Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1993 Aug;102(4):1095–1107. doi: 10.1104/pp.102.4.1095

Interaction of a rhizobial DNA-binding protein with the promoter region of a plant leghemoglobin gene.

P Welters 1, B Metz 1, G Felix 1, K Palme 1, K Szczyglowski 1, F J de Bruijn 1
PMCID: PMC158894  PMID: 8278541

Abstract

A nucleotide sequence was identified approximately 650 bp upstream of the Sesbania rostrata leghemoglobin gene Srglb3 start codon, which interacts specifically with a proteinaceous DNA-binding factor found in nodule extracts but not in extracts from leaves or roots. The binding site for this factor was delimited using footprinting techniques. The DNA-binding activity of this factor was found to be heat stable, dependent on divalent cations, and derived from the (infecting) Azorhizobium caulinodans bacteria or bacteroids (A. caulinodans bacterial binding factor 1, AcBBF1). A 9- to 10-kD protein was isolated from a free-living culture of A. caulinodans that co-purifies with the DNA-binding activity (A. caulinodans bacterial binding protein 1, AcBBP1) and interacts specifically with its target (S. rostrata bacterial binding site 1, SrBBS1). The amino acid sequence of the N-terminal 27 residues of AcBBP1 was determined and was found to share significant similarity (46% identity; 68% similarity) with a domain of the herpes simplex virus major DNA-binding protein infected cell protein 8 (ICP8). An insertion mutation in the SrBBS1 was found to result in a substantial reduction of the expression of a Srglb3-gus reporter gene fusion in nodules of transgenic Lotus corniculatus plants, suggesting a role for this element in Srglb3 promoter activity. Based on these results, we propose that (a) bacterial transacting factor(s) may play a role in infected cell-specific expression of the symbiotically induced plant lb genes.

Full Text

The Full Text of this article is available as a PDF (4.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bayliss G. J., Marsden H. S., Hay J. Herpes simplex virus proteins: DNA-binding proteins in infected cells and in the virus structure. Virology. 1975 Nov;68(1):124–134. doi: 10.1016/0042-6822(75)90154-3. [DOI] [PubMed] [Google Scholar]
  2. Beringer J. E. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974 Sep;84(1):188–198. doi: 10.1099/00221287-84-1-188. [DOI] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  4. Breining P., Piepersberg W. Yeast omnipotent supressor SUP1 (SUP45): nucleotide sequence of the wildtype and a mutant gene. Nucleic Acids Res. 1986 Jul 11;14(13):5187–5197. doi: 10.1093/nar/14.13.5187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bruijn F. J., Downie J. A. Biochemical and molecular studies of symbiotic nitrogen fixation. Curr Opin Biotechnol. 1991 Apr;2(2):184–192. doi: 10.1016/0958-1669(91)90008-s. [DOI] [PubMed] [Google Scholar]
  6. Bustos M. M., Guiltinan M. J., Jordano J., Begum D., Kalkan F. A., Hall T. C. Regulation of beta-glucuronidase expression in transgenic tobacco plants by an A/T-rich, cis-acting sequence found upstream of a French bean beta-phaseolin gene. Plant Cell. 1989 Sep;1(9):839–853. doi: 10.1105/tpc.1.9.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carrington J. C., Freed D. D., Leinicke A. J. Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell. 1991 Sep;3(9):953–962. doi: 10.1105/tpc.3.9.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Citovsky V., Zupan J., Warnick D., Zambryski P. Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science. 1992 Jun 26;256(5065):1802–1805. doi: 10.1126/science.1615325. [DOI] [PubMed] [Google Scholar]
  9. Datta N., Cashmore A. R. Binding of a pea nuclear protein to promoters of certain photoregulated genes is modulated by phosphorylation. Plant Cell. 1989 Nov;1(11):1069–1077. doi: 10.1105/tpc.1.11.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dehio C., de Bruijn F. J. The early nodulin gene SrEnod2 from Sesbania rostrata is inducible by cytokinin. Plant J. 1992 Jan;2(1):117–128. doi: 10.1046/j.1365-313x.1992.t01-51-00999.x. [DOI] [PubMed] [Google Scholar]
  11. Dickstein R., Scheirer D. C., Fowle W. H., Ausubel F. M. Nodules elicited by Rhizobium meliloti heme mutants are arrested at an early stage of development. Mol Gen Genet. 1991 Dec;230(3):423–432. doi: 10.1007/BF00280299. [DOI] [PubMed] [Google Scholar]
  12. Echeverria M., Delcasso-Tremousaygue D., Delseny M. A nuclear protein fraction binding to dA/dT-rich sequences upstream from the radish rDNA promoter [corrected]. Plant J. 1992 Mar;2(2):211–219. [PubMed] [Google Scholar]
  13. Economou A., Hamilton W. D., Johnston A. W., Downie J. A. 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. doi: 10.1002/j.1460-2075.1990.tb08117.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Economou A., Hawkins F. K., Downie J. A., Johnston A. W. Transcription of rhiA, a gene on a Rhizobium leguminosarum bv. viciae Sym plasmid, requires rhiR and is repressed by flavanoids that induce nod genes. Mol Microbiol. 1989 Jan;3(1):87–93. doi: 10.1111/j.1365-2958.1989.tb00107.x. [DOI] [PubMed] [Google Scholar]
  15. Gao M., Bouchey J., Curtin K., Knipe D. M. Genetic identification of a portion of the herpes simplex virus ICP8 protein required for DNA-binding. Virology. 1988 Apr;163(2):319–329. doi: 10.1016/0042-6822(88)90272-3. [DOI] [PubMed] [Google Scholar]
  16. Gao M., Knipe D. M. Potential role for herpes simplex virus ICP8 DNA replication protein in stimulation of late gene expression. J Virol. 1991 May;65(5):2666–2675. doi: 10.1128/jvi.65.5.2666-2675.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garcia-Bustos J., Heitman J., Hall M. N. Nuclear protein localization. Biochim Biophys Acta. 1991 Mar 7;1071(1):83–101. doi: 10.1016/0304-4157(91)90013-m. [DOI] [PubMed] [Google Scholar]
  18. Goodman L. E., Perou C. M., Fujiyama A., Tamanoi F. Structure and expression of yeast DPR1, a gene essential for the processing and intracellular localization of ras proteins. Yeast. 1988 Dec;4(4):271–281. doi: 10.1002/yea.320040405. [DOI] [PubMed] [Google Scholar]
  19. Howard E. A., Zupan J. R., Citovsky V., Zambryski P. C. The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell. 1992 Jan 10;68(1):109–118. doi: 10.1016/0092-8674(92)90210-4. [DOI] [PubMed] [Google Scholar]
  20. Jacobsen K., Laursen N. B., Jensen E. O., Marcker A., Poulsen C., Marcker K. A. HMG I-like proteins from leaf and nodule nuclei interact with different AT motifs in soybean nodulin promoters. Plant Cell. 1990 Jan;2(1):85–94. doi: 10.1105/tpc.2.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jordano J., Almoguera C., Thomas T. L. A sunflower helianthinin gene upstream sequence ensemble contains an enhancer and sites of nuclear protein interaction. Plant Cell. 1989 Sep;1(9):855–866. doi: 10.1105/tpc.1.9.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lamb C. J., Lawton M. A., Dron M., Dixon R. A. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell. 1989 Jan 27;56(2):215–224. doi: 10.1016/0092-8674(89)90894-5. [DOI] [PubMed] [Google Scholar]
  23. Lee C. K., Knipe D. M. An immunoassay for the study of DNA-binding activities of herpes simplex virus protein ICP8. J Virol. 1985 Jun;54(3):731–738. doi: 10.1128/jvi.54.3.731-738.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Metz B. A., Welters P., Hoffmann H. J., Jensen E. O., Schell J., de Bruijn F. J. Primary structure and promoter analysis of leghemoglobin genes of the stem-nodulated tropical legume Sesbania rostrata: conserved coding sequences, cis-elements and trans-acting factors. Mol Gen Genet. 1988 Oct;214(2):181–191. doi: 10.1007/BF00337709. [DOI] [PubMed] [Google Scholar]
  27. Nap J. P., Bisseling T. Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science. 1990 Nov 16;250(4983):948–954. doi: 10.1126/science.250.4983.948. [DOI] [PubMed] [Google Scholar]
  28. Orberg P. K., Schaffer P. A. Expression of herpes simplex virus type 1 major DNA-binding protein, ICP8, in transformed cell lines: complementation of deletion mutants and inhibition of wild-type virus. J Virol. 1987 Apr;61(4):1136–1146. doi: 10.1128/jvi.61.4.1136-1146.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Powell K. L., Littler E., Purifoy D. J. Nonstructural proteins of herpes simplex virus. II. Major virus-specific DNa-binding protein. J Virol. 1981 Sep;39(3):894–902. doi: 10.1128/jvi.39.3.894-902.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Purifoy D. J., Powell K. L. DNA-binding proteins induced by herpes simplex virus type 2 in HEp-2 cells. J Virol. 1976 Aug;19(2):717–731. doi: 10.1128/jvi.19.2.717-731.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Restrepo M. A., Freed D. D., Carrington J. C. Nuclear transport of plant potyviral proteins. Plant Cell. 1990 Oct;2(10):987–998. doi: 10.1105/tpc.2.10.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Riggs C. D., Voelker T. A., Chrispeels M. J. Cotyledon nuclear proteins bind to DNA fragments harboring regulatory elements of phytohemagglutinin genes. Plant Cell. 1989 Jun;1(6):609–621. doi: 10.1105/tpc.1.6.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stougaard J., Jørgensen J. E., Christensen T., Kühle A., Marcker K. A. Interdependence and nodule specificity of cis-acting regulatory elements in the soybean leghemoglobin lbc3 and N23 gene promoters. Mol Gen Genet. 1990 Feb;220(3):353–360. doi: 10.1007/BF00391738. [DOI] [PubMed] [Google Scholar]
  34. Szabados L., Ratet P., Grunenberg B., de Bruijn F. J. Functional analysis of the Sesbania rostrata leghemoglobin glb3 gene 5'-upstream region in transgenic Lotus corniculatus and Nicotiana tabacum plants. Plant Cell. 1990 Oct;2(10):973–986. doi: 10.1105/tpc.2.10.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Verma DPS. Signals in Root Nodule Organogenesis and Endocytosis of Rhizobium. Plant Cell. 1992 Apr;4(4):373–382. doi: 10.1105/tpc.4.4.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Welters P., Metz B. A., Schell J., de Bruijn F. J. Nucleotide sequence of the Sesbania rostrata leghemoglobin (Srglb3) gene. Nucleic Acids Res. 1989 Feb 11;17(3):1253–1253. doi: 10.1093/nar/17.3.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  38. de Bruijn F. J., Felix G., Grunenberg B., Hoffmann H. J., Metz B., Ratet P., Simons-Schreier A., Szabados L., Welters P., Schell J. Regulation of plant genes specifically induced in nitrogen-fixing nodules: role of cis-acting elements and trans-acting factors in leghemoglobin gene expression. Plant Mol Biol. 1989 Sep;13(3):319–325. doi: 10.1007/BF00025320. [DOI] [PubMed] [Google Scholar]
  39. de Maagd R. A., Spaink H. P., Pees E., Mulders I. H., Wijfjes A., Wijffelman C. A., Okker R. J., Lugtenberg B. J. Localization and symbiotic function of a region on the Rhizobium leguminosarum Sym plasmid pRL1JI responsible for a secreted, flavonoid-inducible 50-kilodalton protein. J Bacteriol. 1989 Feb;171(2):1151–1157. doi: 10.1128/jb.171.2.1151-1157.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES