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. 1998 Jun;10(6):995–1007. doi: 10.1105/tpc.10.6.995

Identification of a negative regulator of gibberellin action, HvSPY, in barley.

M Robertson 1, S M Swain 1, P M Chandler 1, N E Olszewski 1
PMCID: PMC144045  PMID: 9634587

Abstract

To broaden our understanding of the molecular mechanisms of gibberellin (GA) action, we isolated a spindly clone (HvSPY) from barley cultivar Himalaya and tested whether the HvSPY protein would modulate GA action in barley aleurone. The HvSPY cDNA showed high sequence identity to Arabidopsis SPY along its entire length, and the barley protein functionally complemented the spy-3 mutation. HvSPY and SPY proteins showed sequence relatedness with animal O-linked N-acetylglucosamine transferases (OGTs), suggesting that they may also have OGT activity. HvSPY has a locus distinct from that of Sln, a mutation that causes the constitutive GA responses of slender barley, which phenotypically resembles Arabidopsis spy mutants. The possibility that the HvSPY gene encodes a negative regulator of GA action was tested by expressing HvSPY in a barley aleurone transient assay system. HvSPY coexpression largely abolished GA3-induced activity of an alpha-amylase promoter. Surprisingly, HvSPY coexpression increased reporter gene activity from an abscisic acid (ABA)-inducible gene promoter (dehydrin), even in the absence of exogenous ABA. These results show that HvSPY modulates the transcriptional activities of two hormonally regulated promoters: negatively for a GA-induced promoter and positively for an ABA-induced promoter.

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Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Close T. J., Kortt A. A., Chandler P. M. A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol. 1989 Jul;13(1):95–108. doi: 10.1007/BF00027338. [DOI] [PubMed] [Google Scholar]
  4. Croker S. J., Hedden P., Lenton J. R., Stoddart J. L. Comparison of gibberellins in normal and slender barley seedlings. Plant Physiol. 1990 Sep;94(1):194–200. doi: 10.1104/pp.94.1.194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Gilroy S., Jones R. L. Perception of Gibberellin and Abscisic Acid at the External Face of the Plasma Membrane of Barley (Hordeum vulgare L.) Aleurone Protoplasts. Plant Physiol. 1994 Apr;104(4):1185–1192. doi: 10.1104/pp.104.4.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Goebl M., Yanagida M. The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem Sci. 1991 May;16(5):173–177. doi: 10.1016/0968-0004(91)90070-c. [DOI] [PubMed] [Google Scholar]
  9. Gubler F., Kalla R., Roberts J. K., Jacobsen J. V. Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell. 1995 Nov;7(11):1879–1891. doi: 10.1105/tpc.7.11.1879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harberd N. P., Freeling M. Genetics of dominant gibberellin-insensitive dwarfism in maize. Genetics. 1989 Apr;121(4):827–838. doi: 10.1093/genetics/121.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hart G. W. Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Annu Rev Biochem. 1997;66:315–335. doi: 10.1146/annurev.biochem.66.1.315. [DOI] [PubMed] [Google Scholar]
  12. Hattori T., Vasil V., Rosenkrans L., Hannah L. C., McCarty D. R., Vasil I. K. The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev. 1992 Apr;6(4):609–618. doi: 10.1101/gad.6.4.609. [DOI] [PubMed] [Google Scholar]
  13. Hedden Peter, Kamiya Yuji. GIBBERELLIN BIOSYNTHESIS: Enzymes, Genes and Their Regulation. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):431–460. doi: 10.1146/annurev.arplant.48.1.431. [DOI] [PubMed] [Google Scholar]
  14. Hoecker U., Vasil I. K., McCarty D. R. Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize. Genes Dev. 1995 Oct 15;9(20):2459–2469. doi: 10.1101/gad.9.20.2459. [DOI] [PubMed] [Google Scholar]
  15. Hooley R. Gibberellins: perception, transduction and responses. Plant Mol Biol. 1994 Dec;26(5):1529–1555. doi: 10.1007/BF00016489. [DOI] [PubMed] [Google Scholar]
  16. Jacobsen J. V., Close T. J. Control of transient expression of chimaeric genes by gibberellic acid and abscisic acid in protoplasts prepared from mature barley aleurone layers. Plant Mol Biol. 1991 Apr;16(4):713–724. doi: 10.1007/BF00023435. [DOI] [PubMed] [Google Scholar]
  17. Jacobsen S. E., Binkowski K. A., Olszewski N. E. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9292–9296. doi: 10.1073/pnas.93.17.9292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jacobsen S. E., Olszewski N. E. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell. 1993 Aug;5(8):887–896. doi: 10.1105/tpc.5.8.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jones R. L., Jacobsen J. V. Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int Rev Cytol. 1991;126:49–88. doi: 10.1016/s0074-7696(08)60682-8. [DOI] [PubMed] [Google Scholar]
  20. Keleher C. A., Redd M. J., Schultz J., Carlson M., Johnson A. D. Ssn6-Tup1 is a general repressor of transcription in yeast. Cell. 1992 Feb 21;68(4):709–719. doi: 10.1016/0092-8674(92)90146-4. [DOI] [PubMed] [Google Scholar]
  21. Kreppel L. K., Blomberg M. A., Hart G. W. Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J Biol Chem. 1997 Apr 4;272(14):9308–9315. doi: 10.1074/jbc.272.14.9308. [DOI] [PubMed] [Google Scholar]
  22. Lubas W. A., Frank D. W., Krause M., Hanover J. A. O-Linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J Biol Chem. 1997 Apr 4;272(14):9316–9324. doi: 10.1074/jbc.272.14.9316. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. McElroy D., Zhang W., Cao J., Wu R. Isolation of an efficient actin promoter for use in rice transformation. Plant Cell. 1990 Feb;2(2):163–171. doi: 10.1105/tpc.2.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moore G., Devos K. M., Wang Z., Gale M. D. Cereal genome evolution. Grasses, line up and form a circle. Curr Biol. 1995 Jul 1;5(7):737–739. doi: 10.1016/s0960-9822(95)00148-5. [DOI] [PubMed] [Google Scholar]
  26. Okamuro J. K., den Boer B. G., Lotys-Prass C., Szeto W., Jofuku K. D. Flowers into shoots: photo and hormonal control of a meristem identity switch in Arabidopsis. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13831–13836. doi: 10.1073/pnas.93.24.13831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Olszewski N. E., Martin F. B., Ausubel F. M. Specialized binary vector for plant transformation: expression of the Arabidopsis thaliana AHAS gene in Nicotiana tabacum. Nucleic Acids Res. 1988 Nov 25;16(22):10765–10782. doi: 10.1093/nar/16.22.10765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Phinney B. O. GROWTH RESPONSE OF SINGLE-GENE DWARF MUTANTS IN MAIZE TO GIBBERELLIC ACID. Proc Natl Acad Sci U S A. 1956 Apr;42(4):185–189. doi: 10.1073/pnas.42.4.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schultz J., Carlson M. Molecular analysis of SSN6, a gene functionally related to the SNF1 protein kinase of Saccharomyces cerevisiae. Mol Cell Biol. 1987 Oct;7(10):3637–3645. doi: 10.1128/mcb.7.10.3637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shpungin S., Liberzon A., Bangio H., Yona E., Katcoff D. J. Association of yeast SIN1 with the tetratrico peptide repeats of CDC23. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8274–8277. doi: 10.1073/pnas.93.16.8274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Silverstone A. L., Mak P. Y., Martínez E. C., Sun T. P. The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics. 1997 Jul;146(3):1087–1099. doi: 10.1093/genetics/146.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith R. L., Redd M. J., Johnson A. D. The tetratricopeptide repeats of Ssn6 interact with the homeo domain of alpha 2. Genes Dev. 1995 Dec 1;9(23):2903–2910. doi: 10.1101/gad.9.23.2903. [DOI] [PubMed] [Google Scholar]
  33. Swain S. M., Olszewski N. E. Genetic Analysis of Gibberellin Signal Transduction. Plant Physiol. 1996 Sep;112(1):11–17. doi: 10.1104/pp.112.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Williams F. E., Varanasi U., Trumbly R. J. The CYC8 and TUP1 proteins involved in glucose repression in Saccharomyces cerevisiae are associated in a protein complex. Mol Cell Biol. 1991 Jun;11(6):3307–3316. doi: 10.1128/mcb.11.6.3307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]
  36. Xie X., Kokubo T., Cohen S. L., Mirza U. A., Hoffmann A., Chait B. T., Roeder R. G., Nakatani Y., Burley S. K. Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature. 1996 Mar 28;380(6572):316–322. doi: 10.1038/380316a0. [DOI] [PubMed] [Google Scholar]

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