Genetic analysis of the individual contribution to virulence of the type III effector inventory of Pseudomonas syringae pv. phaseolicola

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Macho, Alberto P ^a,b   Zumaquero, Adela ^a   Gonzalez Plaza, Juan J ^a   Ortiz Martín, Inmaculada ^a   Rufián, José S ^a   Beuzón, Carmen R ^a  

^a INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

^b SAINSBURY LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN AVRB2; PROTEIN HOPAB1; PROTEIN HOPAS1; PROTEIN HOPAU1; PROTEIN HOPI1; PROTEIN HOPR1; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

APOPLAST; ARTICLE; BACTERIAL GROWTH; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CANCELLED OUT INDEX; COMPETITIVE INDEX; CONTROLLED STUDY; DISEASE COURSE; GENETIC ANALYSIS; GENETIC COMPLEMENTATION; GENETIC EPISTASIS; MICROBIAL ATTENUATION; MICROBIAL POPULATION DYNAMICS; MICROBIOLOGICAL PARAMETERS; MOLECULAR DYNAMICS; NATURAL HOST; NONHUMAN; PHASEOLUS VULGARIS; PHENOTYPE; PLANT LEAF; PLANT MICROORGANISM INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS SYRINGAE; TYPE III SECRETION SYSTEM; FABACEAE; GENE EXPRESSION REGULATION; GENETICS; MICROBIOLOGY; MUTATION; PATHOGENICITY; PLANT DISEASE; TOBACCO; TOMATO; VIRULENCE;

LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. PHASEOLICOLA; PSEUDOMONAS SYRINGAE PV. TOMATO;

BACTERIAL PROTEINS; FABACEAE; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; LYCOPERSICON ESCULENTUM; MUTATION; PLANT DISEASES; PSEUDOMONAS SYRINGAE; TOBACCO; VIRULENCE; VIRULENCE FACTORS;

EID: 84860465535     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035871     Document Type: Article

References (60)

1. Alfano JR, Collmer A, (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179: 5655-5662.
2. Alfano JR, Collmer A, (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42: 385-414.
3. He P, Shan L, Lin NC, Martin GB, Kemmerling B, et al. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563-575.
4. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, et al. (2007) A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17: 499-508.
5. Lim MT, Kunkel BN, (2005) The Pseudomonas syringae avrRpt2 gene contributes to virulence on tomato. Mol Plant Microbe Interact 18: 626-633.
6. Losada L, Sussan T, Pak K, Zeyad S, Rozenbaum I, et al. (2004) Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulence functions by a HrpL-dependent promoter-trap assay. Mol Plant Microbe Interact 17: 254-262.
7. Ritter C, Dangl JL, (1995) The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol Plant Microbe Interact 8: 444-453.
8. Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T, et al. (2000) The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci 97: 4856-4861.
9. Badel JL, Oh HS, Collmer A, (2006) A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol Plant Microbe Interact pp. 99-111.
10. Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB, et al. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5: e1000388.
11. Guo M, Tian F, Wamboldt Y, Alfano JR, (2009) The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol Plant Microbe Interact 22: 1069-1080.
12. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, et al. (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18: 74-80.
13. Shan L, He P, Li J, Heese A, Peck SC, et al. (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4: 17-27.
14. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, et al. (2011) Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108: 2975-2980.
15. Macho AP, Zumaquero A, Ortiz-Martín I, Beuzón CR, (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.
16. Macho AP, Guidot A, Barberis P, Beuzón CR, Genin S, (2010) A competitive index assay identifies several Ralstonia solanacearum type III effector mutant strains with reduced fitness in host plants. Mol Plant Microbe Interact 23: 1197-1205.
17. Zumaquero A, Macho AP, Rufián JS, Beuzón CR, (2010) Analysis of the role of the type III effector inventory of Pseudomonas syringae pv. phaseolicola 1448a in interaction with the plant. J Bacteriol 192: 4474-4488.
18. Beuzón CR, Holden DW, (2001) Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3: 1345-1352.
19. Ortiz-Martín I, Thwaites R, Macho AP, Mansfield JW, Beuzón CR, (2010) Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 23: 665-681.
20. Ortiz-Martín I, Thwaites R, Mansfield JW, Beuzón CR, (2010) Negative regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 23: 682-701.
21. Macho AP, Guevara CM, Tornero P, Ruiz-Albert J, Beuzón CR, (2010) The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity. New Phytol 187: 1018-1033.
22. Macho AP, Beuzón CR, (2010) Insights into plant immunity signalling: the bacterial competitive index angle. Plant Signal Behav 5: 1590-1593.
23. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, et al. (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.
24. Keith LW, Boyd C, Keen NT, Partridge JE, (1997) Comparison of avrD alleles from Pseudomonas syringae pv. glycinea. Mol Plant Microbe Interact 10: 416-422.
25. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, et al. (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci 102: 2549-2554.
26. Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S, et al. (2006) Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol Plant-Microbe Interact 19: 1193-1206.
27. Oh HS, Kvitko BH, Morello JE, Collmer A, (2007) Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells. J Bacteriol 189: 8277-8289.
28. Kvitko BH, Ramos AR, Morello JE, Oh HS, Collmer A, (2007) Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. J Bacteriol 189: 8059-8072.
29. Macho AP, Ruiz-Albert J, Tornero P, Beuzón CR, (2009) Identification of new type III effectors and analysis of the plant response by competitive index. Mol Plant Pathol 10: 69-80.
30. Melotto M, Underwood W, He SY, (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46: 101-122.
31. Ortiz-Martín I, Macho AP, Lambersten L, Ramos C, Beuzón CR, (2006) Suicide vectors for antibiotic marker exchange and rapid generation of multiple knockout mutants by allelic exchange in Gram-negative bacteria. Journal of Microbiological Methods 67: 395-407.
32. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci 99: 2275-2280.
33. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW, (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176: 1025-1036.
34. Xiao Y, Hutcheson SW, (1994) A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J Bacteriol 176: 3089-3091.
35. Melotto M, Underwood W, Koczan J, Nomura K, He SY, (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
36. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.
37. Gohre V, Robatzek S, (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46: 189-215.
38. Jackson RW, Mansfield JW, Ammouneh H, Dutton LC, Wharton B, et al. (2002) Location and activity of members of a family of virPphA homologues in pathovars of Pseudomonas syringae and P. savastanoi. Molecular Plant Pathology 3: 205-216.
39. Jelenska J, van Hal JA, Greenberg JT, (2010) Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc Natl Acad Sci U S A 107: 13177-13182.
40. DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY, (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci 101: 9927-9932.
41. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, et al. (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. Proc Natl Acad Sci 96: 10875-10880.
42. Shea JE, Beuzón CR, Gleeson C, Mundy R, Holden DW, (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 67: 213-219.
43. Beuzón CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
44. Beuzón CR, Unsworth KE, Holden DW, (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. Infect Immun 69: 7254-7261.
45. Ruiz-Albert J, Yu XJ, Beuzón CR, Blakey AN, Galyov EE, et al. (2002) Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44: 645-661.
46. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, et al. (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7: e1002132.
47. de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, et al. (2006) Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant J 47: 368-382.
48. Bogdanove AJ, Kim JF, Wei Z, Kolchinsky P, Charkowski AO, et al. (1998) Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc Natl Acad Sci 95: 1325-1330.
49. Brooks DM, Hernandez-Guzman G, Kloek AP, Alarcón-Chaidez F, Sreedharan A, et al. (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.
50. Gaudriault S, Malandrin L, Paulin JP, Barny MA, (1997) DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol 26: 1057-1069.
51. Qian W, Jia Y, Ren SX, He YQ, Feng JX, et al. (2005) Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 15: 757-767.
52. Eitas TK, Nimchuk ZL, Dangl JL, (2008) Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. Proc Natl Acad Sci U S A 105: 6475-6480.
53. Shang Y, Li X, Cui H, He P, Thilmony R, et al. (2006) RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB. Proc Natl Acad Sci U S A 103: 19200-19205.
54. Ashfield T, Keen NT, Buzzell RI, Innes RW, (1995) Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141: 1597-1604.
55. 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.
56. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, et al. (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448: 370-374.
57. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
58. Freter R, Allweiss B, O'Brien PC, Halstead SA, Macsai MS, (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vitro studies. Infect Immun 34: 241-249.
59. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ, (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci 84: 2833-2837.
60. Teverson DM, (1991) Genetics of pathogenicity and resistance in the halo-blight disease of beans in Africa. PhD Thesis Birmingham, United Kingdom University of Birmingham.