Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1997 Aug;114(4):1421–1431. doi: 10.1104/pp.114.4.1421

The Arabidopsis 14-3-3 multigene family.

K Wu 1, M F Rooney 1, R J Ferl 1
PMCID: PMC158435  PMID: 9276953

Abstract

The 14-3-3 proteins are ubiquitous eukaryotic proteins and are encoded by a gene family in many species. We examined the 14-3-3 gene family in Arabidopsis thaliana and found that it contains 10 members. Four new cDNAs, GF14 epsilon, GF14 kappa, GF14 mu, and GF14 nu, and two new genomic clones of GF14 phi and GF14 nu were isolated and characterized. Together with the six previously described 14-3-3 isoforms in Arabidopsis, they constitute a complete family of 10 distinct 14-3-3 proteins of 248 to 268 amino acids. Phylogenetic analysis revealed the presence of two ancient, distinct 14-3-3 gene classes in Arabidopsis and other plants. The epsilon forms diverged early from the other plant isoforms, and plant 14-3-3 genes displayed a different evolutionary course from that of mammals.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. Aitken A. 14-3-3 proteins on the MAP. Trends Biochem Sci. 1995 Mar;20(3):95–97. doi: 10.1016/s0968-0004(00)88971-9. [DOI] [PubMed] [Google Scholar]
  2. Alam R., Hachiya N., Sakaguchi M., Kawabata S., Iwanaga S., Kitajima M., Mihara K., Omura T. cDNA cloning and characterization of mitochondrial import stimulation factor (MSF) purified from rat liver cytosol. J Biochem. 1994 Aug;116(2):416–425. doi: 10.1093/oxfordjournals.jbchem.a124541. [DOI] [PubMed] [Google Scholar]
  3. Bachmann M., Huber J. L., Athwal G. S., Wu K., Ferl R. J., Huber S. C. 14-3-3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation of Ser-543 by endogenous protein phosphatases. FEBS Lett. 1996 Nov 25;398(1):26–30. doi: 10.1016/s0014-5793(96)01188-x. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chong S. S., Tanigami A., Roschke A. V., Ledbetter D. H. 14-3-3 epsilon has no homology to LIS1 and lies telomeric to it on chromosome 17p13.3 outside the Miller-Dieker syndrome chromosome region. Genome Res. 1996 Aug;6(8):735–741. doi: 10.1101/gr.6.8.735. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Fantl W. J., Muslin A. J., Kikuchi A., Martin J. A., MacNicol A. M., Gross R. W., Williams L. T. Activation of Raf-1 by 14-3-3 proteins. Nature. 1994 Oct 13;371(6498):612–614. doi: 10.1038/371612a0. [DOI] [PubMed] [Google Scholar]
  8. Ferl R. J., Lu G., Bowen B. W. Evolutionary implications of the family of 14-3-3 brain protein homologs in Arabidopsis thaliana. Genetica. 1994;92(2):129–138. doi: 10.1007/BF00163762. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Ford J. C., al-Khodairy F., Fotou E., Sheldrick K. S., Griffiths D. J., Carr A. M. 14-3-3 protein homologs required for the DNA damage checkpoint in fission yeast. Science. 1994 Jul 22;265(5171):533–535. doi: 10.1126/science.8036497. [DOI] [PubMed] [Google Scholar]
  12. Freed E., Symons M., Macdonald S. G., McCormick F., Ruggieri R. Binding of 14-3-3 proteins to the protein kinase Raf and effects on its activation. Science. 1994 Sep 16;265(5179):1713–1716. doi: 10.1126/science.8085158. [DOI] [PubMed] [Google Scholar]
  13. Fu H., Xia K., Pallas D. C., Cui C., Conroy K., Narsimhan R. P., Mamon H., Collier R. J., Roberts T. M. Interaction of the protein kinase Raf-1 with 14-3-3 proteins. Science. 1994 Oct 7;266(5182):126–129. doi: 10.1126/science.7939632. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Irie K., Gotoh Y., Yashar B. M., Errede B., Nishida E., Matsumoto K. Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf protein kinase. Science. 1994 Sep 16;265(5179):1716–1719. doi: 10.1126/science.8085159. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Korthout H. A., de Boer A. H. A fusicoccin binding protein belongs to the family of 14-3-3 brain protein homologs. Plant Cell. 1994 Nov;6(11):1681–1692. doi: 10.1105/tpc.6.11.1681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lu G., Rooney M. F., Wu K., Ferl R. J. Five cDNAs encoding Arabidopsis GF14 proteins. Plant Physiol. 1994 Aug;105(4):1459–1460. doi: 10.1104/pp.105.4.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lu G., de Vetten N. C., Sehnke P. C., Isobe T., Ichimura T., Fu H., van Heusden G. P., Ferl R. J. A single Arabidopsis GF14 isoform possesses biochemical characteristics of diverse 14-3-3 homologues. Plant Mol Biol. 1994 Jul;25(4):659–667. doi: 10.1007/BF00029604. [DOI] [PubMed] [Google Scholar]
  20. Muratake T., Hayashi S., Ichikawa T., Kumanishi T., Ichimura Y., Kuwano R., Isobe T., Wang Y., Minoshima S., Shimizu N. Structural organization and chromosomal assignment of the human 14-3-3 eta chain gene (YWHAH). Genomics. 1996 Aug 15;36(1):63–69. doi: 10.1006/geno.1996.0426. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Nielsen P. J. Primary structure of a human protein kinase regulator protein. Biochim Biophys Acta. 1991 Mar 26;1088(3):425–428. doi: 10.1016/0167-4781(91)90136-a. [DOI] [PubMed] [Google Scholar]
  23. Oecking C., Eckerskorn C., Weiler E. W. The fusicoccin receptor of plants is a member of the 14-3-3 superfamily of eukaryotic regulatory proteins. FEBS Lett. 1994 Sep 26;352(2):163–166. doi: 10.1016/0014-5793(94)00949-x. [DOI] [PubMed] [Google Scholar]
  24. Pallas D. C., Fu H., Haehnel L. C., Weller W., Collier R. J., Roberts T. M. Association of polyomavirus middle tumor antigen with 14-3-3 proteins. Science. 1994 Jul 22;265(5171):535–537. doi: 10.1126/science.8036498. [DOI] [PubMed] [Google Scholar]
  25. Reuther G. W., Fu H., Cripe L. D., Collier R. J., Pendergast A. M. Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family. Science. 1994 Oct 7;266(5182):129–133. doi: 10.1126/science.7939633. [DOI] [PubMed] [Google Scholar]
  26. Rooney M. F., Ferl R. J. Sequences of three Arabidopsis general regulatory factor genes encoding GF14 (14-3-3) proteins. Plant Physiol. 1995 Jan;107(1):283–284. doi: 10.1104/pp.107.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roseboom P. H., Weller J. L., Babila T., Aitken A., Sellers L. A., Moffett J. R., Namboodiri M. A., Klein D. C. Cloning and characterization of the epsilon and zeta isoforms of the 14-3-3 proteins. DNA Cell Biol. 1994 Jun;13(6):629–640. doi: 10.1089/dna.1994.13.629. [DOI] [PubMed] [Google Scholar]
  28. Stanković B., Garić-Stanković A., Smith C. M., Davies E. Isolation, sequencing, and analysis of a 14-3-3 brain protein homolog from pea (Pisum sativum L.). Plant Physiol. 1995 Apr;107(4):1481–1482. doi: 10.1104/pp.107.4.1481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tanji M., Horwitz R., Rosenfeld G., Waymire J. C. Activation of protein kinase C by purified bovine brain 14-3-3: comparison with tyrosine hydroxylase activation. J Neurochem. 1994 Nov;63(5):1908–1916. doi: 10.1046/j.1471-4159.1994.63051908.x. [DOI] [PubMed] [Google Scholar]
  30. Toker A., Sellers L. A., Amess B., Patel Y., Harris A., Aitken A. Multiple isoforms of a protein kinase C inhibitor (KCIP-1/14-3-3) from sheep brain. Amino acid sequence of phosphorylated forms. Eur J Biochem. 1992 Jun 1;206(2):453–461. doi: 10.1111/j.1432-1033.1992.tb16946.x. [DOI] [PubMed] [Google Scholar]
  31. Watanabe M., Isobe T., Ichimura T., Kuwano R., Takahashi Y., Kondo H. Molecular cloning of rat cDNAs for beta and gamma subtypes of 14-3-3 protein and developmental changes in expression of their mRNAs in the nervous system. Brain Res Mol Brain Res. 1993 Jan;17(1-2):135–146. doi: 10.1016/0169-328x(93)90082-z. [DOI] [PubMed] [Google Scholar]
  32. Watanabe M., Isobe T., Okuyama T., Ichimura T., Kuwano R., Takahashi Y., Kondo H. Molecular cloning of cDNA to rat 14-3-3 eta chain polypeptide and the neuronal expression of the mRNA in the central nervous system. Brain Res Mol Brain Res. 1991 May;10(2):151–158. doi: 10.1016/0169-328x(91)90105-7. [DOI] [PubMed] [Google Scholar]
  33. Zupan L. A., Steffens D. L., Berry C. A., Landt M., Gross R. W. Cloning and expression of a human 14-3-3 protein mediating phospholipolysis. Identification of an arachidonoyl-enzyme intermediate during catalysis. J Biol Chem. 1992 May 5;267(13):8707–8710. [PubMed] [Google Scholar]
  34. de Vetten N. C., Ferl R. J. Transcriptional regulation of environmentally inducible genes in plants by an evolutionary conserved family of G-box binding factors. Int J Biochem. 1994 Sep;26(9):1055–1068. doi: 10.1016/0020-711x(94)90128-7. [DOI] [PubMed] [Google Scholar]
  35. de Vetten N. C., Ferl R. J. Two genes encoding GF14 (14-3-3) proteins in Zea mays. Structure, expression, and potential regulation by the G-box binding complex. Plant Physiol. 1994 Dec;106(4):1593–1604. doi: 10.1104/pp.106.4.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. van Heusden G. P., Griffiths D. J., Ford J. C., Chin-A-Woeng T. F., Schrader P. A., Carr A. M., Steensma H. Y. The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. Eur J Biochem. 1995 Apr 1;229(1):45–53. [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES