Previous Article | Next Article 
Microbiology and Molecular Biology Reviews, June 1999, p. 266-292, Vol. 63, No. 2
1092-2172/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Pseudomonas syringae Phytotoxins: Mode
of Action, Regulation, and Biosynthesis by Peptide and
Polyketide Synthetases
Carol L.
Bender,1,*
Francisco
Alarcón-Chaidez,1 and
Dennis C.
Gross2
Department of Entomology and Plant Pathology,
Oklahoma State University, Stillwater, Oklahoma
74078-3032,1 and Department of Plant
Pathology, Washington State University, Pullman, Washington
99164-64302
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.
*
Corresponding author. Mailing address: 110 Noble
Research Center, Oklahoma State University, Stillwater, OK 74078-3032. Phone: (405) 744-9945. Fax: (405) 744-7373. E-mail:
cbender{at}okstate.edu.
Microbiology and Molecular Biology Reviews, June 1999, p. 266-292, Vol. 63, No. 2
1092-2172/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Vallet-Gely, I., Novikov, A., Augusto, L., Liehl, P., Bolbach, G., Pechy-Tarr, M., Cosson, P., Keel, C., Caroff, M., Lemaitre, B.
(2010). Association of Hemolytic Activity of Pseudomonas entomophila, a Versatile Soil Bacterium, with Cyclic Lipopeptide Production. Appl. Environ. Microbiol.
76: 910-921
[Abstract]
[Full Text]
-
Wangdi, T., Uppalapati, S. R., Nagaraj, S., Ryu, C.-M., Bender, C. L., Mysore, K. S.
(2010). A Virus-Induced Gene Silencing Screen Identifies a Role for Thylakoid Formation1 in Pseudomonas syringae pv tomato Symptom Development in Tomato and Arabidopsis. Plant Physiol.
152: 281-292
[Abstract]
[Full Text]
-
Sammer, U. F., Volksch, B., Mollmann, U., Schmidtke, M., Spiteller, P., Spiteller, M., Spiteller, D.
(2009). 2-Amino-3-(Oxirane-2,3-Dicarboxamido)-Propanoyl-Valine, an Effective Peptide Antibiotic from the Epiphyte Pantoea agglomerans 48b/90. Appl. Environ. Microbiol.
75: 7710-7717
[Abstract]
[Full Text]
-
Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W., Luo, H., Nan, F., Wang, Z., Xie, D.
(2009). The Arabidopsis CORONATINE INSENSITIVE1 Protein Is a Jasmonate Receptor. Plant Cell
21: 2220-2236
[Abstract]
[Full Text]
-
Collmer, A., Schneider, D. J., Lindeberg, M.
(2009). Lifestyles of the Effector Rich: Genome-Enabled Characterization of Bacterial Plant Pathogens. Plant Physiol.
150: 1623-1630
[Full Text]
-
Murakami, T., Maeda, T., Yokota, A., Wada, M.
(2009). Gene Cloning and Expression of Pyridoxal 5'-Phosphate-Dependent L-threo-3-Hydroxyaspartate Dehydratase from Pseudomonas sp. T62, and Characterization of the Recombinant Enzyme. J Biochem
145: 661-668
[Abstract]
[Full Text]
-
Bergougnoux, V., Hlavackova, V., Plotzova, R., Novak, O., Fellner, M.
(2009). The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. J Exp Bot
60: 1219-1230
[Abstract]
[Full Text]
-
Attaran, E., Zeier, T. E., Griebel, T., Zeier, J.
(2009). Methyl Salicylate Production and Jasmonate Signaling Are Not Essential for Systemic Acquired Resistance in Arabidopsis. Plant Cell
21: 954-971
[Abstract]
[Full Text]
-
Gudesblat, G. E., Torres, P. S., Vojnov, A. A.
(2009). Xanthomonas campestris Overcomes Arabidopsis Stomatal Innate Immunity through a DSF Cell-to-Cell Signal-Regulated Virulence Factor. Plant Physiol.
149: 1017-1027
[Abstract]
[Full Text]
-
Herrero, A. B., Astudillo, A. M., Balboa, M. A., Cuevas, C., Balsinde, J., Moreno, S.
(2008). Levels of SCS7/FA2H-Mediated Fatty Acid 2-Hydroxylation Determine the Sensitivity of Cells to Antitumor PM02734. Cancer Res.
68: 9779-9787
[Abstract]
[Full Text]
-
Dubern, J.-F., Coppoolse, E. R., Stiekema, W. J., Bloemberg, G. V.
(2008). Genetic and functional characterization of the gene cluster directing the biosynthesis of putisolvin I and II in Pseudomonas putida strain PCL1445. Microbiology
154: 2070-2083
[Abstract]
[Full Text]
-
Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y., Howe, G. A.
(2008). From the Cover: COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl. Acad. Sci. USA
105: 7100-7105
[Abstract]
[Full Text]
-
Mohr, T. J., Liu, H., Yan, S., Morris, C. E., Castillo, J. A., Jelenska, J., Vinatzer, B. A.
(2008). Naturally Occurring Nonpathogenic Isolates of the Plant Pathogen Pseudomonas syringae Lack a Type III Secretion System and Effector Gene Orthologues. J. Bacteriol.
190: 2858-2870
[Abstract]
[Full Text]
-
Chen, Z., Agnew, J. L., Cohen, J. D., He, P., Shan, L., Sheen, J., Kunkel, B. N.
(2007). Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. USA
104: 20131-20136
[Abstract]
[Full Text]
-
Spoel, S. H., Johnson, J. S., Dong, X.
(2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. USA
104: 18842-18847
[Abstract]
[Full Text]
-
Brinsmade, S. R., Escalante-Semerena, J. C.
(2007). In Vivo and in Vitro Analyses of Single-amino Acid Variants of the Salmonella enterica Phosphotransacetylase Enzyme Provide Insights into the Function of Its N-terminal Domain. J. Biol. Chem.
282: 12629-12640
[Abstract]
[Full Text]
-
Belimov, A., Dodd, I., Safronova, V., Hontzeas, N, Davies, W.
(2007). Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. J Exp Bot
58: 1485-1495
[Abstract]
[Full Text]
-
Sarkar, S. F., Gordon, J. S., Martin, G. B., Guttman, D. S.
(2006). Comparative Genomics of Host-Specific Virulence in Pseudomonas syringae. Genetics
174: 1041-1056
[Abstract]
[Full Text]
-
Yun, M. H., Torres, P. S., Oirdi, M. E., Rigano, L. A., Gonzalez-Lamothe, R., Marano, M. R., Castagnaro, A. P., Dankert, M. A., Bouarab, K., Vojnov, A. A.
(2006). Xanthan Induces Plant Susceptibility by Suppressing Callose Deposition. Plant Physiol.
141: 178-187
[Abstract]
[Full Text]
-
Alice, A. F., Lopez, C. S., Lowe, C. A., Ledesma, M. A., Crosa, J. H.
(2006). Genetic and Transcriptional Analysis of the Siderophore Malleobactin Biosynthesis and Transport Genes in the Human Pathogen Burkholderia pseudomallei K96243. J. Bacteriol.
188: 1551-1566
[Abstract]
[Full Text]
-
Wang, N., Lu, S.-E., Yang, Q., Sze, S.-H., Gross, D. C.
(2006). Identification of the syr-syp Box in the Promoter Regions of Genes Dedicated to Syringomycin and Syringopeptin Production by Pseudomonas syringae pv. syringae B301D. J. Bacteriol.
188: 160-168
[Abstract]
[Full Text]
-
Jenke-Kodama, H., Sandmann, A., Muller, R., Dittmann, E.
(2005). Evolutionary Implications of Bacterial Polyketide Synthases. Mol Biol Evol
22: 2027-2039
[Abstract]
[Full Text]
-
Joardar, V., Lindeberg, M., Jackson, R. W., Selengut, J., Dodson, R., Brinkac, L. M., Daugherty, S. C., DeBoy, R., Durkin, A. S., Giglio, M. G., Madupu, R., Nelson, W. C., Rosovitz, M. J., Sullivan, S., Crabtree, J., Creasy, T., Davidsen, T., Haft, D. H., Zafar, N., Zhou, L., Halpin, R., Holley, T., Khouri, H., Feldblyum, T., White, O., Fraser, C. M., Chatterjee, A. K., Cartinhour, S., Schneider, D. J., Mansfield, J., Collmer, A., Buell, C. R.
(2005). Whole-Genome Sequence Analysis of Pseudomonas syringae pv. phaseolicola 1448A Reveals Divergence among Pathovars in Genes Involved in Virulence and Transposition. J. Bacteriol.
187: 6488-6498
[Abstract]
[Full Text]
-
Li, X., Lin, H., Zhang, W., Zou, Y., Zhang, J., Tang, X., Zhou, J.-M.
(2005). Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc. Natl. Acad. Sci. USA
102: 12990-12995
[Abstract]
[Full Text]
-
Kang, H., Gross, D. C.
(2005). Characterization of a Resistance-Nodulation-Cell Division Transporter System Associated with the syr-syp Genomic Island of Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol.
71: 5056-5065
[Abstract]
[Full Text]
-
Hwang, M. S. H., Morgan, R. L., Sarkar, S. F., Wang, P. W., Guttman, D. S.
(2005). Phylogenetic Characterization of Virulence and Resistance Phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol.
71: 5182-5191
[Abstract]
[Full Text]
-
Dubern, J.-F., Lagendijk, E. L., Lugtenberg, B. J. J., Bloemberg, G. V.
(2005). The Heat Shock Genes dnaK, dnaJ, and grpE Are Involved in Regulation of Putisolvin Biosynthesis in Pseudomonas putida PCL1445. J. Bacteriol.
187: 5967-5976
[Abstract]
[Full Text]
-
Feil, H., Feil, W. S., Chain, P., Larimer, F., DiBartolo, G., Copeland, A., Lykidis, A., Trong, S., Nolan, M., Goltsman, E., Thiel, J., Malfatti, S., Loper, J. E., Lapidus, A., Detter, J. C., Land, M., Richardson, P. M., Kyrpides, N. C., Ivanova, N., Lindow, S. E.
(2005). Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. USA
102: 11064-11069
[Abstract]
[Full Text]
-
Hasegawa, H., Chatterjee, A., Cui, Y., Chatterjee, A. K.
(2005). Elevated Temperature Enhances Virulence of Erwinia carotovora subsp. carotovora Strain EC153 to Plants and Stimulates Production of the Quorum Sensing Signal, N-Acyl Homoserine Lactone, and Extracellular Proteins. Appl. Environ. Microbiol.
71: 4655-4663
[Abstract]
[Full Text]
-
Brencic, A., Winans, S. C.
(2005). Detection of and Response to Signals Involved in Host-Microbe Interactions by Plant-Associated Bacteria. Microbiol. Mol. Biol. Rev.
69: 155-194
[Abstract]
[Full Text]
-
Cui, J., Bahrami, A. K., Pringle, E. G., Hernandez-Guzman, G., Bender, C. L., Pierce, N. E., Ausubel, F. M.
(2005). Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc. Natl. Acad. Sci. USA
102: 1791-1796
[Abstract]
[Full Text]
-
Chen, H., McCaig, B. C., Melotto, M., He, S. Y., Howe, G. A.
(2004). Regulation of Plant Arginase by Wounding, Jasmonate, and the Phytotoxin Coronatine. J. Biol. Chem.
279: 45998-46007
[Abstract]
[Full Text]
-
Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T. G., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J. C., Mungall, K., Atkin, R., Bason, N., Brooks, K., Chillingworth, T., Clark, K., Doggett, J., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Norbertczak, H., Ormond, D., Price, C., Quail, M. A., Sanders, M., Walker, D., Whitehead, S., Salmond, G. P. C., Birch, P. R. J., Parkhill, J., Toth, I. K.
(2004). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. USA
101: 11105-11110
[Abstract]
[Full Text]
-
Bretz, J. R., Hutcheson, S. W.
(2004). Role of Type III Effector Secretion during Bacterial Pathogenesis in Another Kingdom. Infect. Immun.
72: 3697-3705
[Full Text]
-
Seidle, H., Rangaswamy, V., Couch, R., Bender, C. L., Parry, R. J.
(2004). Characterization of Cfa1, a Monofunctional Acyl Carrier Protein Involved in the Biosynthesis of the Phytotoxin Coronatine. J. Bacteriol.
186: 2499-2503
[Abstract]
[Full Text]
-
Couch, R., O'Connor, S. E., Seidle, H., Walsh, C. T., Parry, R.
(2004). Characterization of CmaA, an Adenylation-Thiolation Didomain Enzyme Involved in the Biosynthesis of Coronatine. J. Bacteriol.
186: 35-42
[Abstract]
[Full Text]
-
Monier, J.-M., Lindow, S. E.
(2004). Frequency, Size, and Localization of Bacterial Aggregates on Bean Leaf Surfaces. Appl. Environ. Microbiol.
70: 346-355
[Abstract]
[Full Text]
-
Lu, S.-E., Soule, J. D., Gross, D. C.
(2003). Characterization of the argA Gene Required for Arginine Biosynthesis and Syringomycin Production by Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol.
69: 7273-7280
[Abstract]
[Full Text]
-
Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q., Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W.-L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., Collmer, A.
(2003). The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA
100: 10181-10186
[Abstract]
[Full Text]
-
Hauck, P., Thilmony, R., He, S. Y.
(2003). A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA
100: 8577-8582
[Abstract]
[Full Text]
-
Keith, R. C., Keith, L. M. W., Hernandez-Guzman, G., Uppalapati, S. R., Bender, C. L.
(2003). Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and non-host plants. Microbiology
149: 1127-1138
[Abstract]
[Full Text]
-
Lindow, S. E., Brandl, M. T.
(2003). Microbiology of the Phyllosphere. Appl. Environ. Microbiol.
69: 1875-1883
[Full Text]
-
Nowak-Thompson, B., Hammer, P. E., Hill, D. S., Stafford, J., Torkewitz, N., Gaffney, T. D., Lam, S. T., Molnar, I., Ligon, J. M.
(2003). 2,5-Dialkylresorcinol Biosynthesis in Pseudomonas aurantiaca: Novel Head-to-Head Condensation of Two Fatty Acid-Derived Precursors. J. Bacteriol.
185: 860-869
[Abstract]
[Full Text]
-
Koch, B., Nielsen, T. H., Sorensen, D., Andersen, J. B., Christophersen, C., Molin, S., Givskov, M., Sorensen, J., Nybroe, O.
(2002). Lipopeptide Production in Pseudomonas sp. Strain DSS73 Is Regulated by Components of Sugar Beet Seed Exudate via the Gac Two-Component Regulatory System. Appl. Environ. Microbiol.
68: 4509-4516
[Abstract]
[Full Text]
-
Baidyaroy, D., Brosch, G., Graessle, S., Trojer, P., Walton, J. D.
(2002). Characterization of Inhibitor-Resistant Histone Deacetylase Activity in Plant-Pathogenic Fungi. Eukaryot Cell
1: 538-547
[Abstract]
[Full Text]
-
Nielsen, T. H., Sorensen, D., Tobiasen, C., Andersen, J. B., Christophersen, C., Givskov, M., Sorensen, J.
(2002). Antibiotic and Biosurfactant Properties of Cyclic Lipopeptides Produced by Fluorescent Pseudomonas spp. from the Sugar Beet Rhizosphere. Appl. Environ. Microbiol.
68: 3416-3423
[Abstract]
[Full Text]
-
Marits, R., Tshuikina, M., Pirhonen, M., Laasik, E., Mae, A.
(2002). Regulation of the expression of prtW::gusA fusions in Erwinia carotovora subsp. carotovora. Microbiology
148: 835-842
[Abstract]
[Full Text]
-
Fouts, D. E., Abramovitch, R. B., Alfano, J. R., Baldo, A. M., Buell, C. R., Cartinhour, S., Chatterjee, A. K., D'Ascenzo, M., Gwinn, M. L., Lazarowitz, S. G., Lin, N.-C., Martin, G. B., Rehm, A. H., Schneider, D. J., van Dijk, K., Tang, X., Collmer, A.
(2002). Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. USA
99: 2275-2280
[Abstract]
[Full Text]
-
Scholthof, H. B.
(2001). Molecular Plant-Microbe Interactions That Cut the Mustard. Plant Physiol.
127: 1476-1483
[Full Text]
-
Chicharro, C., Granata, C., Lozano, R., Andreu, D., Rivas, L.
(2001). N-Terminal Fatty Acid Substitution Increases the Leishmanicidal Activity of CA(1-7)M(2-9), a Cecropin-Melittin Hybrid Peptide. Antimicrob. Agents Chemother.
45: 2441-2449
[Abstract]
[Full Text]
-
Sesma, A., Sundin, G. W., Murillo, J.
(2000). Phylogeny of the replication regions of pPT23A-like plasmids from Pseudomonas syringae. Microbiology
146: 2375-2384
[Abstract]
[Full Text]
-
Peñaloza-Vázquez, A., Preston, G. M., Collmer, A., Bender, C. L.
(2000). Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. Microbiology
146: 2447-2456
[Abstract]
[Full Text]
-
Hendrickson, E. L., Guevera, P., Penaloza-Vazquez, A., Shao, J., Bender, C., Ausubel, F. M.
(2000). Virulence of the Phytopathogen Pseudomonas syringae pv. Maculicola Is rpoN Dependent. J. Bacteriol.
182: 3498-3507
[Abstract]
[Full Text]
-
Hendrickson, E. L., Guevera, P., Ausubel, F. M.
(2000). The Alternative Sigma Factor RpoN Is Required for hrp Activity in Pseudomonas syringae pv. Maculicola and Acts at the Level of hrpL Transcription. J. Bacteriol.
182: 3508-3516
[Abstract]
[Full Text]
-
Pernestig, A.-K., Melefors, O., Georgellis, D.
(2001). Identification of UvrY as the Cognate Response Regulator for the BarA Sensor Kinase in Escherichia coli. J. Biol. Chem.
276: 225-231
[Abstract]
[Full Text]
-
Lee, J., Klusener, B., Tsiamis, G., Stevens, C., Neyt, C., Tampakaki, A. P., Panopoulos, N. J., Noller, J., Weiler, E. W., Cornelis, G. R., Mansfield, J. W., Nurnberger, T.
(2001). HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore invitro. Proc. Natl. Acad. Sci. USA
98: 289-294
[Abstract]
[Full Text]
-
Mach, J. M., Castillo, A. R., Hoogstraten, R., Greenberg, J. T.
(2001). The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA
98: 771-776
[Abstract]
[Full Text]
-
Benedetti, C. E., Arruda, P.
(2002). Altering the Expression of the Chlorophyllase Gene ATHCOR1 in Transgenic Arabidopsis Caused Changes in the Chlorophyll-to-Chlorophyllide Ratio. Plant Physiol.
128: 1255-1263
[Abstract]
[Full Text]