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. 1995 Sep;61(9):3422–3429. doi: 10.1128/aem.61.9.3422-3429.1995

Cloning of nod gene regions from mesquite rhizobia and bradyrhizobia and nucleotide sequence of the nodD gene from mesquite rhizobia.

P M Thomas 1, K F Golly 1, R A Virginia 1, J W Zyskind 1
PMCID: PMC167620  PMID: 7574650

Abstract

Nitrogen-fixing symbiosis between bacteria and the tree legume mesquite (Prosopis glandulosa) is important for the maintenance of many desert ecosystems. Genes essential for nodulation and for extending the host range to mesquite were isolated from cosmid libraries of Rhizobium (mesquite) sp. strain HW17b and Bradyrhizobium (mesquite) sp. strain HW10h and were shown to be closely linked. All of the cosmid clones of rhizobia that extended the host range of Rhizobium (Parasponia) sp. strain NGR234CS to mesquite also supported nodulation of a Sym- mesquite strain. The cosmid clones of bradyrhizobia that extended the host range of Rhizobium (Parasponia) sp. strain NGR234CS to mesquite were only able to confer nodulation ability in the Sym- mesquite strain if they also contained a nodD-hybridizing region. Subclones containing just the nodD genes of either genus did not extend the host range of Rhizobium (Parasponia) sp. to mesquite, indicating that the nodD gene is insufficient for mesquite nodulation. The nodD gene region is conserved among mesquite-nodulating rhizobia regardless of the soil depth from which they were collected, indicating descent from a common ancestor. In a tree of distance relationships, the NodD amino acid sequence from mesquite rhizobia clusters with homologs from symbionts that can infect both herbaceous and tree legumes, including Rhizobium tropici, Rhizobium leguminosarum bv; phaseoli, Rhizobium loti, and Bradyrhizobium japonicum.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Atkinson E. M., Long S. R. Homology of Rhizobium meliloti NodC to polysaccharide polymerizing enzymes. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):439–442. doi: 10.1094/mpmi-5-439. [DOI] [PubMed] [Google Scholar]
  3. Borthakur D., Lamb J. W., Johnston A. W. Identification of two classes of Rhizobium phaseoli genes required for melanin synthesis, one of which is required for nitrogen fixation and activates the transcription of the other. Mol Gen Genet. 1987 Apr;207(1):155–160. doi: 10.1007/BF00331503. [DOI] [PubMed] [Google Scholar]
  4. Brennan R. G., Matthews B. W. The helix-turn-helix DNA binding motif. J Biol Chem. 1989 Feb 5;264(4):1903–1906. [PubMed] [Google Scholar]
  5. Burn J. E., Hamilton W. D., Wootton J. C., Johnston A. W. Single and multiple mutations affecting properties of the regulatory gene nodD of Rhizobium. Mol Microbiol. 1989 Nov;3(11):1567–1577. doi: 10.1111/j.1365-2958.1989.tb00142.x. [DOI] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Flores M., González V., Pardo M. A., Leija A., Martínez E., Romero D., Piñero D., Dávila G., Palacios R. Genomic instability in Rhizobium phaseoli. J Bacteriol. 1988 Mar;170(3):1191–1196. doi: 10.1128/jb.170.3.1191-1196.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Friedman A. M., Long S. R., Brown S. E., Buikema W. J., Ausubel F. M. Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene. 1982 Jun;18(3):289–296. doi: 10.1016/0378-1119(82)90167-6. [DOI] [PubMed] [Google Scholar]
  10. Györgypal Z., Kiss G. B., Kondorosi A. Transduction of plant signal molecules by the Rhizobium NodD proteins. Bioessays. 1991 Nov;13(11):575–581. doi: 10.1002/bies.950131106. [DOI] [PubMed] [Google Scholar]
  11. Göttfert M. Regulation and function of rhizobial nodulation genes. FEMS Microbiol Rev. 1993 Jan;10(1-2):39–63. doi: 10.1111/j.1574-6968.1993.tb05863.x. [DOI] [PubMed] [Google Scholar]
  12. Hahn M., Hennecke H. Mapping of a Bradyrhizobium japonicum DNA Region Carrying Genes for Symbiosis and an Asymmetric Accumulation of Reiterated Sequences. Appl Environ Microbiol. 1987 Sep;53(9):2247–2252. doi: 10.1128/aem.53.9.2247-2252.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Henikoff S., Haughn G. W., Calvo J. M., Wallace J. C. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. doi: 10.1073/pnas.85.18.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  15. Jenkins M. B., Virginia R. A., Jarrell W. M. Rhizobial Ecology of the Woody Legume Mesquite (Prosopis glandulosa) in the Sonoran Desert. Appl Environ Microbiol. 1987 Jan;53(1):36–40. doi: 10.1128/aem.53.1.36-40.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. John M., Röhrig H., Schmidt J., Wieneke U., Schell J. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):625–629. doi: 10.1073/pnas.90.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kahn M. L., Timblin C. R. Gene fusion vehicles for the analysis of gene expression in Rhizobium meliloti. J Bacteriol. 1984 Jun;158(3):1070–1077. doi: 10.1128/jb.158.3.1070-1077.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kofoid E. C., Parkinson J. S. Transmitter and receiver modules in bacterial signaling proteins. Proc Natl Acad Sci U S A. 1988 Jul;85(14):4981–4985. doi: 10.1073/pnas.85.14.4981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuykendall L. D. Transfer of R factors to and between genetically marked sublines of Rhizobium japonicum. Appl Environ Microbiol. 1979 May;37(5):862–866. doi: 10.1128/aem.37.5.862-866.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Martínez-Romero E., Segovia L., Mercante F. M., Franco A. A., Graham P., Pardo M. A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol. 1991 Jul;41(3):417–426. doi: 10.1099/00207713-41-3-417. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Peters N. K., Frost J. W., Long S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science. 1986 Aug 29;233(4767):977–980. doi: 10.1126/science.3738520. [DOI] [PubMed] [Google Scholar]
  24. Putnoky P., Petrovics G., Kereszt A., Grosskopf E., Ha D. T., Bánfalvi Z., Kondorosi A. Rhizobium meliloti lipopolysaccharide and exopolysaccharide can have the same function in the plant-bacterium interaction. J Bacteriol. 1990 Sep;172(9):5450–5458. doi: 10.1128/jb.172.9.5450-5458.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Relić B., Talmont F., Kopcinska J., Golinowski W., Promé J. C., Broughton W. J. Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant Microbe Interact. 1993 Nov-Dec;6(6):764–774. doi: 10.1094/mpmi-6-764. [DOI] [PubMed] [Google Scholar]
  26. Schlaman H. R., Okker R. J., Lugtenberg B. J. Regulation of nodulation gene expression by NodD in rhizobia. J Bacteriol. 1992 Aug;174(16):5177–5182. doi: 10.1128/jb.174.16.5177-5182.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smith D. W. A complete, yet flexible, system for DNA/protein sequence analysis using VAX/VMS computers. Comput Appl Biosci. 1988 Mar;4(1):212–212. doi: 10.1093/bioinformatics/4.1.212. [DOI] [PubMed] [Google Scholar]
  28. Spaink H. P. Rhizobial lipo-oligosaccharides: answers and questions. Plant Mol Biol. 1992 Dec;20(5):977–986. doi: 10.1007/BF00027167. [DOI] [PubMed] [Google Scholar]
  29. Thomas P. M., Golly K. F., Zyskind J. W., Virginia R. A. Variation of clonal, mesquite-associated rhizobial and bradyrhizobial populations from surface and deep soils by symbiotic gene region restriction fragment length polymorphism and plasmid profile analysis. Appl Environ Microbiol. 1994 Apr;60(4):1146–1153. doi: 10.1128/aem.60.4.1146-1153.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Waldon H. B., Jenkins M. B., Virginia R. A., Harding E. E. Characteristics of woodland rhizobial populations from surface- and deep-soil environments of the sonoran desert. Appl Environ Microbiol. 1989 Dec;55(12):3058–3064. doi: 10.1128/aem.55.12.3058-3064.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Winsor B. A. A nod at differentiation: the nodD gene product and initiation of Rhizobium nodulation. Trends Genet. 1989 Jul;5(7):199–201. doi: 10.1016/0168-9525(89)90079-6. [DOI] [PubMed] [Google Scholar]

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