Home LiteratureArticle Details
PMID: 20159621 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4.

Cell host & microbe ·Vol. 7 ·No. 2 ·2010-02-18 ·Pages 164-75

Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J, Chen M, Innes RW, Zhou JM

Abstract

Pathogenic microbes often modulate phytohormone physiology in the host to their advantage. We previously showed that the Pseudomonas syringae effector protein AvrB perturbs hormone signaling, as exemplified by upregulated expression of jasmonic acid response genes, and enhances plant susceptibility. Here we show that these effects of AvrB require the Arabidopsis mitogen-activated protein kinase MAP kinase 4 (MPK4), HSP90 chaperone components, and the AvrB-interacting protein, RIN4. AvrB interacts with MPK4 and the HSP90 chaperone, and AvrB induces MPK4 activation in a manner promoted by HSP90; RIN4 likely acts downstream of MPK4. These findings link Arabidopsis proteins MPK4, HSP90, and RIN4 into a pathway that P. syringae AvrB activates for the benefit of the bacterium, perturbing hormone signaling and enhancing plant susceptibility.

MeSH Terms
Arabidopsis/microbiology Arabidopsis Proteins/biosynthesis,metabolism Bacterial Proteins/physiology Carrier Proteins/metabolism HSP90 Heat-Shock Proteins/metabolism Host-Pathogen Interactions Intracellular Signaling Peptides and Proteins Mitogen-Activated Protein Kinases/biosynthesis Protein Interaction Mapping Pseudomonas syringae/physiology Signal Transduction Virulence Factors/physiology
Chemicals
Arabidopsis Proteins AvrB protein, Pseudomonas syringae Bacterial Proteins Carrier Proteins HSP90 Heat-Shock Proteins Intracellular Signaling Peptides and Proteins RIN4 protein, Arabidopsis Virulence Factors AtMPK4 protein, Arabidopsis Mitogen-Activated Protein Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Cui Haitao
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.
Wang Yujing
Xue Li
Chu Jinfang
Yan Cunyu
Fu Jihong
Chen Mingsheng
Innes Roger W
Zhou Jian-Min
References (49)
49 references, click to expand
  1. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions.
    Curr Opin Microbiol. 2009 Feb;12(1):53-60 PMID: 19168384
  2. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity.
    Cell. 2006 May 5;125(3):563-75 PMID: 16678099
  3. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance.
    Cell. 2000 Dec 22;103(7):1111-20 PMID: 11163186
  4. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease.
    EMBO J. 2007 Mar 7;26(5):1434-43 PMID: 17304219
  5. Convergent evolution of disease resistance gene specificity in two flowering plant families.
    Plant Cell. 2004 Feb;16(2):309-18 PMID: 14742871
  6. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine.
    Plant J. 2004 Feb;37(4):589-602 PMID: 14756769
  7. Type III effector activation via nucleotide binding, phosphorylation, and host target interaction.
    PLoS Pathog. 2007 Mar;3(3):e48 PMID: 17397263
  8. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity.
    Nature. 2007 May 17;447(7142):284-8 PMID: 17450127
  9. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death.
    Plant Cell. 1996 Jul;8(7):1095-105 PMID: 8768370
  10. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity.
    Plant Cell. 2007 Nov;19(11):3791-804 PMID: 18032631
  11. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death.
    Plant Physiol. 2006 Jan;140(1):249-62 PMID: 16377744
  12. Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4.
    Plant J. 2006 Aug;47(4):532-46 PMID: 16813576
  13. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein.
    EMBO J. 2003 Nov 3;22(21):5679-89 PMID: 14592967
  14. Structural basis of EZH2 recognition by EED.
    Structure. 2007 Oct;15(10):1306-15 PMID: 17937919
  15. Structure and mechanism of the Hsp90 molecular chaperone machinery.
    Annu Rev Biochem. 2006;75:271-94 PMID: 16756493
  16. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens.
    Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8955-9 PMID: 8090752
  17. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.
    Science. 2002 Mar 15;295(5562):2073-6 PMID: 11847307
  18. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases.
    Curr Biol. 2008 Jan 8;18(1):74-80 PMID: 18158241
  19. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis.
    Cell. 2005 Jun 3;121(5):749-59 PMID: 15935761
  20. The HSP90-SGT1 chaperone complex for NLR immune sensors.
    Annu Rev Plant Biol. 2009;60:139-64 PMID: 19014346
  21. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis.
    J Exp Bot. 2009;60(13):3849-60 PMID: 19596700
  22. RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB.
    Proc Natl Acad Sci U S A. 2006 Dec 12;103(50):19200-5 PMID: 17148606
  23. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB.
    Curr Biol. 2008 Dec 9;18(23):1824-32 PMID: 19062288
  24. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants.
    Curr Biol. 2009 Mar 10;19(5):423-9 PMID: 19249211
  25. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis.
    Plant Cell. 2009 Aug;21(8):2527-40 PMID: 19717619
  26. A bacterial virulence protein suppresses host innate immunity to cause plant disease.
    Science. 2006 Jul 14;313(5784):220-3 PMID: 16840699
  27. AvrB mutants lose both virulence and avirulence activities on soybean and Arabidopsis.
    Mol Microbiol. 2006 May;60(4):951-62 PMID: 16677306
  28. Making sense of hormone crosstalk during plant immune responses.
    Cell Host Microbe. 2008 Jun 12;3(6):348-51 PMID: 18541211
  29. Plant stomata function in innate immunity against bacterial invasion.
    Cell. 2006 Sep 8;126(5):969-80 PMID: 16959575
  30. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae.
    Cell. 2000 May 12;101(4):353-63 PMID: 10830163
  31. Pathological hormone imbalances.
    Curr Opin Plant Biol. 2007 Aug;10(4):372-9 PMID: 17646123
  32. Role of SGT1 in resistance protein accumulation in plant immunity.
    EMBO J. 2006 May 3;25(9):2007-16 PMID: 16619029
  33. Crystal structure of the type III effector AvrB from Pseudomonas syringae.
    Structure. 2004 Mar;12(3):487-94 PMID: 15016364
  34. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor.
    Plant Cell. 2009 Aug;21(8):2220-36 PMID: 19717617
  35. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance.
    Science. 1995 Aug 11;269(5225):843-6 PMID: 7638602
  36. Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus.
    Genetics. 1995 Dec;141(4):1597-604 PMID: 8601497
  37. Plant pathogenic bacterial type III effectors subdue host responses.
    Curr Opin Microbiol. 2008 Apr;11(2):179-85 PMID: 18372208
  38. Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB.
    Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6475-80 PMID: 18424557
  39. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11777-82 PMID: 14504384
  40. Antagonistic control of disease resistance protein stability in the plant immune system.
    Science. 2005 Aug 5;309(5736):929-32 PMID: 15976272
  41. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  42. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors.
    Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12990-5 PMID: 16123135
  43. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase.
    Plant Cell. 1999 Dec;11(12):2419-28 PMID: 10590168
  44. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1.
    Plant Physiol. 2008 Sep;148(1):212-22 PMID: 18599650
  45. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):20131-6 PMID: 18056646
  46. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants.
    Cell Res. 2008 Dec;18(12):1190-8 PMID: 18982020
  47. Microbe-associated molecular patterns (MAMPs) probe plant immunity.
    Curr Opin Plant Biol. 2007 Aug;10(4):335-41 PMID: 17652011
  48. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.
    Cell Host Microbe. 2007 May 17;1(3):175-85 PMID: 18005697
  49. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
Article Info
Journal
Cell host & microbe
Abbr.
Cell Host Microbe
ISSN
1934-6069
DOI
10.1016/j.chom.2010.01.009
Published
2010-02-18
Pages
164-75
Language
English
Region
United States
NLM ID
101302316
PMCID
PMC3328509
Subset
IM
Grants
NIGMS NIH HHS · R01 GM046451 · United States
NIGMS NIH HHS · R01 GM046451-09 · United States
NIGMS NIH HHS · R01 GM046451-10 · United States
NIGMS NIH HHS · GM045461 · United States
External Links
PubMed source DOI: 10.1016/j.chom.2010.01.009 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2