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PMID: 11148282 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Nuclear localization of NPR1 is required for activation of PR gene expression.

The Plant cell ·Vol. 12 ·No. 12 ·2000-12-00 ·Pages 2339-2350

Kinkema M, Fan W, Dong X

Abstract

Systemic acquired resistance (SAR) is a broad-spectrum resistance in plants that involves the upregulation of a battery of pathogenesis-related (PR) genes. NPR1 is a key regulator in the signal transduction pathway that leads to SAR. Mutations in NPR1 result in a failure to induce PR genes in systemic tissues and a heightened susceptibility to pathogen infection, whereas overexpression of the NPR1 protein leads to increased induction of the PR genes and enhanced disease resistance. We analyzed the subcellular localization of NPR1 to gain insight into the mechanism by which this protein regulates SAR. An NPR1-green fluorescent protein fusion protein, which functions the same as the endogenous NPR1 protein, was shown to accumulate in the nucleus in response to activators of SAR. To control the nuclear transport of NPR1, we made a fusion of NPR1 with the glucocorticoid receptor hormone binding domain. Using this steroid-inducible system, we clearly demonstrate that nuclear localization of NPR1 is essential for its activity in inducing PR genes.

MeSH Terms
Arabidopsis Proteins Base Sequence Cell Nucleus/metabolism DNA Primers Fungal Proteins/genetics,metabolism Gene Expression Regulation, Plant Green Fluorescent Proteins Luminescent Proteins/genetics Nuclear Localization Signals Plant Proteins/genetics Protein Kinases Recombinant Fusion Proteins/genetics,metabolism Saccharomyces cerevisiae Proteins
Chemicals
Arabidopsis Proteins DNA Primers Fungal Proteins Luminescent Proteins Nuclear Localization Signals Plant Proteins Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins proline-rich protein, Arabidopsis Green Fluorescent Proteins NPR1 protein, S cerevisiae Protein Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kinkema M
Developmental, Cell, and Molecular Biology Group, Department of Biology, Duke University, Durham, North Carolina 27708-1000, USA.
Fan W
Dong X
References (60)
60 references, click to expand
  1. 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
  2. GFP in plants.
    Trends Genet. 1995 Aug;11(8):328-9 PMID: 8585134
  3. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7327-31 PMID: 8346252
  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. A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity.
    Plant Physiol. 1994 Jan;104(1):109-18 PMID: 8115541
  7. Nuclear targeting in plants.
    Plant Physiol. 1992 Dec;100(4):1627-32 PMID: 16653177
  8. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2122-7 PMID: 9122158
  9. Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans.
    Plant Cell. 1991 Jun;3(6):619-28 PMID: 1841721
  10. The conserved ELK-homeodomain of KNOTTED-1 contains two regions that signal nuclear localization.
    Plant Mol Biol. 1996 Jan;30(1):1-14 PMID: 8616227
  11. Developmental and hormonal regulation of the arabidopsis CER2 gene that codes for a nuclear-localized protein required for the normal accumulation of cuticular waxes.
    Plant Physiol. 1997 Nov;115(3):925-37 PMID: 9390429
  12. A steroid-inducible gene expression system for plant cells.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10421-5 PMID: 1961707
  13. Overexpression, purification, characterization, and crystallization of the BTB/POZ domain from the PLZF oncoprotein.
    J Biol Chem. 1997 Oct 24;272(43):27324-9 PMID: 9341182
  14. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance.
    Plant Cell. 1994 Dec;6(12):1845-57 PMID: 7866028
  15. Small cysteine-rich antifungal proteins from radish: their role in host defense.
    Plant Cell. 1995 May;7(5):573-88 PMID: 7780308
  16. Optimizing the biolistic process for different biological applications.
    Methods Enzymol. 1993;217:483-509 PMID: 8474348
  17. Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco.
    Plant Cell. 1995 Nov;7(11):1773-85 PMID: 8535134
  18. Nuclear targeting sequences--a consensus?
    Trends Biochem Sci. 1991 Dec;16(12):478-81 PMID: 1664152
  19. 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
  20. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection.
    Science. 1990 Nov 16;250(4983):1002-4 PMID: 17746925
  21. Antifungal Hydrolases in Pea Tissue : II. Inhibition of Fungal Growth by Combinations of Chitinase and beta-1,3-Glucanase.
    Plant Physiol. 1988 Nov;88(3):936-42 PMID: 16666407
  22. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis.
    Plant J. 1998 Oct;16(2):223-33 PMID: 9839467
  23. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber.
    Science. 1990 Nov 16;250(4983):1004-6 PMID: 17746926
  24. 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
  25. The generation of radiolabeled DNA and RNA probes with polymerase chain reaction.
    Anal Biochem. 1989 Feb 15;177(1):90-4 PMID: 2742155
  26. 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
  27. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat.
    Plant Cell. 1996 Apr;8(4):629-43 PMID: 8624439
  28. Gene regulation by steroid hormones.
    Cell. 1989 Feb 10;56(3):335-44 PMID: 2644044
  29. Engineered GFP as a vital reporter in plants.
    Curr Biol. 1996 Mar 1;6(3):325-30 PMID: 8805250
  30. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway.
    Plant J. 1996 Jul;10(1):71-82 PMID: 8758979
  31. Vectors for constitutive and inducible gene expression in yeast.
    Methods Enzymol. 1991;194:389-98 PMID: 2005799
  32. Systemic acquired resistance induced by localized virus infections in plants.
    Virology. 1961 Jul;14:340-58 PMID: 13743578
  33. Requirement of salicylic Acid for the induction of systemic acquired resistance.
    Science. 1993 Aug 6;261(5122):754-6 PMID: 17757215
  34. 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
  35. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
    Plant Cell. 1991 Oct;3(10):1085-1094 PMID: 12324583
  36. Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor.
    Mol Cell Biol. 1999 Feb;19(2):1025-37 PMID: 9891038
  37. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration.
    Methods Mol Biol. 1998;82:259-66 PMID: 9664431
  38. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell.
    Cell. 1996 Dec 27;87(7):1307-16 PMID: 8980236
  39. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco.
    Virology. 1979 Dec;99(2):410-2 PMID: 18631626
  40. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
    Genetics. 1996 Jun;143(2):973-82 PMID: 8725243
  41. The ANK repeat: a ubiquitous motif involved in macromolecular recognition.
    Trends Cell Biol. 1992 May;2(5):127-9 PMID: 14731966
  42. Systemic Induction of Salicylic Acid Accumulation in Cucumber after Inoculation with Pseudomonas syringae pv syringae.
    Plant Physiol. 1991 Dec;97(4):1342-7 PMID: 16668554
  43. A movable and regulable inactivation function within the steroid binding domain of the glucocorticoid receptor.
    Cell. 1988 Sep 23;54(7):1073-80 PMID: 2843290
  44. 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
  45. A glucocorticoid-mediated transcriptional induction system in transgenic plants.
    Plant J. 1997 Mar;11(3):605-12 PMID: 9107046
  46. 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
  47. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene.
    Mol Plant Microbe Interact. 1995 Nov-Dec;8(6):863-70 PMID: 8664495
  48. Transcriptional activation of APETALA1 by LEAFY.
    Science. 1999 Jul 23;285(5427):582-4 PMID: 10417387
  49. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds.
    J Biol Chem. 1992 Aug 5;267(22):15301-9 PMID: 1639777
  50. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally?
    Proteins. 1993 Dec;17(4):363-74 PMID: 8108379
  51. Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2.
    Plant Cell. 1992 Oct;4(10):1213-27 PMID: 1332794
  52. Nucleocytoplasmic transport: signals, mechanisms and regulation.
    Nature. 1997 Apr 24;386(6627):779-87 PMID: 9126736
  53. A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA.
    Cell. 1998 Jan 9;92(1):93-103 PMID: 9489703
  54. 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
  55. Activation of floral meristem identity genes in Arabidopsis.
    Nature. 1996 Nov 7;384(6604):59-62 PMID: 8900276
  56. A central role of salicylic Acid in plant disease resistance.
    Science. 1994 Nov 18;266(5188):1247-50 PMID: 17810266
  57. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  58. Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani.
    Science. 1991 Nov 22;254(5035):1194-7 PMID: 17776411
  59. Systemic Acquired Resistance.
    Plant Cell. 1996 Oct;8(10):1809-1819 PMID: 12239363
  60. Osmotin overexpression in potato delays development of disease symptoms.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1888-92 PMID: 11607463
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2000-12-00
Pages
2339-2350
Language
English
Region
England
NLM ID
9208688
PMCID
PMC102222
Subset
IM
Grants
NIGMS NIH HHS · F32 GM019498 · United States
NIGMS NIH HHS · F32-GM19498 · United States
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