• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Feb 1994; 176(3): 620–633.
PMCID: PMC205098

nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum.

Abstract

The nodulation genes of rhizobia are regulated by the nodD gene product in response to host-produced flavonoids and appear to encode enzymes involved in the production of a lipo-chitose signal molecule required for infection and nodule formation. We have identified the nodZ gene of Bradyrhizobium japonicum, whose product is required for the addition of a 2-O-methylfucose residue to the terminal reducing N-acetylglucosamine of the nodulation signal. This substitution is essential for the biological activity of this molecule. Mutations in nodZ result in defective nodulation of siratro. Surprisingly, although nodZ clearly codes for nodulation function, it is not regulated by NodD and, indeed, shows elevated expression in planta. Therefore, nodZ represents a unique nodulation gene that is not under the control of NodD and yet is essential for the synthesis of an active nodulation signal.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (3.2M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aiba H, Adhya S, de Crombrugghe B. Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem. 1981 Nov 25;256(22):11905–11910. [PubMed]
  • Amann E, Brosius J. "ATG vectors' for regulated high-level expression of cloned genes in Escherichia coli. Gene. 1985;40(2-3):183–190. [PubMed]
  • Banfalvi Z, Kondorosi A. Production of root hair deformation factors by Rhizobium meliloti nodulation genes in Escherichia coli: HsnD (NodH) is involved in the plant host-specific modification of the NodABC factor. Plant Mol Biol. 1989 Jul;13(1):1–12. [PubMed]
  • 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. [PubMed]
  • Bassam BJ, Djordjevic MA, Redmond JW, Batley M, Rolfe BG. Identification of a nodD-dependent locus in the Rhizobium strain NGR234 activated by phenolic factors secreted by soybeans and other legumes. Mol Plant Microbe Interact. 1988 Apr;1(4):161–168. [PubMed]
  • Beringer JE. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974 Sep;84(1):188–198. [PubMed]
  • Carlson RW, Sanjuan J, Bhat UR, Glushka J, Spaink HP, Wijfjes AH, van Brussel AA, Stokkermans TJ, Peters NK, Stacey G. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and II strains of Bradyrhizobium japonicum. J Biol Chem. 1993 Aug 25;268(24):18372–18381. [PubMed]
  • de Maagd RA, Wijfjes AH, Spaink HP, Ruiz-Sainz JE, Wijffelman CA, Okker RJ, Lugtenberg BJ. nodO, a new nod gene of the Rhizobium leguminosarum biovar viciae sym plasmid pRL1JI, encodes a secreted protein. J Bacteriol. 1989 Dec;171(12):6764–6770. [PMC free article] [PubMed]
  • Demont N, Debellé F, Aurelle H, Dénarié J, Promé JC. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem. 1993 Sep 25;268(27):20134–20142. [PubMed]
  • Dénarié J, Cullimore J. Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell. 1993 Sep 24;74(6):951–954. [PubMed]
  • Dénarié J, Debellé F, Rosenberg C. Signaling and host range variation in nodulation. Annu Rev Microbiol. 1992;46:497–531. [PubMed]
  • Deshmane N, Stacey G. Identification of Bradyrhizobium nod genes involved in host-specific nodulation. J Bacteriol. 1989 Jun;171(6):3324–3330. [PMC free article] [PubMed]
  • Ditta G, Stanfield S, Corbin D, Helinski DR. 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. [PMC free article] [PubMed]
  • Economou A, Hamilton WD, Johnston AW, Downie JA. The Rhizobium nodulation gene nodO encodes a Ca2(+)-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J. 1990 Feb;9(2):349–354. [PMC free article] [PubMed]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed]
  • Festl H, Ludwig W, Schleifer KH. DNA hybridization probe for the Pseudomonas fluorescens group. Appl Environ Microbiol. 1986 Nov;52(5):1190–1194. [PMC free article] [PubMed]
  • Fischer HM, Alvarez-Morales A, Hennecke H. The pleiotropic nature of symbiotic regulatory mutants: Bradyrhizobium japonicum nifA gene is involved in control of nif gene expression and formation of determinate symbiosis. EMBO J. 1986 Jun;5(6):1165–1173. [PMC free article] [PubMed]
  • Fisher RF, Long SR. Rhizobium--plant signal exchange. Nature. 1992 Jun 25;357(6380):655–660. [PubMed]
  • Geiger O, Spaink HP, Kennedy EP. Isolation of the Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4'-phosphopantetheine prosthetic group. J Bacteriol. 1991 May;173(9):2872–2878. [PMC free article] [PubMed]
  • Goldberg RB, Bender RA, Streicher SL. Direct selection for P1-sensitive mutants of enteric bacteria. J Bacteriol. 1974 Jun;118(3):810–814. [PMC free article] [PubMed]
  • Halverson LJ, Stacey G. Host recognition in the Rhizobium-soybean symbiosis: detection of a protein factor in soybean root exudate which is involved in the nodulation process. Plant Physiol. 1984 Jan;74(1):84–89. [PMC free article] [PubMed]
  • Horvath B, Bachem CW, 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. [PMC free article] [PubMed]
  • Kassavetis GA, Geiduschek EP. Bacteriophage T4 late promoters: mapping 5' ends of T4 gene 23 mRNAs. EMBO J. 1982;1(1):107–114. [PMC free article] [PubMed]
  • Kuykendall LD, Elkan GH. Rhizobium japonicum derivatives differing in nitrogen-fixing efficiency and carbohydrate utilization. Appl Environ Microbiol. 1976 Oct;32(4):511–519. [PMC free article] [PubMed]
  • Leong SA, Ditta GS, Helinski DR. 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]
  • Long SR. Rhizobium-legume nodulation: life together in the underground. Cell. 1989 Jan 27;56(2):203–214. [PubMed]
  • Messing J, Crea R, Seeburg PH. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. [PMC free article] [PubMed]
  • Nieuwkoop AJ, Banfalvi Z, Deshmane N, Gerhold D, Schell MG, Sirotkin KM, 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. [PMC free article] [PubMed]
  • Ogawa J, Brierley HL, Long SR. Analysis of Rhizobium meliloti nodulation mutant WL131: novel insertion sequence ISRm3 in nodG and altered nodH protein product. J Bacteriol. 1991 May;173(10):3060–3065. [PMC free article] [PubMed]
  • Price NP, Relić B, Talmont F, Lewin A, Promé D, Pueppke SG, Maillet F, Dénarié J, Promé JC, Broughton WJ. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol Microbiol. 1992 Dec;6(23):3575–3584. [PubMed]
  • Quinto M, Bender RA. Use of bacteriophage P1 as a vector for Tn5 insertion mutagenesis. Appl Environ Microbiol. 1984 Feb;47(2):436–438. [PMC free article] [PubMed]
  • Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, Truchet G, Dénarié J, Promé JC. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell. 1991 Dec 20;67(6):1131–1143. [PubMed]
  • Russell P, Schell MG, Nelson KK, Halverson LJ, Sirotkin KM, Stacey G. Isolation and characterization of the DNA region encoding nodulation functions in Bradyrhizobium japonicum. J Bacteriol. 1985 Dec;164(3):1301–1308. [PMC free article] [PubMed]
  • Ruvkun GB, Ausubel FM. A general method for site-directed mutagenesis in prokaryotes. Nature. 1981 Jan 1;289(5793):85–88. [PubMed]
  • Sancar A, Hack AM, Rupp WD. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, Glushka J, Stacey G. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8789–8793. [PMC free article] [PubMed]
  • Scheu AK, Economou A, Hong GF, Ghelani S, Johnston AW, Downie JA. Secretion of the Rhizobium leguminosarum nodulation protein NodO by haemolysin-type systems. Mol Microbiol. 1992 Jan;6(2):231–238. [PubMed]
  • Schwedock J, Long SR. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature. 1990 Dec 13;348(6302):644–647. [PubMed]
  • Smit G, Puvanesarajah V, Carlson RW, Barbour WM, Stacey G. Bradyrhizobium japonicum nodD1 can be specifically induced by soybean flavonoids that do not induce the nodYABCSUIJ operon. J Biol Chem. 1992 Jan 5;267(1):310–318. [PubMed]
  • So JS, Hodgson AL, Haugland R, Leavitt M, Banfalvi Z, Nieuwkoop AJ, Stacey G. Transposon-induced symbiotic mutants of Bradyrhizobium japonicum: isolation of two gene regions essential for nodulation. Mol Gen Genet. 1987 Apr;207(1):15–23. [PubMed]
  • Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed]
  • Spaink HP. Rhizobial lipo-oligosaccharides: answers and questions. Plant Mol Biol. 1992 Dec;20(5):977–986. [PubMed]
  • Spaink HP, Aarts A, Stacey G, Bloemberg GV, Lugtenberg BJ, Kennedy EP. Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin-layer chromatography. Mol Plant Microbe Interact. 1992 Jan-Feb;5(1):72–80. [PubMed]
  • Stachel SE, An G, Flores C, Nester EW. 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. [PMC free article] [PubMed]

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

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...