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. 1998 May;10(5):837–847. doi: 10.1105/tpc.10.5.837

14-3-3 proteins are part of an abscisic acid-VIVIPAROUS1 (VP1) response complex in the Em promoter and interact with VP1 and EmBP1.

T F Schultz 1, J Medina 1, A Hill 1, R S Quatrano 1
PMCID: PMC144375  PMID: 9596641

Abstract

Protein-DNA complexes were formed when nuclear extracts from embryogenic rice suspension cultures or maize embryos were incubated with an abscisic acid-VIVIPAROUS1 (VP1) response element (Em1a) from the Em promoter. Monoclonal antibodies generated to GF14, a 14-3-3 protein from plants, resulted in gel retardation of the Em1a-protein complexes. Antibodies generated to the C and N termini of GF14 detected protein isoforms in rice nuclear and cytoplasmic extracts, but no differences in distribution of the GF14 isoforms were recognized between the nucleus and cytoplasm or when abscisic acid-treated and untreated tissues were compared. When recombinant GF14 fusion proteins from rice were added to nuclear extracts, novel complexes were formed that required the dimerization domain of GF14. Chemical cross-linking showed that GF-14 interacted with the basic leucine zipper factor EmBP1, which binds specifically to Em1a, and with VP1, which transactivates Em through Em1a. GF14 proteins from rice were shown to interact with VP1 in yeast through the dimerization domain of GF14. Our results indicated that GF14 interacts with both site-specific DNA binding proteins (i.e., EmBP1) and tissue-specific regulatory factors (i.e., VP1) and may provide a structural link between VP1 and the Em1a transcriptional complex.

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Selected References

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  1. Aitken A. 14-3-3 and its possible role in co-ordinating multiple signalling pathways. Trends Cell Biol. 1996 Sep;6(9):341–347. doi: 10.1016/0962-8924(96)10029-5. [DOI] [PubMed] [Google Scholar]
  2. Bobb A. J., Eiben H. G., Bustos M. M. PvAlf, an embryo-specific acidic transcriptional activator enhances gene expression from phaseolin and phytohemagglutinin promoters. Plant J. 1995 Sep;8(3):331–343. doi: 10.1046/j.1365-313x.1995.08030331.x. [DOI] [PubMed] [Google Scholar]
  3. Chen Z., Fu H., Liu D., Chang P. F., Narasimhan M., Ferl R., Hasegawa P. M., Bressan R. A. A NaCl-regulated plant gene encoding a brain protein homology that activates ADP ribosyltransferase and inhibits protein kinase C. Plant J. 1994 Nov;6(5):729–740. doi: 10.1046/j.1365-313x.1994.6050729.x. [DOI] [PubMed] [Google Scholar]
  4. Daugherty C. J., Rooney M. F., Miller P. W., Ferl R. J. Molecular organization and tissue-specific expression of an Arabidopsis 14-3-3 gene. Plant Cell. 1996 Aug;8(8):1239–1248. doi: 10.1105/tpc.8.8.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Estojak J., Brent R., Golemis E. A. Correlation of two-hybrid affinity data with in vitro measurements. Mol Cell Biol. 1995 Oct;15(10):5820–5829. doi: 10.1128/mcb.15.10.5820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ferl Robert J. 14-3-3 PROTEINS AND SIGNAL TRANSDUCTION. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):49–73. doi: 10.1146/annurev.arplant.47.1.49. [DOI] [PubMed] [Google Scholar]
  7. Finkelstein R. R. Abscisic acid-insensitive mutations provide evidence for stage-specific signal pathways regulating expression of an Arabidopsis late embryogenesis-abundant (lea) gene. Mol Gen Genet. 1993 Apr;238(3):401–408. doi: 10.1007/BF00291999. [DOI] [PubMed] [Google Scholar]
  8. Giraudat J., Hauge B. M., Valon C., Smalle J., Parcy F., Goodman H. M. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell. 1992 Oct;4(10):1251–1261. doi: 10.1105/tpc.4.10.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giraudat J., Parcy F., Bertauche N., Gosti F., Leung J., Morris P. C., Bouvier-Durand M., Vartanian N. Current advances in abscisic acid action and signalling. Plant Mol Biol. 1994 Dec;26(5):1557–1577. doi: 10.1007/BF00016490. [DOI] [PubMed] [Google Scholar]
  10. Goodrich J. A., Cutler G., Tjian R. Contacts in context: promoter specificity and macromolecular interactions in transcription. Cell. 1996 Mar 22;84(6):825–830. doi: 10.1016/s0092-8674(00)81061-2. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Hattori T., Terada T., Hamasuna S. T. Sequence and functional analyses of the rice gene homologous to the maize Vp1. Plant Mol Biol. 1994 Mar;24(5):805–810. doi: 10.1007/BF00029862. [DOI] [PubMed] [Google Scholar]
  13. Hattori T., Terada T., Hamasuna S. Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J. 1995 Jun;7(6):913–925. doi: 10.1046/j.1365-313x.1995.07060913.x. [DOI] [PubMed] [Google Scholar]
  14. Hill A., Nantel A., Rock C. D., Quatrano R. S. A conserved domain of the viviparous-1 gene product enhances the DNA binding activity of the bZIP protein EmBP-1 and other transcription factors. J Biol Chem. 1996 Feb 16;271(7):3366–3374. doi: 10.1074/jbc.271.7.3366. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Jahn T., Fuglsang A. T., Olsson A., Brüntrup I. M., Collinge D. B., Volkmann D., Sommarin M., Palmgren M. G., Larsson C. The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. Plant Cell. 1997 Oct;9(10):1805–1814. doi: 10.1105/tpc.9.10.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jones H. D., Peters N. C., Holdsworth M. J. Genotype and environment interact to control dormancy and differential expression of the VIVIPAROUS 1 homologue in embryos of Avena fatua. Plant J. 1997 Oct;12(4):911–920. doi: 10.1046/j.1365-313x.1997.12040911.x. [DOI] [PubMed] [Google Scholar]
  18. Kidou S., Umeda M., Kato A., Uchimiya H. Isolation and characterization of a rice cDNA similar to the bovine brain-specific 14-3-3 protein gene. Plant Mol Biol. 1993 Jan;21(1):191–194. doi: 10.1007/BF00039631. [DOI] [PubMed] [Google Scholar]
  19. Knetsch MLW., Wang M., Snaar-Jagalska B. E., Heimovaara-Dijkstra S. Abscisic Acid Induces Mitogen-Activated Protein Kinase Activation in Barley Aleurone Protoplasts. Plant Cell. 1996 Jun;8(6):1061–1067. doi: 10.1105/tpc.8.6.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leung J., Bouvier-Durand M., Morris P. C., Guerrier D., Chefdor F., Giraudat J. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science. 1994 Jun 3;264(5164):1448–1452. doi: 10.1126/science.7910981. [DOI] [PubMed] [Google Scholar]
  21. Leung J., Merlot S., Giraudat J. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell. 1997 May;9(5):759–771. doi: 10.1105/tpc.9.5.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Liu D., Bienkowska J., Petosa C., Collier R. J., Fu H., Liddington R. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature. 1995 Jul 13;376(6536):191–194. doi: 10.1038/376191a0. [DOI] [PubMed] [Google Scholar]
  23. Lu G., DeLisle A. J., de Vetten N. C., Ferl R. J. Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11490–11494. doi: 10.1073/pnas.89.23.11490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lu G., Sehnke P. C., Ferl R. J. Phosphorylation and calcium binding properties of an Arabidopsis GF14 brain protein homolog. Plant Cell. 1994 Apr;6(4):501–510. doi: 10.1105/tpc.6.4.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marcotte W. R., Jr, Russell S. H., Quatrano R. S. Abscisic acid-responsive sequences from the em gene of wheat. Plant Cell. 1989 Oct;1(10):969–976. doi: 10.1105/tpc.1.10.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marra M., Fullone M. R., Fogliano V., Pen J., Mattei M., Masi S., Aducci P. The 30-kilodalton protein present in purified fusicoccin receptor preparations is a 14-3-3-like protein. Plant Physiol. 1994 Dec;106(4):1497–1501. doi: 10.1104/pp.106.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McCarty D. R., Carson C. B., Stinard P. S., Robertson D. S. Molecular Analysis of viviparous-1: An Abscisic Acid-Insensitive Mutant of Maize. Plant Cell. 1989 May;1(5):523–532. doi: 10.1105/tpc.1.5.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Meyer K., Leube M. P., Grill E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science. 1994 Jun 3;264(5164):1452–1455. doi: 10.1126/science.8197457. [DOI] [PubMed] [Google Scholar]
  30. Muslin A. J., Tanner J. W., Allen P. M., Shaw A. S. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell. 1996 Mar 22;84(6):889–897. doi: 10.1016/s0092-8674(00)81067-3. [DOI] [PubMed] [Google Scholar]
  31. Nantel A., Quatrano R. S. Characterization of three rice basic/leucine zipper factors, including two inhibitors of EmBP-1 DNA binding activity. J Biol Chem. 1996 Dec 6;271(49):31296–31305. doi: 10.1074/jbc.271.49.31296. [DOI] [PubMed] [Google Scholar]
  33. Parcy F., Valon C., Raynal M., Gaubier-Comella P., Delseny M., Giraudat J. Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell. 1994 Nov;6(11):1567–1582. doi: 10.1105/tpc.6.11.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pei Z. M., Kuchitsu K., Ward J. M., Schwarz M., Schroeder J. I. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell. 1997 Mar;9(3):409–423. doi: 10.1105/tpc.9.3.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Razik M. A., Quatrano R. S. Effect of the nuclear factors EmBP1 and viviparous1 on the transcription of the Em gene in HeLa nuclear extracts. Plant Cell. 1997 Oct;9(10):1791–1803. doi: 10.1105/tpc.9.10.1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rock C. D., Quatrano R. S. Plant regulators. Insensitivity is in the genes. Curr Biol. 1994 Nov 1;4(11):1013–1015. doi: 10.1016/s0960-9822(00)00229-3. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Schultz T. F., Quatrano R. S. Characterization and expression of a rice RAD23 gene. Plant Mol Biol. 1997 Jun;34(3):557–562. doi: 10.1023/a:1005870227632. [DOI] [PubMed] [Google Scholar]
  39. Strynadka N. C., James M. N. Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem. 1989;58:951–998. doi: 10.1146/annurev.bi.58.070189.004511. [DOI] [PubMed] [Google Scholar]
  40. Suzuki M., Kao C. Y., McCarty D. R. The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell. 1997 May;9(5):799–807. doi: 10.1105/tpc.9.5.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vasil V., Marcotte W. R., Jr, Rosenkrans L., Cocciolone S. M., Vasil I. K., Quatrano R. S., McCarty D. R. Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell. 1995 Sep;7(9):1511–1518. doi: 10.1105/tpc.7.9.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wu K., Rooney M. F., Ferl R. J. The Arabidopsis 14-3-3 multigene family. Plant Physiol. 1997 Aug;114(4):1421–1431. doi: 10.1104/pp.114.4.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. de Vetten N. C., Lu G., Feri R. J. A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. Plant Cell. 1992 Oct;4(10):1295–1307. doi: 10.1105/tpc.4.10.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]

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