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Gene Review

nodD1  -  LysR family transcriptional regulator

Sinorhizobium fredii NGR234

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Disease relevance of nodD1

  • The predicted NodD1 and NodD2 proteins shared 62% identical amino acid residues at corresponding positions and exhibited different degrees of homology with NodD proteins of other Bradyrhizobium, Azorhizobium, and Rhizobium strains [1].
  • Structural and functional analysis of two different nodD genes in Bradyrhizobium japonicum USDA110 [1].
  • Six others (Escherichia coli LysR, IlvY, CysB; Salmonella typhimurium MetR; Rhizobium NodD; and Enterobacter cloacae AmpR) are known to activate other genes [2].
  • Evidence that the protein that binds to the regulatory sequences is the nodD gene product came from the observation that a complex was formed between the nod box preceding nodA and protein from a cell-free extract isolated from Escherichia coli containing the cloned nodD gene [3].
  • Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti [4].

High impact information on nodD1

  • Novel features revealed by these studies include nod expression in the meristem, regulated in planta expression of control genes nodD1 and nodD3, disappearance of nod expression late in organogenesis, and properties of syrM [5].
  • Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes [6].
  • Transcription of the nod operons is under the control of NodD regulatory proteins, which are specifically activated by plant flavonoid signals [7].
  • 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 [8].
  • Symbiotic loci were localized by probing a representative set of cosmids with both homologous and heterologous genes. nodABC, nodD1, nodD2, nodSU, nolB, and region II are widely dispersed over pNGR234a, while the two functional copies of nifKDH are separated by only 28 kilobases [9].

Chemical compound and disease context of nodD1

  • Nine flavonoid aglycones released from black bean (Phaseolus vulgaris 'PI165426CS') seeds and roots induced nodC::lacZ transcription in Rhizobium leguminosarum bv. phaseoli strains containing extra cloned copies of the regulatory genes nodD1, nodD2, or nodD3 from that biovar [10].
  • The NahR protein of the Pseudomonas naphthalene degradation plasmid NAH7 encodes a 300-residue transcription activator which is very similar to the NodD transcription activator of Rhizobium and other proteins in the LysR activator family [11].
  • Expression of these gene fusions also was activated by a NodD gene product from Rhizobium leguminosarum in the presence of the inducer naringenin, as was a virA::lacZ fusion [12].
  • Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234 [13].
  • We demonstrated that in E. coli the regulatory gene nodD together with luteolin can activate nod genes [14].

Biological context of nodD1

  • Induction of the nodYABCSUIJ operon, as measured by expression of a translational nodC'-'lacZ fusion, required the nodD1 gene, but not nodD2 [1].
  • We report here the nucleotide sequence and mutational analyses of both nodD copies [1].
  • Bradyrhizobium japonicum has two closely linked homologs of the nodulation regulatory gene, nodD; these homologs are located upstream of and in divergent orientation to the nodYABCSUIJ gene cluster [1].
  • The nod box::nolL construct was also introduced into ANU265 (NGR234 cured of its symbiotic plasmid), along with extra copies of the nodD1 gene [15].
  • Analysis of the sequence showed open reading frames highly homologous to nolA, nodD2, nodD1, and nodKABC from other bradyrhizobial sources [16].

Anatomical context of nodD1

  • Efficient transcription of nodD1 required nodD1 and was enhanced by exposure of the cells to bean exudate consistent with the presence of a nod-box preceding the noIE-nodD1 operon [17].
  • Upstream of nodD1 and in the same operon is a newly described gene, noIE, whose product appears to be exported into the periplasm [18].
  • A 35-bp sequence containing the ribosome binding site for the nodD gene and an AT-rich core sequence has been identified by comparison with sequences from other Rhizobium strains and is likely to be implicated in the plant-mediated induction of nodulation gene expression [19].
  • Using these antibodies, we determined that the NodD protein is located exclusively in the cytoplasmic membrane of wild-type R. leguminosarum biovar viciae cells [20].
  • The amount of nodD transcript in bacteroids was reduced only two- to threefold compared with that in cultured cells [21].

Associations of nodD1 with chemical compounds

  • Surprisingly, many genes remained transcribed in the nodD1- mutant suggesting the presence of other flavonoid-dependent activators in NGR234 [22].
  • It required syrM for expression, was activated by nodD1 in the presence of luteolin and was positively autoregulated [23].
  • The most effective HPLC fractions induced R. galegae nodD1 up to the level obtained by intact G. orientalis root exudate while apigenin and luteolin, which were also present in the root exudate, were only moderate inducers [24].
  • These results indicate that extracellular accumulation of N-acetylglutamic acid is linked to flavone-dependent metabolism involving nodD, nodL, and nodM in R. trifolii ANU843 [25].
  • Surprisingly, although they do not stimulate nod gene expression in S. meliloti, the flavonoids naringenin, eriodictyol, and daidzein also stimulated an increase in the DNA binding affinity of NodD1 to nod gene promoters [4].

Regulatory relationships of nodD1

  • We show that expression of the noeL gene is under the control of NodD1 in S. fredii and is most probably mediated by the nod box that precedes nodZ [26].

Other interactions of nodD1

  • Together with extra copies of the nodD1 gene, the nodZ gene and its associated nod box were introduced into ANU265, which is NGR234 cured of the symbiotic plasmid [27].
  • The nodD1 gene product activates expression of the nodABC operon, as measured by a nodC-lacZ fusion or by transcript analysis, in the presence of crude seed or plant wash or the inducer, luteolin [28].
  • The open reading frame identified between nodD1 and nodA in the B. elkanii sequence was far more similar to nodK from Bradyrhizobium sp. (Parasponia) than to nodY from B. japonicum [16].
  • The gene is not inducible in a mutant of strain USDA191 that lacks the regulatory nodD1 gene, and its expression is greatly attenuated in a nodD2 mutant. nolX is also present and flavonoid-inducible in HH103, a second R. fredii strain that nodulates McCall soybean normally [29].

Analytical, diagnostic and therapeutic context of nodD1


  1. Structural and functional analysis of two different nodD genes in Bradyrhizobium japonicum USDA110. Göttfert, M., Holzhäuser, D., Bäni, D., Hennecke, H. Mol. Plant Microbe Interact. (1992) [Pubmed]
  2. A large family of bacterial activator proteins. Henikoff, S., Haughn, G.W., Calvo, J.M., Wallace, J.C. Proc. Natl. Acad. Sci. U.S.A. (1988) [Pubmed]
  3. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Hong, G.F., Burn, J.E., Johnston, A.W. Nucleic Acids Res. (1987) [Pubmed]
  4. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. Peck, M.C., Fisher, R.F., Long, S.R. J. Bacteriol. (2006) [Pubmed]
  5. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Sharma, S.B., Signer, E.R. Genes Dev. (1990) [Pubmed]
  6. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Fisher, R.F., Egelhoff, T.T., Mulligan, J.T., Long, S.R. Genes Dev. (1988) [Pubmed]
  7. Signaling and host range variation in nodulation. Dénarié, J., Debellé, F., Rosenberg, C. Annu. Rev. Microbiol. (1992) [Pubmed]
  8. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Goethals, K., Van Montagu, M., Holsters, M. Proc. Natl. Acad. Sci. U.S.A. (1992) [Pubmed]
  9. Canonical ordered cosmid library of the symbiotic plasmid of Rhizobium species NGR234. Perret, X., Broughton, W.J., Brenner, S. Proc. Natl. Acad. Sci. U.S.A. (1991) [Pubmed]
  10. Effects of flavonoids released naturally from bean (Phaseolus vulgaris) on nodD-regulated gene transcription in Rhizobium leguminosarum bv. phaseoli. Hungria, M., Johnston, A.W., Phillips, D.A. Mol. Plant Microbe Interact. (1992) [Pubmed]
  11. Use of saturation mutagenesis to localize probable functional domains in the NahR protein, a LysR-type transcription activator. Schell, M.A., Brown, P.H., Raju, S. J. Biol. Chem. (1990) [Pubmed]
  12. Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Hubber, A.M., Sullivan, J.T., Ronson, C.W. Mol. Plant Microbe Interact. (2007) [Pubmed]
  13. Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Theunis, M., Kobayashi, H., Broughton, W.J., Prinsen, E. Mol. Plant Microbe Interact. (2004) [Pubmed]
  14. Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Baev, N., Endre, G., Petrovics, G., Banfalvi, Z., Kondorosi, A. Mol. Gen. Genet. (1991) [Pubmed]
  15. NolL of Rhizobium sp. strain NGR234 is required for O-acetyltransferase activity. Berck, S., Perret, X., Quesada-Vincens, D., Promé, J., Broughton, W.J., Jabbouri, S. J. Bacteriol. (1999) [Pubmed]
  16. DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Dobert, R.C., Breil, B.T., Triplett, E.W. Mol. Plant Microbe Interact. (1994) [Pubmed]
  17. Regulatory functions of the three nodD genes of Rhizobium leguminosarum biovar phaseoli. Davis, E.O., Johnston, A.W. Mol. Microbiol. (1990) [Pubmed]
  18. Analysis of three nodD genes in Rhizobium leguminosarum biovar phaseoli; nodD1 is preceded by noIE, a gene whose product is secreted from the cytoplasm. Davis, E.O., Johnston, A.W. Mol. Microbiol. (1990) [Pubmed]
  19. Conserved nodulation genes from the non-legume symbiont Bradyrhizobium sp. (Parasponia). Scott, K.F. Nucleic Acids Res. (1986) [Pubmed]
  20. Subcellular localization of the nodD gene product in Rhizobium leguminosarum. Schlaman, H.R., Spaink, H.P., Okker, R.J., Lugtenberg, B.J. J. Bacteriol. (1989) [Pubmed]
  21. Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. Schlaman, H.R., Horvath, B., Vijgenboom, E., Okker, R.J., Lugtenberg, B.J. J. Bacteriol. (1991) [Pubmed]
  22. Organization of host-inducible transcripts on the symbiotic plasmid of Rhizobium sp. NGR234. Fellay, R., Perret, X., Viprey, V., Broughton, W.J., Brenner, S. Mol. Microbiol. (1995) [Pubmed]
  23. Role of the nodD and syrM genes in the activation of the regulatory gene nodD3, and of the common and host-specific nod genes of Rhizobium meliloti. Maillet, F., Debellé, F., Dénarié, J. Mol. Microbiol. (1990) [Pubmed]
  24. Activation of the nodA promoter by the nodD genes of Rhizobium galegae induced by synthetic flavonoids or Galega orientalis root exudate. Suominen, L., Luukkainen, R., Roos, C., Lindström, K. FEMS Microbiol. Lett. (2003) [Pubmed]
  25. N-Acetylglutamic acid: an extracellular nod signal of Rhizobium trifolii ANU843 that induces root hair branching and nodule-like primordia in white clover roots. Philip-Hollingsworth, S., Hollingsworth, R.I., Dazzo, F.B. J. Biol. Chem. (1991) [Pubmed]
  26. Mutation in GDP-fucose synthesis genes of Sinorhizobium fredii alters Nod factors and significantly decreases competitiveness to nodulate soybeans. Lamrabet, Y., Bellogín, R.A., Cubo, T., Espuny, R., Gil, A., Krishnan, H.B., Megias, M., Ollero, F.J., Pueppke, S.G., Ruiz-Sainz, J.E., Spaink, H.P., Tejero-Mateo, P., Thomas-Oates, J., Vinardell, J.M. Mol. Plant Microbe Interact. (1999) [Pubmed]
  27. Rhizobium sp. strain NGR234 NodZ protein is a fucosyltransferase. Quesada-Vincens, D., Fellay, R., Nasim, T., Viprey, V., Burger, U., Prome, J.C., Broughton, W.J., Jabbouri, S. J. Bacteriol. (1997) [Pubmed]
  28. A family of activator genes regulates expression of Rhizobium meliloti nodulation genes. Mulligan, J.T., Long, S.R. Genetics (1989) [Pubmed]
  29. The soybean cultivar specificity gene nolX is present, expressed in a nodD-dependent manner, and of symbiotic significance in cultivar-nonspecific strains of Rhizobium (Sinorhizobium) fredii. Bellato, C., Krishnan, H.B., Cubo, T., Temprano, F., Pueppke, S.G. Microbiology (Reading, Engl.) (1997) [Pubmed]
  30. Evidence that two genomic species of Rhizobium are associated with Medicago truncatula. Rome, S., Brunel, B., Normand, P., Fernandez, M., Cleyet-Marel, J.C. Arch. Microbiol. (1996) [Pubmed]
  31. DNA footprint analysis of the transcriptional activator proteins NodD1 and NodD3 on inducible nod gene promoters. Fisher, R.F., Long, S.R. J. Bacteriol. (1989) [Pubmed]
  32. Sequence and mutational analysis of the 6.7-kb region containing nodAFEG genes of Rhizobium sp. strain N33: evidence of DNA rearrangements. Cloutier, J., Laberge, S., Antoun, H. Mol. Plant Microbe Interact. (1997) [Pubmed]
  33. Sulfation of nod factors via nodHPQ is nodD independent in Rhizobium tropici CIAT899. Folch-Mallol, J.L., Manyani, H., Marroquí, S., Sousa, C., Vargas, C., Nava, N., Colmenero-Flores, J.M., Quinto, C., Megías, M. Mol. Plant Microbe Interact. (1998) [Pubmed]
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