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Rhizobium nodulation genes involved in root hair curling (Hac) are functionally conserved

Plant Molecular Biology volume 4, pages 147–160 (1985)Cite this article

Summary

Five specific transposon-induced nodulation defective (Nod−) mutants from different fast-growing species ofRhizobium were used as the recipients for the transfer of each of several endogenous Sym(biosis) plasmids or for recombinant plasmids that encode early nodulation and host-specificity functions. The Nod− mutants were derived fromR. trifolii, R. meliloti and from a broad-host-rangeRhizobium strain which is able to nodulate both cowpea (tropical) legumes and the non-legumeParasponia. These mutants had several common features (a), they were Nod− on all their known plant hosts, (b), they could not induce root hair curling (Hac−) and (c), the mutations were all located on the endogenous Sym-plasmid of the respective strain. Transfer to these mutants of Sym plasmids (or recombinant plasmids) encoding heterologous information for clover nodulation (pBR1AN, pRt032, pRt038), for pea nodulation (pJB5JI, pRL1JI::Tn1831), for lucerne nodulation (pRmSL26), or for the nodulation of both tropical legumes and non-legumes (pNM4AN), was able to restore root hair curling capacity and in most cases, nodulation capacity of the original plant host(s). This demonstrated a functional conservation of at least some genes involved in root hair curling. Positive hybridization between Nod DNA sequences fromR. trifolii and from a broad-host-rangeRhizobium strain (ANU240) was obtained to other fast-growingRhizobium strains. These results indicate that at least some of the early nodulation functions are common in a broad spectrum ofRhizobium strains.

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References

  1. Banfalvi Z, Sakanyan Y, Koncz C, Kiss A, Dusha I, Kondorosi A: Location of nodulation and nitrogen fixation genes on a high molecular weight plasmid ofRhizobium meliloti. Mol Gen Genet 184:318–325, 1981.

    CAS  PubMed  Google Scholar 

  2. Banfalvi Z, Randhawa GS, Kondorosi E, Kiss A, Kondorosi A: Construction and characterization of R-prime plasmids carrying symbiotic genes ofR. meliloti. Mol Gen Genet 189:129–135, 1983.

    Article  CAS  Google Scholar 

  3. Brewin NJ, Beringer JE, Buchanan-Wollaston AV, Johnston AWB, Hirsch PR: Transfer of symbiotic genes with bacteriocinogenic plasmids inRhizobium leguminosarum. J Gen Microbiol 116:261–270, 1980.

    CAS  Google Scholar 

  4. Buchanan-Wollaston AV, Beringer JE, Brewin NJ, Hirsch PR, Johnston AWB: Isolation of symbiotically defective mutants inRhizobium leguminosarum by insertion of transposon Tn5 into a transmissible plasmid. Mol Gen Genet 178:185–190, 1980.

    Article  CAS  Google Scholar 

  5. Ditta G, Stanfield S, Corbin D, Helinski DR: Broad host range DNA cloning system for gram-negative bacteria; construction of a gene bank ofRhizobium meliloti. Proc Natl Acad Sci USA 77:7347–7351, 1980.

    CAS  PubMed  Google Scholar 

  6. Djordjevic MA, Zurkowski W, Rolfe BG: Plasmids and stability of symbiotic properties ofRhizobium trifolii. J Bacteriol 151:560–568, 1983.

    Google Scholar 

  7. Djordjevic MA, Zurkowski W, Shine J, Rolfe BG: Sym plasmid transfer to various symbiotic mutants ofRhizobium trifolii, R. leguminosarum, andR. meliloti. J Bacteriol 156:1035–1045, 1983.

    CAS  PubMed  Google Scholar 

  8. Downie JA, Ma QS, Knight CD, Hombrecher G, Johnston AWB: Cloning of the symbiotic region ofRhizobium leguminosarum: the nodulation genes are between the nitrogenase genes andnif A-like gene. EMBO J 2:947–952, 1983a.

    CAS  PubMed  Google Scholar 

  9. Downie JA, Hombrecher G, Ma QS, Knight CD, Wells B, Johnston AWB: Cloned nodulation genes ofRhizobium leguminosarum determine host-range specificity. Mol Gen Genet 190:359–365, 1983b.

    Article  CAS  Google Scholar 

  10. Eckhardt T: A rapid method for the identification of plasmid deoxyribonucleic acid in bacteria. Plasmid 1:584–588, 1978.

    Article  CAS  PubMed  Google Scholar 

  11. Hombrecher G, Brewin NJ, Johnston AWB: Linkage of genes for nitrogenase and nodulation ability on plasmids inRhizobium leguminosarum and R. phaseoli. Mol Gen Genet 182:133–136, 1981.

    Article  CAS  Google Scholar 

  12. Hooykaas PJJ, Van Brussel AAN, den Dulk-Ras H, van Slogteren GMS, Schilperoort RA: Sym-plasmid ofRhizobium trifolii expressed in different rhizobial species and inAgrobacterium tumefaciens. Nature 291:351–353, 1981.

    Article  CAS  Google Scholar 

  13. Johnston AWB, Benyon JL, Buchanan-Wollaston AV, Setchell SM, Hirsch PR, Beringer JE: High frequency transfer of nodulating ability between strains and species ofRhizobium. Nature 276:634–636, 1978.

    Article  Google Scholar 

  14. Kondorosi A, Kondorosi E, Pankhurst CE, Broughton WJ, Banfalvi Z: Mobilization of aRhizobium meliloti megaplasmid carrying nodulation and nitrogen fixation genes into other rhizobia andAgrobacterium. Mol Gen Genet 188:433–439, 1982.

    Article  CAS  Google Scholar 

  15. Kondorosi A, Kondorosi E, Banfalvi Z, Broughton WJ, Pankhurst CE, Randhawa GS, Wong C-H, Schell J: Analysis of symbiotic nitrogen fixation genes carried by theRhizobium meliloti megaplasmid. In: Pühler A (ed) Molecular Genetics of the Bacterial-Plant Interaction. Springer-Verlag, Berlin, 1983, pp 55–63.

    Google Scholar 

  16. Kondorosi E, Banfalvi Z, Salska-Kiss C, Kondorosi A: Analysis of symbiotic nitrogen fixation genes carried byRhizobium meliloti megaplasmid. In: Goldberg RB (ed) Plant Molecular Biology, UCLA Symposia on Molecular and Cellular Biology, New Series V.1 XII. Alan R Liss, New York, 1983, pp 259–275.

    Google Scholar 

  17. Long SR, Buikema WJ, Ausubel FM: Cloning ofRhizobium meliloti nodulation genes by direct complementation of Nod− mutants. Nature 298:485–488, 1982.

    Article  CAS  Google Scholar 

  18. Marvel DJ, Kuldau G, Hirsch AM, Park J, Torrey JG, Ausubel FM: Cloning and characterisation of a nodulation locus fromRhizobium parasponium. In: Veeger C, Newton WE (eds) Advances in Nitrogen Fixation Research. Nijhoff/Junk, 1984, p 691.

  19. Morrison NA, Cen YH, Trinick MJ, Shine J, Rolfe BG: Heat curing of a Sym plasmid in a fast-growingRhizobium sp. that is able to nodulate legumes and the non-legumeParasponia sp. J Bacteriol 153:527–531, 1983.

    CAS  PubMed  Google Scholar 

  20. Morrison N, Chen HC, Bassam B, Plazinski J, Ridge R, Rolfe B: Tn5 mutagenesis and symbiotic mutants of a fast-growing cowpeaRhizobium. In: Veeger C, Newton WE (eds) Advances in Nitrogen Fixation Research. Nijhoff/Junk, Pudoc, 1984, p 692.

    Google Scholar 

  21. Pankhurst CE, Broughton WJ, Bachem C, Kondorosi I, Kondorosi A: Identification of Nitrogen Fixation and Nodulation genes on a Large Plasmid from a Broad Host RangeRhizobium sp. In: Pühler A (ed) Molecular Genetics of the Bacterial-Plant Interaction. Springer-Verlag, Berlin, 1983, pp 169–176.

    Google Scholar 

  22. Pühler A, Aguilar MD, Hynes M, Müller P, Klipp W, Priefer U, Simon R, Weber G: Advances in the genetics of free-living and symbiotic nitrogen fixing bacteria. In: Veeger C, Newton WE (eds) Advances in Nitrogen Fixation Research. Nijhoff/Junk, 1984, pp 609–619.

  23. Rolfe BG, Gresshoff PM, Shine J: Rapid screening for symbiotic mutants ofRhizobium and white clover. Plant Sci Lett 19:277–284, 1980.

    Article  Google Scholar 

  24. Rolfe BG, Djordjevic M, Scott KF, Hughes JE, Badenoch-Jones J, Gresshoff PM, Cen Y, Dudman WF, Zurkowski W, Shine J: Analysis of the nodule forming ability of fast-growingRhizobium strains. In: Gibson AH, Newton EW (eds) Current Perspectives in Nitrogen Fixation. Australian Academy of Sciences, Canberra, 1984, pp 142–145.

    Google Scholar 

  25. Ruvkun GB, Ausubel FM: A general method for site-directed mutagenesis in procaryotes. Nature 289:85–88, 1981.

    Article  CAS  PubMed  Google Scholar 

  26. Schofield PR, Djordjevic MA, Rolfe BG, Shine J, Watson JM: A molecular linkage map of nitrogenase and nodulation genes inRhizobium trifolii. Mol Gen Genet 192:459–465, 1983.

    Article  CAS  Google Scholar 

  27. Schofield PR, Ridge RW, Rolfe BG, Shine J, Watson JM: Host-specific nodulation is encoded on a 14 kb DNA fragment inRhizobium trifolii. Plant Mol Biol (in press).

  28. Scott KF, Hughes JE, Gresshoff PM, Beringer JE, Rolfe BG, Shine J: Molecular cloning ofRhizobium trifolii genes involved in symbiotic nitrogen fixation. J Mol Appl Genet 1:315–326, 1982.

    CAS  PubMed  Google Scholar 

  29. Simon R, Weber G, Arnold W, Pühler A: Analysis of plasmid borne genes inRhizobium meliloti by Tn5 mutagenesis. In: Clark and Stephens (eds) Proceedings of the 8th North American Rhizobium Conference. Winnipeg, Canada: University of Manitoba Press, 1982, pp 67–89.

    Google Scholar 

  30. Southern EM: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–518, 1975.

    CAS  PubMed  Google Scholar 

  31. Vincent JM: A manual for the practical study of root-nodule bacteria. IBP Handbook No. 15 Blackwell Scientific Publications, Oxford, 1970.

  32. Vincent JM: Factors controlling the legume-Rhizobium symbiosis. In: Newton WE, Orme-Johnson WH (eds) Nitrogen Fixation 2. University Park Press, Baltimore, 1980, pp 103–129.

    Google Scholar 

  33. Watson JM, Schofield PR, Ridge RW, Djordjevic MA, Rolfe BG, Shine J: Molecular cloning and analysis of a region of the Sym plasmid ofRhizobium trifolii encoding clover nodulation functions. In: Goldberg RB (ed) Plant Molecular Biology, UCLA Symposia on Molecular and Cellular Biology, new Series Vol XII. Alan R Liss, New York, 1983, pp 303–318.

    Google Scholar 

  34. Yao PY, Vincent JM: Host specificity in the root hair ‘curling factor’ ofRhizobium spp. Aust J Biol Sci 22:413–423, 1969.

    Google Scholar 

  35. Yao PY, Vincent JM: Factors responsible for the curling and branching of clover root hairs byRhizobium. Plant and Soil 45:1–16, 1976.

    Article  Google Scholar 

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Affiliations

  1. Department of Genetics, Research School of Biological Sciences, Australian National University, P.O. Box 475, 2601, Canberra City, Australia

    M. A. Djordjevic, P. R. Schofield, R. W. Ridge, N. A. Morrison, B. J. Bassam, J. Plazinski, J. M. Watson & B. G. Rolfe

  2. Centre for Recombinant DNA Research, Research School of Biological Sciences, Australian National University, P.O. Box 475, 2601, Canberra City, Australia

    J. M. Watson

Authors
  1. M. A. Djordjevic
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  2. P. R. Schofield
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  3. R. W. Ridge
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  4. N. A. Morrison
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  5. B. J. Bassam
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  6. J. Plazinski
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  7. J. M. Watson
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  8. B. G. Rolfe
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Djordjevic, M.A., Schofield, P.R., Ridge, R.W. et al. Rhizobium nodulation genes involved in root hair curling (Hac) are functionally conserved. Plant Mol Biol 4, 147–160 (1985). https://doi.org/10.1007/BF02418762

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  • DOI: https://doi.org/10.1007/BF02418762

Keywords

  • Rhizobium Nod genes
  • functional conservation