid pRL1JI by plant flavanones and flavones. J Bacteriol, in press.

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Agricultural University, De Dreijen 11, 6703 BC, Wageningen, The Netherlands

    Marja Moerman, Jan-Peter Nap, Francine Govers, Albert van Kammen & Ton Bisseling

  2. Department of Plant Molecular Biology, University of Leiden, Leiden, The Netherlands

    Rob Schilperoort

Authors
  1. Marja Moerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan-Peter Nap
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francine Govers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rob Schilperoort
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Albert van Kammen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ton Bisseling
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moerman, M., Nap, JP., Govers, F. et al. Rhizobium nod genes are involved in the induction of two early nodulin genes in Vicia sativa root nodules. Plant Mol Biol 9, 171–179 (1987). https://doi.org/10.1007/BF00015649

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00015649

Key words

Search

Navigation