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PMID: 20617163 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response.

PLoS pathogens ·Vol. 6 ·2010-07-01 ·Pages e1000970

García AV, Blanvillain-Baufumé S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE

Abstract

An important layer of plant innate immunity to host-adapted pathogens is conferred by intracellular nucleotide-binding/oligomerization domain-leucine rich repeat (NB-LRR) receptors recognizing specific microbial effectors. Signaling from activated receptors of the TIR (Toll/Interleukin-1 Receptor)-NB-LRR class converges on the nucleo-cytoplasmic immune regulator EDS1 (Enhanced Disease Susceptibility1). In this report we show that a receptor-stimulated increase in accumulation of nuclear EDS1 precedes or coincides with the EDS1-dependent induction and repression of defense-related genes. EDS1 is capable of nuclear transport receptor-mediated shuttling between the cytoplasm and nucleus. By enhancing EDS1 export from inside nuclei (through attachment of an additional nuclear export sequence (NES)) or conditionally releasing EDS1 to the nucleus (by fusion to a glucocorticoid receptor (GR)) in transgenic Arabidopsis we establish that the EDS1 nuclear pool is essential for resistance to biotrophic and hemi-biotrophic pathogens and for transcriptional reprogramming. Evidence points to post-transcriptional processes regulating receptor-triggered accumulation of EDS1 in nuclei. Changes in nuclear EDS1 levels become equilibrated with the cytoplasmic EDS1 pool and cytoplasmic EDS1 is needed for complete resistance and restriction of host cell death at infection sites. We propose that coordinated nuclear and cytoplasmic activities of EDS1 enable the plant to mount an appropriately balanced immune response to pathogen attack.

MeSH Terms
Arabidopsis/genetics,immunology,ultrastructure Arabidopsis Proteins/immunology,physiology Cell Nucleus/metabolism Cytoplasm/metabolism DNA-Binding Proteins/immunology,physiology Dexamethasone/pharmacology Gene Expression Regulation, Plant Immunity, Innate Plant Diseases/immunology Protein Transport
Chemicals
Arabidopsis Proteins DNA-Binding Proteins EDS1 protein, Arabidopsis Dexamethasone
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
García Ana V
Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany.
Blanvillain-Baufumé Servane
Huibers Robin P
Wiermer Marcel
Li Guangyong
Gobbato Enrico
Rietz Steffen
Parker Jane E
References (65)
65 references, click to expand
  1. Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana.
    Plant J. 1999 Dec;20(6):695-705 PMID: 10652141
  2. The role and regulation of programmed cell death in plant-pathogen interactions.
    Cell Microbiol. 2004 Mar;6(3):201-11 PMID: 14764104
  3. Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate.
    J Biol Chem. 2009 Apr 10;284(15):9742-54 PMID: 19189963
  4. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis.
    Plant Cell. 2008 Sep;20(9):2339-56 PMID: 18790826
  5. A putative stimulatory role for activator turnover in gene expression.
    Nature. 2005 Nov 3;438(7064):113-6 PMID: 16267558
  6. Identification of a signal for rapid export of proteins from the nucleus.
    Cell. 1995 Aug 11;82(3):463-73 PMID: 7634336
  7. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components.
    Plant J. 2002 Feb;29(4):439-51 PMID: 11846877
  8. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  9. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector.
    Cell. 2008 Feb 8;132(3):449-62 PMID: 18267075
  10. Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope.
    Plant Mol Biol. 2004 May;55(1):135-47 PMID: 15604670
  11. CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis.
    PLoS Genet. 2009 Aug;5(8):e1000605 PMID: 19680533
  12. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9323-8 PMID: 10900264
  13. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense.
    Curr Biol. 2007 Dec 4;17(23):2023-9 PMID: 17997306
  14. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling.
    PLoS Genet. 2009 Jul;5(7):e1000545 PMID: 19578402
  15. Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):334-9 PMID: 19106299
  16. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4.
    EMBO J. 2001 Oct 1;20(19):5400-11 PMID: 11574472
  17. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.
    Science. 2007 Feb 23;315(5815):1098-103 PMID: 17185563
  18. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy.
    Plant Physiol. 2004 Sep;136(1):2818-30 PMID: 15347794
  19. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  20. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity.
    Plant Cell. 2005 Sep;17(9):2601-13 PMID: 16040633
  21. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1.
    Plant Cell. 2003 Nov;15(11):2636-46 PMID: 14576290
  22. Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci.
    Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1708-13 PMID: 17237218
  23. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates.
    Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1075-80 PMID: 17215350
  24. NOD-like receptors: role in innate immunity and inflammatory disease.
    Annu Rev Pathol. 2009;4:365-98 PMID: 18928408
  25. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation.
    Plant Cell. 1999 Aug;11(8):1393-404 PMID: 10449575
  26. Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis.
    Development. 2002 Jul;129(13):3207-17 PMID: 12070095
  27. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis.
    Plant Cell. 1998 Jun;10(6):1021-30 PMID: 9634589
  28. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis.
    Plant Cell. 2009 Aug;21(8):2503-16 PMID: 19700630
  29. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae.
    Plant Cell. 2003 Feb;15(2):317-30 PMID: 12566575
  30. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses.
    Plant Cell. 2007 Dec;19(12):4061-76 PMID: 18065690
  31. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana.
    Nature. 2003 May 1;423(6935):74-7 PMID: 12721627
  32. A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1.
    Plant Cell. 2005 Apr;17(4):1306-16 PMID: 15772285
  33. Systemic acquired resistance: the elusive signal(s).
    Curr Opin Plant Biol. 2008 Aug;11(4):436-42 PMID: 18614393
  34. A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana.
    Plant J. 2001 Nov;28(4):475-81 PMID: 11737784
  35. Ratjadone and leptomycin B block CRM1-dependent nuclear export by identical mechanisms.
    FEBS Lett. 2004 Oct 8;576(1-2):27-30 PMID: 15474004
  36. The Drosophila nucleoporin DNup88 localizes DNup214 and CRM1 on the nuclear envelope and attenuates NES-mediated nuclear export.
    J Cell Biol. 2003 Nov 24;163(4):701-6 PMID: 14638854
  37. A novel role for the TIR domain in association with pathogen-derived elicitors.
    PLoS Biol. 2007 Mar;5(3):e68 PMID: 17298188
  38. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance.
    Mol Plant Microbe Interact. 2001 Oct;14(10):1131-9 PMID: 11605952
  39. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming.
    Cell Host Microbe. 2008 Mar 13;3(3):126-35 PMID: 18329612
  40. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance.
    Plant Physiol. 2006 Aug;141(4):1666-75 PMID: 16778014
  41. ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina.
    Plant J. 2005 Jul;43(2):165-80 PMID: 15998304
  42. The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing.
    Cell. 2005 Mar 25;120(6):887-99 PMID: 15797387
  43. Heaven's Gate: nuclear accessibility and activities of plant immune regulators.
    Trends Plant Sci. 2009 Sep;14(9):479-87 PMID: 19716748
  44. STANDing strong, resistance proteins instigators of plant defence.
    Curr Opin Plant Biol. 2009 Aug;12(4):427-36 PMID: 19394891
  45. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306-11 PMID: 9707643
  46. A nuclear export signal in the N-terminal regulatory domain of IkappaBalpha controls cytoplasmic localization of inactive NF-kappaB/IkappaBalpha complexes.
    Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1014-9 PMID: 10655476
  47. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae.
    PLoS Pathog. 2009 Feb;5(2):e1000301 PMID: 19214217
  48. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  49. An importin alpha homolog, MOS6, plays an important role in plant innate immunity.
    Curr Biol. 2005 Jun 21;15(12):1129-35 PMID: 15964279
  50. Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. The role of p23 is to stabilize receptor.hsp90 heterocomplexes formed by hsp90.p60.hsp70.
    J Biol Chem. 1997 Aug 22;272(34):21213-20 PMID: 9261129
  51. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes.
    Plant J. 1999 Nov;20(3):265-77 PMID: 10571887
  52. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis.
    Science. 2005 Nov 18;310(5751):1180-3 PMID: 16293760
  53. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6.
    Plant Cell. 1997 Jun;9(6):879-94 PMID: 9212464
  54. Activation of floral meristem identity genes in Arabidopsis.
    Nature. 1996 Nov 7;384(6604):59-62 PMID: 8900276
  55. IMPa-4, an Arabidopsis importin alpha isoform, is preferentially involved in agrobacterium-mediated plant transformation.
    Plant Cell. 2008 Oct;20(10):2661-80 PMID: 18836040
  56. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana.
    Science. 2007 Jul 20;317(5836):338-42 PMID: 17641193
  57. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7.
    Plant Cell. 2006 Apr;18(4):1038-51 PMID: 16531493
  58. ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt.
    Plant J. 2003 Nov;36(3):353-65 PMID: 14617092
  59. Inappropriate annotation of a key defence marker in Arabidopsis: will the real PR-1 please stand up?
    Planta. 2004 Oct;219(6):1089-92 PMID: 15293050
  60. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis.
    Plant Cell. 2001 Oct;13(10):2211-24 PMID: 11595797
  61. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity.
    Cell. 2009 May 29;137(5):860-72 PMID: 19490895
  62. Early molecular events in PAMP-triggered immunity.
    Curr Opin Plant Biol. 2009 Aug;12(4):414-20 PMID: 19608450
  63. Fumonisin B1-induced cell death in arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways.
    Plant Cell. 2000 Oct;12(10):1823-36 PMID: 11041879
  64. Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis.
    Plant J. 2010 May 1;62(4):628-40 PMID: 20163553
  65. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3292-7 PMID: 10077677
Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
DOI
10.1371/journal.ppat.1000970
Published
2010-07-01
Epub
2010-00-01
Pages
e1000970
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC2895645
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/J/00000603 · United Kingdom
External Links
PubMed source DOI: 10.1371/journal.ppat.1000970 PMC Full Text View journal details
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