Wake of the flood: Ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria

Current Opinion in Microbiology

Volumn 7, Issue 1, 2004, Pages 11-18

  Chang, Jeff H ^a   Goel, Ajay K ^a   Grant, Sarah R ^a   Dangl, Jeffery L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE PROTEINASE; HAPTOCORRIN; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PECTATE LYASE; PROTEIN AVRB; PROTEIN AVRBS3; PROTEIN AVRPPHB; PROTEIN AVRPTO; PROTEIN AVRPTOB; PROTEIN AVRRPT2; PROTEIN HOPPTOA1; PROTEIN HOPPTOA2; PROTEIN HOPPTOD2; PROTEIN HOPPTOM; PROTEIN HRPW; PROTEIN SERINE THREONINE KINASE; PROTEIN XOPD; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; BACTERIAL GENOME; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM; CARBOXY TERMINAL SEQUENCE; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; KNOCKOUT GENE; MULTIGENE FAMILY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PHYLOGENY; PLANT CELL; PLANT DISEASE; PLANT MICROORGANISM INTERACTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TOMATO; WILD TYPE; XANTHOMONAS CAMPESTRIS; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EUKARYOTA; LYCOPERSICON ESCULENTUM; XANTHOMONAS CAMPESTRIS; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 1242306495     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2003.12.006     Document Type: Review

References (59)

1. He S.Y., Jin Q. The Hrp pilus: learning from flagella. Curr Opin Microbiol. 6:2003;15-19.
2. Dangl J.L., Jones J.D.G. Plant pathogens and integrated defence responses to infection. Nature. 411:2001;826-833.
3. Martin G.B., Bogdanove A.J., Sessa G. Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol. 54:2003;23-61.
4. Nimchuk Z, Eulgem T, Holt BF, Dangl JL: Recognition and response in the plant immune system. Annu Rev Genet 2003, 37:579-609.
5. Crute IR: The genetic bases of relationships between microbial parasites and their hosts. In Mechanisms of Resistance to Plant Diseases. Edited by Fraser RSS. Dordrecht: Kluwer Academic Press; 1985:80-143.
6. Bonas U., Lahaye T. Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Curr Opin Microbiol. 5:2002;44-50.
7. van der Biezen E.A., Jones J.D.G. Plant disease resistance proteins and the 'gene-for-gene' concept. Trends Biochem Sci. 23:1998;454-456.
8. Glazebrook J., Rogers E.E., Ausubel F.M. Use of Arabidopsis for genetic dissection of plant defense responses. Annu Rev Genet. 31:1997;547-569.
9. Yang Y., De Feyter R., Gabriel D.W. Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves are determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol Plant Microbe Interact. 7:1994;345-355.
10. Guttman D.S., Greenberg J.T. Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol Plant Microbe Interact. 14:2001;145-155.
11. 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. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A. 100:2003;10181-10186.
12. 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. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature. 417:2002;459-463.
13. Salanoubat M., Genin S., Artiguenave F., Gouzy J., Mangenot S., Arlat M., Billault A., Brottier P., Camus J.C., Cattolico L.et al. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature. 415:2002;497-502.
14. Boch J., Joardar V., Gao L., Robertson T.L., Lim M., Kunkel B.N. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol. 44:2002;73-88.
15. Guttman D.S., Vinatzer B.A., Sarkar S., Ranall M.V., Kettler G., Greenberg J.T. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science. 295:2002;1722-1726.
16. Zwiesler-Vollick J., Plovanich-Jones A.E., Nomura K., Bandyopadhyay S., Joardar V., Kunkel B.N., He S.Y. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol. 45:2002;1207-1218.
17. Fouts D.E., Abramovitch R.B., Alfano J.R., Baldo A.M., Buell C.R., Cartinhour S., Chatterjee A.K., D'Ascenzo M., Gwinn M.L., Lazarowitz S.G.et al. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci U S A. 99:2002;2275-2280.
18. Petnicki-Ocwieja T., Schneider D.J., Tam V.C., Chancey S.T., Shan L., Jamir Y., Schechter L.M., Janes M.D., Buell C.R., Tang X.et al. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A. 99:2002;7652-7657.
19. Collmer A., Lindeberg M., Petnicki-Ocwieja T., Schneider D., Alfano J. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:2002;462-469.
20. Greenberg J.T., Vinatzer B.A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol. 6:2003;20-28 This precedes the current review and highlights the different methods used in mining genome sequences for type III effector genes. Also of interest is the comparison of effector suites between Pto DC3000 and Psy B728a.
21. Nimchuk Z., Rohmer L., Chang J.H., Dangl J.L. Knowing the dancer from the dance: R gene products and their interactions with other proteins from host and pathogen. Curr Opin Plant Biol. 4:2001;288-294.
22. Orth K., Xu Z., Mudgett M.B., Bao Z.Q., Palmer L.E., Bliska J.B., Mangel W.F., Staskawicz B., Dixon J.E. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science. 290:2000;1594-1597.
23. Melchior F. SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol. 16:2000;591-626.
24. Noel L., Thieme F., Nennstiel D., Bonas U. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol. 184:2002;1340-1348.
25. Hotson A., Chosed R., Shu H., Orth K., Mudgett M.B. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol. 50:2003;377-389 The authors used a homology-based approach to determine that the Xanthomonas effector XopD, might encode a SUMO-protease. Further characterizations provided evidence for such activity both in vitro and in planta.
26. Shao F., Merritt P.M., Bao Z., Innes R.W., Dixon J.E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell. 109:2002;575-588.
27. Shao F., Golstein C., Ade J., Stoutemyer M., Dixon J.E., Innes R.W. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science. 301:2003;1230-1233 AvrPphB was previously shown to encode a cysteine protease. In this study, the authors demonstrate that AvrPphB acts directly on PBS1. This protein is an Arabidopsis serine/threonine kinase that is required for the resistance response mediated by recognition of AvrPphB by RPS5. This interaction can be re-capitulated in vitro using purified proteins indicating no other host proteins are required. Furthermore, they show that cleavage of PBS1 is required for the HR.
28. •].
29. •], the authors found that the carboxy terminal portion of HopPtoD2 encodes a protein tyrosine phosphatase. Evidence is presented showing that a functional tyrosine phosphatase is required for full virulence and suppression of PR1 gene expression in host plants as well as suppression of the HR and delay of the oxidative burst in non-host tobacco.
30. Hacker J., Blum-Oehler G., Muhldorfer I., Tschape H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol. 23:1997;1089-1097.
31. Hacker J., Kaper J.B. Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol. 54:2000;641-679.
32. Kjemtrup S., Nimchuk Z., Dangl J.L. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr Opin Microbiol. 3:2000;73-78.
33. Charkowski A.O., Alfano J.R., Preston G., Yuan J., He S.Y., Collmer A. The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J Bacteriol. 180:1998;5211-5217.
34. Deng W.L., Rehm A.H., Charkowski A.O., Rojas C.M., Collmer A. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J Bacteriol. 185:2003;2592-2602.
35. Badel J.L., Charkowski A.O., Deng W.L., Collmer A. A gene in the Pseudomonas syringae pv. tomato Hrp pathogenicity island conserved effector locus, hopPtoA1, contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. Mol Plant Microbe Interact. 15:2002;1014-1024.
36. Badel J.L., Nomura K., Bandyopadhyay S., Shimizu R., Collmer A., He S.Y. Pseudomonas syringae pv. tomato DC3000 HopPtoM (CEL ORF3) is important for lesion formation but not growth in tomato and is secreted and translocated by the Hrp type III secretion system in a chaperone-dependent manner. Mol Microbiol. 49:2003;1239-1251.
37. Hauck P., Thilmony R., He S.Y. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A. 100:2003;8577-8582 The authors used transcriptional profiling of the host genes to arrive at a putative function for a type III effector. A larger percentage of genes predicted to encode putatively secreted cell wall and defense proteins were suppressed in transgenic Arabidopsis plants expressing AvrPto. This observation suggested AvrPto suppresses cell-wall based defense and was supported by the lack of the papillary response in these same transgenic plants.
38. Swarup S., De Feyter R., Brlansky R.H., Gabriel D.W. A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit cancer-like lesions on citrus. Phytopathology. 81:1991;802-809.
39. Swarup S., Yang Y., Kingsley M.T., Gabriel D.W. A Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on non-hosts. Mol Plant Microbe Interact. 5:1992;204-213.
40. Yang B., Zhu W., Johnson L.B., White F.F. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci U S A. 97:2000;9807-9812.
41. Marois E., Van den Ackerveken G., Bonas U. The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact. 15:2002;637-646.
42. Bai J., Choi S.-H., Ponciano G., Leung H., Leach J.E. Xanthomonas oryzae pv. oryzae avirulence genes contribute differentially and specifically to pathogen aggressiveness. Mol Plant Pathol. 13:2000;1322-1329.
43. Ritter C., Dangl J.L. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell. 8:1996;251-257.
44. Reuber T.L., Ausubel F.M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell. 8:1996;241-249.
45. Tsiamis G., Mansfield J.W., Hockenhull R., Jackson R.W., Sesma A., Athanassopoulos E., Bennett M.A., Stevens C., Vivian A., Taylor J.D.et al. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19:2000;3204-3214.
46. ••].
47. ••] describe the mechanism by which AvrRpt2 interferes with the RPM1-AvrRpm1-mediated resistance response. Both RPM1 and RPS2, which recognize AvrRpt2, require a common host protein, RIN4. Expression of AvrRpt2 leads to the degradation of RIN4 and the destabilization of RPM1. However, disappearance of RIN4 is required for RPS2 resistance. These observations also led to the hypothesis that AvrRpt2 encodes a cysteine protease.
48. Axtell M.J., Chisholm S.T., Dahlbeck D., Staskawicz B.J. Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol. 49:2003;1537-1546.
49. Jin P., Wood M.D., Wu Y., Xie Z., Katagiri F. Cleavage of the Pseudomonas syringae type III effector AvrRpt2 requires a host factor(s) common among Eukaryotes and is important for AvrRpt2 localization in the host cell. Plant Physiol. 133:2003;1072-1082.
50. Mudgett M., Staskawicz B. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol Microbiol. 32:1999;927-941.
51. Viboud G.I., So S.S., Ryndak M.B., Bliska J.B. Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol Microbiol. 47:2003;1305-1315 YopB is a component of the type III secretion system of Yersinia pseudotuberculosis that triggers the release of interleukin-8, a marker for the proinflammatory response, from infected HeLa cells. These authors demonstrate that any of three Yop effectors, YopE, YopH or YopJ is sufficient to block the YopB-dependent production of IL-8.
52. Abramovitch R.B., Kim Y.J., Chen S., Dickman M.B., Martin G.B. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22:2003;60-69.
53. Venisse J.S., Barny M.A., Paulin J.P., Brisset M.N. Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS Lett. 537:2003;198-202.
54. Shan L., Thara V.K., Martin G.B., Zhou J.M., Tang X. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell. 12:2000;2323-2338.
55. Chang J.H., Rathjen J.P., Bernal A.J., Staskawicz B.J., Michelmore R.W. avrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking either Pto or Prf. Mol Plant Microbe Interact. 13:2000;568-571.
56. Chen Z., Kloek A.P., Boch J., Katagiri F., Kunkel B.N. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol Plant Microbe Interact. 13:2000;1312-1321.
57. Nimchuk Z., Marois E., Kjemtrup S., Leister R.T., Katagiri F., Dangl J.L. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell. 101:2000;353-363.
58. Jin Q., Thilmony R., Zwiesler-Vollick J., He S.Y. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5:2003;301-310.
59. Lee CC, Wood MD, Ng K, Andersen C, Liu Y, Luginbühl P, Spraggon G, Katagiri F: Crystal Structure of the Type III effector AvrB from Pseudomonas syringae. Structure, 12:in press.