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PMID: 20011122 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Network properties of robust immunity in plants.

PLoS genetics ·Vol. 5 ·No. 12 ·2009-12-00 ·Pages e1000772

Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F

Abstract

Two modes of plant immunity against biotrophic pathogens, Effector Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), are triggered by recognition of pathogen effectors and Microbe-Associated Molecular Patterns (MAMPs), respectively. Although the jasmonic acid (JA)/ethylene (ET) and salicylic acid (SA) signaling sectors are generally antagonistic and important for immunity against necrotrophic and biotrophic pathogens, respectively, their precise roles and interactions in ETI and PTI have not been clear. We constructed an Arabidopsis dde2/ein2/pad4/sid2-quadruple mutant. DDE2, EIN2, and SID2 are essential components of the JA, ET, and SA sectors, respectively. The pad4 mutation affects the SA sector and a poorly characterized sector. Although the ETI triggered by the bacterial effector AvrRpt2 (AvrRpt2-ETI) and the PTI triggered by the bacterial MAMP flg22 (flg22-PTI) were largely intact in plants with mutations in any one of these genes, they were mostly abolished in the quadruple mutant. For the purposes of this study, AvrRpt2-ETI and flg22-PTI were measured as relative growth of Pseudomonas syringae bacteria within leaves. Immunity to the necrotrophic fungal pathogen Alternaria brassicicola was also severely compromised in the quadruple mutant. Quantitative measurements of the immunity levels in all combinatorial mutants and wild type allowed us to estimate the effects of the wild-type genes and their interactions on the immunity by fitting a mixed general linear model. This signaling allocation analysis showed that, contrary to current ideas, each of the JA, ET, and SA signaling sectors can positively contribute to immunity against both biotrophic and necrotrophic pathogens. The analysis also revealed that while flg22-PTI and AvrRpt2-ETI use a highly overlapping signaling network, the way they use the common network is very different: synergistic relationships among the signaling sectors are evident in PTI, which may amplify the signal; compensatory relationships among the sectors dominate in ETI, explaining the robustness of ETI against genetic and pathogenic perturbations.

MeSH Terms
Bacteria/growth & development Fungi/growth & development Genes, Plant Plants/genetics,immunology,microbiology Signal Transduction/genetics
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Tsuda Kenichi
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St. Paul, Minnesota, USA.
Sato Masanao
Stoddard Thomas
Glazebrook Jane
Katagiri Fumiaki
Conflict of Interest

The authors have declared that no competing interests exist.

References (58)
58 references, click to expand
  1. 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
  2. Interference between Two Specific Pathogen Recognition Events Mediated by Distinct Plant Disease Resistance Genes.
    Plant Cell. 1996 Feb;8(2):251-257 PMID: 12239384
  3. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  4. 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
  5. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats.
    Cell. 1994 Sep 23;78(6):1089-99 PMID: 7923358
  6. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance.
    Science. 1995 Aug 11;269(5225):843-6 PMID: 7638602
  7. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants.
    Plant Cell. 2004 Dec;16(12):3496-507 PMID: 15548740
  8. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19613-8 PMID: 18042724
  9. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis.
    Plant Cell. 2008 Feb;20(2):471-81 PMID: 18263776
  10. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):517-22 PMID: 11756663
  11. Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs.
    J Biol Chem. 2007 Aug 24;282(34):25020-9 PMID: 17586809
  12. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling.
    Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13583-8 PMID: 10557364
  13. The salicylic acid loop in plant defense.
    Curr Opin Plant Biol. 2003 Aug;6(4):365-71 PMID: 12873532
  14. The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana.
    Mol Plant Pathol. 2005 Nov 1;6(6):629-39 PMID: 20565685
  15. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles.
    Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18842-7 PMID: 17998535
  16. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance.
    Cell. 2003 Feb 7;112(3):379-89 PMID: 12581527
  17. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway.
    Planta. 2002 Nov;216(1):187-92 PMID: 12430030
  18. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis.
    Cell. 2005 Jun 3;121(5):749-59 PMID: 15935761
  19. Systems biology. Attractors and democratic dynamics.
    Science. 2009 Feb 20;323(5917):1016-7 PMID: 19229023
  20. Purification of low-abundance Arabidopsis plasma-membrane protein complexes and identification of candidate components.
    Plant J. 2009 Mar;57(5):932-44 PMID: 19000159
  21. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping.
    Plant J. 2003 Apr;34(2):217-28 PMID: 12694596
  22. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):15107-11 PMID: 9844023
  23. Interplay between MAMP-triggered and SA-mediated defense responses.
    Plant J. 2008 Mar;53(5):763-75 PMID: 18005228
  24. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants.
    Plant Physiol. 2007 Feb;143(2):661-9 PMID: 17142480
  25. Bacterial elicitation and evasion of plant innate immunity.
    Nat Rev Mol Cell Biol. 2006 Aug;7(8):601-11 PMID: 16936700
  26. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.
    Annu Rev Phytopathol. 2005;43:205-27 PMID: 16078883
  27. CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis.
    Plant Physiol. 2006 Aug;141(4):1248-54 PMID: 16766671
  28. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation.
    Plant J. 2000 Jun;22(6):523-9 PMID: 10886772
  29. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):661-5 PMID: 17637677
  30. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis.
    Plant Cell. 1998 Jun;10(6):1021-30 PMID: 9634589
  31. A bacterial virulence protein suppresses host innate immunity to cause plant disease.
    Science. 2006 Jul 14;313(5784):220-3 PMID: 16840699
  32. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis.
    Plant Cell. 2004 Dec;16(12):3386-99 PMID: 15539472
  33. Plant disease resistance protein signaling: NBS-LRR proteins and their partners.
    Curr Opin Plant Biol. 2004 Aug;7(4):391-9 PMID: 15231261
  34. Plasmid-mediated production of the phytotoxin coronatine in Pseudomonas syringae pv. tomato.
    J Bacteriol. 1989 Feb;171(2):807-12 PMID: 2536682
  35. Cleavage of Arabidopsis PBS1 by a bacterial type III effector.
    Science. 2003 Aug 29;301(5637):1230-3 PMID: 12947197
  36. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis.
    Plant Cell. 2007 Jan;19(1):63-73 PMID: 17259259
  37. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.
    Cell. 2006 May 19;125(4):749-60 PMID: 16713565
  38. Suppression of the microRNA pathway by bacterial effector proteins.
    Science. 2008 Aug 15;321(5891):964-7 PMID: 18703740
  39. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  40. Real-time PCR monitoring of fungal development in Arabidopsis thaliana infected by Alternaria brassicicola and Botrytis cinerea.
    Plant Physiol Biochem. 2004 May;42(5):367-71 PMID: 15191738
  41. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  42. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana.
    Plant J. 1999 May;18(3):277-84 PMID: 10377993
  43. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity.
    Nature. 2007 May 17;447(7142):284-8 PMID: 17450127
  44. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes.
    Science. 1994 Sep 23;265(5180):1856-60 PMID: 8091210
  45. The interplay between MAMP and SA signaling.
    Plant Signal Behav. 2008 Jun;3(6):359-61 PMID: 19513222
  46. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity.
    Nature. 2007 Jul 19;448(7151):370-4 PMID: 17637671
  47. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling.
    Curr Biol. 2008 May 6;18(9):650-5 PMID: 18450451
  48. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  49. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis.
    Plant Cell. 2007 May;19(5):1665-81 PMID: 17513501
  50. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  51. Bacterial disease resistance in Arabidopsis through flagellin perception.
    Nature. 2004 Apr 15;428(6984):764-7 PMID: 15085136
  52. A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis.
    Plant J. 2002 Jul;31(1):1-12 PMID: 12100478
  53. Signals and transduction mechanisms for activation of plant defenses against microbial attack.
    Cell. 1989 Jan 27;56(2):215-24 PMID: 2643475
  54. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.
    Nature. 2007 Jul 26;448(7152):497-500 PMID: 17625569
  55. Loss of a callose synthase results in salicylic acid-dependent disease resistance.
    Science. 2003 Aug 15;301(5635):969-72 PMID: 12920300
  56. 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
  57. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling.
    Science. 2006 Apr 21;312(5772):436-9 PMID: 16627744
  58. MAP kinase signalling cascade in Arabidopsis innate immunity.
    Nature. 2002 Feb 28;415(6875):977-83 PMID: 11875555
Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
DOI
10.1371/journal.pgen.1000772
Published
2009-12-00
Epub
2009-00-11
Pages
e1000772
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC2782137
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pgen.1000772 PMC Full Text View journal details
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