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. 1994 Feb;6(2):287–301. doi: 10.1105/tpc.6.2.287

PF1: an A-T hook-containing DNA binding protein from rice that interacts with a functionally defined d(AT)-rich element in the oat phytochrome A3 gene promoter.

J Nieto-Sotelo 1, A Ichida 1, P H Quail 1
PMCID: PMC160434  PMID: 8148649

Abstract

Phytochrome-imposed down-regulation of the expression of its own phytochrome A gene (PHYA) is one of the fastest light-induced effects on transcription reported in plants to date. Functional analysis of the oat PHYA3 promoter in a transfection assay has revealed two positive elements, PE1 and PE3, that function synergistically to support high levels of transcription in the absence of light. We have isolated a rice cDNA clone (pR4) encoding a DNA binding protein that binds to the AT-rich PE1 element. We tested the selectivity of the pR4-encoded DNA binding activity using linker substitution mutations of PE1 that are known to disrupt positive expression supported by the PHYA3 promoter in vivo. Binding to these linker substitution mutants was one to two orders of magnitude less than to the native PE1 element. Because this is the behavior expected of positive factor 1 (PF1), the presumptive nuclear transcription factor that acts in trans at the PE1 element in vivo, the data support the conclusion that the protein encoded by pR4 is in fact rice PF1. The PF1 polypeptide encoded by pR4 is 213 amino acids long and contains four repeats of the A-T hook DNA binding motif found in high-mobility group I-Y (HMGI-Y) proteins. In addition, PF1 contains an 11-amino acid-long hydrophobic region characteristic of HMG I proteins, its N-terminal region shows strong similarities to a pea H1 histone sequence and a short peptide sequence from wheat HMGa, and it shows a high degree of similarity along its entire length to the HMG Y-like protein encoded by a soybean cDNA, SB16. In vitro footprinting and quantitative gel shift analyses showed that PF1 binds preferentially to the PE1 element but also at lower affinity to two other AT-rich regions upstream of PE1. This feature is consistent with the binding characteristics of HMG I-Y proteins that are known to bind to most runs of six or more AT base pairs. Taken together, the properties of PF1 suggest that it belongs to a newly described family of nuclear proteins containing both histone H1 domains and A-T hook DNA binding domains.

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Selected References

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  1. Arwood L. J., Spiker S. Binding of wheat and chicken high mobility group chromosomal proteins to DNA and to wheat and chicken mononucleosomes. J Biol Chem. 1990 Jun 15;265(17):9771–9777. [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. Bruce W. B., Christensen A. H., Klein T., Fromm M., Quail P. H. Photoregulation of a phytochrome gene promoter from oat transferred into rice by particle bombardment. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9692–9696. doi: 10.1073/pnas.86.24.9692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bruce W. B., Deng X. W., Quail P. H. A negatively acting DNA sequence element mediates phytochrome-directed repression of phyA gene transcription. EMBO J. 1991 Oct;10(10):3015–3024. doi: 10.1002/j.1460-2075.1991.tb07852.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Churchill M. E., Travers A. A. Protein motifs that recognize structural features of DNA. Trends Biochem Sci. 1991 Mar;16(3):92–97. doi: 10.1016/0968-0004(91)90040-3. [DOI] [PubMed] [Google Scholar]
  7. Cole R. D. A minireview of microheterogeneity in H1 histone and its possible significance. Anal Biochem. 1984 Jan;136(1):24–30. doi: 10.1016/0003-2697(84)90303-8. [DOI] [PubMed] [Google Scholar]
  8. Cushman J. C., Bohnert H. J. Salt stress alters A/T-rich DNA-binding factor interactions within the phosphoenolpyruvate carboxylase promoter from Mesembryanthemum crystallinum. Plant Mol Biol. 1992 Nov;20(3):411–424. doi: 10.1007/BF00040601. [DOI] [PubMed] [Google Scholar]
  9. Czarnecka E., Ingersoll J. C., Gurley W. B. AT-rich promoter elements of soybean heat shock gene Gmhsp17.5E bind two distinct sets of nuclear proteins in vitro. Plant Mol Biol. 1992 Sep;19(6):985–1000. doi: 10.1007/BF00040530. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  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. Eckner R., Birnstiel M. L. Cloning of cDNAs coding for human HMG I and HMG Y proteins: both are capable of binding to the octamer sequence motif. Nucleic Acids Res. 1989 Aug 11;17(15):5947–5959. doi: 10.1093/nar/17.15.5947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fashena S. J., Reeves R., Ruddle N. H. A poly(dA-dT) upstream activating sequence binds high-mobility group I protein and contributes to lymphotoxin (tumor necrosis factor-beta) gene regulation. Mol Cell Biol. 1992 Feb;12(2):894–903. doi: 10.1128/mcb.12.2.894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gantt J. S., Key J. L. Molecular cloning of a pea H1 histone cDNA. Eur J Biochem. 1987 Jul 1;166(1):119–125. doi: 10.1111/j.1432-1033.1987.tb13490.x. [DOI] [PubMed] [Google Scholar]
  16. Gilmartin P. M., Sarokin L., Memelink J., Chua N. H. Molecular light switches for plant genes. Plant Cell. 1990 May;2(5):369–378. doi: 10.1105/tpc.2.5.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grunstein M. Histone function in transcription. Annu Rev Cell Biol. 1990;6:643–678. doi: 10.1146/annurev.cb.06.110190.003235. [DOI] [PubMed] [Google Scholar]
  18. Herbomel P. Synergistic activation of eukaryotic transcription: the multiacceptor target hypothesis. New Biol. 1990 Dec;2(12):1063–1070. [PubMed] [Google Scholar]
  19. Hershey H. P., Barker R. F., Idler K. B., Murray M. G., Quail P. H. Nucleotide sequence and characterization of a gene encoding the phytochrome polypeptide from Avena. Gene. 1987;61(3):339–348. doi: 10.1016/0378-1119(87)90197-1. [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. 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]
  23. Laurent B. C., Treitel M. A., Carlson M. Functional interdependence of the yeast SNF2, SNF5, and SNF6 proteins in transcriptional activation. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2687–2691. doi: 10.1073/pnas.88.7.2687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Laux T., Seurinck J., Goldberg R. B. A soybean embryo cDNA encodes a DNA binding protein with histone and HMG-protein-like domains. Nucleic Acids Res. 1991 Sep 11;19(17):4768–4768. doi: 10.1093/nar/19.17.4768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lissemore J. L., Quail P. H. Rapid transcriptional regulation by phytochrome of the genes for phytochrome and chlorophyll a/b-binding protein in Avena sativa. Mol Cell Biol. 1988 Nov;8(11):4840–4850. doi: 10.1128/mcb.8.11.4840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maier U. G., Grasser K. D., Haass M. M., Feix G. Multiple proteins bind to the P2 promoter region of the zein gene pMS1 of maize. Mol Gen Genet. 1990 Apr;221(2):164–170. doi: 10.1007/BF00261716. [DOI] [PubMed] [Google Scholar]
  27. Mermod N., O'Neill E. A., Kelly T. J., Tjian R. The proline-rich transcriptional activator of CTF/NF-I is distinct from the replication and DNA binding domain. Cell. 1989 Aug 25;58(4):741–753. doi: 10.1016/0092-8674(89)90108-6. [DOI] [PubMed] [Google Scholar]
  28. Pedersen T. J., Arwood L. J., Spiker S., Guiltinan M. J., Thompson W. F. High mobility group chromosomal proteins bind to AT-rich tracts flanking plant genes. Plant Mol Biol. 1991 Jan;16(1):95–104. doi: 10.1007/BF00017920. [DOI] [PubMed] [Google Scholar]
  29. Pederson D. S., Thoma F., Simpson R. T. Core particle, fiber, and transcriptionally active chromatin structure. Annu Rev Cell Biol. 1986;2:117–147. doi: 10.1146/annurev.cb.02.110186.001001. [DOI] [PubMed] [Google Scholar]
  30. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  31. Quail P. H. Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annu Rev Genet. 1991;25:389–409. doi: 10.1146/annurev.ge.25.120191.002133. [DOI] [PubMed] [Google Scholar]
  32. Rochester D. E., Winer J. A., Shah D. M. The structure and expression of maize genes encoding the major heat shock protein, hsp70. EMBO J. 1986 Mar;5(3):451–458. doi: 10.1002/j.1460-2075.1986.tb04233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
  34. Rottmann W. H., Peter G. F., Oeller P. W., Keller J. A., Shen N. F., Nagy B. P., Taylor L. P., Campbell A. D., Theologis A. 1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J Mol Biol. 1991 Dec 20;222(4):937–961. doi: 10.1016/0022-2836(91)90587-v. [DOI] [PubMed] [Google Scholar]
  35. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
  36. Seto D. An improved method for sequencing double stranded plasmid DNA from minipreps using DMSO and modified template preparation. Nucleic Acids Res. 1990 Oct 11;18(19):5905–5906. doi: 10.1093/nar/18.19.5905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shaw D. R., Richter H., Giorda R., Ohmachi T., Ennis H. L. Nucleotide sequences of Dictyostelium discoideum developmentally regulated cDNAs rich in (AAC) imply proteins that contain clusters of asparagine, glutamine, or threonine. Mol Gen Genet. 1989 Sep;218(3):453–459. doi: 10.1007/BF00332409. [DOI] [PubMed] [Google Scholar]
  38. Struhl K. Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8419–8423. doi: 10.1073/pnas.82.24.8419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thanos D., Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell. 1992 Nov 27;71(5):777–789. doi: 10.1016/0092-8674(92)90554-p. [DOI] [PubMed] [Google Scholar]
  40. Vinson C. R., LaMarco K. L., Johnson P. F., Landschulz W. H., McKnight S. L. In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. Genes Dev. 1988 Jul;2(7):801–806. doi: 10.1101/gad.2.7.801. [DOI] [PubMed] [Google Scholar]
  41. Wu R. S., Panusz H. T., Hatch C. L., Bonner W. M. Histones and their modifications. CRC Crit Rev Biochem. 1986;20(2):201–263. doi: 10.3109/10409238609083735. [DOI] [PubMed] [Google Scholar]
  42. Zhao K., Käs E., Gonzalez E., Laemmli U. K. SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J. 1993 Aug;12(8):3237–3247. doi: 10.1002/j.1460-2075.1993.tb05993.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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