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Balanced Nuclear and Cytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response


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.


Vyšlo v časopise: Balanced Nuclear and Cytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response. PLoS Pathog 6(7): e32767. doi:10.1371/journal.ppat.1000970
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000970

Souhrn

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.


Zdroje

1. JonesJD

DanglJL

2006 The plant immune system. Nature 444 323 329

2. ZipfelC

2009 Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12 414 420

3. ChenG

ShawMH

KimYG

NunezG

2009 NOD-like receptors: role in innate immunity and inflammatory disease. Annu Rev Pathol 4 365 398

4. ClarkRM

SchweikertG

ToomajianC

OssowskiS

ZellerG

2007 Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317 338 342

5. BartschM

GobbatoE

BednarekP

DebeyS

SchultzeJL

2006 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 18 1038 1051

6. TaoY

XieZ

ChenW

GlazebrookJ

ChangHS

2003 Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15 317 330

7. GreenbergJT

YaoN

2004 The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6 201 211

8. LukasikE

TakkenFL

2009 STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol 12 427 436

9. Burch-SmithTM

SchiffM

CaplanJL

TsaoJ

CzymmekK

2007 A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5 e68

10. WirthmuellerL

ZhangY

JonesJD

ParkerJE

2007 Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr Biol 17 2023 2029

11. ShenQH

SaijoY

MauchS

BiskupC

BieriS

2007 Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315 1098 1103

12. CaplanJ

PadmanabhanM

Dinesh-KumarSP

2008 Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3 126 135

13. CaplanJL

MamillapalliP

Burch-SmithTM

CzymmekK

Dinesh-KumarSP

2008 Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132 449 462

14. GarciaAV

ParkerJE

2009 Heaven's Gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci 14 479 487

15. BhattacharjeeS

LeeLY

OltmannsH

CaoH

Veena

2008 IMPa-4, an Arabidopsis importin alpha isoform, is preferentially involved in agrobacterium-mediated plant transformation. Plant Cell 20 2661 2680

16. ChengYT

GermainH

WiermerM

BiD

XuF

2009 Nuclear Pore Complex Component MOS7/Nup88 Is Required for Innate Immunity and Nuclear Accumulation of Defense Regulators in Arabidopsis. Plant Cell 21 2503 2516

17. PalmaK

ZhangY

LiX

2005 An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr Biol 15 1129 1135

18. ZhangY

LiX

2005 A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell 17 1306 1316

19. FalkA

FeysBJ

FrostLN

JonesJD

DanielsMJ

1999 EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci U S A 96 3292 3297

20. FeysBJ

MoisanLJ

NewmanMA

ParkerJE

2001 Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. Embo J 20 5400 5411

21. LipkaV

DittgenJ

BednarekP

BhatR

WiermerM

2005 Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310 1180 1183

22. FeysBJ

WiermerM

BhatRA

MoisanLJ

Medina-EscobarN

2005 Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17 2601 2613

23. AartsN

MetzM

HolubE

StaskawiczBJ

DanielsMJ

1998 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 95 10306 10311

24. VenugopalSC

JeongRD

MandalMK

ZhuS

Chandra-ShekaraAC

2009 Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genet 5 e1000545

25. LiX

ClarkeJD

ZhangY

DongX

2001 Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14 1131 1139

26. ZhangY

GoritschnigS

DongX

LiX

2003 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 15 2636 2646

27. GassmannW

HinschME

StaskawiczBJ

1999 The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20 265 277

28. WangL

TsudaK

SatoM

CohenJD

KatagiriF

2009 Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5 e1000301

29. OkrentRA

BrooksMD

WildermuthMC

2009 Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J Biol Chem 284 9742 9754

30. WildermuthMC

DewdneyJ

WuG

AusubelFM

2001 Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414 562 565

31. MishinaTE

ZeierJ

2006 The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol 141 1666 1675

32. LairdJ

ArmengaudP

GiuntiniP

LavalV

MilnerJJ

2004 Inappropriate annotation of a key defence marker in Arabidopsis: will the real PR-1 please stand up? Planta 219 1089 1092

33. CloughSJ

FenglerKA

YuIC

LippokB

SmithRKJr

2000 The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97 9323 9328

34. GodiardL

SauviacL

ToriiKU

GrenonO

ManginB

2003 ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J 36 353 365

35. LlorenteF

Alonso-BlancoC

Sanchez-RodriguezC

JordaL

MolinaA

2005 ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43 165 180

36. RothP

XylourgidisN

SabriN

UvA

FornerodM

2003 The Drosophila nucleoporin DNup88 localizes DNup214 and CRM1 on the nuclear envelope and attenuates NES-mediated nuclear export. J Cell Biol 163 701 706

37. HaasenD

KohlerC

NeuhausG

MerkleT

1999 Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant J 20 695 705

38. MeissnerT

KrauseE

VinkemeierU

2004 Ratjadone and leptomycin B block CRM1-dependent nuclear export by identical mechanisms. FEBS Lett 576 27 30

39. WenW

MeinkothJL

TsienRY

TaylorSS

1995 Identification of a signal for rapid export of proteins from the nucleus. Cell 82 463 473

40. van der BiezenEA

FreddieCT

KahnK

ParkerJE

JonesJD

2002 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 29 439 451

41. SimonR

IgenoMI

CouplandG

1996 Activation of floral meristem identity genes in Arabidopsis. Nature 384 59 62

42. DittmarKD

DemadyDR

StancatoLF

KrishnaP

PrattWB

1997 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 272 21213 21220

43. GalloisJL

WoodwardC

ReddyGV

SablowskiR

2002 Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129 3207 3217

44. ParkerJE

ColemanMJ

SzaboV

FrostLN

SchmidtR

1997 The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9 879 894

45. AlcazarR

GarciaAV

ParkerJE

ReymondM

2009 Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci U S A 106 334 339

46. TianD

TrawMB

ChenJQ

KreitmanM

BergelsonJ

2003 Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423 74 77

47. ZhouN

TootleTL

TsuiF

KlessigDF

GlazebrookJ

1998 PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10 1021 1030

48. NawrathC

MetrauxJP

1999 Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11 1393 1404

49. VlotAC

KlessigDF

ParkSW

2008 Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11 436 442

50. RusterucciC

AvivDH

HoltBF3rd

DanglJL

ParkerJE

2001 The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13 2211 2224

51. TrumanW

BennettMH

KubigsteltigI

TurnbullC

GrantM

2007 Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci U S A 104 1075 1080

52. KeurentjesJJ

FuJ

TerpstraIR

GarciaJM

van den AckervekenG

2007 Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proc Natl Acad Sci U S A 104 1708 1713

53. HuangTT

KudoN

YoshidaM

MiyamotoS

2000 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 97 1014 1019

54. LipfordJR

SmithGT

ChiY

DeshaiesRJ

2005 A putative stimulatory role for activator turnover in gene expression. Nature 438 113 116

55. MurataniM

KungC

ShokatKM

TanseyWP

2005 The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing. Cell 120 887 899

56. SpoelSH

MouZ

TadaY

SpiveyNW

GenschikP

2009 Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137 860 872

57. StrausMR

RietzS

Ver Loren van ThemaatE

BartschM

ParkerJE

2010 Salicylic acid antagonism of EDS1-driven cell death is important for Arabidopsis immune and oxidative stress responses. Plant J In press

58. MateoA

MuhlenbockP

RusterucciC

ChangCC

MiszalskiZ

2004 LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136 2818 2830

59. MuhlenbockP

Szechynska-HebdaM

PlaszczycaM

BaudoM

MullineauxPM

2008 Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20 2339 2356

60. TorneroP

DanglJL

2001 A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J 28 475 481

61. WitteCP

NoelLD

GielbertJ

ParkerJE

RomeisT

2004 Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol Biol 55 135 147

62. CloughSJ

BentAF

1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743

63. NoelLD

CagnaG

StuttmannJ

WirthmullerL

BetsuyakuS

2007 Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19 4061 4076

64. AichingerE

VillarCB

FarronaS

ReyesJC

HennigL

2009 CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5 e1000605

65. AsaiT

StoneJM

HeardJE

KovtunY

YorgeyP

2000 Fumonisin B1-induced cell death in arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12 1823 1836

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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