Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1990 Sep;2(9):925–939. doi: 10.1105/tpc.2.9.925

Nuclear factors interact with conserved A/T-rich elements upstream of a nodule-enhanced glutamine synthetase gene from French bean.

B G Forde 1, J Freeman 1, J E Oliver 1, M Pineda 1
PMCID: PMC159942  PMID: 1983793

Abstract

The gln-gamma gene, encoding the gamma subunit of glutamine synthetase in French bean (Phaseolus vulgaris), is strongly induced during nodule development. We have determined the nucleotide sequence of a 1.3-kilobase region at its 5' end and have identified several sequences common to the promoter regions of late nodulin genes from other legume species. The 5'-flanking region was analyzed for sequence-specific interactions with nuclear factors from French bean. A factor from nodules (PNF-1) was identified that binds to multiple sites between -860 and -154, and a related but distinct factor (PRF-1) was detected in extracts from uninfected roots. PNF-1 and PRF-1 bound strongly to a synthetic oligonucleotide containing the sequence of an A/T-rich 21-base pair imperfect repeat found at positions -516 and -466. The same factors also had a high affinity for a protein binding site from a soybean leghemoglobin gene and appeared to be closely related to the soybean nodule factor NAT2, which binds to A/T-rich sequences in the lbc3 and nodulin 23 genes [Jacobsen et al. (1990). Plant Cell 2, 85-94]. Comparison of NAT2/PNF-1 binding sites from a variety of nodulin genes revealed the conservation of the short consensus core motif TATTTWAT, and evidence was obtained that this sequence is important for protein recognition. Cross-recognition by PNF-1 of a protein binding site in a soybean seed protein gene points to the existence of a ubiquitous family of factors with related binding affinities. Our data suggest that PNF-1 and PRF-1 belong to an evolutionarily conserved group of nuclear factors that interact with specific A/T-rich sequences in a diverse set of plant genes. We consider the possible role of these factors in coregulating the expression of gln-gamma and other late nodulin genes.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. Allen R. D., Bernier F., Lessard P. A., Beachy R. N. Nuclear factors interact with a soybean beta-conglycinin enhancer. Plant Cell. 1989 Jun;1(6):623–631. doi: 10.1105/tpc.1.6.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Cullimore J. V., Gebhardt C., Saarelainen R., Miflin B. J., Idler K. B., Barker R. F. Glutamine synthetase of Phaseolus vulgaris L.: organ-specific expression of a multigene family. J Mol Appl Genet. 1984;2(6):589–599. [PubMed] [Google Scholar]
  5. 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]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Forde B. G., Day H. M., Turton J. F., Shen W. J., Cullimore J. V., Oliver J. E. Two glutamine synthetase genes from Phaseolus vulgaris L. display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell. 1989 Apr;1(4):391–401. doi: 10.1105/tpc.1.4.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gebhardt C., Oliver J. E., Forde B. G., Saarelainen R., Miflin B. J. Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J. 1986 Jul;5(7):1429–1435. doi: 10.1002/j.1460-2075.1986.tb04379.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Jensen E. Ø, Marcker K. A., Schell J., Bruijn F. J. Interaction of a nodule specific, trans-acting factor with distinct DNA elements in the soybean leghaemoglobin Ibc(3) 5' upstream region. EMBO J. 1988 May;7(5):1265–1271. doi: 10.1002/j.1460-2075.1988.tb02940.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jofuku K. D., Okamuro J. K., Goldberg R. B. Interaction of an embryo DNA binding protein with a soybean lectin gene upstream region. Nature. 1987 Aug 20;328(6132):734–737. doi: 10.1038/328734a0. [DOI] [PubMed] [Google Scholar]
  12. Jørgensen J. E., Stougaard J., Marcker A., Marcker K. A. Root nodule specific gene regulation: analysis of the soybean nodulin N23 gene promoter in heterologous symbiotic systems. Nucleic Acids Res. 1988 Jan 11;16(1):39–50. doi: 10.1093/nar/16.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  15. Morrison N. A., Bisseling T., Verma D. P. Development and differentiation of the root nodule. Involvement of plant and bacterial genes. Dev Biol (N Y 1985) 1988;5:405–425. doi: 10.1007/978-1-4615-6817-9_15. [DOI] [PubMed] [Google Scholar]
  16. Sauer R. T., Pabo C. O., Meyer B. J., Ptashne M., Backman K. C. Regulatory functions of the lambda repressor reside in the amino-terminal domain. Nature. 1979 May 31;279(5712):396–400. doi: 10.1038/279396a0. [DOI] [PubMed] [Google Scholar]
  17. Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Stougaard J., Sandal N. N., Grøn A., Kühle A., Marcker K. A. 5' Analysis of the soybean leghaemoglobin lbc(3) gene: regulatory elements required for promoter activity and organ specificity. EMBO J. 1987 Dec 1;6(12):3565–3569. doi: 10.1002/j.1460-2075.1987.tb02686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Supakar P. C., Zhang X. Y., Githens S., Khan R., Ehrlich K. C., Ehrlich M. How different DNA sequences are recognized by a DNA-binding protein: effects of partial proteolysis. Nucleic Acids Res. 1989 Nov 11;17(21):8611–8629. doi: 10.1093/nar/17.21.8611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Svaren J., Inagami S., Lovegren E., Chalkley R. DNA denatures upon drying after ethanol precipitation. Nucleic Acids Res. 1987 Nov 11;15(21):8739–8754. doi: 10.1093/nar/15.21.8739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Turton J. F., Hopley A. P., Forde B. G. 5'-flanking sequence of a glutamine synthetase gene specifying the beta subunit of the cytosolic enzyme from Phaseolus vulgaris L. Nucleic Acids Res. 1988 Dec 9;16(23):11367–11367. doi: 10.1093/nar/16.23.11367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Willmitzer L., Wagner K. G. The isolation of nuclei from tissue-cultured plant cells. Exp Cell Res. 1981 Sep;135(1):69–77. doi: 10.1016/0014-4827(81)90300-1. [DOI] [PubMed] [Google Scholar]
  23. 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]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES