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PubMed2002

RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis.

In Arabidopsis, RPM1 confers resistance against Pseudomonas syringae expressing either of two sequence unrelated type III effectors, AvrRpm1 or AvrB. An RPM1-interacting protein (RIN4) coimmunoprecipitates from plant cell extracts with AvrB, AvrRpm1, or RPM1. Reduction of RIN4 protein levels inhibits both the hypersensitive response and the restriction of pathogen growth controlled by RPM1. RIN4 reduction causes diminution of RPM1. RIN4 reduction results in heightened resistance to virulent Peronospora parasitica and P. syringae, and ectopic defense gene expression. Thus, RIN4 positively regulates RPM1-mediated resistance yet is, formally, a negative regulator of basal defense responses. AvrRpm1 and AvrB induce RIN4 phosphorylation. This may enhance RIN4 activity as a negative regulator of plant defense, facilitating pathogen growth. RPM1 may "guard" against pathogens that use AvrRpm1 and AvrB to manipulate RIN4 activity.

Amino Acid Sequence↗

PubMed2001

Interaction of a mulberry leaf lectin with a phytopathogenic bacterium, P. syringae pv mori.

Two N-glycolylneuraminic acid-specific lectins, MLL 1 and 2, from leaves of Morus alba were studied for their anti-bacterial activity against P. syringae pv mori, which was a specific pathogenic bacterium of the mulberry leaf. MLL 1 but not MLL 2 was found to induce the agglutination of P. syringae pv mori. The MLL 1 can induce the agglutination only at the exponential phase of the bacterial growth in a liquid medium and the agglutination was specifically inhibited by N-glycolylneuraminic acid, N-acetylgalactosamine at 12.5 mM and bovine submaxillary mucin at 0.05 &mgr;g/ml.

Journal Article↗

PubMed2002

Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors.

Many bacterial pathogens of plants and animals use a type III secretion system (TTSS) to deliver virulence effector proteins into host cells. Because effectors are heterogeneous in sequence and function, there has not been a systematic way to identify the genes encoding them in pathogen genomes, and our current inventories are probably incomplete. A pre-closure draft sequence of Pseudomonas syringae pv. tomato DC3000, a pathogen of tomato and Arabidopsis, has recently supported five complementary studies which, collectively, identify 36 TTSS-secreted proteins and many more candidate effectors in this strain. These studies demonstrate the advantages of combining experimental and computational approaches, and they yield new insights into TTSS effectors and virulence regulation in P. syringae, potential effector targeting signals in all TTSS-dependent pathogens, and strategies for finding TTSS effectors in other bacteria that have sequenced genomes.

Arabidopsis↗

PubMed2003

Electroporation and stable maintenance of plasmid DNAs in a biocontrol strain of Pseudomonas syringae.

Transformation efficiencies as high as 10(7) transformants microg(-1) DNA have been previously reported for pseudomonads using electroporation protocols established for E. coli with plasmid DNAs prepared from methylation proficient E. coli hosts. We report here a protocol for electroporation of plasmid DNAs into a biocontrol strain of Pseudomonas syringae which could not be electroporated by standard E. coli methods. Transformation efficiencies of 10(7) or higher were obtained with DNA recovered from initial P. syringae transformation or with DNA prepared from methylation deficient E. coli. Both plasmids used in this study were stably maintained in the absence of selection for at least 50 generations.

Ampicillin↗

PubMed1992

Expression of a bacterial phaseolotoxin-resistant ornithyl transcarbamylase in transgenic tobacco confers resistance to Pseudomonas syringae pv. phaseolicola.

Toxins have been shown to be an important virulence component for most pathovars of Pseudomonas syringae. Here we have examined the role of phaseolotoxin in the virulence mechanism of P. syringae pv. phaseolicola by producing transgenic tobacco plants that express a pathogen-derived toxin-resistant target enzyme. Such plants are insensitive to the toxin and less prone to infection by the pathogen.

Drug Resistance↗

PubMed2000

Colonization strategies and conjugal gene transfer of inoculated Pseudomonas syringae on the leaf surface.

Survival, colonization and activity of Pseudomonas syringae bacteria inoculated onto the leaf surface of the common bean (Phaseolus vulgaris) was studied. Inoculated Ps. syringae cells shortened by half their size in 100% humidity and by an average of one fifth in 40-60% humidity. The respiring portion of the population, measured by the formation of 5-cyano-2,3-ditolyl tetrazolium chloride (CTC)-formazan crystals, decreased more in 40-60% humidity than in 100% humidity. In scanning electron micrographs, the bacterial cells on leaf surfaces were seen embedded in a mucoid matrix. Intraspecies conjugation of plasmid RP1 also occurred in 40-60% humidity conditions. The portion of transconjugants temporally rose higher than the same portion in 100% humidity conditions. Therefore, although only a small proportion of the inoculated cells remained active on the leaf surface in 40-60% humidity, a relatively high rate of conjugation was still seen. Gene spreading was thus efficient on the leaf surface also when conditions did not allow bacterial population growth.

Biofilms↗

PubMed2002

Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana.

Phytopathogenic bacteria possess a large number of genes that allow them to grow and cause disease on plants. Many of these genes should be induced when the bacteria come in contact with plant tissue. We used a modified in vivo expression technology (IVET) approach to identify genes from the plant pathogen Pseudomonas syringae pv. tomato that are induced upon infection of Arabidopsis thaliana and isolated over 500 in planta-expressed (ipx) promoter fusions. Sequence analysis of 79 fusions revealed several known and potential virulence genes, including hrp/hrc, avr and coronatine biosynthetic genes. In addition, we identified metabolic genes presumably important for adaptation to growth in plant tissue, as well as several genes with unknown function that may encode novel virulence factors. Many ipx fusions, including several corresponding to novel genes, are dependent on HrpL, an alternative RNA polymerase sigma factor that regulates the expression of virulence genes. Expression analysis indicated that several ipx fusions are strongly induced upon inoculation into plant tissue. Disruption of one ipx gene, conserved effector locus (CEL) orf1, encoding a putative lytic murein transglycosylase, resulted in decreased virulence of P. syringae. Our results demonstrate that this screen can be used successfully to isolate genes that are induced in planta, including many novel genes potentially involved in pathogenesis.

Arabidopsis↗

PubMed2002

Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome.

Pseudomonas syringae pv. tomato (Pst) strain DC3000 infects the model plants Arabidopsis thaliana and tomato, causing disease symptoms characterized by necrotic lesions surrounded by chlorosis. One mechanism used by Pst DC3000 to infect host plants is the type III protein secretion system, which is thought to deliver multiple effector proteins to the plant cell. The exact number of type III effectors in Pst DC3000 or any other plant pathogenic bacterium is not known. All known type III effector genes of P. syringae are regulated by HrpS, an NtrC family protein, and the HrpL alternative sigma factor, which presumably binds to a conserved cis element (called the "hrp box") in the promoters of type III secretion-associated genes. In this study, we designed a search motif based on the promoter sequences conserved in 12 published hrp operons and putative effector genes in Pst DC3000. Seventy-three predicted genes were retrieved from the January 2001 release of the Pst DC3000 genome sequence, which had 95% genome coverage. The expression of the 73 genes was analysed by microarray and Northern blotting, revealing 24 genes/operons (including eight novel genes), the expression of which was consistently higher in hrp-inducing minimal medium than in nutrient-rich Luria-Bertani broth. Expression of all eight genes was dependent on the hrpS gene. Most were also dependent on the hrpL gene, but at least one was dependent on the hrpS gene, but not on the hrpL gene. An AvrRpt2-based type III translocation assay provides evidence that some of the hrpS-regulated novel genes encode putative effector proteins.

Arabidopsis↗

PubMed2003

The lower cell density of leaf parenchyma in the Arabidopsis thaliana mutant lcd1-1 is associated with increased sensitivity to ozone and virulent Pseudomonas syringae.

Under optimal growth conditions (120 micro mol photons m-2 sec-1 photosynthetically active radiation (PAR), 16-h photoperiod), the recessive ozone-sensitive Arabidopsis thaliana L. Heynh. mutant lcd1-1 exhibits a pale phenotype compared to the wild type. Confocal and multiphoton microscopy revealed that the paleness of lcd1-1 is because of a lower cell density in the leaf palisade parenchyma, resulting in decreased chlorophyll content. When exposed to ozone, lcd1-1 leaves become paler and contain an increased amount of the lipid peroxidation product malondialdehyde compared to the wild type, suggesting that lcd1-1 suffers from elevated levels of reactive oxygen species (ROS) generated in the apoplast. Infection of leaves with virulent Pseudomonas syringae reveals higher bacterial growth as well as lower pathogenesis-related protein 1 (PR-1) and PR-5 expression in lcd1-1 than in the wild type. When the wild type and lcd1-1 are exposed to short-term high-light stress, leaves do not bleach in lcd1-1 and potential activities of photosystems I (PSI) and II (PSII) decrease to a similar extent in both the genotypes, indicating that the photosynthetic apparatus is not affected by lcd1-1 mutation. The LCD1 gene, found to contain a nonsense mutation in the mutant, has been identified. It is located at the bottom of chromosome 2 of the Arabidopsis genome. However, the function of the protein encoded by LCD1 is not yet known. We hypothesize that LCD1 plays a role in normal leaf development, and that the increased sensitivity to ozone and virulent P. syringae is a secondary effect that presumably results from the lower-cell-density phenotype in lcd1-1.

Adaptation, Physiological↗

PubMed2002

Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000.

The ability of Pseudomonas syringae pv. tomato DC3000 to be pathogenic on plants depends on the Hrp (hypersensitive response and pathogenicity) type III protein secretion system and the effector proteins it translocates into plant cells. Through iterative application of experimental and computational techniques, the DC3000 effector inventory has been substantially enlarged. Five homologs of known avirulence (Avr) proteins and five effector candidates, encoded by genes with putative Hrp promoters and signatures of horizontal acquisition, were demonstrated to be secreted in culture and/or translocated into Arabidopsis in a Hrp-dependent manner. These 10 Hrp-dependent outer proteins (Hops) were designated HopPtoC (AvrPpiC2 homolog), HopPtoD1 and HopPtoD2 (AvrPphD homologs), HopPtoK (AvrRps4 homolog), HopPtoJ (AvrXv3 homolog), HopPtoE, HopPtoG, HopPtoH, HopPtoI, and HopPtoS1 (an ADP-ribosyltransferase homolog). Analysis of the enlarged collection of proteins traveling the Hrp pathway in P. syringae revealed an export-associated pattern of equivalent solvent-exposed amino acids in the N-terminal five positions, a lack of Asp or Glu residues in the first 12 positions, and amphipathicity in the first 50 positions. These characteristics were used to search the unfinished DC3000 genome, yielding 32 additional candidate effector genes that predicted proteins with Hrp export signals and that also possessed signatures of horizontal acquisition. Among these were genes encoding additional ADP-ribosyltransferases, a homolog of SrfC (a candidate effector in Salmonella enterica), a catalase, and a glucokinase. One ADP-ribosyltransferase and the SrfC homolog were tested and shown to be secreted in a Hrp-dependent manner. These proteins, designated HopPtoS2 and HopPtoL, respectively, bring the DC3000 Hrp-secreted protein inventory to 22.

Amino Acid Sequence↗

PubMed1997

Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000.

Hypersensitive response and pathogenicity (hrp) genes control the ability of major groups of plant pathogenic bacteria to elicit the hypersensitive response (HR) in resistant plants and to cause disease in susceptible plants. A number of Hrp proteins share significant similarities with components of the type III secretion apparatus and flagellar assembly apparatus in animal pathogenic bacteria. Here we report that Pseudomonas syringae pv. tomato strain DC3000 (race 0) produces a filamentous surface appendage (Hrp pilus) of 6-8 nm in diameter in a solid minimal medium that induces hrp genes. Formation of the Hrp pilus is dependent on at least two hrp genes, hrpS and hrpH (recently renamed hrcC), which are involved in gene regulation and protein secretion, respectively. Our finding of the Hrp pilus, together with recent reports of Salmonella typhimurium surface appendages that are involved in bacterial invasion into the animal cell and of the Agrobacterium tumefaciens virB-dependent pilus that is involved in the transfer of T-DNA into plant cells, suggests that surface appendage formation is a common feature of animal and plant pathogenic bacteria in the infection of eukaryotic cells. Furthermore, we have identified HrpA as a major structural protein of the Hrp pilus. Finally, we show that a nonpolar hrpA mutant of P. syringae pv. tomato DC3000 is unable to form the Hrp pilus or to cause either an HR or disease in plants.

Bacterial Proteins↗

PubMed1998

Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato.

The "disease-specific" (dsp) region next to the hrp gene cluster of Erwinia amylovora is required for pathogenicity but not for elicitation of the hypersensitive reaction. A 6.6-kb apparent operon, dspEF, was found responsible for this phenotype. The operon contains genes dspE and dspF and is positively regulated by hrpL. A BLAST search revealed similarity in the dspE gene to a partial sequence of the avrE locus of Pseudomonas syringae pathovar tomato. The entire avrE locus was sequenced. Homologs of dspE and dspF were found in juxtaposed operons and were designated avrE and avrF. Introduced on a plasmid, the dspEF locus rendered P. syringae pv. glycinea race 4 avirulent on soybean. An E. amylovora dspE mutant, however, elicited a hypersensitive reaction in soybean. The avrE locus in trans restored pathogenicity to dspE strains of E. amylovora, although restored strains were low in virulence. DspE and AvrE are large (198 kDa and 195 kDa) and hydrophilic. DspF and AvrF are small (16 kDa and 14 kDa) and acidic with predicted amphipathic alpha helices in their C termini; they resemble chaperones for virulence factors secreted by type III secretion systems of animal pathogens.

DNA Transposable Elements↗

PubMed1999

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.

The 154-kb plasmid was cured from race 7 strain 1449B of the phytopathogen Pseudomonas syringae pv. phaseolicola (Pph). Cured strains lost virulence toward bean, causing the hypersensitive reaction in previously susceptible cultivars. Restoration of virulence was achieved by complementation with cosmid clones spanning a 30-kb region of the plasmid that contained previously identified avirulence (avr) genes avrD, avrPphC, and avrPphF. Single transposon insertions at multiple sites (including one located in avrPphF) abolished restoration of virulence by genomic clones. Sequencing 11 kb of the complementing region identified three potential virulence (vir) genes that were predicted to encode hydrophilic proteins and shared the hrp-box promoter motif indicating regulation by HrpL. One gene achieved partial restoration of virulence when cloned on its own and therefore was designated virPphA as the first (A) gene from Pph to be identified for virulence function. In soybean, virPphA acted as an avr gene controlling expression of a rapid cultivar-specific hypersensitive reaction. Sequencing also revealed the presence of homologs of the insertion sequence IS100 from Yersinia and transposase Tn501 from P. aeruginosa. The proximity of several avr and vir genes together with mobile elements, as well as G+C content significantly lower than that expected for P. syringae, indicates that we have located a plasmid-borne pathogenicity island equivalent to those found in mammalian pathogens.

Bacterial Proteins↗

PubMed2001

Accumulation of soluble and wall-bound indolic metabolites in Arabidopsis thaliana leaves infected with virulent or avirulent Pseudomonas syringae pathovar tomato strains.

The chemical structures and accumulation kinetics of several major soluble as well as wall-bound, alkali-hydrolyzable compounds induced upon infection of Arabidopsis thaliana leaves with Pseudomonas syringae pathovar tomato were established. All identified accumulating products were structurally related to tryptophan. Most prominent among the soluble substances were tryptophan, beta-d-glucopyranosyl indole-3-carboxylic acid, 6-hydroxyindole-3-carboxylic acid 6-O-beta-d-glucopyranoside, and the indolic phytoalexin camalexin. The single major accumulating wall component detectable under these conditions was indole-3-carboxylic acid. All of these compounds increased more rapidly, and camalexin as well as indole-3-carboxylic acid reached much higher levels, in the incompatible than in the compatible P. syringae/A. thaliana interaction. The only three prominent phenylpropanoid derivatives present in the soluble extract behaved differently. Two kaempferol glycosides remained largely unaffected, and sinapoyl malate decreased strongly upon bacterial infection with a time course inversely correlated with that of the accumulating tryptophan-related products. The accumulation patterns of both soluble and wall-bound compounds, as well as the disease resistance phenotypes, were essentially the same for infected wild-type and tt4 (no kaempferol glycosides) or fah1 (no sinapoyl malate) mutant plants. Largely different product combinations accumulated in wounded or senescing A. thaliana leaves. It seems unlikely that any one of the infection-induced compounds identified so far has a decisive role in the resistance response to P. syringae.

Arabidopsis↗

PubMed1995

Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus.

RPG1 and RPM1 are disease resistance genes in soybean and Arabidopsis, respectively, that confer resistance to Pseudomonas syringae strains expressing the avirulence gene avrB. RPM1 has recently been demonstrated to have a second specificity, also conferring resistance to P. syringae strains expressing avrRpm1. Here we show that alleles, or closely linked genes, exist at the RPG1 locus in soybean that are specific for either avrB or avrRpm1 and thus can distinguish between these two avirulence genes.

Alleles↗

PubMedDate not supplied

Localization of ice nucleation activity and the iceC gene product in Pseudomonas syringae and Escherichia coli.

Ice nucleation activity and the iceC gene product were quantified in different subcellular fractions of the Pseudomonas syringae source strain and in Escherichia coli containing the cloned iceC gene to determine the activity of this protein in different subcellular locations. Ice nuclei were nearly completely retained during isolation of cell envelopes but exhibited a decrease in the temperature at which they were expressed. Ice nucleation activity was found in Triton X-100 insoluble membrane fragments as well as in slowly sedimenting and high-density membrane fragments. Nearly all ice nucleation activity was associated with the outer membrane because the partitioning of 3-ketodeoxyoctonate (a lipopolysaccharide component) and ice nuclei in cell fractions were similar to and opposite that of NADH oxidase (a cytoplasmic membrane component). The iceC gene product had an apparent mass of 150,000 Da based on migration in SDS-polyacrylamide gels. This protein was not found in soluble cell components. Nearly all of the iceC gene product, which occurred in low abundance, was associated with the outer membrane of both P. syringae and E. coli. Therefore, the iceC gene product is located at and is maximally active in or on the outer membrane of cells of the source strain and heterologous strains.

Bacterial Outer Membrane Proteins↗

PubMedDate not supplied

Molecular characterization of avirulence gene D from Pseudomonas syringae pv. tomato.

Avirulence gene D, cloned from Pseudomonas syringae pv. tomato, caused P. s. pv. glycinea to elicit a hypersensitive defense response on certain cultivars of soybean. Nucleotide sequence data for a 5.6-kb HindIII fragment containing avrD disclosed five long open-reading frames (ORFs) occurring in tandem. The phenotype conferred by avrD was expressed in P. s. pv. glycinea solely by the first of these ORFs (933 bases) that encoded a protein of 34,115 daltons. Neither a signal peptide sequence nor significant regions of hydrophobicity were present that would indicate secretion of the protein or its membrane association. Hybridization analyses revealed that some but not all P. syringae pathovars contained DNA homologous to avrD. This included weak hybridization to all tested races of P. s. pv. glycinea, although none of them express the phenotype conferred by avrD. The avrD gene occurred on an indigenous 75-kb plasmid in several P. s. pv. tomato isolates.

Amino Acid Sequence↗

PubMedDate not supplied

Two different classes of avrD alleles occur in pathovars of Pseudomonas syringae.

Considerable variation was observed in the occurrence of avirulence gene D (avrD) in different isolates and pathovars of Pseudomonas syringae. Three functional alleles of avrD were cloned and characterized from P. s. pv. phaseolicola and P. s. pv. lachrymans. These avrD genes occurred on indigenous plasmids in both pathovars, like the allele originally cloned from P. s. pv. tomato. P. s. pv. lachrymans was unique in that it carried two different alleles on plasmids of different sizes. These alleles were cloned on 5.6- or 3.8-kb HindIII fragments that are conserved in several other P. syringae pathovars. Surprisingly, the two avrD alleles from P. s. pv. lachrymans were the most divergent of those compared, with only 85% amino acid identity. Allele 1 from P. s. pv. lachrymans was 95% identical to avrD from P. s. pv. tomato but less similar to the other three avrD genes. These two alleles were accordingly called homology class I. The avrD gene from P. s. pv. phaseolicola and allele 2 from P. s. pv. lachrymans were 97 and 98% identical, respectively, at the amino acid level with the nonfunctional P. s. pv. glycinea allele. These three alleles were therefore grouped into homology class II. Comparison of all the avrD alleles permitted the identification of four amino acid substitutions unique to the P. s. pv. glycinea allele at positions 19, 245, 280, and 304.

Alleles↗