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PMID: 19915088 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The BTB/POZ domain of the Arabidopsis disease resistance protein NPR1 interacts with the repression domain of TGA2 to negate its function.

The Plant cell ·Vol. 21 ·No. 11 ·2009-11-00 ·Pages 3700-13

Boyle P, Le Su E, Rochon A, Shearer HL, Murmu J, Chu JY, Fobert PR, Després C

Abstract

TGA2 and NONEXPRESSER OF PR GENES1 (NPR1) are activators of systemic acquired resistance (SAR) and of the SAR marker gene pathogenesis-related-1 (PR-1) in Arabidopsis thaliana. TGA2 is a transcriptional repressor required for basal repression of PR-1, but during SAR, TGA2 recruits NPR1 as part of an enhanceosome. Transactivation by the enhanceosome requires the NPR1 BTB/POZ domain. However, the NPR1 BTB/POZ domain does not contain an autonomous transactivation domain; thus, its molecular role within the enhanceosome remains elusive. We now show by gel filtration analyses that TGA2 binds DNA as a dimer, tetramer, or oligomer. Using in vivo plant transcription assays, we localize the repression domain of TGA2 to the N terminus and demonstrate that this domain is responsible for modulating the DNA binding activity of the oligomer both in vitro and in vivo. We confirm that the NPR1 BTB/POZ domain interacts with and negates the molecular function of the TGA2 repression domain by excluding TGA2 oligomers from cognate DNA. These data distinguish the NPR1 BTB/POZ domain from other known BTB/POZ domains and establish its molecular role in the context of the Arabidopsis PR-1 gene enhanceosome.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/chemistry,genetics,metabolism Basic-Leucine Zipper Transcription Factors/chemistry,genetics,metabolism Chromatography, Gel DNA, Plant/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Enhancer Elements, Genetic/genetics Gene Expression Regulation, Plant/genetics Immunity, Innate/genetics Nuclear Proteins/chemistry,genetics,metabolism Organelles/genetics Protein Structure, Tertiary/genetics Repressor Proteins/genetics Transcriptional Activation/genetics
Chemicals
AHBP-1b protein, Arabidopsis Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors DNA, Plant DNA-Binding Proteins NPR1 protein, Arabidopsis Nuclear Proteins Repressor Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Boyle Patrick
Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada.
Le Su Errol
Rochon Amanda
Shearer Heather L
Murmu Jhadeswar
Chu Jee Yan
Fobert Pierre R
Després Charles
References (44)
44 references, click to expand
  1. Nuclear localization of NPR1 is required for activation of PR gene expression.
    Plant Cell. 2000 Dec;12(12):2339-2350 PMID: 11148282
  2. 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
  3. 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
  4. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.
    Cell. 2003 Jun 27;113(7):935-44 PMID: 12837250
  5. Sequence and structural analysis of BTB domain proteins.
    Genome Biol. 2005;6(10):R82 PMID: 16207353
  6. The translin ring specifically recognizes DNA ends at recombination hot spots in the human genome.
    J Biol Chem. 1997 Apr 25;272(17):11402-7 PMID: 9111049
  7. 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
  8. Crystal structure of the BTB domain from PLZF.
    Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12123-8 PMID: 9770450
  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. 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
  11. Identification of a novel dimer stabilization region in a plant bZIP transcription activator.
    Mol Cell Biol. 1992 Nov;12(11):4809-16 PMID: 1406663
  12. 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
  13. All in the family: the BTB/POZ, KRAB, and SCAN domains.
    Mol Cell Biol. 2001 Jun;21(11):3609-15 PMID: 11340155
  14. Crystal structures of Drosophila mutant translin and characterization of translin variants reveal the structural plasticity of translin proteins.
    FEBS J. 2008 Aug;275(16):4235-49 PMID: 18647346
  15. Dimerization and the control of transcription by Krüppel.
    Nature. 1993 Jul 29;364(6436):454-7 PMID: 8332216
  16. Tissue-Specific Expression of as-1 in Transgenic Tobacco.
    Plant Cell. 1994 Jun;6(6):827-834 PMID: 12244260
  17. Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis.
    Plant Cell. 2005 Apr;17(4):1279-91 PMID: 15749762
  18. The POZ domain: a conserved protein-protein interaction motif.
    Genes Dev. 1994 Jul 15;8(14):1664-77 PMID: 7958847
  19. 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
  20. 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
  21. 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
  22. Structure-function studies of the BTB/POZ transcriptional repression domain from the promyelocytic leukemia zinc finger oncoprotein.
    Cancer Res. 1999 Oct 15;59(20):5275-82 PMID: 10537309
  23. NPR1: the spider in the web of induced resistance signaling pathways.
    Curr Opin Plant Biol. 2004 Aug;7(4):456-64 PMID: 15231270
  24. FOXP3 is a homo-oligomer and a component of a supramolecular regulatory complex disabled in the human XLAAD/IPEX autoimmune disease.
    Int Immunol. 2007 Jul;19(7):825-35 PMID: 17586580
  25. Direct visualization of protein interactions in plant cells.
    Nat Biotechnol. 2001 Aug;19(8):769-72 PMID: 11479572
  26. A novel group of transcriptional repressors in Arabidopsis.
    Plant Cell Physiol. 2009 May;50(5):970-5 PMID: 19324928
  27. 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
  28. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
    Plant Cell. 1991 Oct;3(10):1085-1094 PMID: 12324583
  29. Recruitment of SMRT/N-CoR-mSin3A-HDAC-repressing complexes is not a general mechanism for BTB/POZ transcriptional repressors: the case of HIC-1 and gammaFBP-B.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14831-6 PMID: 10611298
  30. Concentration-dependent transcriptional activation or repression by Krüppel from a single binding site.
    Nature. 1991 Oct 10;353(6344):563-6 PMID: 1922363
  31. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis.
    Plant J. 2003 Jun;34(5):733-9 PMID: 12787253
  32. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines.
    Plant Cell. 2006 Dec;18(12):3670-85 PMID: 17172357
  33. The transcriptional activator Pti4 is required for the recruitment of a repressosome nucleated by repressor SEBF at the potato PR-10a gene.
    Plant Cell. 2008 Nov;20(11):3136-47 PMID: 19028963
  34. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  35. 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
  36. Systemic Acquired Resistance.
    Plant Cell. 1996 Oct;8(10):1809-1819 PMID: 12239363
  37. The DNA binding activity of Translin is mediated by a basic region in the ring-shaped structure conserved in evolution.
    FEBS Lett. 1999 Jan 29;443(3):363-6 PMID: 10025964
  38. Systemic acquired resistance.
    Annu Rev Phytopathol. 2004;42:185-209 PMID: 15283665
  39. POZ for effect--POZ-ZF transcription factors in cancer and development.
    Trends Cell Biol. 2006 Nov;16(11):578-87 PMID: 16996269
  40. Ankyrin repeat: a unique motif mediating protein-protein interactions.
    Biochemistry. 2006 Dec 26;45(51):15168-78 PMID: 17176038
  41. A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR.
    BMC Biotechnol. 2008 May 08;8:47 PMID: 18466619
  42. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis.
    Plant J. 1998 Oct;16(2):223-33 PMID: 9839467
  43. 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
  44. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2009-11-00
Epub
2009-00-13
Pages
3700-13
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2798319
Subset
IM
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