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PMID: 17827286 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells.

Journal of bacteriology ·Vol. 189 ·No. 22 ·2007-11-00 ·Pages 8277-89

Oh HS, Kvitko BH, Morello JE, Collmer A

Abstract

Pseudomonas syringae translocates virulence effector proteins into plant cells via a type III secretion system (T3SS) encoded by hrp (for hypersensitive response and pathogenicity) genes. Three genes coregulated with the Hrp T3SS system in P. syringae pv. tomato DC3000 have predicted lytic transglycosylase domains: PSPTO1378 (here designated hrpH), PSPTO2678 (hopP1), and PSPTO852 (hopAJ1). hrpH is located between hrpR and avrE1 in the Hrp pathogenicity island and is carried in the functional cluster of P. syringae pv. syringae 61 hrp genes cloned in cosmid pHIR11. Strong expression of DC3000 hrpH in Escherichia coli inhibits bacterial growth unless the predicted catalytic glutamate at position 148 is mutated. Translocation tests involving C-terminal fusions with a Cya (Bordetella pertussis adenylate cyclase) reporter indicate that HrpH and HopP1, but not HopAJ1, are T3SS substrates. Pseudomonas fluorescens carrying a pHIR11 derivative lacking hrpH is poorly able to translocate effector HopA1, and this deficiency can be restored by HopP1 and HopAJ1, but not by HrpH(E148A) or HrpH(1-241). DC3000 mutants lacking hrpH or hrpH, hopP1, and hopAJ1 combined are variously reduced in effector translocation, elicitation of the hypersensitive response, and virulence. However, the mutants are not reduced in secretion of T3SS substrates in culture. When produced in wild-type DC3000, the HrpH(E148A) and HrpH(1-241) variants have a dominant-negative effect on the ability of DC3000 to elicit the hypersensitive response in nonhost tobacco and to grow and cause disease in host tomato. The three Hrp-associated lytic transglycosylases in DC3000 appear to have overlapping functions in contributing to T3SS functions during infection.

MeSH Terms
Amino Acid Sequence Bacterial Outer Membrane Proteins/chemistry,genetics,metabolism Bacterial Proteins/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Gene Expression Regulation, Bacterial Lycopersicon esculentum/cytology,microbiology Molecular Sequence Data Mutation Plant Leaves/microbiology Protein Transport Pseudomonas syringae/enzymology,genetics Sigma Factor/genetics,metabolism Tobacco/metabolism,microbiology Transferases/genetics,metabolism
Chemicals
Bacterial Outer Membrane Proteins Bacterial Proteins DNA-Binding Proteins HrpL protein, Pseudomonas syringae Sigma Factor hrpH protein, Pseudomonas syringae Transferases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Oh Hye-Sook
Department of Plant Pathology, Cornell University, Ithaca, NY 14853, USA.
Kvitko Brian H
Morello Joanne E
Collmer Alan
References (55)
55 references, click to expand
  1. Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12839-43 PMID: 10536009
  2. 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. 2007 Nov;189(22):8059-72 PMID: 17873033
  3. The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato.
    Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2247-52 PMID: 10681465
  4. Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae.
    J Bacteriol. 2000 Apr;182(7):1844-53 PMID: 10714988
  5. 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 U S A. 2000 Apr 25;97(9):4856-61 PMID: 10781092
  6. The N- and C-terminal portions of the Agrobacterium VirB1 protein independently enhance tumorigenesis.
    J Bacteriol. 2000 Jun;182(12):3437-45 PMID: 10852875
  7. Identification of four families of peptidoglycan lytic transglycosylases.
    J Mol Evol. 2001 Jan;52(1):78-84 PMID: 11139297
  8. Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex.
    J Bacteriol. 2001 Feb;183(4):1159-67 PMID: 11157927
  9. N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis.
    Plant Physiol. 2001 Apr;125(4):1880-90 PMID: 11299367
  10. Functional and mutational analysis of p19, a DNA transfer protein with muramidase activity.
    J Bacteriol. 2001 May;183(10):3176-83 PMID: 11325947
  11. Proteins involved in the production and perception of oligosaccharides in relation to plant and animal development.
    Curr Opin Struct Biol. 2001 Oct;11(5):608-16 PMID: 11785763
  12. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island.
    J Bacteriol. 2002 Mar;184(5):1340-8 PMID: 11844763
  13. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae.
    Science. 2002 Mar 1;295(5560):1722-6 PMID: 11872842
  14. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana.
    Mol Microbiol. 2002 Apr;44(1):73-88 PMID: 11967070
  15. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco.
    J Biol Chem. 2003 Feb 21;278(8):6201-8 PMID: 12471032
  16. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan.
    Science. 2003 Jun 6;300(5625):1584-7 PMID: 12791997
  17. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000.
    Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10181-6 PMID: 12928499
  18. Lytic transglycosylases in macromolecular transport systems of Gram-negative bacteria.
    Cell Mol Life Sci. 2003 Nov;60(11):2371-88 PMID: 14625683
  19. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter.
    J Bacteriol. 2004 Jan;186(2):543-55 PMID: 14702323
  20. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast.
    Plant J. 2004 Feb;37(4):554-65 PMID: 14756767
  21. VirB1 orthologs from Brucella suis and pKM101 complement defects of the lytic transglycosylase required for efficient type IV secretion from Agrobacterium tumefaciens.
    J Bacteriol. 2004 Mar;186(5):1415-22 PMID: 14973016
  22. Dissecting virulence: systematic and functional analyses of a pathogenicity island.
    Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3597-602 PMID: 14988506
  23. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen.
    Appl Environ Microbiol. 2004 Apr;70(4):1999-2012 PMID: 15066790
  24. Improved prediction of signal peptides: SignalP 3.0.
    J Mol Biol. 2004 Jul 16;340(4):783-95 PMID: 15223320
  25. Type III secretion system effector proteins: double agents in bacterial disease and plant defense.
    Annu Rev Phytopathol. 2004;42:385-414 PMID: 15283671
  26. Size distribution of DNA replicative intermediates in bacteriophage P4 and in Escherichia coli.
    J Mol Biol. 1979 Mar 15;128(4):501-25 PMID: 374741
  27. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648-52 PMID: 377280
  28. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347-51 PMID: 7012838
  29. Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants.
    J Bacteriol. 1988 Oct;170(10):4748-56 PMID: 3139635
  30. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension.
    Gene. 1989 Apr 15;77(1):61-8 PMID: 2744488
  31. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity.
    Science. 1989 Sep 22;245(4924):1374-7 PMID: 2781284
  32. The Pseudomonas syringae pv. syringae 61 hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants.
    J Bacteriol. 1992 Nov;174(21):6878-85 PMID: 1400238
  33. Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus.
    Infect Immun. 1993 May;61(5):1707-14 PMID: 8478058
  34. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria.
    Mol Microbiol. 1996 May;20(3):681-3 PMID: 8736546
  35. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations.
    Mol Microbiol. 1996 Feb;19(4):715-28 PMID: 8820642
  36. Peptidoglycan as a barrier to transenvelope transport.
    J Bacteriol. 1996 Oct;178(19):5555-62 PMID: 8824596
  37. VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1.
    J Bacteriol. 1997 Feb;179(4):1203-10 PMID: 9023203
  38. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells.
    Mol Plant Microbe Interact. 1997 Jul;10(5):580-8 PMID: 9204563
  39. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6456-61 PMID: 10339609
  40. Two simple media for the demonstration of pyocyanin and fluorescin.
    J Lab Clin Med. 1954 Aug;44(2):301-7 PMID: 13184240
  41. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae.
    Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2549-54 PMID: 15701698
  42. Suppression of host defense in compatible plant-Pseudomonas syringae interactions.
    Curr Opin Plant Biol. 2005 Aug;8(4):361-8 PMID: 15936244
  43. Bioinformatics correctly identifies many type III secretion substrates in the plant pathogen Pseudomonas syringae and the biocontrol isolate P. fluorescens SBW25.
    Mol Plant Microbe Interact. 2005 Aug;18(8):877-88 PMID: 16134900
  44. Genome-wide analysis of gene expression in Ralstonia solanacearum reveals that the hrpB gene acts as a regulatory switch controlling multiple virulence pathways.
    Mol Plant Microbe Interact. 2005 Sep;18(9):938-49 PMID: 16167764
  45. Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems.
    Microbiology. 2005 Nov;151(Pt 11):3455-67 PMID: 16272370
  46. Identification of Erwinia amylovora genes induced during infection of immature pear tissue.
    J Bacteriol. 2005 Dec;187(23):8088-103 PMID: 16291682
  47. Intracellular pattern recognition receptors in the host response.
    Nature. 2006 Jul 6;442(7098):39-44 PMID: 16823444
  48. Bacterial elicitation and evasion of plant innate immunity.
    Nat Rev Mol Cell Biol. 2006 Aug;7(8):601-11 PMID: 16936700
  49. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria.
    Annu Rev Microbiol. 2006;60:425-49 PMID: 16753033
  50. The type III secretion injectisome.
    Nat Rev Microbiol. 2006 Nov;4(11):811-25 PMID: 17041629
  51. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains.
    Mol Plant Microbe Interact. 2006 Nov;19(11):1151-8 PMID: 17073298
  52. Whole-genome expression profiling defines the HrpL regulon of Pseudomonas syringae pv. tomato DC3000, allows de novo reconstruction of the Hrp cis clement, and identifies novel coregulated genes.
    Mol Plant Microbe Interact. 2006 Nov;19(11):1167-79 PMID: 17073300
  53. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana.
    Plant J. 2007 Jul;51(1):32-46 PMID: 17559511
  54. Identification of Pseudomonas syringae pv. syringae 61 type III secretion system Hrp proteins that can travel the type III pathway and contribute to the translocation of effector proteins into plant cells.
    J Bacteriol. 2007 Aug;189(15):5773-8 PMID: 17526708
  55. Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster.
    J Mol Evol. 1999 Nov;49(5):627-44 PMID: 10552044
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
1098-5530
Published
2007-11-00
Epub
2007-00-07
Pages
8277-89
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC2168667
Subset
IM
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