Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Dec 1;89(23):11490–11494. doi: 10.1073/pnas.89.23.11490

Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex.

G Lu 1, A J DeLisle 1, N C de Vetten 1, R J Ferl 1
PMCID: PMC50577  PMID: 1454838

Abstract

The G box is a well-characterized cis-acting DNA regulatory element found in the promoters of several seemingly unrelated plant genes, including the alcohol dehydrogenase (Adh) gene of Arabidopsis thaliana. Using a monoclonal antibody screening approach coupled with electrophoretic mobility shift assays, we have isolated a cDNA clone encoding a protein that is part of the in vitro protein/G box complex. The derived amino acid sequence is homologous to a class of proteins in mammalian brains described as protein kinase C inhibitors and as activators of tyrosine and tryptophan hydroxylases, the rate-limiting enzymes in the pathways leading to the catecholamines and serotonin. The fact that a homologous member of this regulatory protein family is found in plants and is associated with binding to transcriptional regulatory elements suggests a much wider role for these proteins.

Full text

PDF
11493

Images in this article

Selected References

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

  1. Abel T., Maniatis T. Gene regulation. Action of leucine zippers. Nature. 1989 Sep 7;341(6237):24–25. doi: 10.1038/341024a0. [DOI] [PubMed] [Google Scholar]
  2. Aitken A., Ellis C. A., Harris A., Sellers L. A., Toker A. Kinase and neurotransmitters. Nature. 1990 Apr 12;344(6267):594–594. doi: 10.1038/344594a0. [DOI] [PubMed] [Google Scholar]
  3. Bray S. J., Burke B., Brown N. H., Hirsh J. Embryonic expression pattern of a family of Drosophila proteins that interact with a central nervous system regulatory element. Genes Dev. 1989 Aug;3(8):1130–1145. doi: 10.1101/gad.3.8.1130. [DOI] [PubMed] [Google Scholar]
  4. Chiu R., Boyle W. J., Meek J., Smeal T., Hunter T., Karin M. The c-Fos protein interacts with c-Jun/AP-1 to stimulate transcription of AP-1 responsive genes. Cell. 1988 Aug 12;54(4):541–552. doi: 10.1016/0092-8674(88)90076-1. [DOI] [PubMed] [Google Scholar]
  5. Chodosh L. A., Buratowski S., Sharp P. A. A yeast protein possesses the DNA-binding properties of the adenovirus major late transcription factor. Mol Cell Biol. 1989 Feb;9(2):820–822. doi: 10.1128/mcb.9.2.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeLisle A. J., Ferl R. J. Characterization of the Arabidopsis Adh G-box binding factor. Plant Cell. 1990 Jun;2(6):547–557. doi: 10.1105/tpc.2.6.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Donald R. G., Schindler U., Batschauer A., Cashmore A. R. The plant G box promoter sequence activates transcription in Saccharomyces cerevisiae and is bound in vitro by a yeast activity similar to GBF, the plant G box binding factor. EMBO J. 1990 Jun;9(6):1727–1735. doi: 10.1002/j.1460-2075.1990.tb08296.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ferl R. J., Nick H. S. In vivo detection of regulatory factor binding sites in the 5' flanking region of maize Adh1. J Biol Chem. 1987 Jun 15;262(17):7947–7950. [PubMed] [Google Scholar]
  9. Fried M., Crothers D. M. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. doi: 10.1093/nar/9.23.6505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Giuliano G., Pichersky E., Malik V. S., Timko M. P., Scolnik P. A., Cashmore A. R. An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7089–7093. doi: 10.1073/pnas.85.19.7089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gonzalez G. A., Yamamoto K. K., Fischer W. H., Karr D., Menzel P., Biggs W., 3rd, Vale W. W., Montminy M. R. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature. 1989 Feb 23;337(6209):749–752. doi: 10.1038/337749a0. [DOI] [PubMed] [Google Scholar]
  12. Guiltinan M. J., Marcotte W. R., Jr, Quatrano R. S. A plant leucine zipper protein that recognizes an abscisic acid response element. Science. 1990 Oct 12;250(4978):267–271. doi: 10.1126/science.2145628. [DOI] [PubMed] [Google Scholar]
  13. Hirsch S., Aitken A., Bertsch U., Soll J. A plant homologue to mammalian brain 14-3-3 protein and protein kinase C inhibitor. FEBS Lett. 1992 Jan 20;296(2):222–224. doi: 10.1016/0014-5793(92)80384-s. [DOI] [PubMed] [Google Scholar]
  14. Hope I. A., Mahadevan S., Struhl K. Structural and functional characterization of the short acidic transcriptional activation region of yeast GCN4 protein. Nature. 1988 Jun 16;333(6174):635–640. doi: 10.1038/333635a0. [DOI] [PubMed] [Google Scholar]
  15. Ichimura T., Isobe T., Okuyama T., Takahashi N., Araki K., Kuwano R., Takahashi Y. Molecular cloning of cDNA coding for brain-specific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7084–7088. doi: 10.1073/pnas.85.19.7084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ichimura T., Sugano H., Kuwano R., Sunaya T., Okuyama T., Isobe T. Widespread distribution of the 14-3-3 protein in vertebrate brains and bovine tissues: correlation with the distributions of calcium-dependent protein kinases. J Neurochem. 1991 Apr;56(4):1449–1451. doi: 10.1111/j.1471-4159.1991.tb11446.x. [DOI] [PubMed] [Google Scholar]
  17. Isobe T., Ichimura T., Sunaya T., Okuyama T., Takahashi N., Kuwano R., Takahashi Y. Distinct forms of the protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. J Mol Biol. 1991 Jan 5;217(1):125–132. doi: 10.1016/0022-2836(91)90616-e. [DOI] [PubMed] [Google Scholar]
  18. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Lawton M. A., Yamamoto R. T., Hanks S. K., Lamb C. J. Molecular cloning of plant transcripts encoding protein kinase homologs. Proc Natl Acad Sci U S A. 1989 May;86(9):3140–3144. doi: 10.1073/pnas.86.9.3140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ma J., Ptashne M. Deletion analysis of GAL4 defines two transcriptional activating segments. Cell. 1987 Mar 13;48(5):847–853. doi: 10.1016/0092-8674(87)90081-x. [DOI] [PubMed] [Google Scholar]
  22. McCarty D. R., Hattori T., Carson C. B., Vasil V., Lazar M., Vasil I. K. The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell. 1991 Sep 6;66(5):895–905. doi: 10.1016/0092-8674(91)90436-3. [DOI] [PubMed] [Google Scholar]
  23. McKendree W. L., Jr, Ferl R. J. Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol Biol. 1992 Aug;19(5):859–862. doi: 10.1007/BF00027081. [DOI] [PubMed] [Google Scholar]
  24. McKendree W. L., Paul A. L., DeLisle A. J., Ferl R. J. In vivo and in vitro characterization of protein interactions with the dyad G-box of the Arabidopsis Adh gene. Plant Cell. 1990 Mar;2(3):207–214. doi: 10.1105/tpc.2.3.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miskimins W. K., Roberts M. P., McClelland A., Ruddle F. H. Use of a protein-blotting procedure and a specific DNA probe to identify nuclear proteins that recognize the promoter region of the transferrin receptor gene. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6741–6744. doi: 10.1073/pnas.82.20.6741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  27. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  28. Oeda K., Salinas J., Chua N. H. A tobacco bZip transcription activator (TAF-1) binds to a G-box-like motif conserved in plant genes. EMBO J. 1991 Jul;10(7):1793–1802. doi: 10.1002/j.1460-2075.1991.tb07704.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Paul A. L., Vasil V., Vasil I. K., Ferl R. J. Constitutive and anaerobically induced DNase-I-hypersensitive sites in the 5' region of the maize Adh1 gene. Proc Natl Acad Sci U S A. 1987 Feb;84(3):799–803. doi: 10.1073/pnas.84.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sachs M. M., Freeling M., Okimoto R. The anaerobic proteins of maize. Cell. 1980 Jul;20(3):761–767. doi: 10.1016/0092-8674(80)90322-0. [DOI] [PubMed] [Google Scholar]
  32. Schindler U., Menkens A. E., Beckmann H., Ecker J. R., Cashmore A. R. Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. EMBO J. 1992 Apr;11(4):1261–1273. doi: 10.1002/j.1460-2075.1992.tb05170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schulze-Lefert P., Dangl J. L., Becker-André M., Hahlbrock K., Schulz W. Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J. 1989 Mar;8(3):651–656. doi: 10.1002/j.1460-2075.1989.tb03422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  35. Toker A., Ellis C. A., Sellers L. A., Aitken A. Protein kinase C inhibitor proteins. Purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. Eur J Biochem. 1990 Jul 31;191(2):421–429. doi: 10.1111/j.1432-1033.1990.tb19138.x. [DOI] [PubMed] [Google Scholar]
  36. Vinson C. R., Sigler P. B., McKnight S. L. Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science. 1989 Nov 17;246(4932):911–916. doi: 10.1126/science.2683088. [DOI] [PubMed] [Google Scholar]
  37. Weisshaar B., Armstrong G. A., Block A., da Costa e Silva O., Hahlbrock K. Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness. EMBO J. 1991 Jul;10(7):1777–1786. doi: 10.1002/j.1460-2075.1991.tb07702.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES