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PMID: 16810321 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors.

The EMBO journal ·Vol. 25 ·No. 13 ·2006-07-12 ·Pages 3133-43

Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schütze K, Alonso R, Harter K, Vicente-Carbajosa J, Dröge-Laser W

Abstract

Proline metabolism has been implicated in plant responses to abiotic stresses. The Arabidopsis thaliana proline dehydrogenase (ProDH) is catalysing the first step in proline degradation. Transcriptional activation of ProDH by hypo-osmolarity is mediated by an ACTCAT cis element, a typical binding site of basic leucine zipper (bZIP) transcription factors. In this study, we demonstrate by gain-of-function and loss-of-function approaches, as well as chromatin immunoprecipitation (ChIP), that ProDH is a direct target gene of the group-S bZIP factor AtbZIP53. Dimerisation studies making use of yeast and Arabidopsis protoplast-based two-hybrid systems, as well as bimolecular fluorescence complementation (BiFC) reveal that AtbZIP53 does not preferentially form dimers with group-S bZIPs but strongly interacts with members of group-C. In particular, a synergistic interplay of AtbZIP53 and group-C AtbZIP10 was demonstrated by colocalisation studies, strong enhancement of ACTCAT-mediated transcription as well as complementation studies in atbzip53 atbzip10 T-DNA insertion lines. Heterodimer mediated activation of transcription has been found to operate independent of the DNA-binding properties and is described as a crucial mechanism to modulate transcription factor activity and function.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,physiology Basic-Leucine Zipper Transcription Factors/genetics,physiology Dimerization Gene Expression Regulation, Plant Mutation Osmolar Concentration Proline Oxidase/genetics,physiology Promoter Regions, Genetic Regulatory Elements, Transcriptional Transcriptional Activation Yeasts/genetics,metabolism
Chemicals
Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors Proline Oxidase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Weltmeier Fridtjof
Albrecht-von-Haller Institut, Universität Göttingen, Göttingen, Germany.
Ehlert Andrea
Mayer Caroline S
Dietrich Katrin
Wang Xuan
Schütze Katia
Alonso Rosario
Harter Klaus
Vicente-Carbajosa Jesús
Dröge-Laser Wolfgang
References (53)
53 references, click to expand
  1. Reciprocal regulation of delta 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants.
    Mol Gen Genet. 1996 Dec 13;253(3):334-41 PMID: 9003320
  2. Certain bZIP peptides bind DNA sequentially as monomers and dimerize on the DNA.
    Nat Struct Biol. 1997 Feb;4(2):115-7 PMID: 9033590
  3. Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana.
    FEBS Lett. 1999 Nov 19;461(3):205-10 PMID: 10567698
  4. Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis.
    J Biol Chem. 1993 Sep 5;268(25):18673-8 PMID: 8103048
  5. Dimerization specificity of all 67 B-ZIP motifs in Arabidopsis thaliana: a comparison to Homo sapiens B-ZIP motifs.
    Nucleic Acids Res. 2004;32(11):3435-45 PMID: 15226410
  6. LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants.
    Plant Cell Physiol. 2005 Oct;46(10):1623-34 PMID: 16051676
  7. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds.
    FEBS Lett. 2004 Mar 12;561(1-3):127-31 PMID: 15013763
  8. Interactions of coiled coils in transcription factors: where is the specificity?
    Curr Opin Genet Dev. 1993 Apr;3(2):278-85 PMID: 8504253
  9. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death.
    Cell. 1997 Mar 7;88(5):685-94 PMID: 9054508
  10. Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant.
    Plant Cell. 1996 Aug;8(8):1437-46 PMID: 8776904
  11. Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors.
    Plant J. 2006 Jun;46(5):890-900 PMID: 16709202
  12. A conserved upstream open reading frame mediates sucrose-induced repression of translation.
    Plant Cell. 2004 Jul;16(7):1717-29 PMID: 15208401
  13. The role of [Delta]1-pyrroline-5-carboxylate dehydrogenase in proline degradation.
    Plant Cell. 2004 Dec;16(12):3413-25 PMID: 15548746
  14. A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis.
    Plant Physiol. 1998 Dec;118(4):1233-41 PMID: 9847097
  15. An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera.
    Yeast. 1991 Oct;7(7):691-2 PMID: 1776359
  16. Mechanisms of plant desiccation tolerance.
    Trends Plant Sci. 2001 Sep;6(9):431-8 PMID: 11544133
  17. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation.
    Plant J. 2004 Nov;40(3):428-38 PMID: 15469500
  18. Comprehensive identification of human bZIP interactions with coiled-coil arrays.
    Science. 2003 Jun 27;300(5628):2097-101 PMID: 12805554
  19. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins.
    Nature. 1994 Feb 10;367(6463):568-72 PMID: 8107826
  20. ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis.
    Plant Physiol. 2002 Oct;130(2):709-19 PMID: 12376638
  21. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex.
    Cell. 1992 Dec 24;71(7):1223-37 PMID: 1473154
  22. Fos-Jun dimerization promotes interaction of the basic region with TFIIE-34 and TFIIF.
    Mol Cell Biol. 1996 May;16(5):2110-8 PMID: 8628277
  23. Proline metabolism in the wild-type and in a salt-tolerant mutant of nicotiana plumbaginifolia studied by (13)C-nuclear magnetic resonance imaging
    Plant Physiol. 1999 Dec;121(4):1281-90 PMID: 10594115
  24. Isolation and characterization of four novel parsley proteins that interact with the transcriptional regulators CPRF1 and CPRF2.
    Mol Genet Genomics. 2001 Aug;265(6):964-76 PMID: 11523788
  25. Toxicity of free proline revealed in an arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase.
    Plant Cell Physiol. 2003 May;44(5):541-8 PMID: 12773641
  26. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins.
    Science. 1988 Jun 24;240(4860):1759-64 PMID: 3289117
  27. Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis.
    Mol Plant Microbe Interact. 2004 Apr;17(4):343-50 PMID: 15077666
  28. Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application.
    Plant Physiol. 2000 Feb;122(2):357-68 PMID: 10677429
  29. Transcriptional coactivator complexes.
    Annu Rev Biochem. 2001;70:475-501 PMID: 11395415
  30. bZIP transcription factors in Arabidopsis.
    Trends Plant Sci. 2002 Mar;7(3):106-11 PMID: 11906833
  31. Transactivation properties of parsley proline-rich bZIP transcription factors.
    Plant J. 2000 Apr;22(1):1-8 PMID: 10792815
  32. Predicting specificity in bZIP coiled-coil protein interactions.
    Genome Biol. 2004;5(2):R11 PMID: 14759261
  33. 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 PMID: 1392590
  34. BZI-1 specifically heterodimerises with the tobacco bZIP transcription factors BZI-2, BZI-3/TBZF and BZI-4, and is functionally involved in flower development.
    Plant J. 2001 Nov;28(4):397-408 PMID: 11737777
  35. Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8787-91 PMID: 8710950
  36. A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in Arabidopsis.
    Plant Cell Physiol. 2004 Mar;45(3):309-17 PMID: 15047879
  37. The role of the leucine zipper in the fos-jun interaction.
    Nature. 1988 Dec 15;336(6200):646-51 PMID: 2974122
  38. Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress.
    Plant Physiol Biochem. 2004 Jan;42(1):57-63 PMID: 15061085
  39. Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2.
    J Biol Chem. 2003 Jun 6;278(23):21003-11 PMID: 12657652
  40. Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca 7000 full-length cDNA microarray.
    Plant J. 2003 Jun;34(6):868-87 PMID: 12795706
  41. Monomeric and dimeric bZIP transcription factor GCN4 bind at the same rate to their target DNA site.
    Biochemistry. 2004 Jan 27;43(3):718-27 PMID: 14730976
  42. The leucine zipper symmetrically positions the adjacent basic regions for specific DNA binding.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6901-5 PMID: 1871104
  43. Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis.
    Genes Dev. 2002 May 15;16(10):1247-59 PMID: 12023303
  44. Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis.
    Plant Physiol. 1997 Jun;114(2):591-6 PMID: 9193091
  45. Effect of Hydrogen Cyanamide on Amino Acid Profiles in Kiwifruit Buds during Budbreak.
    Plant Physiol. 1991 Nov;97(3):1256-9 PMID: 16668518
  46. The tobacco bZIP transcription factor BZI-1 binds to G-box elements in the promoters of phenylpropanoid pathway genes in vitro, but it is not involved in their regulation in vivo.
    Mol Genet Genomics. 2002 Mar;267(1):16-26 PMID: 11919711
  47. Specific DNA binding of GAL4, a positive regulatory protein of yeast.
    Cell. 1985 Apr;40(4):767-74 PMID: 3886158
  48. A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis.
    Plant Cell. 1996 Aug;8(8):1323-35 PMID: 8776899
  49. DNA sequence-dependent folding determines the divergence in binding specificities between Maf and other bZIP proteins.
    EMBO J. 2001 Feb 15;20(4):828-40 PMID: 11179227
  50. In vivo target promoter-binding activities of a xenobiotic stress-activated TGA factor.
    Plant J. 2001 Oct;28(2):237-43 PMID: 11722767
  51. Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana.
    Biochem Biophys Res Commun. 1999 Aug 11;261(3):766-72 PMID: 10441499
  52. Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins.
    EMBO J. 1992 Apr;11(4):1261-73 PMID: 1373374
  53. NAN fusions: a synthetic sialidase reporter gene as a sensitive and versatile partner for GUS.
    Plant J. 2002 Nov;32(3):391-400 PMID: 12410816
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1038/sj.emboj.7601206
Published
2006-07-12
Epub
2006-00-29
Pages
3133-43
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1500977
Subset
IM
External Links
PubMed source DOI: 10.1038/sj.emboj.7601206 PMC Full Text View journal details
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