Skip to main content
Log in

Host immunity-suppressive molecular weapons of phytopathogenic bacteria

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The co-evolution of phytopathogenic bacteria and their hosts has determined the outcome of interactions between these organisms. The sophisticated plant immune system ensures the resistance of most plants to most microbial attacks and thus the ability of phytopathogens to cause disease is an exception rather than the rule in nature. In susceptible plants, however, bacterial virulence factors manipulate a number of host cellular pathways, thereby facilitating successful colonization. These virulence factors include effector proteins that are delivered into host cellsvia the type III secretion system (TTSS) and suppress host defenses. The type III effectors (TTEs) perturb various host cellular processes including the hypersensitive response, MAPK signaling, cellular trafficking, transcription, hormone signaling, host protein modification, and stomatal reopening. This review summarizes the observations of recent studies focusing on the interactions between the two model organismsArabidopsis thaliana andPseudomonas syringae that have shed light on the TTSS and the virulent activities of TTSS-translocated effector

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103: 2851–2856

    Article  PubMed  CAS  Google Scholar 

  • Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EmboJ 22: 60–69

    Article  CAS  Google Scholar 

  • Ade J, DeYoung BJ, Golstein C, Innes RW (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA 104: 2531–2536

    Article  PubMed  CAS  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977–983

    Article  PubMed  CAS  Google Scholar 

  • Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973–979

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-Specified Disease Resistance in Arabidopsis Is Coupled to the AvrRpt2-Directed Elimination of RIN4. Cell 112: 369–377

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Chisholm ST, Dahlbeck D, Staskawicz BJ (2003) Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol 49: 1537–1546

    Article  PubMed  CAS  Google Scholar 

  • Beattie GA, Lindow SE (1994) Epiphytic fitness of phytopathogenic bacteria: physiological adaptations for growth and survival. In Bacterial Pathogenesis of Plants and Animals: Molecular and Cellular Mechanisms., J.D. Dangl, ed (Heidelberg: Springer Verlag), pp. 1–28

    Google Scholar 

  • Bretz JR, Mock NM, Charity JC, Zeyad S, Baker CJ, Hutcheson SW (2003) A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol Microbiol 49: 389–400

    Article  PubMed  CAS  Google Scholar 

  • Brooks DM, Hernandez-Guzman G, Kloek AP, Alarcon-Chaidez F, Sreedharan A, Rangaswamy V, Penaloza-Vazquez A, Bender CL, Kunkel BN (2004) Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 17: 162–174

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104: 20131–20136

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Dahlbeck D, Krishnamurthy N, Day B, Sjolander K, Staskawicz BJ (2005) Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc Natl Acad Sci USA 102: 2087–2092

    Article  PubMed  CAS  Google Scholar 

  • Cohn JR, Martin GB (2005) Pseudomonas syringae pv. tomato type III effectors AvrPto and AvrPtoB promote ethylene-dependent cell death in tomato. Plant J 44: 139–154

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973–977

    Article  PubMed  CAS  Google Scholar 

  • Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10: 462–469

    Article  PubMed  CAS  Google Scholar 

  • Collmer A, Badel JL, Charkowski AO, Deng WL, Fouts DE, Ramos AR, Rehm AH, Anderson DM, Schneewind O, van Dijk K, Alfano JR (2000) Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc Natl Acad Sci USA 97: 8770–8777

    Article  PubMed  CAS  Google Scholar 

  • Cuppels DA (1986) Generation and Characterization of Tn5 Insertion Mutations in Pseudomonas syringae pv. tomato. Appl Environ Microbiol 51: 323–327

    PubMed  CAS  Google Scholar 

  • da Cunha L, McFall AJ, Mackey D (2006) Innate immunity in plants: a continuum of layered defenses. Microbes Infect 8: 1372–1381

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826–833

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Holub E, Debener T, Lehnackers H, Ritter C, Crute IR (1992) Genetic definition of loci involved in Arabidopsis-pathogen interactions. In Methods in Arabidopsis Research, C. Koncz, N.-H. Chua, and J. Schell, eds (Singapore: World Scientific), pp. 393–418

    Google Scholar 

  • DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acidmediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci USA 101: 9927–9932

    Article  PubMed  CAS  Google Scholar 

  • Espinosa A, Guo M, Tam VC, Fu ZQ, Alfano JR (2003) The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol Microbiol 49: 377–387

    Article  PubMed  CAS  Google Scholar 

  • Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7: 537–546

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7: 251–256

    Article  PubMed  Google Scholar 

  • Galan JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322–1328

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277–284

    Article  PubMed  Google Scholar 

  • Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White FF, Yin Z (2005). R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435: 1122–1125

    Article  PubMed  CAS  Google Scholar 

  • Gurlebeck D, Thieme F, Bonas U (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol 163: 233–255

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Jones JD (1997). Plant Disease Resistance Genes. Annu Rev Plant Physiol Plant Mol Biol 48: 575–607

    Article  PubMed  CAS  Google Scholar 

  • Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100: 8577–8582

    Article  PubMed  CAS  Google Scholar 

  • He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nurnberger T, Sheen J (2006). Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563–575

    Article  PubMed  CAS  Google Scholar 

  • He P, Chintamanani S, Chen Z, Zhu L, Kunkel BN, Alfano JR, Tang X, Zhou JM (2004) Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J 37: 589–602

    Article  PubMed  CAS  Google Scholar 

  • He SY (1997) Hrp-controlled interkingdom protein transport: learning from flagellar assembly? Trends Microbiol 5: 489–495

    Article  PubMed  CAS  Google Scholar 

  • Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44: 321–334

    Article  PubMed  CAS  Google Scholar 

  • Holt BF, 3rd Mackey D, Dangl JL (2000) Recognition of pathogens by plants. Curr Biol 10: R5–7

    Article  PubMed  CAS  Google Scholar 

  • Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003). Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Molecular microbiology 50: 377–389

    Article  PubMed  CAS  Google Scholar 

  • Israelsson M, Siegel RS, Young J, Hashimoto M, Iba K, Schroeder JI (2006) Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9: 654–663

    Article  PubMed  CAS  Google Scholar 

  • Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer A, Alfano JR (2004) Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J 37: 554–565

    Article  PubMed  CAS  Google Scholar 

  • Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311: 222–226

    Article  PubMed  CAS  Google Scholar 

  • Jin Q, Thilmony R, Zwiesler-Vollick J, He SY (2003) Type III protein secretion in Pseudomonas syringae. Microbes Infect 5: 301–310

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323–329

    Article  PubMed  CAS  Google Scholar 

  • Kang L, Tang X, Mysore KS (2004) Pseudomonas Type III effector AvrPto suppresses the programmed cell death induced by two nonhost pathogens in Nicotiana benthamiana and tomato. Mol Plant Microbe Interact 17: 1328–1336

    Article  PubMed  CAS  Google Scholar 

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648–651

    Article  PubMed  CAS  Google Scholar 

  • Keen NT, Tamaki S, Kobayashi D, Gerhold D, Stayton M, Shen H, Gold S, Lorang J, Thordal-Christenson H, Dahlbeck D, Staskawicz BJ (1990) Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Mol. Plant-Microbe Interact 3: 112–121

    CAS  Google Scholar 

  • Kim CY, Zhang S (2004) Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J 38: 142–151

    Article  PubMed  CAS  Google Scholar 

  • Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005a) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci USA 102: 6496–6501

    Article  PubMed  CAS  Google Scholar 

  • Kim MG, Mackey D (2008) Measuring Cell Wall-Based Defenses and Their Effect on Bacterial Growth in Arabidopsis. In Methods in Molecular Biology: Innate Immunity, E. Vivier and J. Ewbank, eds (Humana Press,Berlin)

    Google Scholar 

  • Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005b) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121: 749–759

    Article  PubMed  CAS  Google Scholar 

  • Kubori T, Sukhan A, Aizawa SI, Galan JE (2000) Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc Natl Acad Sci USA 97: 10225–10230

    Article  PubMed  CAS  Google Scholar 

  • Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galan JE, Aizawa SI (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602–605

    Article  PubMed  CAS  Google Scholar 

  • Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jurgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451: 835–840

    Article  PubMed  CAS  Google Scholar 

  • Laurie-Berry N, Joardar V, Street IH, Kunkel BN (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact 19: 789–800

    Article  PubMed  CAS  Google Scholar 

  • Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou J (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315: 1000–1003

    Article  PubMed  CAS  Google Scholar 

  • Lin NC, Martin GB (2005) An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol Plant Microbe Interact 18: 43–51

    Article  PubMed  CAS  Google Scholar 

  • Lindgren PB, Peet RC, Panopoulos NJ (1986) Gene cluster of Pseudomonas syringae pv. “phaseolicola” controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J Bacteriol 168: 512–522

    PubMed  CAS  Google Scholar 

  • Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23: 147–174

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Solanilla E, Bronstein PA, Schneider AR, Collmer A (2004). HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogeninduced necrosis associated with both compatible and incompatible plant interactions. Mol Microbiol 54: 353–365

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938–1950

    Article  PubMed  CAS  Google Scholar 

  • Mackey D, Holt III BF, WiigA, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae Type III effector molecules and is required for RPM1-mediated disease resistance in Arabidopsis. Cell 108: 743–754

    Article  PubMed  CAS  Google Scholar 

  • Mackey D, Belkhadir Y, AlonsoJM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 Is a Target of the Type III Virulence Effector AvrRpt2 and Modulates RPS2-Mediated Resistance. Cell 112: 379–389

    Article  PubMed  CAS  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436–439

    Article  PubMed  CAS  Google Scholar 

  • Nimchuk ZL, Fisher EJ, Desveaux D, Chang JH, Dangl JL (2007) The HopX (AvrPphE) family of Pseudomonas syringae type III effectors require a catalytic triad and a novel N-terminal domain for function. Mol Plant Microbe Interact 20: 346–357

    Article  PubMed  CAS  Google Scholar 

  • Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220–223

    Article  PubMed  CAS  Google Scholar 

  • Nurnberger T, Brunner F, Kemmerling B, Piater L (2004). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266

    Article  PubMed  Google Scholar 

  • Pedley KF, Martin GB (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu Rev Phytopathol 41: 215–243

    Article  PubMed  CAS  Google Scholar 

  • Rahme LG, Mindrinos MN, Panopoulos NJ (1992) Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J Bacteriol 174: 3499–3507

    PubMed  CAS  Google Scholar 

  • Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Molecular plant-microbe interactions 17: 633–643

    Article  PubMed  CAS  Google Scholar 

  • Rooney HC, van ‘t Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ (2005) Cladosporium Avr2 Inhibits Tomato Rcr3 Protease Required for Cf-2-Dependent Disease Resistance. Science 308: 1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thalianaidentified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molec. Plant-Microbe Interact 10: 69–78

    Article  CAS  Google Scholar 

  • Shang Y, Li X, Cui H, He P, Thilmony R, Chintamanani S, Zwiesler-Vollick J, Gopalan S, Tang X, Zhou J (2006) RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB. PNAS 103: 19200–19205

    Article  PubMed  CAS  Google Scholar 

  • Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301: 1230–1233

    Article  PubMed  CAS  Google Scholar 

  • Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46: 34–53

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308: 1036–1040

    Article  PubMed  CAS  Google Scholar 

  • Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R genespecified disease resistance in Arabidopsis. Genetics 152: 401–412

    PubMed  CAS  Google Scholar 

  • Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49–59

    Article  PubMed  CAS  Google Scholar 

  • Xiao Y, Lu Y, Heu S, Hutcheson SW (1992) Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J Bacteriol 174: 1 734–1741

    CAS  Google Scholar 

  • Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103: 10503–10508

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11: 1621–1639

    Article  PubMed  CAS  Google Scholar 

  • Young JJ, Mehta S, Israelsson M, Godoski J, Grill E, Schroeder JI (2006). CO(2) signaling in guard cells: calcium sensitivity response modulation, a Ca(2+)-independent phase, and CO(2) insensitivity of the gca2 mutant. Proc Natl Acad Sci USA 103: 7506–7511

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8: 353–360

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sang Yeol Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, M.G., Kim, W.Y., Lee, J.R. et al. Host immunity-suppressive molecular weapons of phytopathogenic bacteria. J. Plant Biol. 51, 233–239 (2008). https://doi.org/10.1007/BF03036121

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03036121

Keywords

Navigation