Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1998 Jan;10(1):75–89. doi: 10.1105/tpc.10.1.75

Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression.

S Yanagisawa 1, J Sheen 1
PMCID: PMC143930  PMID: 9477573

Abstract

Dof is a novel family of plant proteins that share a unique and highly conserved DNA binding domain with one C2-C2 zinc finger motif. Although multiple Dof proteins associated with diverse gene promoters have recently been identified in a variety of plants, their physiological functions and regulation remain elusive. In maize, Dof1 (MNB1a) is constitutively expressed in leaves, stems, and roots, whereas the closely related Dof2 is expressed mainly in stems and roots. Here, by using a maize leaf protoplast transient assay, we show that Dof1 is a transcriptional activator, whereas Dof2 can act as a transcriptional repressor. Thus, differential expression of Dof1 and Dof2 may permit leaf-specific gene expression. Interestingly, in vivo analyses showed that although DNA binding activity of Dof1 is regulated by light-dependent development, its transactivation activity and nuclear localization are not. Moreover, in vivo transcription and in vitro electrophoretic mobility shift assays revealed that Dof1 can interact specifically with the maize C4 phosphoenolpyruvate carboxylase gene promoter and enhance its promoter activity, which displays a light-regulated expression pattern matching Dof1 activity. We propose that the evolutionarily conserved Dof proteins can function as transcriptional activators or repressors of tissue-specific and light-regulated gene expression in plants.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

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

  1. Baranowskij N., Frohberg C., Prat S., Willmitzer L. A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J. 1994 Nov 15;13(22):5383–5392. doi: 10.1002/j.1460-2075.1994.tb06873.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benfey P. N., Chua N. H. The Cauliflower Mosaic Virus 35S Promoter: Combinatorial Regulation of Transcription in Plants. Science. 1990 Nov 16;250(4983):959–966. doi: 10.1126/science.250.4983.959. [DOI] [PubMed] [Google Scholar]
  3. Björklund S., Kim Y. J. Mediator of transcriptional regulation. Trends Biochem Sci. 1996 Sep;21(9):335–337. doi: 10.1016/s0968-0004(96)10051-7. [DOI] [PubMed] [Google Scholar]
  4. Chen W., Chao G., Singh K. B. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J. 1996 Dec;10(6):955–966. doi: 10.1046/j.1365-313x.1996.10060955.x. [DOI] [PubMed] [Google Scholar]
  5. Chiu W., Niwa Y., Zeng W., Hirano T., Kobayashi H., Sheen J. Engineered GFP as a vital reporter in plants. Curr Biol. 1996 Mar 1;6(3):325–330. doi: 10.1016/s0960-9822(02)00483-9. [DOI] [PubMed] [Google Scholar]
  6. Chory J., Chatterjee M., Cook R. K., Elich T., Fankhauser C., Li J., Nagpal P., Neff M., Pepper A., Poole D. From seed germination to flowering, light controls plant development via the pigment phytochrome. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12066–12071. doi: 10.1073/pnas.93.22.12066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chory J. Out of darkness: mutants reveal pathways controlling light-regulated development in plants. Trends Genet. 1993 May;9(5):167–172. doi: 10.1016/0168-9525(93)90163-c. [DOI] [PubMed] [Google Scholar]
  8. Christensen A. H., Sharrock R. A., Quail P. H. Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol. 1992 Feb;18(4):675–689. doi: 10.1007/BF00020010. [DOI] [PubMed] [Google Scholar]
  9. Crétin C., Santi S., Keryer E., Lepiniec L., Tagu D., Vidal J., Gadal P. The phosphoenolpyruvate carboxylase gene family of Sorghum: promoter structures, amino acid sequences and expression of genes. Gene. 1991 Mar 1;99(1):87–94. doi: 10.1016/0378-1119(91)90037-c. [DOI] [PubMed] [Google Scholar]
  10. De Paolis A., Sabatini S., De Pascalis L., Costantino P., Capone I. A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J. 1996 Aug;10(2):215–223. doi: 10.1046/j.1365-313x.1996.10020215.x. [DOI] [PubMed] [Google Scholar]
  11. Degenhardt J., Tobin E. M. A DNA binding activity for one of two closely defined phytochrome regulatory elements in an Lhcb promoter is more abundant in etiolated than in green plants. Plant Cell. 1996 Jan;8(1):31–41. doi: 10.1105/tpc.8.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dehesh K., Bruce W. B., Quail P. H. A trans-acting factor that binds to a GT-motif in a phytochrome gene promoter. Science. 1990 Dec 7;250(4986):1397–1399. doi: 10.1126/science.2255908. [DOI] [PubMed] [Google Scholar]
  13. Dehesh K., Hung H., Tepperman J. M., Quail P. H. GT-2: a transcription factor with twin autonomous DNA-binding domains of closely related but different target sequence specificity. EMBO J. 1992 Nov;11(11):4131–4144. doi: 10.1002/j.1460-2075.1992.tb05506.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilmartin P. M., Memelink J., Hiratsuka K., Kay S. A., Chua N. H. Characterization of a gene encoding a DNA binding protein with specificity for a light-responsive element. Plant Cell. 1992 Jul;4(7):839–849. doi: 10.1105/tpc.4.7.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Green P. J., Kay S. A., Chua N. H. Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J. 1987 Sep;6(9):2543–2549. doi: 10.1002/j.1460-2075.1987.tb02542.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hagen G., Müller S., Beato M., Suske G. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 1994 Aug 15;13(16):3843–3851. doi: 10.1002/j.1460-2075.1994.tb06695.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Izawa T., Foster R., Chua N. H. Plant bZIP protein DNA binding specificity. J Mol Biol. 1993 Apr 20;230(4):1131–1144. doi: 10.1006/jmbi.1993.1230. [DOI] [PubMed] [Google Scholar]
  19. Izawa T., Foster R., Nakajima M., Shimamoto K., Chua N. H. The rice bZIP transcriptional activator RITA-1 is highly expressed during seed development. Plant Cell. 1994 Sep;6(9):1277–1287. doi: 10.1105/tpc.6.9.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jang J. C., Sheen J. Sugar sensing in higher plants. Plant Cell. 1994 Nov;6(11):1665–1679. doi: 10.1105/tpc.6.11.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Katagiri F., Chua N. H. Plant transcription factors: present knowledge and future challenges. Trends Genet. 1992 Jan;8(1):22–27. doi: 10.1016/0168-9525(92)90020-5. [DOI] [PubMed] [Google Scholar]
  23. Katagiri F., Yamazaki K., Horikoshi M., Roeder R. G., Chua N. H. A plant DNA-binding protein increases the number of active preinitiation complexes in a human in vitro transcription system. Genes Dev. 1990 Nov;4(11):1899–1909. doi: 10.1101/gad.4.11.1899. [DOI] [PubMed] [Google Scholar]
  24. Kehoe D. M., Degenhardt J., Winicov I., Tobin E. M. Two 10-bp regions are critical for phytochrome regulation of a Lemna gibba Lhcb gene promoter. Plant Cell. 1994 Aug;6(8):1123–1134. doi: 10.1105/tpc.6.8.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ku M. S., Kano-Murakami Y., Matsuoka M. Evolution and expression of C4 photosynthesis genes. Plant Physiol. 1996 Aug;111(4):949–957. doi: 10.1104/pp.111.4.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lam E., Chua N. H. GT-1 binding site confers light responsive expression in transgenic tobacco. Science. 1990 Apr 27;248(4954):471–474. doi: 10.1126/science.2330508. [DOI] [PubMed] [Google Scholar]
  27. Lam E., Kano-Murakami Y., Gilmartin P., Niner B., Chua N. H. A metal-dependent DNA-binding protein interacts with a constitutive element of a light-responsive promoter. Plant Cell. 1990 Sep;2(9):857–866. doi: 10.1105/tpc.2.9.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Langdale J. A., Taylor W. C., Nelson T. Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site greater than 3 kb upstream of the gene. Mol Gen Genet. 1991 Jan;225(1):49–55. doi: 10.1007/BF00282641. [DOI] [PubMed] [Google Scholar]
  29. Lohmer S., Maddaloni M., Motto M., Di Fonzo N., Hartings H., Salamini F., Thompson R. D. The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO J. 1991 Mar;10(3):617–624. doi: 10.1002/j.1460-2075.1991.tb07989.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ma J., Przibilla E., Hu J., Bogorad L., Ptashne M. Yeast activators stimulate plant gene expression. Nature. 1988 Aug 18;334(6183):631–633. doi: 10.1038/334631a0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Martin C., Paz-Ares J. MYB transcription factors in plants. Trends Genet. 1997 Feb;13(2):67–73. doi: 10.1016/s0168-9525(96)10049-4. [DOI] [PubMed] [Google Scholar]
  33. Menkens A. E., Schindler U., Cashmore A. R. The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci. 1995 Dec;20(12):506–510. doi: 10.1016/s0968-0004(00)89118-5. [DOI] [PubMed] [Google Scholar]
  34. Millar A. J., McGrath R. B., Chua N. H. Phytochrome phototransduction pathways. Annu Rev Genet. 1994;28:325–349. doi: 10.1146/annurev.ge.28.120194.001545. [DOI] [PubMed] [Google Scholar]
  35. Ni M., Dehesh K., Tepperman J. M., Quail P. H. GT-2: in vivo transcriptional activation activity and definition of novel twin DNA binding domains with reciprocal target sequence selectivity. Plant Cell. 1996 Jun;8(6):1041–1059. doi: 10.1105/tpc.8.6.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Perisic O., Lam E. A tobacco DNA binding protein that interacts with a light-responsive box II element. Plant Cell. 1992 Jul;4(7):831–838. doi: 10.1105/tpc.4.7.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. Phytochromes: photosensory perception and signal transduction. Science. 1995 May 5;268(5211):675–680. doi: 10.1126/science.7732376. [DOI] [PubMed] [Google Scholar]
  39. Raikhel N. Nuclear targeting in plants. Plant Physiol. 1992 Dec;100(4):1627–1632. doi: 10.1104/pp.100.4.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sablowski R. W., Moyano E., Culianez-Macia F. A., Schuch W., Martin C., Bevan M. A flower-specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. EMBO J. 1994 Jan 1;13(1):128–137. doi: 10.1002/j.1460-2075.1994.tb06242.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sarokin L. P., Chua N. H. Binding sites for two novel phosphoproteins, 3AF5 and 3AF3, are required for rbcS-3A expression. Plant Cell. 1992 Apr;4(4):473–483. doi: 10.1105/tpc.4.4.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schindler U., Cashmore A. R. Photoregulated gene expression may involve ubiquitous DNA binding proteins. EMBO J. 1990 Nov;9(11):3415–3427. doi: 10.1002/j.1460-2075.1990.tb07549.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Schindler U., Terzaghi W., Beckmann H., Kadesch T., Cashmore A. R. DNA binding site preferences and transcriptional activation properties of the Arabidopsis transcription factor GBF1. EMBO J. 1992 Apr;11(4):1275–1289. doi: 10.1002/j.1460-2075.1992.tb05171.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Schmidt R. J., Ketudat M., Aukerman M. J., Hoschek G. Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell. 1992 Jun;4(6):689–700. doi: 10.1105/tpc.4.6.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schäffner A. R., Sheen J. Maize C4 photosynthesis involves differential regulation of phosphoenolpyruvate carboxylase genes. Plant J. 1992 Mar;2(2):221–232. doi: 10.1046/j.1365-313x.1992.t01-44-00999.x. [DOI] [PubMed] [Google Scholar]
  47. Schäffner A. R., Sheen J. Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell. 1991 Sep;3(9):997–1012. doi: 10.1105/tpc.3.9.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sheen J. Y., Bogorad L. Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem. 1987 Aug 25;262(24):11726–11730. [PubMed] [Google Scholar]
  49. Sheen J. Ca2+-dependent protein kinases and stress signal transduction in plants. Science. 1996 Dec 13;274(5294):1900–1902. doi: 10.1126/science.274.5294.1900. [DOI] [PubMed] [Google Scholar]
  50. Sheen J., Hwang S., Niwa Y., Kobayashi H., Galbraith D. W. Green-fluorescent protein as a new vital marker in plant cells. Plant J. 1995 Nov;8(5):777–784. doi: 10.1046/j.1365-313x.1995.08050777.x. [DOI] [PubMed] [Google Scholar]
  51. Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990 Oct;2(10):1027–1038. doi: 10.1105/tpc.2.10.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sheen J. Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell. 1991 Mar;3(3):225–245. doi: 10.1105/tpc.3.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sheen J. Protein phosphatase activity is required for light-inducible gene expression in maize. EMBO J. 1993 Sep;12(9):3497–3505. doi: 10.1002/j.1460-2075.1993.tb06024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Solano R., Nieto C., Avila J., Cañas L., Diaz I., Paz-Ares J. Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J. 1995 Apr 18;14(8):1773–1784. doi: 10.1002/j.1460-2075.1995.tb07166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Staiger D., Kaulen H., Schell J. A CACGTG motif of the Antirrhinum majus chalcone synthase promoter is recognized by an evolutionarily conserved nuclear protein. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6930–6934. doi: 10.1073/pnas.86.18.6930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sun L., Liu A., Georgopoulos K. Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J. 1996 Oct 1;15(19):5358–5369. [PMC free article] [PubMed] [Google Scholar]
  57. Urao T., Noji M., Yamaguchi-Shinozaki K., Shinozaki K. A transcriptional activation domain of ATMYB2, a drought-inducible Arabidopsis Myb-related protein. Plant J. 1996 Dec;10(6):1145–1148. doi: 10.1046/j.1365-313x.1996.10061145.x. [DOI] [PubMed] [Google Scholar]
  58. Vicente-Carbajosa J., Moose S. P., Parsons R. L., Schmidt R. J. A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7685–7690. doi: 10.1073/pnas.94.14.7685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Von Arnim Albrecht, Deng Xing-Wang. LIGHT CONTROL OF SEEDLING DEVELOPMENT. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):215–243. doi: 10.1146/annurev.arplant.47.1.215. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Yanagisawa S. A novel DNA-binding domain that may form a single zinc finger motif. Nucleic Acids Res. 1995 Sep 11;23(17):3403–3410. doi: 10.1093/nar/23.17.3403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Yanagisawa S. A novel multigene family that the gene for a maize DNA-binding protein, MNB1a belongs to: isolation of genomic clones from this family and some aspects of its molecular evolution. Biochem Mol Biol Int. 1996 Apr;38(4):665–673. [PubMed] [Google Scholar]
  63. Yanagisawa S. Dof DNA-binding domains of plant transcription factors contribute to multiple protein-protein interactions. Eur J Biochem. 1997 Dec 1;250(2):403–410. doi: 10.1111/j.1432-1033.1997.0403a.x. [DOI] [PubMed] [Google Scholar]
  64. Yanagisawa S., Izui K. Maize phosphoenolpyruvate carboxylase involved in C4 photosynthesis: nucleotide sequence analysis of the 5' flanking region of the gene. J Biochem. 1989 Dec;106(6):982–987. doi: 10.1093/oxfordjournals.jbchem.a122986. [DOI] [PubMed] [Google Scholar]
  65. Yanagisawa S., Izui K. Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. J Biol Chem. 1993 Jul 25;268(21):16028–16036. [PubMed] [Google Scholar]
  66. Zhang B., Chen W., Foley R. C., Büttner M., Singh K. B. Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell. 1995 Dec;7(12):2241–2252. doi: 10.1105/tpc.7.12.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES