The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity
Article first published online: 15 JUL 2010
© The Authors (2010). Journal compilation © New Phytologist Trust (2010)
Special Issue: Featured papers on ‘Effectors in plant–microbe interactions’
Volume 187, Issue 4, pages 1018–1033, September 2010
How to Cite
Macho, A. P., Guevara, C. M., Tornero, P., Ruiz-Albert, J. and Beuzón, C. R. (2010), The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity. New Phytologist, 187: 1018–1033. doi: 10.1111/j.1469-8137.2010.03381.x
- Issue published online: 12 AUG 2010
- Article first published online: 15 JUL 2010
- Received: 25 February 2010, Accepted: 2 June 2010
- 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, USA 95: 10306–10311. , , , , , .
- 2006. Bacterial elicitation and evasion of plant innate immunity. Nature Reviews Molecular Cell Biology 7: 601–611. , , .
- 1999. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148–2152. , , , , .
- 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369–377. , .
- 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073–2076. , , , , , .
- 2006. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18: 1038–1051. , , , , , , .
- 1996. Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiology 111: 525–531. , , .
- 2002. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant Journal 29: 23–32. , , .
- 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes and Infection 3: 1345–1352. , .
- 2001. In vivo genetic analysis indicates that PhoP-PhoQ and the Salmonella pathogenicity island 2 type III secretion system contribute independently to Salmonella enterica serovar Typhimurium virulence. Infection and Immunity 69: 7254–7261. , , .
- 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927–933. , , , , .
- 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proceedings of the National Academy of Sciences, USA 95: 15849–15854. , , .
- 1994. Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant Journal 5: 715–725. , , .
- 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592. , , , .
- 1995. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proceedings of the National Academy of Sciences, USA 92: 6597–6601. , , .
- 2000. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Molecular Plant-Microbe Interactions 13: 1312–1321. , , , , .
- 2004. The Pseudomonas syringae type III effector AvrRpt2 functions downstream or independently of SA to promote virulence on Arabidopsis thaliana. Plant Journal 37: 494–504. , , , , , , , , .
- 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814. , , , .
- 2004. Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant Journal 40: 225–237. , , , , , .
- 1986. Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Applied and Environmental Microbiology 51: 323–327. .
- 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology 142: 352–363. , , , , , , .
- 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250. , , , , , , , , , et al.
- 2003. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. Journal of Bacteriology 185: 2592–25602. , , , , .
- 1997. ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana. FEBS Letters 400: 168–172. , , .
- 2004. Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiology 6: 1027–1040. , .
- 1994. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751–759. , , , .
- 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO Journal 20: 5400–5411. , , , .
- 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227. .
- 2008. Breaking the barriers: microbial effector molecules subvert plant immunity. Annual Review of Phytopathology 46: 189–215. , .
- 1992. Fundamentals of bacterial plant pathology. New York, NY, USA: Academic Press Inc. .
- 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843–846. , , , , , , , .
- 2009. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Molecular Plant-Microbe Interactions 22: 1069–1080. , , , .
- 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513–523. , .
- 1983. Studies of transformation of Escherichia coli with plasmids. Journal of Molecular Biology 166: 557–580. .
- 1996. Identification of a new Arabidopsis disease resistance locus, RPS4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi. Molecular Plant-Microbe Interactions 9: 55–61. , .
- 2003. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO Journal 22: 5679–5689. , , , , , , .
- 1999. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proceedings of the National Academy of Sciences, USA 96: 10875–10880. , , , , , , , , , .
- 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proceedings of the National Academy of Sciences, USA 96: 13583–13588. , , , , , , , .
- 2006. The plant immune system. Nature 444: 323–329. , .
- 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346: 385–386. , .
- 2005a. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proceedings of the National Academy of Sciences, USA 102: 6496–6501. , , , , , .
- 2005b. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121: 749–759. , , , , , , .
- 2009. The Pseudomonas syringae type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2. Plant Journal 57: 645–653. , , , .
- 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175–176. , , , , , , .
- 1995. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant-Microbe Interactions 8: 863–870. , , , , , .
- 2007. A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. Molecular Plant-Microbe Interactions 20: 1192–1200. , , , .
- 2008. The HopZ family of Pseudomonas syringae type III effectors require myristoylation for virulence and avirulence functions in Arabidopsis thaliana. Journal of Bacteriology 190: 2880–2891. , , , , .
- 2004. The Pseudomonas syringae type III effector AvrRpt2 promotes virulence independently of RIN4, a predicted virulence target in Arabidopsis thaliana. Plant Journal 40: 790–798. , .
- 2001. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13: 437–447. , , .
- 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genetics 2: e209. , , , .
- 2009. Identification of new type III effectors and analysis of the plant response by competitive index. Molecular Plant Pathology 10: 69–80. , , , .
- 2007. Competitive index in mixed infections: a sensitive and accurate assay for the genetic analysis of Pseudomonas syringae-plant interactions. Molecular Plant Pathology 8: 437–450. , , , .
- 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379–389. , , , , .
- 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743–754. , , , .
- 2009. From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Molecular Plant Pathology 10: 721–734. .
- 1999. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Molecular Microbiology 32: 927–941. , .
- 2006. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology 140: 249–262. , , , , .
- 1994. Characterization of pPT23B, the plasmid involved in syringolide production by Pseudomonas syringae pv. tomato PT23. Plasmid 31: 275–287. , , , , , .
- 2002. Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14: 979–992. , , , , , , , .
- 2004. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Molecular Plant Pathology 5: 425–434. , , , , , , , .
- 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198: 249–266. , , , .
- 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033–2046. , , , , , .
- 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Molecular Plant-Microbe Interactions 8: 444–453. , .
- 1996. Systemic acquired resistance. Plant Cell 8: 1809–1819. , , , , , .
- 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109: 575–588. , , , , .
- 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology 60: 139–164. .
- 2009. The Pseudomonas syringae effector protein, AvrRPS4, requires in planta processing and the KRVY domain to function. Plant Journal 57: 1079–1091. , , .
- 2004. Complete nucleotide sequence and analysis of pPSR1 (72,601 bp), a pPT23A-family plasmid from Pseudomonas syringae pv. syringae A2. Molecular Genetics and Genomics 270: 462–476. , , , , , .
- 1991. Genetics of pathogenicity and resistance in the halo-blight disease of beans in Africa. PhD thesis, Birmingham, UK: University of Birmingham. .
- 2002. RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005–1015. , , , , , .
- 2007. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences, USA 104: 1075–1080. , , , , .
- 2009. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genetics 5: e1000545. , , , , , , , , , et al.
- 2006. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Molecular Microbiology 62: 26–44. , , , , , , , .
- 2000. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 97: 8711–8716. , , , , .
- 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308: 1036–1040. , , , .
- 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562–565. , , , .
- 2010. The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proceedings of the National Academy of Sciences, USA 107: 2349–2354. , , , , , .
- 1998. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091–1094. , , , , .
- 2009. Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Molecular Plant-Microbe Interactions 22: 176–189. , , , .
- 2008. Pattern-recognition receptors in plant innate immunity. Current Opinion in Immunology 20: 10–16. .