Home LiteratureArticle Details
PMID: 17172357 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines.

The Plant cell ·Vol. 18 ·No. 12 ·2006-12-00 ·Pages 3670-85

Rochon A, Boyle P, Wignes T, Fobert PR, Després C

Abstract

NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1) regulates systemic acquired resistance (SAR) in Arabidopsis thaliana, and current models propose that after treatment with salicylic acid (SA), Cys-82 and Cys-216 of NPR1 are reduced, leading to nuclear import. The interaction of nucleus-localized NPR1 with TGA transcription factors results in the activation of defense genes, including the SAR marker PATHOGENESIS-RELATED-1 (PR-1), and the deployment of SAR. Little is known about how TGA factors or NPR1 regulate transcription or whether a TGA-NPR1 complex forms on DNA. We show that TGA2 and NPR1 are recruited to PR-1 independently of each other and of SA treatment. Consistent with the result that a triple knockout in TGA2/5/6 derepresses PR-1, in vivo plant transcription assays revealed that TGA2 is not an autonomous transcription activator but is a transcriptional repressor in both untreated and SA-treated cells. However, after stimulation with SA, TGA2 is incorporated into a transactivating complex with NPR1, forming an enhanceosome that requires the core of the NPR1 BTB/POZ domain (residues 80 to 91) and the oxidation of NPR1 Cys-521 and Cys-529. These Cys residues are found in a new type of transactivation domain that we term Cys-oxidized. These data further our understanding of the mechanism by which TGA2 and NPR1 activate Arabidopsis PR-1.

MeSH Terms
Amino Acid Sequence Arabidopsis/cytology,drug effects,genetics,metabolism Arabidopsis Proteins/chemistry,genetics,metabolism Basic-Leucine Zipper Transcription Factors/genetics,metabolism Cysteine/metabolism Gene Expression Regulation, Plant/drug effects Models, Genetic Molecular Sequence Data Nuclear Proteins/genetics,metabolism Oxidation-Reduction/drug effects Plant Proteins/genetics Promoter Regions, Genetic/drug effects,genetics Protein Structure, Tertiary/drug effects Protein Transport/drug effects RNA, Messenger/genetics,metabolism Salicylic Acid/pharmacology Structure-Activity Relationship Transcriptional Activation/drug effects
Chemicals
AHBP-1b protein, Arabidopsis Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors NPR1 protein, Arabidopsis Nuclear Proteins Plant Proteins RNA, Messenger pathogenesis-related proteins, plant Cysteine Salicylic Acid
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Rochon Amanda
Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1.
Boyle Patrick
Wignes Tracy
Fobert Pierre R
Després Charles
References (48)
48 references, click to expand
  1. In-depth mutational analysis of the promyelocytic leukemia zinc finger BTB/POZ domain reveals motifs and residues required for biological and transcriptional functions.
    Mol Cell Biol. 2000 Sep;20(17):6550-67 PMID: 10938130
  2. Critical structural elements of the VP16 transcriptional activation domain.
    Science. 1991 Jan 4;251(4989):87-90 PMID: 1846049
  3. Fold prediction and evolutionary analysis of the POZ domain: structural and evolutionary relationship with the potassium channel tetramerization domain.
    J Mol Biol. 1999 Jan 29;285(4):1353-61 PMID: 9917379
  4. The POZ domain: a conserved protein-protein interaction motif.
    Genes Dev. 1994 Jul 15;8(14):1664-77 PMID: 7958847
  5. Systemic acquired resistance.
    Annu Rev Phytopathol. 2004;42:185-209 PMID: 15283665
  6. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B.
    Plant Cell. 1997 Mar;9(3):425-39 PMID: 9090885
  7. Protein secondary structure prediction based on position-specific scoring matrices.
    J Mol Biol. 1999 Sep 17;292(2):195-202 PMID: 10493868
  8. Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica.
    Plant J. 2002 Oct;32(2):151-63 PMID: 12383081
  9. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis.
    Plant Cell. 2002 Jun;14(6):1377-89 PMID: 12084833
  10. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis.
    Plant Cell. 2003 Aug;15(8):1846-58 PMID: 12897257
  11. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome.
    Cell. 1995 Dec 29;83(7):1091-100 PMID: 8548797
  12. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602-6 PMID: 11607555
  13. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis.
    Plant J. 1998 Oct;16(2):223-33 PMID: 9839467
  14. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors.
    Plant Cell. 2000 Feb;12(2):279-90 PMID: 10662863
  15. ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments.
    Genomics. 2004 Mar;83(3):349-60 PMID: 14986705
  16. Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1.
    Cell. 1999 Aug 6;98(3):329-39 PMID: 10458608
  17. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  18. Pfam: clans, web tools and services.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D247-51 PMID: 16381856
  19. An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance.
    Plant J. 2005 Jan;41(2):304-18 PMID: 15634206
  20. Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis.
    Plant Cell. 2005 Apr;17(4):1279-91 PMID: 15749762
  21. Regulation of the yeast Yap1p nuclear export signal is mediated by redox signal-induced reversible disulfide bond formation.
    Mol Cell Biol. 2001 Sep;21(18):6139-50 PMID: 11509657
  22. Direct visualization of protein interactions in plant cells.
    Nat Biotechnol. 2001 Aug;19(8):769-72 PMID: 11479572
  23. Nuclear localization of NPR1 is required for activation of PR gene expression.
    Plant Cell. 2000 Dec;12(12):2339-2350 PMID: 11148282
  24. NPR1: the spider in the web of induced resistance signaling pathways.
    Curr Opin Plant Biol. 2004 Aug;7(4):456-64 PMID: 15231270
  25. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4328-32 PMID: 1903539
  26. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  27. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
    Plant Cell. 1991 Oct;3(10):1085-1094 PMID: 12324583
  28. An intermolecular disulfide bond stabilizes E2A homodimers and is required for DNA binding at physiological temperatures.
    Cell. 1994 Dec 16;79(6):1057-67 PMID: 8001133
  29. Redox regulation of fos and jun DNA-binding activity in vitro.
    Science. 1990 Sep 7;249(4973):1157-61 PMID: 2118682
  30. The repression of nuclear factor I/CCAAT transcription factor (NFI/CTF) transactivating domain by oxidative stress is mediated by a critical cysteine (Cys-427).
    Biochem J. 2000 May 15;348 Pt 1:235-40 PMID: 10794737
  31. Sequence and structural analysis of BTB domain proteins.
    Genome Biol. 2005;6(10):R82 PMID: 16207353
  32. Crystal structure of the BTB domain from PLZF.
    Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12123-8 PMID: 9770450
  33. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6531-6 PMID: 9601001
  34. Salicylic acid-inducible Arabidopsis CK2-like activity phosphorylates TGA2.
    Plant Mol Biol. 2005 Mar;57(4):541-57 PMID: 15821979
  35. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6523-8 PMID: 10339621
  36. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance.
    Plant Cell. 2003 Nov;15(11):2647-53 PMID: 14576289
  37. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1.
    Plant Cell. 2003 Sep;15(9):2181-91 PMID: 12953119
  38. The ankyrin repeat as molecular architecture for protein recognition.
    Protein Sci. 2004 Jun;13(6):1435-48 PMID: 15152081
  39. A redox mechanism controls differential DNA binding activities of hypoxia-inducible factor (HIF) 1alpha and the HIF-like factor.
    J Biol Chem. 2000 Feb 18;275(7):4618-27 PMID: 10671489
  40. The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements.
    Plant Cell. 2003 Dec;15(12):3033-50 PMID: 14630974
  41. A "Whirly" transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis.
    Dev Cell. 2004 Feb;6(2):229-40 PMID: 14960277
  42. Allosteric effects of DNA on transcriptional regulators.
    Nature. 1998 Apr 30;392(6679):885-8 PMID: 9582068
  43. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.
    Cell. 2003 Jun 27;113(7):935-44 PMID: 12837250
  44. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  45. SMART 5: domains in the context of genomes and networks.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D257-60 PMID: 16381859
  46. Enhanceosomes.
    Curr Opin Genet Dev. 2001 Apr;11(2):205-8 PMID: 11250145
  47. Systemic Acquired Resistance.
    Plant Cell. 1996 Oct;8(10):1809-1819 PMID: 12239363
  48. A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity.
    Plant Cell. 2006 Jul;18(7):1750-65 PMID: 16766691
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2006-12-00
Epub
2006-00-15
Pages
3670-85
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1785396
Subset
IM
Databases
PDB
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com