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PMID: 12084833 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis.

The Plant cell ·Vol. 14 ·No. 6 ·2002-06-00 ·Pages 1377-89

Fan W, Dong X

Abstract

The Arabidopsis NPR1 protein is a key regulator of salicylic acid (SA)-mediated gene expression in systemic acquired resistance. Based on yeast two-hybrid analysis, NPR1 has been suggested to interact with members of the TGA family of transcription factors, including TGA2 (AHBP-1b). However, genetic evidence demonstrating that the NPR1-TGA interaction occurs in planta is still lacking, and the role of this interaction in SA-mediated gene activation has yet to be determined. In this study, we expressed a truncated form of TGA2 in Arabidopsis and found that the resulting transgenic lines displayed phenotypes similar to those of npr1 mutants. This dominant-negative effect of the TGA2 mutant shows that TGA2 and NPR1 interact in planta. We also present biochemical evidence indicating that this interaction is specific and enhanced by SA treatment. Moreover, using a chimera reporter system, we found that a chimeric TGA2GAL4 transcription factor activated a UAS(GAL)::GUS reporter gene in response to SA and that this activation was abolished in the npr1 mutant. NPR1 is required for the DNA binding activity of the transcription factor. These genetic data clearly demonstrate that TGA2 is a SA-responsive and NPR1-dependent transcription activator.

MeSH Terms
Arabidopsis/drug effects,genetics Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors DNA-Binding Proteins/genetics,metabolism Gene Expression Regulation, Plant Glucuronidase/genetics Mutagenesis Nuclear Proteins Phenotype Plant Proteins/genetics,metabolism Plants, Genetically Modified Salicylic Acid/pharmacology Transcription Factors/genetics,metabolism Transcriptional Activation
Chemicals
AHBP-1b protein, Arabidopsis Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors DNA-Binding Proteins NPR1 protein, Arabidopsis Nuclear Proteins Plant Proteins Transcription Factors HBP-1b protein, plant Glucuronidase Salicylic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Fan Weihua
Developmental, Cell, and Molecular Biology Group, Department of Biology, Duke University, Durham, NC 27708-1000, USA.
Dong Xinnian
References (48)
48 references, click to expand
  1. Trans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses.
    Plant J. 2001 Sep;27(6):529-38 PMID: 11576436
  2. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats.
    Cell. 1994 Sep 23;78(6):1089-99 PMID: 7923358
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene.
    Mol Plant Microbe Interact. 1997 Jan;10(1):69-78 PMID: 9002272
  5. 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
  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. Tobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties.
    Plant Mol Biol. 2000 Mar;42(5):775-88 PMID: 10809449
  8. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element.
    Plant J. 1999 Sep;19(6):667-77 PMID: 10571852
  9. Auxin-induced stress potentiates trans-activation by a conserved plant basic/leucine-zipper factor.
    J Biol Chem. 1998 Oct 9;273(41):26631-7 PMID: 9756903
  10. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance.
    Plant Cell. 1994 Dec;6(12):1845-57 PMID: 7866028
  11. Plant bZIP proteins gather at ACGT elements.
    FASEB J. 1994 Feb;8(2):192-200 PMID: 8119490
  12. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil.
    Science. 1991 Oct 25;254(5031):539-44 PMID: 1948029
  13. Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis.
    Plant J. 2001 Jul;27(2):101-13 PMID: 11489188
  14. 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
  15. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis.
    Plant J. 1998 Oct;16(2):223-33 PMID: 9839467
  16. 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
  17. beta-Glucuronidase from Escherichia coli as a gene-fusion marker.
    Proc Natl Acad Sci U S A. 1986 Nov;83(22):8447-51 PMID: 3534890
  18. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant.
    Plant Cell. 1998 Apr;10(4):557-69 PMID: 9548982
  19. 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
  20. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance.
    Plant Cell. 1997 Sep;9(9):1573-84 PMID: 9338960
  21. Identification of a novel dimer stabilization region in a plant bZIP transcription activator.
    Mol Cell Biol. 1992 Nov;12(11):4809-16 PMID: 1406663
  22. NIM1 overexpression in Arabidopsis potentiates plant disease resistance and results in enhanced effectiveness of fungicides.
    Mol Plant Microbe Interact. 2001 Sep;14(9):1114-24 PMID: 11551076
  23. 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
  24. TGA3 is a distinct member of the TGA family of bZIP transcription factors in Arabidopsis thaliana.
    Plant Mol Biol. 1994 Apr;25(1):1-11 PMID: 8003690
  25. Direct visualization of protein interactions in plant cells.
    Nat Biotechnol. 2001 Aug;19(8):769-72 PMID: 11479572
  26. Nuclear localization of NPR1 is required for activation of PR gene expression.
    Plant Cell. 2000 Dec;12(12):2339-2350 PMID: 11148282
  27. Coordinated activation of as-1-type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide.
    Plant Mol Biol. 1996 Nov;32(3):415-26 PMID: 8980490
  28. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  29. 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
  30. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
    Plant Cell. 1991 Oct;3(10):1085-1094 PMID: 12324583
  31. Binding site requirements and differential representation of TGF factors in nuclear ASF-1 activity.
    Nucleic Acids Res. 1995 Sep 25;23(18):3778-85 PMID: 7479010
  32. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
    Genetics. 1996 Jun;143(2):973-82 PMID: 8725243
  33. Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters.
    J Biol Chem. 2000 Jun 30;275(26):19897-905 PMID: 10751419
  34. Acquired resistance in Arabidopsis.
    Plant Cell. 1992 Jun;4(6):645-56 PMID: 1392589
  35. Identification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related beta-1,3-glucanase gene, PR-2d.
    Plant J. 1996 Dec;10(6):1089-101 PMID: 9011089
  36. 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
  37. A glucocorticoid-mediated transcriptional induction system in transgenic plants.
    Plant J. 1997 Mar;11(3):605-12 PMID: 9107046
  38. 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
  39. Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element.
    Plant Cell. 1994 Jun;6(6):863-74 PMID: 8061520
  40. DNA-binding properties, genomic organization and expression pattern of TGA6, a new member of the TGA family of bZIP transcription factors in Arabidopsis thaliana.
    Plant Mol Biol. 1997 Jun;34(3):403-15 PMID: 9225852
  41. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  42. Phosphorylation of nuclear proteins directs binding to salicylic acid-responsive elements.
    Plant J. 1997 Jun;11(6):1315-24 PMID: 9225470
  43. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid.
    Mol Plant Microbe Interact. 2000 Feb;13(2):191-202 PMID: 10659709
  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. Regulation of DNA binding and trans-activation by a xenobiotic stress-activated plant transcription factor.
    J Biol Chem. 2001 Jan 5;276(1):172-8 PMID: 11034999
  46. Yeast activators stimulate plant gene expression.
    Nature. 1988 Aug 18;334(6183):631-3 PMID: 3165494
  47. Activation of the CaMV as-1 cis-element by salicylic acid: differential DNA-binding of a factor related to TGA1a.
    EMBO J. 1996 Oct 15;15(20):5679-89 PMID: 8896461
  48. Systemic Acquired Resistance.
    Plant Cell. 1996 Oct;8(10):1809-1819 PMID: 12239363
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2002-06-00
Pages
1377-89
Language
English
Region
England
NLM ID
9208688
PMCID
PMC150786
Subset
IM
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