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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Jan 15;88(2):637–641. doi: 10.1073/pnas.88.2.637

The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans.

M J Sadowsky 1, P B Cregan 1, M Gottfert 1, A Sharma 1, D Gerhold 1, F Rodriguez-Quinones 1, H H Keyser 1, H Hennecke 1, G Stacey 1
PMCID: PMC50867  PMID: 1988958

Abstract

Several soybean genotypes have been identified which specifically exclude nodulation by members of Bradyrhizobium japonicum serocluster 123. We have identified and sequenced a DNA region from B. japonicum strain USDA 110 which is involved in genotype-specific nodulation of soybeans. This 2.3-kilobase region, cloned in pMJS12, allows B. japonicum serocluster 123 isolates to form nodules on plants of serogroup 123-restricting genotypes. The nodules, however, were ineffective for symbiotic nitrogen fixation. The nodulation-complementing region is located approximately 590 base pairs transcriptionally downstream from nodD2. The 5' end of pMJS12 contains a putative open reading frame (ORF) of 710 base pairs, termed nolA. Transposon Tn3-HoHo mutations only within the ORF abolished nodulation complementation. The N terminus of the predicted nolA gene product has strong similarity with the N terminus of MerR, the regulator of mercury resistance genes. Translational lacZ fusion experiments indicated that nolA was moderately induced by soybean seed extract and the isoflavone genistein. Restriction fragments that hybridize to pMJS12 were detected in genomic DNAs from both nodulation-restricted and -unrestricted strains.

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Selected References

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  1. Banfalvi Z., Nieuwkoop A., Schell M., Besl L., Stacey G. Regulation of nod gene expression in Bradyrhizobium japonicum. Mol Gen Genet. 1988 Nov;214(3):420–424. doi: 10.1007/BF00330475. [DOI] [PubMed] [Google Scholar]
  2. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988 Nov 25;16(22):10881–10890. doi: 10.1093/nar/16.22.10881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cregan P. B., Keyser H. H., Sadowsky M. J. Host Plant Effects on Nodulation and Competitiveness of the Bradyrhizobium japonicum Serotype Strains Constituting Serocluster 123. Appl Environ Microbiol. 1989 Oct;55(10):2532–2536. doi: 10.1128/aem.55.10.2532-2536.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Davis E. O., Evans I. J., Johnston A. W. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol Gen Genet. 1988 Jun;212(3):531–535. doi: 10.1007/BF00330860. [DOI] [PubMed] [Google Scholar]
  5. Deshmane N., Stacey G. Identification of Bradyrhizobium nod genes involved in host-specific nodulation. J Bacteriol. 1989 Jun;171(6):3324–3330. doi: 10.1128/jb.171.6.3324-3330.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dodd I. B., Egan J. B. Systematic method for the detection of potential lambda Cro-like DNA-binding regions in proteins. J Mol Biol. 1987 Apr 5;194(3):557–564. doi: 10.1016/0022-2836(87)90681-4. [DOI] [PubMed] [Google Scholar]
  7. Göttfert M., Grob P., Hennecke H. Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2680–2684. doi: 10.1073/pnas.87.7.2680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Göttfert M., Hitz S., Hennecke H. Identification of nodS and nodU, two inducible genes inserted between the Bradyrhizobium japonicum nodYABC and nodIJ genes. Mol Plant Microbe Interact. 1990 Sep-Oct;3(5):308–316. doi: 10.1094/mpmi-3-308. [DOI] [PubMed] [Google Scholar]
  9. Göttfert M., Lamb J. W., Gasser R., Semenza J., Hennecke H. Mutational analysis of the Bradyrhizobium japonicum common nod genes and further nod box-linked genomic DNA regions. Mol Gen Genet. 1989 Feb;215(3):407–415. doi: 10.1007/BF00427037. [DOI] [PubMed] [Google Scholar]
  10. Helmann J. D., Wang Y., Mahler I., Walsh C. T. Homologous metalloregulatory proteins from both gram-positive and gram-negative bacteria control transcription of mercury resistance operons. J Bacteriol. 1989 Jan;171(1):222–229. doi: 10.1128/jb.171.1.222-229.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Keyser H. H., Cregan P. B. Nodulation and Competition for Nodulation of Selected Soybean Genotypes among Bradyrhizobium japonicum Serogroup 123 Isolates. Appl Environ Microbiol. 1987 Nov;53(11):2631–2635. doi: 10.1128/aem.53.11.2631-2635.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Knauf V. C., Nester E. W. Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid. Plasmid. 1982 Jul;8(1):45–54. doi: 10.1016/0147-619x(82)90040-3. [DOI] [PubMed] [Google Scholar]
  14. Kosslak R. M., Bookland R., Barkei J., Paaren H. E., Appelbaum E. R. Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7428–7432. doi: 10.1073/pnas.84.21.7428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laddaga R. A., Chu L., Misra T. K., Silver S. Nucleotide sequence and expression of the mercurial-resistance operon from Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5106–5110. doi: 10.1073/pnas.84.15.5106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leong S. A., Ditta G. S., Helinski D. R. Heme biosynthesis in Rhizobium. Identification of a cloned gene coding for delta-aminolevulinic acid synthetase from Rhizobium meliloti. J Biol Chem. 1982 Aug 10;257(15):8724–8730. [PubMed] [Google Scholar]
  17. Long S. R. Rhizobium-legume nodulation: life together in the underground. Cell. 1989 Jan 27;56(2):203–214. doi: 10.1016/0092-8674(89)90893-3. [DOI] [PubMed] [Google Scholar]
  18. Moawad H. A., Ellis W. R., Schmidt E. L. Rhizosphere Response as a Factor in Competition Among Three Serogroups of Indigenous Rhizobium japonicum for Nodulation of Field-Grown Soybeans. Appl Environ Microbiol. 1984 Apr;47(4):607–612. doi: 10.1128/aem.47.4.607-612.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nieuwkoop A. J., Banfalvi Z., Deshmane N., Gerhold D., Schell M. G., Sirotkin K. M., Stacey G. A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. J Bacteriol. 1987 Jun;169(6):2631–2638. doi: 10.1128/jb.169.6.2631-2638.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  21. O'Halloran T. V., Frantz B., Shin M. K., Ralston D. M., Wright J. G. The MerR heavy metal receptor mediates positive activation in a topologically novel transcription complex. Cell. 1989 Jan 13;56(1):119–129. doi: 10.1016/0092-8674(89)90990-2. [DOI] [PubMed] [Google Scholar]
  22. Rostas K., Kondorosi E., Horvath B., Simoncsits A., Kondorosi A. Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1757–1761. doi: 10.1073/pnas.83.6.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Russell P., Schell M. G., Nelson K. K., Halverson L. J., Sirotkin K. M., Stacey G. Isolation and characterization of the DNA region encoding nodulation functions in Bradyrhizobium japonicum. J Bacteriol. 1985 Dec;164(3):1301–1308. doi: 10.1128/jb.164.3.1301-1308.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sadowsky M. J., Cregan P. B., Keyser H. H. DNA Hybridization Probe for Use in Determining Restricted Nodulation among Bradyrhizobium japonicum Serocluster 123 Field Isolates. Appl Environ Microbiol. 1990 Jun;56(6):1768–1774. doi: 10.1128/aem.56.6.1768-1774.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sadowsky M. J., Olson E. R., Foster V. E., Kosslak R. M., Verma D. P. Two host-inducible genes of Rhizobium fredii and characterization of the inducing compound. J Bacteriol. 1988 Jan;170(1):171–178. doi: 10.1128/jb.170.1.171-178.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sadowsky M. J., Tully R. E., Cregan P. B., Keyser H. H. Genetic Diversity in Bradyrhizobium japonicum Serogroup 123 and Its Relation to Genotype-Specific Nodulation of Soybean. Appl Environ Microbiol. 1987 Nov;53(11):2624–2630. doi: 10.1128/aem.53.11.2624-2630.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schmidt E. L., Bakole R. O., Bohlool B. B. Fluorescent-antibody approach to study of rhizobia in soil. J Bacteriol. 1968 Jun;95(6):1987–1992. doi: 10.1128/jb.95.6.1987-1992.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmidt E. L., Zidwick M. J., Abebe H. M. Bradyrhizobium japonicum Serocluster 123 and Diversity among Member Isolates. Appl Environ Microbiol. 1986 Jun;51(6):1212–1215. doi: 10.1128/aem.51.6.1212-1215.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schofield P. R., Watson J. M. DNA sequence of Rhizobium trifolii nodulation genes reveals a reiterated and potentially regulatory sequence preceding nodABC and nodFE. Nucleic Acids Res. 1986 Apr 11;14(7):2891–2903. doi: 10.1093/nar/14.7.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stachel S. E., An G., Flores C., Nester E. W. A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J. 1985 Apr;4(4):891–898. doi: 10.1002/j.1460-2075.1985.tb03715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang Y., Moore M., Levinson H. S., Silver S., Walsh C., Mahler I. Nucleotide sequence of a chromosomal mercury resistance determinant from a Bacillus sp. with broad-spectrum mercury resistance. J Bacteriol. 1989 Jan;171(1):83–92. doi: 10.1128/jb.171.1.83-92.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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