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Published: 4 June 2021
Last updated: 21 February 2023

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1

López-López, Karina, José Luis Hernández-Flores, Marisa Cruz-Aguilar, and Ariel Alvarez-Morales. "In Pseudomonas syringae pv. phaseolicola, Expression of the argK Gene, Encoding the Phaseolotoxin-Resistant Ornithine Carbamoyltransferase, Is Regulated Indirectly by Temperature and Directly by a Precursor Resembling Carbamoylphosphate." Journal of Bacteriology 186, no. 1 (January 1, 2004): 146–53. http://dx.doi.org/10.1128/jb.186.1.146-153.2004.

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ABSTRACT Pseudomonas syringae pv. phaseolicola synthesizes a non-host-specific toxin, phaseolotoxin, and also synthesizes a phaseolotoxin-resistant ornithine carbamoyltransferase (ROCT) to protect itself from its own toxin. ROCT is encoded by argK, which is expressed coordinately with phaseolotoxin synthesis at 18°C. To investigate the regulatory mechanisms of this system, null mutants were constructed for argK, argF (encoding the phaseolotoxin-sensitive OCTase [SOCT]), and amtA (encoding an amidinotransferase involved in phaseolotoxin synthesis). The argF mutant did not exhibit arginine auxotrophy when grown in M9 medium at 28°C, because under this condition SOCT was replaced by ROCT. This loss of thermoregulation of argK was apparently caused by accumulation of carbamoylphosphate, one of the substrates of SOCT. Carbamoylphosphate, which has a structure similar to that of the inorganic moiety of phaseolotoxin, was used in induction assays with wild-type P. syringae pv. phaseolicola and was shown to be able to induce argK expression in M9 medium at 28°C. These results indicate that argK expression is independent of temperature and is regulated directly by a compound resembling the inorganic moiety of phaseolotoxin.
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2

Guardado-Valdivia, Lizeth, Alejandra Chacón-López, Jesús Murillo, Jorge Poveda, José Luis Hernández-Flores, Luis Xoca-Orozco, and Selene Aguilera. "The Pbo Cluster from Pseudomonas syringae pv. Phaseolicola NPS3121 Is Thermoregulated and Required for Phaseolotoxin Biosynthesis." Toxins 13, no. 9 (September 7, 2021): 628. http://dx.doi.org/10.3390/toxins13090628.

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The bean (Phaseolus vulgaris) pathogen Pseudomonas syringae pv. phaseolicola NPS3121 synthesizes phaseolotoxin in a thermoregulated way, with optimum production at 18 °C. Gene PSPPH_4550 was previously shown to be thermoregulated and required for phaseolotoxin biosynthesis. Here, we established that PSPPH_4550 is part of a cluster of 16 genes, the Pbo cluster, included in a genomic island with a limited distribution in P. syringae and unrelated to the possession of the phaseolotoxin biosynthesis cluster. We identified typical non-ribosomal peptide synthetase, and polyketide synthetase domains in several of the pbo deduced products. RT-PCR and the analysis of polar mutants showed that the Pbo cluster is organized in four transcriptional units, including one monocistronic and three polycistronic. Operons pboA and pboO are both essential for phaseolotoxin biosynthesis, while pboK and pboJ only influence the amount of toxin produced. The three polycistronic units were transcribed at high levels at 18 °C but not at 28 °C, whereas gene pboJ was constitutively expressed. Together, our data suggest that the Pbo cluster synthesizes secondary metabolite(s), which could participate in the regulation of phaseolotoxin biosynthesis.
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3

Hernández-Guzmán, Gustavo, and Ariel Alvarez-Morales. "Isolation and Characterization of the Gene Coding for the Amidinotransferase Involved in the Biosynthesis of Phaseolotoxin in Pseudomonas syringae pv. phaseolicola." Molecular Plant-Microbe Interactions® 14, no. 4 (April 2001): 545–54. http://dx.doi.org/10.1094/mpmi.2001.14.4.545.

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Pseudomonas syringae pv. phaseolicola is the causal agent of the “halo blight” disease of beans. A key component in the development of the disease is a nonhost-specific toxin, Nδ-(N'-sulphodiaminophosphinyl)-ornithyl-alanyl-homoarginine, known as phaseolotoxin. The homoarginine residue in this molecule has been suggested to be the product of Larginine:lysine amidinotransferase activity, previously detected in extracts of P. syringae pv. phaseolicola grown under conditions of phaseolotoxin production. We report the isolation and characterization of an amidinotransferase gene (amtA) from P. syringae pv. phaseolicola coding for a polypeptide of 362 residues (41.36 kDa) and showing approximately 40% sequence similarity to Larginine:inosamine-phosphate amidinotransferase from three species of Streptomyces spp. and 50.4% with an Larginine:glycine amidinotransferase from human mitochondria. The cysteine, histidine, and aspartic acid residues involved in substrate binding are conserved. Furthermore, expression of the amtA and argK genes and phaseolotoxin production occurs at 18°C but not at 28°C. An amidinotransferase insertion mutant was obtained that lost the capacity to synthesize homoarginine and phaseolotoxin. These results show that the amtA gene isolated is responsible for the amidinotransferase activity detected previously and that phaseolotoxin production depends upon the activity of this gene.
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4

Hernández-Flores, José Luis, Karina López-López, Rogelio Garcidueñas-Piña, Alba E. Jofre-Garfias, and Ariel Alvarez-Morales. "The Global Arginine Regulator ArgR Controls Expression of argF in Pseudomonas syringae pv. phaseolicola but Is Not Required for the Synthesis of Phaseolotoxin or for the Regulated Expression of argK." Journal of Bacteriology 186, no. 11 (June 1, 2004): 3653–55. http://dx.doi.org/10.1128/jb.186.11.3653-3655.2004.

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ABSTRACT In Pseudomonas syringae pv. phaseolicola the enzyme ornithine carbamoyltransferase (OCTase), encoded by argF, is negatively regulated by argR, similar to what has been reported for Pseudomonas aeruginosa. However, production of the phaseolotoxin-resistant OCTase encoded by argK, synthesis of phaseolotoxin, and infectivity for bean pods occur independently of the ArgR protein.
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5

González, Ana Isabel, Marcelino Pérez de la Vega, María Luisa Ruiz, and Carlos Polanco. "Analysis of the argK-tox Gene Cluster in Nontoxigenic Strains of Pseudomonas syringae pv. phaseolicola." Applied and Environmental Microbiology 69, no. 8 (August 2003): 4979–82. http://dx.doi.org/10.1128/aem.69.8.4979-4982.2003.

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ABSTRACT The analysis of 46 isolates obtained directly from different and distant common bean fields from the northwestern part of Spain revealed that they do not produce phaseolotoxin. The isolates were classified as race 5, and their analysis revealed that they do not carry the argK-tox gene cluster involved in the biosynthesis of the phaseolotoxin.
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6

Arvizu-Gómez, Jackeline Lizzeta, Alejandro Hernández-Morales, Rafael Arnulfo Juárez-Navarro, Juan Diego Paredes-Tadeo, Juan Campos-Guillén, Juan Ramiro Pacheco-Aguilar, Abril Bernardette Martínez-Rizo, and Christian González-Reyes. "OxyR Positively Influences Phaseolotoxin Synthesis and Pyoverdin Production in Pseudomonas savastanoi pv. phaseolicola NPS3121." Microorganisms 10, no. 11 (October 27, 2022): 2123. http://dx.doi.org/10.3390/microorganisms10112123.

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Phaseolotoxin is a major virulence factor of the bean pathogen bacterium P. savastanoi pv. phaseolicola. This toxin plays a key role in the development of the halo blight disease in bean plants. So far, the signal transduction pathways involved in the synthesis of phaseolotoxin have not been elucidated. The influence of regulation mechanisms related to the oxidative stress response, in particular the OxyR protein, it has been suggested to be involved in this process.. In this study we evaluated the role of OxyR in P. savastanoi pv. phaseolicola, mainly compared to the synthesis of phaseolotoxin and the virulence of this phytopathogen. Generation of the oxyR-mutant, pathogenicity and virulence tests, and analyses of gene expression by RT-PCR assays were performed. The results showed that OxyR exerts an effect on the synthesis of phaseolotoxin and positively influences the expression of the Pht and Pbo cluster genes. Likewise, OxyR influences the production of pyoverdine by the control of the expression of the genes encoding the PvdS sigma factor, involved in the synthesis of this pigment. This study is the first report on members of the OxyR regulon of P. savastanoi pv. phaseolicola NPS3121.
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7

Aguilera, Selene, Karina López-López, Yudith Nieto, Rogelio Garcidueñas-Piña, Gustavo Hernández-Guzmán, José Luis Hernández-Flores, Jesús Murillo, and Ariel Alvarez-Morales. "Functional Characterization of the Gene Cluster from Pseudomonas syringae pv. phaseolicola NPS3121 Involved in Synthesis of Phaseolotoxin." Journal of Bacteriology 189, no. 7 (January 19, 2007): 2834–43. http://dx.doi.org/10.1128/jb.01845-06.

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ABSTRACT Pseudomonas syringae pv. phaseolicola is the causal agent of halo blight disease of beans (Phaseolus vulgaris L.), which is characterized by water-soaked lesions surrounded by a chlorotic halo resulting from the action of a non-host-specific toxin known as phaseolotoxin. This phytotoxin inhibits the enzyme ornithine carbamoyltransferase involved in arginine biosynthesis. Different evidence suggested that genes involved in phaseolotoxin production were clustered. Two genes had been previously identified in our laboratory within this cluster: argK, which is involved in the immunity of the bacterium to its own toxin, and amtA, which is involved in the synthesis of homoarginine. We sequenced the region around argK and amtA in P. syringae pv. phaseolicola NPS3121 to determine the limits of the putative phaseolotoxin gene cluster and to determine the transcriptional pattern of the genes comprising it. We report that the phaseolotoxin cluster (Pht cluster) is composed of 23 genes and is flanked by insertion sequences and transposases. The mutation of 14 of the genes within the cluster lead to a Tox− phenotype for 11 of them, while three mutants exhibited low levels of toxin production. The analysis of fusions of selected DNA fragments to uidA, Northern probing, and reverse transcription-PCR indicate the presence of five transcriptional units, two monocistronic and three polycistronic; one is internal to a larger operon. The site for transcription initiation has been determined for each promoter, and the putative promoter regions were identified. Preliminary results also indicate that the gene product of phtL is involved in the regulation of the synthesis of phaseolotoxin.
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8

Bender, Carol L., Francisco Alarcón-Chaidez, and Dennis C. Gross. "Pseudomonas syringae Phytotoxins: Mode of Action, Regulation, and Biosynthesis by Peptide and Polyketide Synthetases." Microbiology and Molecular Biology Reviews 63, no. 2 (June 1, 1999): 266–92. http://dx.doi.org/10.1128/mmbr.63.2.266-292.1999.

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SUMMARY Coronatine, syringomycin, syringopeptin, tabtoxin, and phaseolotoxin are the most intensively studied phytotoxins of Pseudomonas syringae, and each contributes significantly to bacterial virulence in plants. Coronatine functions partly as a mimic of methyl jasmonate, a hormone synthesized by plants undergoing biological stress. Syringomycin and syringopeptin form pores in plasma membranes, a process that leads to electrolyte leakage. Tabtoxin and phaseolotoxin are strongly antimicrobial and function by inhibiting glutamine synthetase and ornithine carbamoyltransferase, respectively. Genetic analysis has revealed the mechanisms responsible for toxin biosynthesis. Coronatine biosynthesis requires the cooperation of polyketide and peptide synthetases for the assembly of the coronafacic and coronamic acid moieties, respectively. Tabtoxin is derived from the lysine biosynthetic pathway, whereas syringomycin, syringopeptin, and phaseolotoxin biosynthesis requires peptide synthetases. Activation of phytotoxin synthesis is controlled by diverse environmental factors including plant signal molecules and temperature. Genes involved in the regulation of phytotoxin synthesis have been located within the coronatine and syringomycin gene clusters; however, additional regulatory genes are required for the synthesis of these and other phytotoxins. Global regulatory genes such as gacS modulate phytotoxin production in certain pathovars, indicating the complexity of the regulatory circuits controlling phytotoxin synthesis. The coronatine and syringomycin gene clusters have been intensively characterized and show potential for constructing modified polyketides and peptides. Genetic reprogramming of peptide and polyketide synthetases has been successful, and portions of the coronatine and syringomycin gene clusters could be valuable resources in developing new antimicrobial agents.
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9

Templeton, M. D., R. E. Mitchell, P. A. Sullivan, and M. G. Shepherd. "The inactivation of ornithine transcarbamoylase by Nδ-(N'-sulpho-diaminophosphinyl)-L-ornithine." Biochemical Journal 228, no. 2 (June 1, 1985): 347–52. http://dx.doi.org/10.1042/bj2280347.

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Phaseolotoxin, a tripeptide inhibitor of ornithine transcarbamoylase, is a phytotoxin produced by Pseudomonas syringae pv. phaseolicola, the causal agent of halo-blight in beans. In vivo the toxin is cleaved to release N delta-(N'-sulpho-diaminophosphinyl)-L-ornithine, the major toxic chemical species present in diseased leaf tissue. This paper reports on the interaction between N delta-(N'-sulpho-diaminophosphinyl)-L-ornithine and ornithine transcarbamoylase. N delta-(N'-Sulpho-diaminophosphinyl)-L-ornithine was found to be a potent inactivator of the enzyme, in contrast with phaseolotoxin, which previously has been reported to inhibit the enzyme reversibly. Inactivation by N delta-(N'-[35S]sulpho-diaminophosphinyl)-L-ornithine resulted in the incorporation of 35S into ethanol-precipitated protein. The stoicheiometry of 35S incorporation was approximately 1 mol/mol of active sites. Inactivation was second-order and a rate constant of 10(6) M-1 X s-1 at 0 degree C in 50 mM-Tris/HCl, pH 9.0, was obtained. Carbamoyl phosphate, a substrate of ornithine transcarbamoylase, protected the enzyme from inactivation. A dissociation constant of 3 microM for the enzyme-carbamoyl phosphate complex was calculated. L-Ornithine, the second substrate for ornithine transcarbamoylase, protected the enzyme only at high concentrations. The results are consistent with N delta-(N'-sulpho-diaminophosphinyl)-L-ornithine being a potent affinity label that binds via the carbamoyl phosphate-binding site of ornithine transcarbamoylase. Cleavage of phaseolotoxin to N delta-(N'-sulpho-diaminophosphinyl)-L-ornithine in vivo appears to be an important function in the physiology of the disease.
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10

Rowley, Karla B., Ronghui Xu, and Suresh S. Patil. "Molecular Analysis of Thermoregulation of Phaseolotoxin-Resistant Ornithine Carbamoyltransferase (argK) from Pseudomonas syringae pv. phaseolicola." Molecular Plant-Microbe Interactions® 13, no. 10 (October 2000): 1071–80. http://dx.doi.org/10.1094/mpmi.2000.13.10.1071.

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The phaseolotoxin-resistant ornithine carbamoyltransferase (ROCT) and phaseolotoxin are produced by Pseudo-monas syringae pv. phaseolicola at 18°C but not at 28°C. At 28°C, the pathogen produces a protein(s) that binds (in vitro) to a 485-bp fragment (thermoregulatory region, TRR) from a heterologous clone from the pathogen genomic library, which in multiple copies overrides thermoregulation of phaseolotoxin production in wild-type cells (K. B. Rowley, D. E. Clements, M. Mandel, T. Humphreys, and S. S. Patil, Mol. Microbiol. 8:625-635, 1993). We report here that DNase I protection analysis of the 485-bp fragment shows that a single site is protected from cleavage by the protein in the 28°C extract and that this site contains two repeats of a core motif G/C AAAG separated by a 5-bp spacer. Partially purified binding protein forms specific complexes with a synthetic oligonucleotide containing four tandem repeats of this motif. A 492-bp upstream fragment from argK encoding ROCT also forms specific complexes with the protein in the 28°C crude extract, and a 260-bp subfragment from the TRR containing the binding site cross competes with the argk fragment, indicating that the same protein binds to nucleotides in both fragments. DNase I protection analysis of the fragment from argK revealed four separate protected sequence elements, with element III containing half of the core motif sequence (CTTTG), and the other elements containing similar sequences. Gel shift assays were done with DNA fragments from which one or all of the sites were removed as competitor DNAs against the argK probe. The results of these experiments confirmed that the binding sites (in argK) are necessary for the protein to bind to the argK fragment in a specific manner. Taken together, the results of studies presented here suggest that in cells of P. syringae pv. phaseolicola grown at high temperature argK may be negatively regulated by the protein produced at this temperature.
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11

Nüske, Jörg, and Wolfgang Fritsche. "Phaseolotoxin production byPseudomonas syringae pv.phaseolicola: The influence of temperature." Journal of Basic Microbiology 29, no. 7 (1989): 441–47. http://dx.doi.org/10.1002/jobm.3620290713.

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12

Turner, John G. "Effect of Phaseolotoxin on the Synthesis of Arginine and Protein." Plant Physiology 80, no. 3 (March 1, 1986): 760–65. http://dx.doi.org/10.1104/pp.80.3.760.

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13

Templeton, M. D., P. A. Sullivan, and M. G. Shepherd. "Phaseolotoxin-insensitive L-ornithine transcarbamoylase from Pseudomonas syringae pv. phaseolicola." Physiological and Molecular Plant Pathology 29, no. 3 (November 1986): 393–403. http://dx.doi.org/10.1016/s0048-4059(86)80055-8.

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14

Jahn, O., J. Sauerstein, and G. Reuter. "Inhibition of ornithine carbamoyltransferase fromPseudomonas syringae pv.syringae W50 by phaseolotoxin." Journal of Basic Microbiology 29, no. 5 (1989): 315–18. http://dx.doi.org/10.1002/jobm.3620290521.

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15

Ramírez-Zapata, Diana, Cayo Ramos, Selene Aguilera, Leire Bardaji, Marta Martínez-Gil, and Jesús Murillo. "Two Homologues of the Global Regulator Csr/Rsm Redundantly Control Phaseolotoxin Biosynthesis and Virulence in the Plant Pathogen Pseudomonas amygdali pv. phaseolicola 1448A." Microorganisms 8, no. 10 (October 6, 2020): 1536. http://dx.doi.org/10.3390/microorganisms8101536.

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The widely conserved Csr/Rsm (carbon storage regulator/repressor of stationary-phase metabolites) post-transcriptional regulatory system controls diverse phenotypes involved in bacterial pathogenicity and virulence. Here we show that Pseudomonas amygdali pv. phaseolicola 1448A contains seven rsm genes, four of which are chromosomal. In RNAseq analyses, only rsmE was thermoregulated, with increased expression at 18 °C, whereas the antagonistic sRNAs rsmX1, rsmX4, rsmX5 and rsmZ showed increased levels at 28 °C. Only double rsmA-rsmE mutants showed significantly altered phenotypes in functional analyses, being impaired for symptom elicitation in bean, including in planta growth, and for induction of the hypersensitive response in tobacco. Double mutants were also non-motile and were compromised for the utilization of different carbon sources. These phenotypes were accompanied by reduced mRNA levels of the type III secretion system regulatory genes hrpL and hrpA, and the flagellin gene, fliC. Biosynthesis of the phytotoxin phaseolotoxin by mutants in rsmA and rsmE was delayed, occurring only in older cultures, indicating that these rsm homologues act as inductors of toxin synthesis. Therefore, genes rsmA and rsmE act redundantly, although with a degree of specialization, to positively regulate diverse phenotypes involved in niche colonization. Additionally, our results suggest the existence of a regulatory molecule different from the Rsm proteins and dependent on the GacS/GacA (global activator of antibiotic and cyanide production) system, which causes the repression of phaseolotoxin biosynthesis at high temperatures.
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16

Hirose, Karin, Yasuhiro Ishiga, and Takashi Fujikawa. "Phytotoxin synthesis genes and type III effector genes of Pseudomonas syringae pv. actinidiae biovar 6 are regulated by culture conditions." PeerJ 8 (August 14, 2020): e9697. http://dx.doi.org/10.7717/peerj.9697.

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The kiwifruit bacterial canker (Pseudomonas syringae pv. actinidiae; Psa) causes severe damage to kiwifruit production worldwide. Psa biovar 6 (Psa6), which was isolated in Japan in 2015, produces two types of phytotoxins: coronatine and phaseolotoxin. To elucidate the unique virulence of Psa6, we performed transcriptomic analysis of phytotoxin synthesis genes and type III effector genes in in vitro cultivation using various media. The genes related to phytotoxin synthesis and effectors of Psa6 were strictly regulated in the coronatine-inducing mediums (HS and HSC); 14 of 23 effector genes and a hrpL sigma factor gene were induced at 3 h after transferring to the media (early-inducible genes), and phytotoxin synthesis genes such as argD of phaseolotoxin and cfl of coronatine were induced at 6 and 12 h after transferring to the media (late-inducible genes). In contrast, induction of these genes was not observed in the hrp-inducing medium. Next, to examine whether the changes in gene expression in different media is specific to Psa6, we investigated gene expression in other related bacteria. For Psa biovar 1 (Psa1), biovar 3 (Psa3), and P. s. pv. glycinea (Psg), no clear trends were observed in expression behavior across various culture media and incubation times. Therefore, Psa6 seems to exert its virulence efficiently by using two phytotoxins and effectors according to environmental changes. This is not seen in other biovars and pathovars, so it is thought that Psa6 has acquired its own balance of virulence.
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17

Peet, Richard C., and Nickolas J. Panopoulos. "Ornithine carbamoyltransferase genes and phaseolotoxin immunity in Pseudomonas syringae pv. phaseolicola." EMBO Journal 6, no. 12 (December 1987): 3585–91. http://dx.doi.org/10.1002/j.1460-2075.1987.tb02689.x.

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18

Oguiza, José A., Arantza Rico, Luis A. Rivas, Laurent Sutra, Alan Vivian, and Jesús Murillo. "Pseudomonas syringae pv. phaseolicola can be separated into two genetic lineages distinguished by the possession of the phaseolotoxin biosynthetic cluster." Microbiology 150, no. 2 (February 1, 2004): 473–82. http://dx.doi.org/10.1099/mic.0.26635-0.

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The bean (Phaseolus spp.) plant pathogen Pseudomonas syringae pv. phaseolicola is characterized by the ability to produce phaseolotoxin (Tox+). We recently reported that the majority of the Spanish P. syringae pv. phaseolicola population is unable to synthesize this toxin (Tox−). These Tox− isolates appear to lack the entire DNA region for the biosynthesis of phaseolotoxin (argK-tox gene cluster), as shown by PCR amplification and DNA hybridization using DNA sequences specific for separated genes of this cluster. Tox+ and Tox− isolates also showed genomic divergence that included differences in ERIC-PCR and arbitrarily primed-PCR profiles. Tox+ isolates showed distinct patterns of IS801 genomic insertions and contained a chromosomal IS801 insertion that was absent from Tox− isolates. Using a heteroduplex mobility assay, sequence differences were observed only among the intergenic transcribed spacer of the five rDNA operons of the Tox− isolates. The techniques used allowed the unequivocal differentiation of isolates of P. syringae pv. phaseolicola from the closely related soybean (Glycine max) pathogen, P. syringae pv. glycinea. Finally, a pathogenicity island that is essential for the pathogenicity of P. syringae pv. phaseolicola on beans appears to be conserved among Tox+, but not among Tox− isolates, which also lacked the characteristic large plasmid that carries this pathogenicity island. It is proposed that the results presented here justify the separation of the Tox+ and Tox− P. syringae pv. phaseolicola isolates into two distinct genetic lineages, designated Pph1 and Pph2, respectively, that show relevant genomic differences that include the pathogenicity gene complement.
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19

Rico, Arantza, Ruth López, Carmen Asensio, M. Teresa Aizpún, M. Carmen Asensio-S.-Manzanera, and Jesús Murillo. "Nontoxigenic Strains of Pseudomonas syringae pv. phaseolicola Are a Main Cause of Halo Blight of Beans in Spain and Escape Current Detection Methods." Phytopathology® 93, no. 12 (December 2003): 1553–59. http://dx.doi.org/10.1094/phyto.2003.93.12.1553.

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From a collection of 152 pseudomonads isolated from diseased beans in Spain, 138 (91%) of the strains were identified as Pseudomonas syringae pv. phaseolicola and the rest as P. syringae pv. syringae. The P. syringae pv. phaseolicola strains produced typical water-soaked lesions on bean pods, although 95 of them did not produce phaseolotoxin in vitro. Ninety-four of these isolates did not produce the expected 0.5-kb product after polymerase chain reaction (PCR) amplification using primers specific for open reading frame (ORF) 6 of the phaseolotoxin (tox) gene cluster and did not contain DNA homologous to ORF 6 in Southern hybridization experiments. To our knowledge, this is the first report of the widespread occurrence in the field of strains of P. syringae pv. phaseolicola lacking the tox cluster, which contrasts sharply with the general belief that Tox+ isolates are the only ones with epidemiological importance. Additionally, the tox- isolates were not specifically detected by a commercial polyclonal antisera in an enzyme-linked immunosorbent assay. Accordingly, it is possible that the certification of seed lots as free of the pathogen cannot be reliably done in Spain, or in any other country where tox- strains might occur frequently, using current PCR or serological protocols. The amplification of three avirulence genes by PCR allowed us to make predictions of the P. syringae pv. phaseolicola race structure, as confirmed by plant assays. Six races (races 1, 2, 5, 6, 7, and 9) were identified, with race 7 being the most prevalent (46.1%) followed by races 6 (21.3%) and 1 (9.0%). All the tox- isolates contained gene avrPphF, typical of races 1, 5, 7, and 9.
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20

Tourte, C., and C. Manceau. "A strain ofPseudomonas syringae which does not belong to pathovarphaseolicola produces phaseolotoxin." European Journal of Plant Pathology 101, no. 5 (September 1995): 483–90. http://dx.doi.org/10.1007/bf01874471.

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21

Quigley, Neil B., David Lane, and Peter L. Bergquist. "Genes for phaseolotoxin synthesis are located on the chromosome ofPseudomonas syringae pv.phaseolicola." Current Microbiology 12, no. 5 (September 1985): 295–99. http://dx.doi.org/10.1007/bf01567981.

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22

Peet, R. C., P. B. Lindgren, D. K. Willis, and N. J. Panopoulos. "Identification and cloning of genes involved in phaseolotoxin production by Pseudomonas syringae pv. "phaseolicola"." Journal of Bacteriology 166, no. 3 (1986): 1096–105. http://dx.doi.org/10.1128/jb.166.3.1096-1105.1986.

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23

Bachmann, André S., and Suresh S. Patil. "Characterization of ornithine decarboxylase from Pseudomonas syringae pv. phaseolicola and its inhibition by phaseolotoxin." Physiological and Molecular Plant Pathology 63, no. 2 (August 2003): 57–63. http://dx.doi.org/10.1016/j.pmpp.2003.09.005.

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24

Jahn, O., J. Sauerstein, and G. Reuter. "Characterization of two ornithine carbamoyltransferases from Pseudomonas syringae pv. phaseolicola, the producer of phaseolotoxin." Archives of Microbiology 147, no. 2 (March 1987): 174–78. http://dx.doi.org/10.1007/bf00415280.

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25

Jahn, O., J. Sauerstein, and G. Reuter. "Detection of two ornithine carbamoyltransferases in a phaseolotoxin-producing strain ofPseudomonas syringae pv. phaseolicola." Journal of Basic Microbiology 25, no. 8 (1985): 543–46. http://dx.doi.org/10.1002/jobm.3620250821.

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26

Zhang, Yuan Xin, and Suresh S. Patil. "The phtE Locus in the Phaseolotoxin Gene Cluster Has ORFs with Homologies to Genes Encoding Amino Acid Transferases, the AraC Family of Transcriptional Factors, and Fatty Acid Desaturases." Molecular Plant-Microbe Interactions® 10, no. 8 (November 1997): 947–60. http://dx.doi.org/10.1094/mpmi.1997.10.8.947.

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A cluster of genes involved in the production of phaseolotoxin, a phytotoxin produced by Pseudomonas syringae pv. phaseolicola, contains eight (phtA through phtH) complementation groups (Y. X. Zhang, K. B. Rowley, and S. S. Patil, J. Bacteriol., 175:6451–6458, 1993). In this study, sequencing of the region encompassing the phtE locus revealed six putative open reading frames (ORFs), each preceded by a putative ribosomal binding site, and all oriented in the same direction. Reverse transcription-polymerase chain reaction suggested that the phtE locus is transcribed as one large (6.4 kb) transcript, indicating that the ORFs constitute an operon. Primer extension analysis showed that the transcript begins at a T, located 31 bp upstream of the ATG codon of ORF1. Comparison of the sequences of the putative ORFs with the sequences of known genes revealed that ORF3, encoding a protein containing 395 amino acids, has 55% similarity to the acetylornithine aminotransferase gene from Escherichia coli, and the ornithine aminotransferase genes from other organisms. A lysine residue that is a binding site for pyridoxal phosphate and an arginine residue that is a binding site for the α-carboxylate group of the substrate are conserved in ORF3. These data suggest that ORF3 encodes a protein involved in the biosynthesis of ornithine, a constituent of phaseolotoxin. ORF5, encoding a peptide of 378 amino acid residues, possesses a helix-turn-helix motif at the C-terminal end that is characteristic of the AraC family of transcriptional factors, and there is a possible leucine zipper at the N-terminal end of this peptide. ORF6, encoding a protein of 327 amino acids, has about 40% similarity with the fatty acid desaturase gene, desA, of Synechocystis Pcc6803 and considerable similarity with fatty acid desaturase genes from other organisms. ORF6 and desA show very similar hydropathy profiles and both contain a copper binding signature. Computer searches did not discover significant homologies in the data base for the other ORFs, but hydropathy analysis showed that all of them contain one to several hydrophobic domains, suggesting that the gene products of these ORFs may be membrane associated.
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27

Turner, John G., and Robin E. Mitchell. "Association between Symptom Development and Inhibition of Ornithine Carbamoyltransferase in Bean Leaves Treated with Phaseolotoxin." Plant Physiology 79, no. 2 (October 1, 1985): 468–73. http://dx.doi.org/10.1104/pp.79.2.468.

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Mosqueda, Gilberto, Guido Van den Broeck, Odila Saucedo, Ana Maria Bailey, Ariel Alvarez-Morales, and Luis Herrera-Estrella. "Isolation and characterization of the gene fromPseudomonas syringae pv.phaseolicola encoding the phaseolotoxin-insensitive ornithine carbamoyltransferase." Molecular and General Genetics MGG 222, no. 2-3 (July 1990): 461–66. http://dx.doi.org/10.1007/bf00633857.

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29

Kamdar, H. V., K. B. Rowley, D. Clements, and S. S. Patil. "Pseudomonas syringae pv. phaseolicola genomic clones harboring heterologous DNA sequences suppress the same phaseolotoxin-deficient mutants." Journal of Bacteriology 173, no. 3 (1991): 1073–79. http://dx.doi.org/10.1128/jb.173.3.1073-1079.1991.

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Rowley, Karla B., David E. Clements, Morton Mandel, Tom Humphreys, and Suresh S. Patil. "Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production." Molecular Microbiology 8, no. 3 (May 1993): 625–35. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01606.x.

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Genka, Hiroyuki, Tomoya Baba, Masataka Tsuda, Shigehiko Kanaya, Hirotada Mori, Takanobu Yoshida, Masako Tsujimoto Noguchi, Kenichi Tsuchiya, and Hiroyuki Sawada. "Comparative Analysis of argK-tox Clusters and Their Flanking Regions in Phaseolotoxin-Producing Pseudomonas syringae Pathovars." Journal of Molecular Evolution 63, no. 3 (August 21, 2006): 401–14. http://dx.doi.org/10.1007/s00239-005-0271-4.

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32

Bachmann, A. S., Ph Matile, and A. J. Slusarenko. "Inhibition of ornithine decarboxylase activity by phaseolotoxin: Implications for symptom production in halo blight of French bean." Physiological and Molecular Plant Pathology 53, no. 5-6 (November 1998): 287–99. http://dx.doi.org/10.1006/pmpp.1998.0183.

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Fuente-Martínez, Juan Manuel de la, Gilberto Mosqueda-Cano, Ariel Alvarez-Morales, and Luis Herrera-Estrella. "Expression of a Bacterial Phaseolotoxin–Resistant Ornithyl Transcarbamylase in Transgenic Tobacco Confers Resistance to Pseudomonas Syringae pv. Phaseolicola." Nature Biotechnology 10, no. 8 (August 1992): 905–9. http://dx.doi.org/10.1038/nbt0892-905.

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34

Prosen, D. "Specific Detection ofPseudomonas syringaepv.phaseolicolaDNA in Bean Seed by Polymerase Chain Reaction-Based Amplification of a Phaseolotoxin Gene Region." Phytopathology 83, no. 7 (1993): 965. http://dx.doi.org/10.1094/phyto-83-965.

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ARAI, Toshinobu, and Kuniki KINO. "A NovelL-Amino Acid Ligase Is Encoded by a Gene in the Phaseolotoxin Biosynthetic Gene Cluster fromPseudomonas syringaepv.phaseolicola1448A." Bioscience, Biotechnology, and Biochemistry 72, no. 11 (November 23, 2008): 3048–50. http://dx.doi.org/10.1271/bbb.80439.

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36

Ward, E. W. B., S. S. Gnanamanickam, and A. N. Starratt. "Induction of a resistant reaction-type and glyceollin accumulation in a compatible soybean -Phytophthora megaspermaf. sp.glycineainteraction by phaseolotoxin treatments." Canadian Journal of Plant Pathology 8, no. 4 (December 1986): 361–64. http://dx.doi.org/10.1080/07060668609501770.

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MIYOSHI, T., S. SHIMIZU, and H. SAWADA. "Occurrence and distribution of a defective non-phaseolotoxin-producing mutant of Pseudomonas syringae pv. actinidiae in Ehime Prefecture, Japan." Japanese Journal of Phytopathology 78, no. 2 (2012): 92–103. http://dx.doi.org/10.3186/jjphytopath.78.92.

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38

Tamura, K., M. Imamura, K. Yoneyama, Y. Kohno, Y. Takikawa, I. Yamaguchi, and H. Takahashi. "Role of phaseolotoxin production by Pseudomonas syringae pv. actinidiae in the formation of halo lesions of kiwifruit canker disease." Physiological and Molecular Plant Pathology 60, no. 4 (April 2002): 207–14. http://dx.doi.org/10.1006/pmpp.2002.0405.

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39

Kong, Hye Suk, Daniel P. Roberts, Cheryl D. Patterson, Sarah A. Kuehne, Stephan Heeb, Dilip K. Lakshman, and John Lydon. "Effect of Overexpressing rsmA from Pseudomonas aeruginosa on Virulence of Select Phytotoxin-Producing Strains of P. syringae." Phytopathology® 102, no. 6 (June 2012): 575–87. http://dx.doi.org/10.1094/phyto-09-11-0267.

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The GacS/GacA two-component system functions mechanistically in conjunction with global post-transcriptional regulators of the RsmA family to allow pseudomonads and other bacteria to adapt to changing environmental stimuli. Analysis of this Gac/Rsm signal transduction pathway in phytotoxin-producing pathovars of Pseudmonas syringae is incomplete, particularly with regard to rsmA. Our approach in studying it was to overexpress rsmA in P. syringae strains through introduction of pSK61, a plasmid constitutively expressing this gene. Disease and colonization of plant leaf tissue were consistently diminished in all P. syringae strains tested (pv. phaseolicola NPS3121, pv. syringae B728a, and BR2R) when harboring pSK61 relative to these isolates harboring the empty vector pME6031. Phaseolotoxin, syringomycin, and tabtoxin were not produced in any of these strains when transformed with pSK61. Production of protease and pyoverdin as well as swarming were also diminished in all of these strains when harboring pSK61. In contrast, alginate production, biofilm formation, and the hypersensitive response were diminished in some but not all of these isolates under the same growth conditions. These results indicate that rsmA is consistently important in the overarching phenotypes disease and endophtyic colonization but that its role varies with pathovar in certain underpinning phenotypes in the phytotoxin-producing strains of P. syringae.
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Bachmann, André S., Ronghui Xu, Lal Ratnapala, and Suresh S. Patil. "Inhibitory effects of phaseolotoxin on proliferation of leukemia cells HL-60, K-562 and L1210 and pancreatic cells RIN-m5F." Leukemia Research 28, no. 3 (March 2004): 301–6. http://dx.doi.org/10.1016/j.leukres.2003.07.002.

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Zhang, Lixin, Yanru Shi, Zhiran Wu, and Genjia Tan. "Characterization of response regulator GacA involved in phaseolotoxin production, hypersensitive response and cellular processes in Pseudomonas syringae pv. actinidiae A18." Physiological and Molecular Plant Pathology 103 (August 2018): 137–42. http://dx.doi.org/10.1016/j.pmpp.2018.07.001.

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Hernández-Morales, Alejandro, Jennifer Alexis Rojas-Morales, Marisol Reynoso-López, Abril Bernardette Martínez-Rizo, Jesús Bernardino Velázquez-Fernández, and Jackeline Lizzeta Arvizu-Gómez. "Oxidative stress regulates the expression of the Pht cluster genes involved in phaseolotoxin synthesis in Pseudomonas syringae pv. phaseolicola NPS3121." Journal of General Plant Pathology 84, no. 2 (February 5, 2018): 137–41. http://dx.doi.org/10.1007/s10327-018-0770-y.

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Aguilera, Selene, Susana De la Torre-Zavala, José Luis Hernández-Flores, Jesús Murillo, Jaime Bravo, and Ariel Alvarez-Morales. "Expression of the Gene for Resistance to Phaseolotoxin (argK) Depends on the Activity of Genes phtABC in Pseudomonas syringae pv. phaseolicola." PLoS ONE 7, no. 10 (October 8, 2012): e46815. http://dx.doi.org/10.1371/journal.pone.0046815.

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Aguilera, Selene, Ariel Alvarez-Morales, Jesús Murillo, José Luis Hernández-Flores, Jaime Bravo, and Susana De la Torre-Zavala. "Temperature-mediated biosynthesis of the phytotoxin phaseolotoxin by Pseudomonas syringae pv. phaseolicola depends on the autoregulated expression of the phtABC genes." PLOS ONE 12, no. 6 (June 1, 2017): e0178441. http://dx.doi.org/10.1371/journal.pone.0178441.

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Zhang, Y., K. B. Rowley, and S. S. Patil. "Genetic organization of a cluster of genes involved in the production of phaseolotoxin, a toxin produced by Pseudomonas syringae pv. phaseolicola." Journal of Bacteriology 175, no. 20 (1993): 6451–58. http://dx.doi.org/10.1128/jb.175.20.6451-6458.1993.

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González-Villanueva, Luis, Jackeline Lizzeta Arvizu-Gómez, Alejandro Hernández-Morales, Selene Aguilera-Aguirre, and Ariel Álvarez-Morales. "The PhtL protein of Pseudomonas syringae pv. phaseolicola NPS3121 affects the expression of both phaseolotoxin cluster (Pht) and Non-Pht encoded genes." Microbiological Research 169, no. 2-3 (February 2014): 221–31. http://dx.doi.org/10.1016/j.micres.2013.05.002.

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Murillo, Jesús, Leire Bardaji, Laura Navarro de la Fuente, Ma Elena Führer, Selene Aguilera, and Ariel Álvarez-Morales. "Variation in conservation of the cluster for biosynthesis of the phytotoxin phaseolotoxin in Pseudomonas syringae suggests at least two events of horizontal acquisition." Research in Microbiology 162, no. 3 (April 2011): 253–61. http://dx.doi.org/10.1016/j.resmic.2010.10.011.

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48

Arvizu-Gómez, Jackeline, Alejandro Hernández-Morales, Guillermo Pastor-Palacios, Luis G. Brieba, and Ariel Álvarez-Morales. "Integration Host Factor (IHF) binds to the promoter region of the phtD operon involved in phaseolotoxin synthesis in P. syringae pv. phaseolicola NPS3121." BMC Microbiology 11, no. 1 (2011): 90. http://dx.doi.org/10.1186/1471-2180-11-90.

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Hwang, Michael S. H., Robyn L. Morgan, Sara F. Sarkar, Pauline W. Wang, and David S. Guttman. "Phylogenetic Characterization of Virulence and Resistance Phenotypes of Pseudomonas syringae." Applied and Environmental Microbiology 71, no. 9 (September 2005): 5182–91. http://dx.doi.org/10.1128/aem.71.9.5182-5191.2005.

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ABSTRACT Individual strains of the plant pathogenic bacterium Pseudomonas syringae vary in their ability to produce toxins, nucleate ice, and resist antimicrobial compounds. These phenotypes enhance virulence, but it is not clear whether they play a dominant role in specific pathogen-host interactions. To investigate the evolution of these virulence-associated phenotypes, we used functional assays to survey for the distribution of these phenotypes among a collection of 95 P. syringae strains. All of these strains were phylogenetically characterized via multilocus sequence typing (MLST). We surveyed for the production of coronatine, phaseolotoxin, syringomycin, and tabtoxin; for resistance to ampicillin, chloramphenicol, rifampin, streptomycin, tetracycline, kanamycin, and copper; and for the ability to nucleate ice at high temperatures via the ice-nucleating protein INA. We found that fewer than 50% of the strains produced toxins and significantly fewer strains than expected produced multiple toxins, leading to the speculation that there is a cost associated with the production of multiple toxins. None of these toxins was associated with host of isolation, and their distribution, relative to core genome phylogeny, indicated extensive horizontal genetic exchange. Most strains were resistant to ampicillin and copper and had the ability to nucleate ice, and yet very few strains were resistant to the other antibiotics. The distribution of the rare resistance phenotypes was also inconsistent with the clonal history of the species and did not associate with host of isolation. The present study provides a robust phylogenetic foundation for the study of these important virulence-associated phenotypes in P. syringae host colonization and pathogenesis.
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50

Cooper, Bret, Kimberly B. Campbell, Hunter S. Beard, Wesley M. Garrett, and Marcio E. Ferreira. "The Proteomics of Resistance to Halo Blight in Common Bean." Molecular Plant-Microbe Interactions® 33, no. 9 (September 2020): 1161–75. http://dx.doi.org/10.1094/mpmi-05-20-0112-r.

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Halo blight disease of beans is caused by a gram-negative bacterium, Pseudomonas syringae pv. phaseolicola. The disease is prevalent in South America and Africa and causes crop loss for indigent people who rely on beans as a primary source of daily nutrition. In susceptible beans, P. syringae pv. phaseolicola causes water-soaking at the site of infection and produces phaseolotoxin, an inhibitor of bean arginine biosynthesis. In resistant beans, P. syringae pv. phaseolicola triggers a hypersensitive response that limits the spread of infection. Here, we used high-throughput mass spectrometry to interrogate the responses to two different P. syringae pv. phaseolicola isolates on a single line of common bean, Phaseolus vulgaris PI G19833, with a reference genome sequence. We obtained quantitative information for 4,135 bean proteins. A subset of 160 proteins with similar accumulation changes during both susceptible and resistant reactions included salicylic acid responders EDS1 and NDR1, ethylene and jasmonic acid biosynthesis enzymes, and proteins enabling vesicle secretion. These proteins revealed the activation of a basal defense involving hormonal responses and the mobilization of extracellular proteins. A subset of 29 proteins specific to hypersensitive immunity included SOBIR1, a G-type lectin receptor–like kinase, and enzymes needed for glucoside and phytoalexin production. Virus-induced gene silencing revealed that the G-type lectin receptor–like kinase suppresses bacterial infection. Together, the results define the proteomics of disease resistance to P. syringae pv. phaseolicola in beans and support a model whereby the induction of hypersensitive immunity reinstates defenses targeted by P. syringae pv. phaseolicola.
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