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Proc Natl Acad Sci U S A. Mar 1, 1992; 89(5): 1646–1650.

Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins.


Nodulation of leguminous plants by Rhizobium, Bradyrhizobium, and Azorhizobium spp. is dependent on the induction by the plant host of different bacterial nodulation (nod) loci. The transcription of these nod loci is activated in the presence of plant-produced flavonoids upon binding of the NodD protein--a LysR-type activator--to specific sequences present in the nod promoters. Originally, a 47-base-pair (bp) region called the nod box was shown to be the target sequence for binding of NodD. From the comparison of the nod box sequences of (brady)rhizobia with a more divergent nod box from Azorhizobium caulinodans, we now propose a modular build-up of the nod box with the sequence A-T-C-N9-G-A-T as the binding target of the NodD protein (the NodD box). More generally, we show that LysR-type-regulated promoters contain the characteristic sequence T-N11-A as the core of an inverted repeat and propose this to be the "LysR motif" involved in specific binding to LysR-type proteins. Data obtained upon site-specific mutagenesis of this motif in the NodD box sustains this proposal. Further, we provide strong arguments that the inducer flavonoid, involved in transcriptional activation of Azorhizobium nod genes, interacts directly with the NodD protein, thereby increasing its binding affinities for the NodD box.

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  • Goethals K, Gao M, Tomekpe K, Van Montagu M, Holsters M. Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: nucleotide sequence and plant-inducible expression. Mol Gen Genet. 1989 Oct;219(1-2):289–298. [PubMed]
  • Goethals K, Van den Eeede G, Van Montagu M, Holsters M. Identification and characterization of a functional nodD gene in Azorhizobium caulinodans ORS571. J Bacteriol. 1990 May;172(5):2658–2666. [PMC free article] [PubMed]
  • Henikoff S, Haughn GW, Calvo JM, Wallace JC. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Fisher RF, Egelhoff TT, Mulligan JT, Long SR. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev. 1988 Mar;2(3):282–293. [PubMed]
  • Hong GF, Burn JE, Johnston AW. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucleic Acids Res. 1987 Dec 10;15(23):9677–9690. [PMC free article] [PubMed]
  • Fisher RF, Long SR. DNA footprint analysis of the transcriptional activator proteins NodD1 and NodD3 on inducible nod gene promoters. J Bacteriol. 1989 Oct;171(10):5492–5502. [PMC free article] [PubMed]
  • Van Larebeke N, Engler G, Holsters M, Van den Elsacker S, Zaenen I, Schilperoort RA, Schell J. Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature. 1974 Nov 8;252(5479):169–170. [PubMed]
  • Vieira J, Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. [PubMed]
  • de Maagd RA, Wijffelman CA, Pees E, Lugtenberg BJ. Detection and subcellular localization of two Sym plasmid-dependent proteins of Rhizobium leguminosarum biovar viciae. J Bacteriol. 1988 Sep;170(9):4424–4427. [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]
  • 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]
  • Fried M, Crothers DM. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. [PMC free article] [PubMed]
  • Bowen B, Steinberg J, Laemmli UK, Weintraub H. The detection of DNA-binding proteins by protein blotting. Nucleic Acids Res. 1980 Jan 11;8(1):1–20. [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]
  • Shearman CA, Rossen L, Johnston AW, Downie JA. The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO J. 1986 Apr;5(4):647–652. [PMC free article] [PubMed]
  • Pabo CO, Sauer RT. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. [PubMed]
  • Byerly KA, Urbanowski ML, Stauffer GV. The metR binding site in the Salmonella typhimurium metH gene: DNA sequence constraints on activation. J Bacteriol. 1991 Jun;173(11):3547–3553. [PMC free article] [PubMed]
  • Christman MF, Storz G, Ames BN. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci U S A. 1989 May;86(10):3484–3488. [PMC free article] [PubMed]
  • Schell MA, Poser EF. Demonstration, characterization, and mutational analysis of NahR protein binding to nah and sal promoters. J Bacteriol. 1989 Feb;171(2):837–846. [PMC free article] [PubMed]
  • Wek RC, Hatfield GW. Transcriptional activation at adjacent operators in the divergent-overlapping ilvY and ilvC promoters of Escherichia coli. J Mol Biol. 1988 Oct 5;203(3):643–663. [PubMed]
  • Chang M, Crawford IP. The roles of indoleglycerol phosphate and the TrpI protein in the expression of trpBA from Pseudomonas aeruginosa. Nucleic Acids Res. 1990 Feb 25;18(4):979–988. [PMC free article] [PubMed]
  • van der Meer JR, Frijters AC, Leveau JH, Eggen RI, Zehnder AJ, de Vos WM. Characterization of the Pseudomonas sp. strain P51 gene tcbR, a LysR-type transcriptional activator of the tcbCDEF chlorocatechol oxidative operon, and analysis of the regulatory region. J Bacteriol. 1991 Jun;173(12):3700–3708. [PMC free article] [PubMed]
  • Meijer WG, Arnberg AC, Enequist HG, Terpstra P, Lidstrom ME, Dijkhuizen L. Identification and organization of carbon dioxide fixation genes in Xanthobacter flavus H4-14. Mol Gen Genet. 1991 Feb;225(2):320–330. [PubMed]
  • Schell MA, Sukordhaman M. Evidence that the transcription activator encoded by the Pseudomonas putida nahR gene is evolutionarily related to the transcription activators encoded by the Rhizobium nodD genes. J Bacteriol. 1989 Apr;171(4):1952–1959. [PMC free article] [PubMed]
  • Györgypal Z, Kondorosi A. Homology of the ligand-binding regions of Rhizobium symbiotic regulatory protein NodD and vertebrate nuclear receptors. Mol Gen Genet. 1991 Apr;226(1-2):337–340. [PubMed]

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