The Lectin Receptor Kinase LecRK-I.9 Is a Novel Resistance Component and a Potential Host Target for a RXLR Effector

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In plants, an active defense against biotrophic pathogens is dependent on a functional continuum between the cell wall (CW) and the plasma membrane (PM). It is thus anticipated that proteins maintaining this continuum also function in defense. The legume-like lectin receptor kinase LecRK-I.9 is a putative mediator of CW-PM adhesions in Arabidopsis and is known to bind in vitro to the Phytophthora infestans RXLR-dEER effector IPI-O via a RGD cell attachment motif present in IPI-O. Here we show that LecRK-I.9 is associated with the plasma membrane, and that two T-DNA insertions lines deficient in LecRK-I.9 (lecrk-I.9) have a ‘gain-of-susceptibility’ phenotype specifically towards the oomycete Phytophthora brassicae. Accordingly, overexpression of LecRK-I.9 leads to enhanced resistance to P. brassicae. A similar ‘gain-of-susceptibility’ phenotype was observed in transgenic Arabidopsis lines expressing ipiO (35S-ipiO1). This phenocopy behavior was also observed with respect to other defense-related functions; lecrk-I.9 and 35S-ipiO1 were both disturbed in pathogen- and MAMP-triggered callose deposition. By site-directed mutagenesis, we demonstrated that the RGD cell attachment motif in IPI-O is not only essential for disrupting the CW-PM adhesions, but also for disease suppression. These results suggest that destabilizing the CW-PM continuum is one of the tactics used by Phytophthora to promote infection. As countermeasure the host may want to strengthen CW-PM adhesions and the novel Phytophthora resistance component LecRK-I.9 seems to function in this process.

Vyšlo v časopise: The Lectin Receptor Kinase LecRK-I.9 Is a Novel Resistance Component and a Potential Host Target for a RXLR Effector. PLoS Pathog 7(3): e32767. doi:10.1371/journal.ppat.1001327
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001327

Souhrn

Zdroje

1. BollerT

FelixG

2009

A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.

Annu Rev Plant Biol

379

407

2. HückelhovenR

2008

Cell wall-associated mechanisms of disease resistance and susceptibility.

Annu Rev Phytopathol

101

127

3. MellershDG

HeathMC

2001

Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration.

Plant Cell

413

424

4. RuoslahtiE

1996

RGD and other recognition sequences for integrins.

Annu Rev Cell Dev Biol

697

715

5. WatsonN

DuncanG

AnnanWS

van der WalleCF

2006

A tetravalent RGD ligand for integrin-mediated cell adhesion.

J Pharm Pharmacol

959

966

6. OlfaKZ

JoséL

SalmaD

AmineB

NajetSA

2005

Lebestatin, a disintegrin from Macrovipera venom, inhibits integrin-mediated cell adhesion, migration and angiogenesis.

Lab Invest

1507

1516

7. GarriguesHJ

RubinchikovaYE

DiPersioCM

RoseTM

2008

Integrin αVβ3 binds to the RGD motif of glycoprotein B of Kaposi's sarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor.

J Virol

1570

1580

8. StockbauerKE

MagounL

LiuM

BurnsEHJr

GubbaS

1999

A natural variant of the cysteine protease virulence factor of group A Streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins αvβ3 and αIIbβ3.

Proc Natl Acad Sci U S A

242

247

9. HostetterMK

2000

RGD-mediated adhesion in fungal pathogens of humans, plants and insects.

Curr Opin Microbiol

344

348

10. CalveteJJ

MarcinkiewiczC

SanzL

2007

KTS and RTS-disintegrins: Anti-angiogenic viper venom peptides specifically targeting the α1β1 integrin.

Curr Pharm Des

2853

2859

11. SarmaGN

ManningVA

CiuffettiLM

KarplusPA

2005

Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici-repentis.

Plant Cell

3190

3202

12. ManningVA

CiuffettiLM

2005

Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells.

Plant Cell

3203

3212

13. ManningVA

HamiltonSM

KarplusPA

CiuffettiLM

2008

The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization.

Mol Plant Microbe Interact

315

325

14. SchindlerM

MeinersS

ChereshDA

1989

RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth.

J Cell Biol

108

1955

15. CanutH

CarrascoA

GalaudJP

CassanC

BouyssouH

1998

High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall.

Plant J

16. KibaA

SugimotoM

ToyodaK

IchinoseY

YamadaT

1998

Interaction between cell wall and plasma membrane via RGD motif is implicated in plant defense responses.

Plant Cell Physiol

1245

1249

17. GaoH

GongYW

YuanYJ

2007

RGD-dependent mechanotransduction of suspension cultured Taxus cell in response to shear stress.

Biotechnol Prog

673

679

18. SenchouV

WeideR

CarrascoA

BouyssouH

Pont-LezicaR

2004

High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif.

Cell Mol Life Sci

502

509

19. GougetA

SenchouV

GoversF

SansonA

BarreA

2006

Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis.

Plant Physiol

140

20. BouwmeesterK

GoversF

2009

Arabidopsis L-type lectin receptor kinases: Phylogeny, classification, and expression profiles.

J Exp Bot

4383

4396

21. BouwmeesterK

van PoppelPMJA

GoversF

2009

Genome biology cracks enigmas of oomycete plant pathogens.

ParkerJE

Molecular aspects of plant disease resistance

Oxford, UK

Wiley-Blackwell

102

134

22. WhissonSC

BoevinkPC

MolelekiL

AvrovaAO

MoralesJG

2007

A translocation signal for delivery of oomycete effector proteins into host plant cells.

Nature

450

115

118

23. DouD

KaleSD

WangX

JiangRHY

BruceNA

2008

RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery.

Plant Cell

1930

1947

24. GoversF

BouwmeesterK

2008

Effector trafficking: RXLR-dEER as extra gear for delivery into plant cells.

Plant Cell

1728

1730

25. Van WestP

de JongAJ

JudelsonHS

EmonsAMC

GoversF

1998

The ipiO gene of Phytophthora infestans is highly expressed in invading hyphae during infection.

Fungal Genet Biol

126

138

26. VleeshouwersVGAA

RietmanH

KrenekP

ChampouretN

YoungC

2008

Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes.

PLoS ONE

e2875

27. ChampouretN

BouwmeesterK

RietmanH

van der LeeT

MaliepaardCA

2009

Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato.

Mol Plant Microbe Interact

1535

1545

28. VleeshouwersVGAA

Van DooijeweertW

GoversF

KamounS

ColonLT

2000

The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans.

Planta

210

853

29. RoetschiA

Si-AmmourA

BelbahriL

MauchF

Mauch-ManiB

2001

Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional pad2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling.

Plant J

293

305

30. MauchF

TorcheS

SchlaeppiK

BranciardL

BelhajK

2009

Phytophthora brassicae as a pathogen of Arabidopsis.

LamourK

KamounS

Oomycete genetics and genomic: diversity, interactions and research tools

Hoboken, New Jersey

John Wiley & Sons

333

345

31. BouwmeesterK

GoversF

2009

A novel method for efficient and abundant production of Phytophthora brassicae zoospores on Brussels sprout leaf discs.

BMC Plant Biol

111

32. GougetA

2005

Etude fonctionnelle d'un récepteur lectine kinase (LecRK79), potentiel partenaire dans les contacts paroi-plasmalemme chez Arabidopsis thaliana.

[PhD thesis] Université Paul Sabatier-Toulouse

III

33. TamelingWIL

NooijenC

LudwigN

BoterM

SlootwegE

2010

RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function.

Plant Cell

4176

4194

34. Si-AmmourA

Mauch-ManiB

MauchF

2003

Quantification of induced resistance against Phytophthora species expressing GFP as a vital marker: β-aminobutyric acid but not BTH protects potato and Arabidopsis from infection.

Mol Plant Pathol

237

35. ShibataY

KawakitaK

TakemotoD

2010

Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways.

Mol Plant Microbe Interact

1130

1142

36. HauckP

ThilmonyR

HeSY

2003

A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants.

Proc Natl Acad Sci U S A

100

8577

8582

37. HumphreyTV

BonettaDT

GoringDR

2007

Sentinels at the wall: Cell wall receptors and sensors.

New Phytol

176

38. Van KanJAL

2006

Licensed to kill: the lifestyle of a necrotrophic plant pathogen.

Trends Plant Sci

247

253

39. ParisyV

PoinssotB

OwsianowskiL

BuchalaA

GlazebrookJ

2007

Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis.

Plant J

159

172

40. SchlaeppiK

BodenhausenN

BuchalaA

MauchF

ReymondP

2008

The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis.

Plant J

774

786

41. SchlaeppiK

Abou-MansourE

BuchalaA

MauchF

2010

Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin.

Plant J

840

851

42. BallC

Vinod VijayanK

NguyenT

AnthonyK

BrayPF

2008

Glutathione regulates integrin αIIbβ3-mediated cell adhesion under flow conditions.

Thromb Haemost

100

857

863

43. Lorenc-KukułaK

JafraS

OszmiańskiJ

SzopaJ

2005

Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria.

J Agric Food Chem

272

281

44. QuentinM

AllasiaV

PegardA

AllaisF

DucrotPH

2009

Imbalanced lignin biosynthesis promotes the sexual reproduction of homothallic oomycete pathogens.

PLoS Pathog

e1000264

45. HaasBJ

KamounS

ZodyMC

JiangRHY

HandsakerRE

2009

Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans.

Nature

461

393

398

46. Van EsseHP

BoltonMD

StergiopoulosI

de WitPJGM

ThommaBPHJ

2007

The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor.

Mol Plant Microbe Interact

1092

1101

47. O'ConnellR

HerbertC

SreenivasaprasadS

KhatibM

Esquerré-TugayéMT

2004

A novel Arabidopsis-Colletotrichum pathosystem for the molecular dissection of plant-fungal interactions.

Mol Plant Microbe Interact

272

282

48. CatenCE

JinksJL

1968

Spontaneous variability of single isolates of Phytophthora infestans, I. Cultural variation.

Can J Bot

329

348

49. ErwinDC

RibeiroOK

1996

Phytophthora diseases worldwide.

St. Paul, Mn, USA

American Phytopathological Society

50. JambunathanN

McNellisTW

2003

Regulation of Arabidopsis COPINE 1 gene expression in response to pathogens and abiotic stimuli.

Plant Physiol

132

1370

1381

51. Van der HoornRAL

LaurentF

RothR

de WitPJGM

2000

Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis.

Mol Plant Microbe Interact

439

446

52. CaddickMX

GreenlandAJ

JepsonL

KrauseKP

QuN

1998

An ethanol inducible gene switch for plants used to manipulate carbon metabolism.

Nat Biotechnol

177

180

53. KarimiM

InzeD

DepickerA

2002

GATEWAY vectors for Agrobacterium-mediated plant transformation.

Trends Plant Sci

193

195

54. CloughSJ

BentAF

1998

Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.

Plant J

735

743

55. KeoghRC

DeberallBJ

McLeodS

1980

Comparison of histological and physiological responses to Phakospora pachyrhizi in resistant and susceptible soybean.

Trans Br Mycol Soc

329

333

56. MohrPG

CahillDM

2007

Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato.

Funct Integr Genomics

181

191