The HopX (AvrPphE) family of Pseudomonas syringae type III effectors require a catalytic triad and a novel N-terminal domain for function

Molecular Plant-Microbe Interactions

Volumn 20, Issue 4, 2007, Pages 346-357

  Nimchuk, Zachary L ^a,c   Fisher, Emily J ^a   Desveaux, Darrell ^a,d   Chang, Jeffery H ^a,e   Dangl, Jeffery L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e OREGON STATE UNIVERSITY   (United States)

Author keywords

Bacterial virulence

Indexed keywords

BACTERIAL PROTEIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL DEATH; CHEMISTRY; CYTOLOGY; ENZYME ACTIVE SITE; GENETIC TRANSFECTION; GENETICS; LEGIONELLA; LEGUME; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS SYRINGAE; RHIZOBIUM; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ARABIDOPSIS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELL DEATH; CONSERVED SEQUENCE; FABACEAE; LEGIONELLA; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT LEAVES; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS SYRINGAE; RHIZOBIUM; SEQUENCE ALIGNMENT; TRANSFECTION; VIRULENCE FACTORS;

ANIMALIA; ARABIDOPSIS; BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; NEGIBACTERIA; PSEUDOMONAS SYRINGAE;

EID: 33947416963     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-4-0346     Document Type: Article

References (59)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Axtell, M. J., and Staskawicz, B. J. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369-377.
3. Axtell, M. J., Chisholm, S. T., Dahlbeck, D., and Staskawicz, B. J. 2003. Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol. Microbiol. 49:1537-1546.
4. Belkhadir, Y., Nimchuk, Z., Hubert, D. A., Mackey, D., and Dangl, J. L. 2004a. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16:2822-2835.
5. Belkhadir, Y., Subramaniam, R., and Dangl, J. L. 2004b. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7:391-399.
6. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186.
7. Charity, J. C., Pak, K., Delwiche, C. F., and Hutcheson, S. W. 2003. Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: Evidence for integron-like assembly from transposed gene cassettes. Mol. Plant-Microbe Interact. 16:495-507.
8. Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S. M., Asamani, G., Hill, K., Nuara, J., Feder, M., et al. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
9. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
10. Cianciotto, N. P. 2001. Pathogenicity of Legionella pneumophila. Int. J. Med. Microbiol. 291:331-343.
11. Coaker, G., Falick, A., and Staskawicz, B. 2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548-550.
12. Cuff, J. A., Clamp, M. E., Siddiqui, A. S., Finlay, M., and Barton, G. J. 1998. JPred: A consensus secondary structure prediction server. Bioinformatics 14:892-893.
13. da Silva, A. C., Ferro, J. A., Reinach, F. C., Farah, C. S., Furlan, L. R., Quaggio, R. B., Monteiro-Vitorello, C. B., Van Sluys, M. A., Almeida, N. F., Alves, L. M., et al. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-463.
14. Dangl, J. L., and Jones, J. D. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-833.
15. Debener, T., Lehnackers, H., Arnold, M., and Dangl, J. L. 1991. Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J. 1:289-302.
16. Deng, W. L., Rehm, A. H., Charkowski, A. O., Rojas, C. M., and Collmer, A. 2003. Pseudomonas syringae exchangeable effector loci: Sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J. Bacteriol. 185:2592-2602.
17. Desveaux, D., Singer, A. U., and Dangl, J. L. 2006. Type III effector proteins: Doppelgangers of bacterial virulence. Curr. Opin. Plant Biol. 9:376-382.
18. Dodds, P. N., Lawrence, G. J., Catanzariti, A. M., Teh, T., Wang, C. I., Ayliffe, M. A., Kobe, B., and Ellis, J. G. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103:8888-8893.
19. Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M., and Dangl, J. L. 2006. Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60:425-429.
20. He, P., Shan, L., Lin, N. C., Martin, G. B., Kemmerling, B., Nurnberger, T., and Sheen, J. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563-575.
21. Hirsch, C., Blom, D., and Ploegh, H. L. 2003. A role for N-glycanase in the cytosolic turnover of glycoproteins. EMBO (Eur. Mol. Biol. Organ.) J. 22:1036-1046.
22. Hubber, A., Vergunst, A. C., Sullivan, J. T., Hooykaas, P. J., and Ronson, C. W. 2004. Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain RVA VirB/D4 type IV secretion system. Mol. Microbiol. 54:61-574.
23. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
24. Jamir, Y., Guo, M., Oh, H. S., Petnicki-Ocwieja, T., Chen, S., Tang, X., Dickman, M. B., Collmer, A., and Alfano, J. R. 2004. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37:554-565.
25. Kawasaki, H., Nakayama, S., and Kretsinger, R. H. 1998. Classification and evolution of EF-hand proteins. Biometals 11:277-295.
26. Kjemtrup, S., Nimchuk, Z., and Dangl, J. L. 2000. Effector proteins of phytopathogenic bacteria: Bifunctional signals in virulence and host recognition. Curr. Opin. Microbiol. 3:73-78.
27. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., 2nd, and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lee, J. H., Choi, J. M., Lee, C., Yi, K. J., and Cho, Y. 2005. Structure of a peptide:N-glycanase-Rad23 complex: Insight into the deglycosylation for denatured glycoproteins. Proc. Natl. Acad. Sci. U.S.A. 102:9144-9149.
30. Li, G., Zhou, X., Zhao, G., Schindelin, H., and Lennarz, W. J. 2005. Multiple modes of interaction of the deglycosylation enzyme, mouse peptide N-glycanase, with the proteasome. Proc. Natl. Acad. Sci. U.S.A. 102:15809-15814.
31. Lindeberg, M., Stavrinides, J., Chang, J. H., Alfano, J. R., Collmer, A., Dangl, J. L., Greenberg, J. T., Mansfield, J. W., and Guttman, D. S. 2005. Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol. Plant Microbe-Interact. 18:275-282.
32. Lopez-Solanilla, E., Bronstein, P. A., Schneider, A. R., and Collmer, A. 2004. HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions. Mol. Microbiol. 54:353-365.
33. Lorand, L., and Graham, R. M. 2003. Transglutaminases: Crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4:140-156.
34. Mackey, D., Holt, B. F., 3rd, Wiig, A., and Dangl, J. L. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-754.
35. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl, J. L. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379-389.
36. Makarova, K. S., Aravind, L., and Koonin, E. V. 1999. A superfamily of archaeal, bacterial, and eukaryotic proteins homologous to animal transglutaminases. Protein Sci. 8:1714-1719.
37. Mansfield, J., Jenner, C., Hockenhull, R., Bennett, M. A., and Stewart, R. 1994. Characterization of avrPphE, a gene for cultivar-specific avirulence from Pseudomonas syringae pv. phaseolicola which is physically linked to hrpY, a new hrp gene identified in the halo-blight bacterium. Mol. Plant-Microbe Interact. 7:26-739.
38. McNellis, T. W., Mudgett, M. B., Li, K., Aoyama, T., Horvath, D., Chua, N. H., and Staskawicz, B. J. 1998. Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death. Plant J. 14:247-257.
39. Mudgett, M. B. 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509-531.
40. Nagai, H., Cambronne, E. D., Kagan, J. C., Amor, J. C., Kahn, R. A., and Roy, C. R. 2005. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U.S.A. 102:826-831.
41. Nimchuk, Z., Marois, E., Kjemtrup, S., Leister, R. T., Katagiri, F., and Dangl, J. L. 2000. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several Type III effector proteins from Pseudomonas syringae. Cell 101:353-363.
42. Nimchuk, Z., Rohmer, L., Chang, J. H., and Dangl, J. L. 2001. Knowing the dancer from the dance: R-gene products and their interactions with other proteins from host and pathogen. Curr. Opin. Plant Biol. 4:288-294.
43. Nimchuk, Z., Eulgem, T., Holt, B. F., III, and Dangl, J. L. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579-609.
44. Nomura, K., Melotto, M., and He, S. Y. 2005. Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr. Opin. Plant Biol. 8:361-368.
45. Orth, K., Xu, Z., Mudgett, M. B., Bao, Z. Q., Palmer, L. E., Bliska, J. B., Mangel, W. F., Staskawicz, B., and Dixon, J. E. 2000. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594-1597.
46. Pautsch, A., Vogelsgesang, M., Trankle, J., Herrmann, C., and Aktories, K. 2005. Crystal structure of the C3bot-RalA complex reveals a novel type of action of a bacterial exoenzyme. EMBO (Eur. Mol. Biol. Organ.) J. 24, 3670-3680.
47. Rea, P. A. 2006. Phytochelatin synthase, papain's cousin, in stereo. Proc Natl. Acad. Sci. U.S.A. 103:507-508.
48. Robert-Seilaniantz, A., Shan, L., Zhou, J. M., and Tang, X. 2006. The Pseudomonas syringae pv. tomato DC3000 Type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Mol. Plant-Microbe Interact. 19:130-138.
49. Rohmer, L., Kjemtrup, S., Marchesini, P., and Dangl, J. L. 2003. Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Mol. Microbiol. 47:1545-1562.
50. Romanyuk, N. D., Rigden, D. J., Vatamaniuk, O. K., Lang, A., Cahoon, R. E., Jez, J. M., and Rea, P. A. 2006. Mutagenic definition of papain-like catalytic triad, sufficiency of N-terminal domain for single-site core catalytic enzyme acylation and C-terminal domain for augmentative metal activation of an eukaryotic phytochelatin synthase. Plant Physiol. 141:858-869.
51. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J. C., Cattolico, L., et al. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502.
52. Schechter, L. M., Roberts, K. A., Jamir, Y., Alfano, J. R., and Collmer, A. 2004. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol. 186:543-555.
53. Shan, L., Thara, V. K., Martin, G. B., Zhou, J.-M., and Tang, X. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323-2337.
54. Shao, F., Merritt, P. M., Bao, Z., Innes, R. W., and Dixon, J. E. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-588.
55. Shao, F., Golstein, C., Ade, J., Stoutemyer, M., Dixon, J. E., and Innes, R. W. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230-1233.
56. Sorg, J. A., Miller, N. C., and Schneewind, O. 2005. Substrate recognition of type III secretion machines-testing the RNA signal hypothesis. Cell Microbiol. 7:1217-1225.
57. Stevens, C., Bennett, M. A., Athanassopoulos, E., Tsiamis, G., Taylor, J. D., and Mansfield, J. W. 1998. Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Mol. Microbiol. 29:165-177.
58. Suzuki, T., Park, H., and Lennarz, W. I. 2002. Cytoplasmic peptide:N-glycanase (PNGase) in eukaryotic cells: Occurrence, primary structure, and potential functions. FASEB (Fed. Am. Soc. Exp. Biol.) J. 16:635-641.
59. Warren, R. F., Merritt, P. M., Holub, E., and Innes, R. W. (1999). Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152:401-412.