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PMID: 21304602 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen phytophthora infestans in Nicotiana benthamiana.

PloS one ·Vol. 6 ·No. 1 ·2011-01-27 ·Pages e16608

Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S

Abstract

The filamentous oomycete plant pathogen Phytophthora infestans causes late blight, an economically important disease, on members of the nightshade family (Solanaceae), such as the crop plants potato and tomato. The related plant Nicotiana benthamiana is a model system to study plant-pathogen interactions, and the susceptibility of N. benthamiana to Phytophthora species varies from susceptible to resistant. Little is known about the extent to which plant basal immunity, mediated by membrane receptors that recognise conserved pathogen-associated molecular patterns (PAMPs), contributes to P. infestans resistance. We found that different species of Phytophthora have varying degrees of virulence on N. benthamiana ranging from avirulence (incompatible interaction) to moderate virulence through to full aggressiveness. The leucine-rich repeat receptor-like kinase (LRR-RLK) BAK1/SERK3 is a major modulator of PAMP-triggered immunity (PTI) in Arabidopsis thaliana and N. benthamiana. We cloned two NbSerk3 homologs, NbSerk3A and NbSerk3B, from N. benthamiana based on sequence similarity to the A. thaliana gene. N. benthamiana plants silenced for NbSerk3 showed markedly enhanced susceptibility to P. infestans infection but were not altered in resistance to Phytophthora mirabilis, a sister species of P. infestans that specializes on a different host plant. Furthermore, silencing of NbSerk3 reduced the cell death response triggered by the INF1, a secreted P. infestans protein with features of PAMPs. We demonstrated that N. benthamiana NbSERK3 significantly contributes to resistance to P. infestans and regulates the immune responses triggered by the P. infestans PAMP protein INF1. In the future, the identification of novel surface receptors that associate with NbSERK3A and/or NbSERK3B should lead to the identification of new receptors that mediate recognition of oomycete PAMPs, such as INF1.

MeSH Terms
Host-Pathogen Interactions Molecular Sequence Data Phytophthora infestans/immunology Plant Diseases/immunology,parasitology Plant Immunity Protein Serine-Threonine Kinases/immunology Tobacco/enzymology,immunology,parasitology
Chemicals
Protein Serine-Threonine Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Chaparro-Garcia Angela
The Sainsbury Laboratory, John Innes Centre, Norwich, United Kingdom.
Wilkinson Rachael C
Gimenez-Ibanez Selena
Findlay Kim
Coffey Michael D
Zipfel Cyril
Rathjen John P
Kamoun Sophien
Schornack Sebastian
References (44)
44 references, click to expand
  1. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1.
    Proc Natl Acad Sci U S A. 2010 May 25;107(21):9909-14 PMID: 20457921
  2. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana.
    Plant Cell. 2008 May;20(5):1390-406 PMID: 18515503
  3. Plant systems for recognition of pathogen-associated molecular patterns.
    Semin Cell Dev Biol. 2009 Dec;20(9):1025-31 PMID: 19540353
  4. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions.
    Mol Plant Microbe Interact. 2008 Aug;21(8):1015-26 PMID: 18616398
  5. Entering and breaking: virulence effector proteins of oomycete plant pathogens.
    Cell Microbiol. 2009 Jan;11(1):13-20 PMID: 18783481
  6. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity.
    Cell Host Microbe. 2008 Jul 17;4(1):17-27 PMID: 18621007
  7. Brassinosteroid signal transduction from receptor kinases to transcription factors.
    Annu Rev Plant Biol. 2010;61:681-704 PMID: 20192752
  8. One for all: the receptor-associated kinase BAK1.
    Trends Plant Sci. 2009 Oct;14(10):535-41 PMID: 19748302
  9. Resistance of nicotiana benthamiana to phytophthora infestans is mediated by the recognition of the elicitor protein INF1
    Plant Cell. 1998 Sep;10(9):1413-26 PMID: 9724689
  10. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways.
    Mol Plant Microbe Interact. 2010 Sep;23(9):1130-42 PMID: 20687803
  11. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b.
    Plant Cell. 2008 Apr;20(4):1118-33 PMID: 18390593
  12. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans.
    Nature. 2009 Sep 17;461(7262):393-8 PMID: 19741609
  13. The ipiO gene of Phytophthora infestans is highly expressed in invading hyphae during infection.
    Fungal Genet Biol. 1998 Mar;23(2):126-38 PMID: 9578626
  14. A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato.
    Mol Plant Microbe Interact. 1997 Jan;10(1):13-20 PMID: 9002268
  15. An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus.
    Plant J. 2002 Mar;29(5):569-79 PMID: 11874570
  16. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1.
    Plant J. 2010 Sep;63(5):791-800 PMID: 20561260
  17. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana.
    Plant J. 2006 Oct;48(2):165-76 PMID: 16965554
  18. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture.
    Plant Physiol. 2001 Nov;127(3):803-16 PMID: 11706164
  19. The Colletotrichum orbiculare SSD1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway.
    Plant Cell. 2009 Aug;21(8):2517-26 PMID: 19706796
  20. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9452-7 PMID: 20439716
  21. Ancient class of translocated oomycete effectors targets the host nucleus.
    Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17421-6 PMID: 20847293
  22. Distinct amino acids of the Phytophthora infestans effector AVR3a condition activation of R3a hypersensitivity and suppression of cell death.
    Mol Plant Microbe Interact. 2009 Mar;22(3):269-81 PMID: 19245321
  23. Innate immunity: the virtues of a nonclonal system of recognition.
    Cell. 1997 Oct 31;91(3):295-8 PMID: 9363937
  24. A novel class of elicitin-like genes from Phytophthora infestans.
    Mol Plant Microbe Interact. 1997 Nov;10(8):1028-30 PMID: 9353948
  25. Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors.
    J Biol Chem. 2010 Jun 18;285(25):19035-42 PMID: 20410299
  26. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1.
    Plant Physiol. 2009 May;150(1):320-32 PMID: 19321708
  27. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm.
    Proc Natl Acad Sci U S A. 2005 May 24;102(21):7766-71 PMID: 15894622
  28. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants.
    Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12217-22 PMID: 17626179
  29. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1.
    Science. 2000 Jun 30;288(5475):2360-3 PMID: 10875920
  30. NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death.
    Planta. 2008 Nov;228(6):977-87 PMID: 18682978
  31. A gene encoding a host-specific elicitor protein of Phytophthora parasitica.
    Mol Plant Microbe Interact. 1993 Sep-Oct;6(5):573-81 PMID: 8274771
  32. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  33. Analysis of phosphorylation of the BRI1/BAK1 complex in arabidopsis reveals amino acid residues critical for receptor formation and activation of BR signaling.
    Mol Cells. 2009 Feb 28;27(2):183-90 PMID: 19277500
  34. The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis.
    Plant Signal Behav. 2009 Jun;4(6):539-41 PMID: 19816132
  35. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana.
    Plant J. 2007 Jul;51(1):32-46 PMID: 17559511
  36. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2.
    Plant Cell. 2009 Sep;21(9):2928-47 PMID: 19794118
  37. Plant immunity: towards an integrated view of plant-pathogen interactions.
    Nat Rev Genet. 2010 Aug;11(8):539-48 PMID: 20585331
  38. The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato.
    Plant Cell. 2006 Apr;18(4):1067-83 PMID: 16531490
  39. Mechanisms of specificity in protein phosphorylation.
    Nat Rev Mol Cell Biol. 2007 Jul;8(7):530-41 PMID: 17585314
  40. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  41. Ten things to know about oomycete effectors.
    Mol Plant Pathol. 2009 Nov;10(6):795-803 PMID: 19849785
  42. Pattern-recognition receptors in plant innate immunity.
    Curr Opin Immunol. 2008 Feb;20(1):10-6 PMID: 18206360
  43. Nonhost resistance to Phytophthora: novel prospects for a classical problem.
    Curr Opin Plant Biol. 2001 Aug;4(4):295-300 PMID: 11418338
  44. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.
    Nature. 2007 Jul 26;448(7152):497-500 PMID: 17625569
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0016608
Published
2011-01-27
Epub
2011-00-27
Pages
e16608
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3029390
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · United Kingdom
Databases
GENBANK
HQ332144, HQ332145
External Links
PubMed source DOI: 10.1371/journal.pone.0016608 PMC Full Text View journal details
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