Phevamine A, a small molecule that suppresses plant immune responses

O’Neill, Erinn M.; Mucyn, Tatiana S.; Patteson, Jon B.; Finkel, Omri M.; Chung, Eui-Hwan; Baccile, Joshua A.; Massolo, Elisabetta; Schroeder, Frank C.; Dangl, Jeffery L.; Li, Bo

doi:10.1073/pnas.1803779115

Title: Phevamine A, a small molecule that suppresses plant immune responses

Journal Article · 19 September 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1803779115 · OSTI ID:1599002

O’Neill, Erinn M. ^[1]; Mucyn, Tatiana S. ^[2]; Patteson, Jon B. ^[2]; Finkel, Omri M. ^[2]; Chung, Eui-Hwan ^[2]; Baccile, Joshua A. ^[3]; Massolo, Elisabetta ^[2];

^[3]; Dangl, Jeffery L. ^[2];

^[2]

Univ. of North Carolina, Chapel Hill, NC (United States); University of Nebraska-Lincoln
Univ. of North Carolina, Chapel Hill, NC (United States)
Cornell Univ., Ithaca, NY (United States)

Bacterial plant pathogens cause significant crop damage worldwide. They invade plant cells by producing a variety of virulence factors, including small-molecule toxins and phytohormone mimics. Virulence of the model pathogen Pseudomonas syringae pv. tomato DC3000 (Pto) is regulated in part by the sigma factor HrpL. Our study of the HrpL regulon identified an uncharacterized, three-gene operon in Pto that is controlled by HrpL and related to the Erwinia hrp-associated systemic virulence (hsv) operon. Here, we demonstrate that the hsv operon contributes to the virulence of Pto on Arabidopsis thaliana and suppresses bacteria-induced immune responses. We show that the hsv-encoded enzymes in Pto synthesize a small molecule, phevamine A. This molecule consists of L-phenylalanine, L-valine, and a modified spermidine, and is different from known small molecules produced by phytopathogens. We show that phevamine A suppresses a potentiation effect of spermidine and L-arginine on the reactive oxygen species burst generated upon recognition of bacterial flagellin. The hsv operon is found in the genomes of divergent bacterial genera, including ~37% of P. syringae genomes, suggesting that phevamine A is a widely distributed virulence factor in phytopathogens. Our work identifies a small-molecule virulence factor and reveals a mechanism by which bacterial pathogens overcome plant defense. This work highlights the power of omics approaches in identifying important small molecules in bacteria–host interactions.

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Research Organization:: Univ. of Nebraska, Lincoln, NE (United States)

Sponsoring Organization:: David and Lucile Packard Foundation; National Institutes of Health (NIH); National Science Foundation (NSF); Rita Allen Foundation; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0014395

OSTI ID:: 1599002

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 41 Vol. 115; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (102)

Biosynthesis of Oligopeptides Using ATP-Grasp Enzymes Ogasawara, Yasushi; Dairi, Tohru Chemistry - A European Journal, Vol. 23, Issue 45 https://doi.org/10.1002/chem.201700674	journal	June 2017
Inhibition of ornithine decarboxylase activity by phaseolotoxin: Implications for symptom production in halo blight of French bean Bachmann, A. S.; Matile, Ph.; Slusarenko, A. J. Physiological and Molecular Plant Pathology, Vol. 53, Issue 5-6 https://doi.org/10.1006/pmpp.1998.0183	journal	November 1998
The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae Geng, Xueqing; Jin, Lin; Shimada, Mikiko Planta, Vol. 240, Issue 6 https://doi.org/10.1007/s00425-014-2151-x	journal	August 2014
Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection Yoda, Hiroshi; Fujimura, Kazuki; Takahashi, Hideyuki Plant Molecular Biology, Vol. 70, Issue 1-2 https://doi.org/10.1007/s11103-009-9459-0	journal	February 2009
Pseudomonas syringae pv. syringae harpinPss: A protein that is secreted via the hrp pathway and elicits the hypersensitive response in plants He, Sheng Yang; Huang, Hsiou-Chen; Collmer, Alan Cell, Vol. 73, Issue 7 https://doi.org/10.1016/0092-8674(93)90354-s	journal	July 1993
The ATP-grasp enzymes Fawaz, Maria V.; Topper, Melissa E.; Firestine, Steven M. Bioorganic Chemistry, Vol. 39, Issue 5-6 https://doi.org/10.1016/j.bioorg.2011.08.004	journal	December 2011
Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants Hussain, Syed Sarfraz; Ali, Muhammad; Ahmad, Maqbool Biotechnology Advances, Vol. 29, Issue 3 https://doi.org/10.1016/j.biotechadv.2011.01.003	journal	May 2011
Pseudomonas syringae Type III Effector HopBB1 Promotes Host Transcriptional Repressor Degradation to Regulate Phytohormone Responses and Virulence Yang, Li; Teixeira, Paulo José Pereira Lima; Biswas, Surojit Cell Host & Microbe, Vol. 21, Issue 2 https://doi.org/10.1016/j.chom.2017.01.003	journal	February 2017
Molecular genetics of Erwinia amylovora involved in the development of fire blight Oh, Chang-Sik; Beer, Steven V. FEMS Microbiology Letters, Vol. 253, Issue 2 https://doi.org/10.1016/j.femsle.2005.09.051	journal	December 2005
The ATP-Dependent Amide Ligases DdaG and DdaF Assemble the Fumaramoyl-Dipeptide Scaffold of the Dapdiamide Antibiotics Hollenhorst, Marie A.; Clardy, Jon; Walsh, Christopher T. Biochemistry, Vol. 48, Issue 43 https://doi.org/10.1021/bi9013165	journal	November 2009
Discovery of 3-Formyl-Tyrosine Metabolites from Pseudoalteromonas tunicata through Heterologous Expression Blasiak, Leah C.; Clardy, Jon Journal of the American Chemical Society, Vol. 132, Issue 3 https://doi.org/10.1021/ja9097862	journal	January 2010
Solid-Phase Synthesis of Polyamine Toxin Analogues: Potent and Selective Antagonists of Ca ²⁺ -Permeable AMPA Receptors Kromann, Hasse; Krikstolaityte, Sonata; Andersen, Anne J. Journal of Medicinal Chemistry, Vol. 45, Issue 26 https://doi.org/10.1021/jm020314s	journal	December 2002
Bacterial disease resistance in Arabidopsis through flagellin perception Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel Nature, Vol. 428, Issue 6984 https://doi.org/10.1038/nature02485	journal	April 2004
A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants DebRoy, S.; Thilmony, R.; Kwack, Y. -B. Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0401601101	journal	June 2004
Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae Cunnac, S.; Chakravarthy, S.; Kvitko, B. H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1013031108	journal	January 2011
A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants Hauck, Paula; Thilmony, Roger; He, Sheng Yang Proceedings of the National Academy of Sciences, Vol. 100, Issue 14 https://doi.org/10.1073/pnas.1431173100	journal	June 2003
Genome-Wide Gene Expression Analysis of Pseudomonas syringae pv. tomato DC3000 Reveals Overlapping and Distinct Pathways Regulated by hrpL and hrpRS Lan, Lefu; Deng, Xin; Zhou, Jianmin Molecular Plant-Microbe Interactions, Vol. 19, Issue 9 https://doi.org/10.1094/mpmi-19-0976	journal	September 2006
Components of the Pseudomonas syringae Type III Secretion System Can Suppress and May Elicit Plant Innate Immunity Oh, Hye-Sook; Park, Duck Hwan; Collmer, Alan Molecular Plant-Microbe Interactions, Vol. 23, Issue 6 https://doi.org/10.1094/mpmi-23-6-0727	journal	June 2010
Impact of Temperature on In Planta Expression of Genes Involved in Synthesis of the Pseudomonas syringae Phytotoxin Coronatine Weingart, Helge; Stubner, Stephan; Schenk, Alexander Molecular Plant-Microbe Interactions, Vol. 17, Issue 10 https://doi.org/10.1094/mpmi.2004.17.10.1095	journal	October 2004
Perturbation of spermine synthase Gene Expression and Transcript Profiling Provide New Insights on the Role of the Tetraamine Spermine in Arabidopsis Defense against Pseudomonas viridiflava Gonzalez, María Elisa; Marco, Francisco; Minguet, Eugenio Gómez Plant Physiology, Vol. 156, Issue 4 https://doi.org/10.1104/pp.110.171413	journal	May 2011
Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation Lou, Yann-Ru; Bor, Melike; Yan, Jian Plant Physiology https://doi.org/10.1104/pp.16.00446	journal	April 2016
The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants Kunze, Gernot; Zipfel, Cyril; Robatzek, Silke The Plant Cell, Vol. 16, Issue 12 https://doi.org/10.1105/tpc.104.026765	journal	November 2004
The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception Chinchilla, Delphine; Bauer, Zsuzsa; Regenass, Martin The Plant Cell, Vol. 18, Issue 2 https://doi.org/10.1105/tpc.105.036574	journal	December 2005
Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis de Torres, Marta; Mansfield, John W.; Grabov, Nina The Plant Journal, Vol. 47, Issue 3 https://doi.org/10.1111/j.1365-313x.2006.02798.x	journal	August 2006
A Bacterial Virulence Protein Suppresses Host Innate Immunity to Cause Plant Disease Nomura, K. Science, Vol. 313, Issue 5784 https://doi.org/10.1126/science.1129523	journal	July 2006
The Mangotoxin Biosynthetic Operon ( mbo ) Is Specifically Distributed within Pseudomonas syringae Genomospecies 1 and Was Acquired Only Once during Evolution Carrión, Víctor J.; Gutiérrez-Barranquero, José A.; Arrebola, Eva Applied and Environmental Microbiology, Vol. 79, Issue 3 https://doi.org/10.1128/aem.03007-12	journal	November 2012
The Pseudomonas syringae pv. tomato HrpW Protein Has Domains Similar to Harpins and Pectate Lyases and Can Elicit the Plant Hypersensitive Response and Bind to Pectate Charkowski, Amy O.; Alfano, James R.; Preston, Gail Journal of Bacteriology, Vol. 180, Issue 19 https://doi.org/10.1128/jb.180.19.5211-5217.1998	journal	October 1998
Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners Toruño, Tania Y.; Stergiopoulos, Ioannis; Coaker, Gitta Annual Review of Phytopathology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev-phyto-080615-100204	journal	August 2016
Defense-Related Proteins in Higher Plants Bowles, D. J. Annual Review of Biochemistry, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.bi.59.070190.004301	journal	June 1990
Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S. Genome Biology, Vol. 10, Issue 5 https://doi.org/10.1186/gb-2009-10-5-r51	journal	January 2009
A Novel L -Amino Acid Ligase Is Encoded by a Gene in the Phaseolotoxin Biosynthetic Gene Cluster from Pseudomonas syringae pv. phaseolicola 1448A Arai, Toshinobu; Kino, Kuniki Bioscience, Biotechnology, and Biochemistry, Vol. 72, Issue 11 https://doi.org/10.1271/bbb.80439	journal	November 2008
Dynamic Evolution of Pathogenicity Revealed by Sequencing and Comparative Genomics of 19 Pseudomonas syringae Isolates Baltrus, David A.; Nishimura, Marc T.; Romanchuk, Artur PLoS Pathogens, Vol. 7, Issue 7 https://doi.org/10.1371/journal.ppat.1002132	journal	July 2011
Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny Mucyn, Tatiana S.; Yourstone, Scott; Lind, Abigail L. PLoS Pathogens, Vol. 10, Issue 1 https://doi.org/10.1371/journal.ppat.1003807	journal	January 2014
Cold Calcium Signaling in Arabidopsis Involves Two Cellular Pools and a Change in Calcium Signature after Acclimation Knight, Heather; Trewavas, Anthony J.; Knight, Marc R. The Plant Cell, Vol. 8, Issue 3 https://doi.org/10.2307/3870327	journal	March 1996
Physiological and molecular implications of plant polyamine metabolism during biotic interactions JimÃ©nez-Bremont, Juan F.; Marina, MarÃa; Guerrero-GonzÃ¡lez, MarÃa de la Luz Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00095	journal	March 2014
Synthesis and Biological Activity of Argiotoxin 636 and Analogues: Selective Antagonists for Ionotropic Glutamate Receptors Nelson, Jared K.; Frølund, Sidsel U.; Tikhonov, Dennis B. Angewandte Chemie, Vol. 121, Issue 17 https://doi.org/10.1002/ange.200805426	journal	April 2009
Synthesis and Biological Activity of Argiotoxin 636 and Analogues: Selective Antagonists for Ionotropic Glutamate Receptors Nelson, Jared K.; Frølund, Sidsel U.; Tikhonov, Dennis B. Angewandte Chemie International Edition, Vol. 48, Issue 17 https://doi.org/10.1002/anie.200805426	journal	April 2009
Biosynthesis of Oligopeptides Using ATP-Grasp Enzymes Ogasawara, Yasushi; Dairi, Tohru Chemistry - A European Journal, Vol. 23, Issue 45 https://doi.org/10.1002/chem.201700674	journal	June 2017
Inhibition of ornithine decarboxylase activity by phaseolotoxin: Implications for symptom production in halo blight of French bean Bachmann, A. S.; Matile, Ph.; Slusarenko, A. J. Physiological and Molecular Plant Pathology, Vol. 53, Issue 5-6 https://doi.org/10.1006/pmpp.1998.0183	journal	November 1998
The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae Geng, Xueqing; Jin, Lin; Shimada, Mikiko Planta, Vol. 240, Issue 6 https://doi.org/10.1007/s00425-014-2151-x	journal	August 2014
Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection Yoda, Hiroshi; Fujimura, Kazuki; Takahashi, Hideyuki Plant Molecular Biology, Vol. 70, Issue 1-2 https://doi.org/10.1007/s11103-009-9459-0	journal	February 2009
Phaseolotoxin : chlorosis, ornithine accumulation and inhibition of ornithine carbamoyltransferase in different plants Ferguson, A. R.; Johnston, J. S. Physiological Plant Pathology, Vol. 16, Issue 2 https://doi.org/10.1016/0048-4059(80)90041-7	journal	March 1980
Pseudomonas syringae pv. syringae harpinPss: A protein that is secreted via the hrp pathway and elicits the hypersensitive response in plants He, Sheng Yang; Huang, Hsiou-Chen; Collmer, Alan Cell, Vol. 73, Issue 7 https://doi.org/10.1016/0092-8674(93)90354-S	journal	July 1993
Isolation and structure of a chlorosis-inducing toxin of Pseudomonas phaseolicola Mitchell, Robin E. Phytochemistry, Vol. 15, Issue 12 https://doi.org/10.1016/S0031-9422(00)88851-2	journal	January 1976
The ATP-grasp enzymes Fawaz, Maria V.; Topper, Melissa E.; Firestine, Steven M. Bioorganic Chemistry, Vol. 39, Issue 5-6 https://doi.org/10.1016/j.bioorg.2011.08.004	journal	December 2011
Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants Hussain, Syed Sarfraz; Ali, Muhammad; Ahmad, Maqbool Biotechnology Advances, Vol. 29, Issue 3 https://doi.org/10.1016/j.biotechadv.2011.01.003	journal	May 2011
Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis Kim, Min Gab; da Cunha, Luis; McFall, Aidan J. Cell, Vol. 121, Issue 5 https://doi.org/10.1016/j.cell.2005.03.025	journal	June 2005
Pseudomonas syringae Type III Effector HopBB1 Promotes Host Transcriptional Repressor Degradation to Regulate Phytohormone Responses and Virulence Yang, Li; Teixeira, Paulo José Pereira Lima; Biswas, Surojit Cell Host & Microbe, Vol. 21, Issue 2 https://doi.org/10.1016/j.chom.2017.01.003	journal	February 2017
Molecular genetics of Erwinia amylovora involved in the development of fire blight Oh, Chang-Sik; Beer, Steven V. FEMS Microbiology Letters, Vol. 253, Issue 2 https://doi.org/10.1016/j.femsle.2005.09.051	journal	December 2005
Exploring Peptide Ligase Orthologs in Actinobacteria—Discovery of Pseudopeptide Natural Products, Ketomemicins Ogasawara, Yasushi; Kawata, Junpei; Noike, Motoyoshi ACS Chemical Biology, Vol. 11, Issue 6 https://doi.org/10.1021/acschembio.6b00046	journal	April 2016
The ATP-Dependent Amide Ligases DdaG and DdaF Assemble the Fumaramoyl-Dipeptide Scaffold of the Dapdiamide Antibiotics Hollenhorst, Marie A.; Clardy, Jon; Walsh, Christopher T. Biochemistry, Vol. 49, Issue 29 https://doi.org/10.1021/bi101016e	journal	July 2010
The ATP-Dependent Amide Ligases DdaG and DdaF Assemble the Fumaramoyl-Dipeptide Scaffold of the Dapdiamide Antibiotics Hollenhorst, Marie A.; Clardy, Jon; Walsh, Christopher T. Biochemistry, Vol. 48, Issue 43 https://doi.org/10.1021/bi9013165	journal	November 2009
Discovery of 3-Formyl-Tyrosine Metabolites from Pseudoalteromonas tunicata through Heterologous Expression Blasiak, Leah C.; Clardy, Jon Journal of the American Chemical Society, Vol. 132, Issue 3 https://doi.org/10.1021/ja9097862	journal	January 2010
Solid-Phase Synthesis of Polyamine Toxin Analogues: Potent and Selective Antagonists of Ca ²⁺ -Permeable AMPA Receptors Kromann, Hasse; Krikstolaityte, Sonata; Andersen, Anne J. Journal of Medicinal Chemistry, Vol. 45, Issue 26 https://doi.org/10.1021/jm020314s	journal	December 2002
Bacterial disease resistance in Arabidopsis through flagellin perception Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel Nature, Vol. 428, Issue 6984 https://doi.org/10.1038/nature02485	journal	April 2004
Nonribosomal peptide synthetase biosynthetic clusters of ESKAPE pathogens Gulick, Andrew M. Natural Product Reports, Vol. 34, Issue 8 https://doi.org/10.1039/C7NP00029D	journal	January 2017
Genomics of secondary metabolite production by Pseudomonas spp. Gross, Harald; Loper, Joyce E. Natural Product Reports, Vol. 26, Issue 11 https://doi.org/10.1039/b817075b	journal	January 2009
Nonribosomal peptide synthetase biosynthetic clusters of ESKAPE pathogens Gulick, Andrew M. Natural Product Reports, Vol. 34, Issue 8 https://doi.org/10.1039/c7np00029d	journal	January 2017
Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA Michael, Anthony J.; Furze, Judith M.; Rhodes, Michael J. C. Biochemical Journal, Vol. 314, Issue 1 https://doi.org/10.1042/bj3140241	journal	February 1996
A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana: Sensitivity of A. thaliana to bacterial flagellin Gómez-Gómez, Lourdes; Felix, Georg; Boller, Thomas The Plant Journal, Vol. 18, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.00451.x	journal	May 1999
A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana: Counting bacteria in Arabidopsis Tornero, Pablo; Dangl, Jeffery L. The Plant Journal, Vol. 28, Issue 4 https://doi.org/10.1046/j.1365-313X.2001.01136.x	journal	November 2001
Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor Fouts, D. E.; Abramovitch, R. B.; Alfano, J. R. Proceedings of the National Academy of Sciences, Vol. 99, Issue 4 https://doi.org/10.1073/pnas.032514099	journal	February 2002
A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants DebRoy, S.; Thilmony, R.; Kwack, Y. -B. Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0401601101	journal	June 2004
Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae Cunnac, S.; Chakravarthy, S.; Kvitko, B. H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1013031108	journal	January 2011
A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants Hauck, Paula; Thilmony, Roger; He, Sheng Yang Proceedings of the National Academy of Sciences, Vol. 100, Issue 14 https://doi.org/10.1073/pnas.1431173100	journal	June 2003
Detecting Sequence Homology at the Gene Cluster Level with MultiGeneBlast Medema, Marnix H.; Takano, Eriko; Breitling, Rainer Molecular Biology and Evolution, Vol. 30, Issue 5 https://doi.org/10.1093/molbev/mst025	journal	February 2013
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Genome-Wide Gene Expression Analysis of Pseudomonas syringae pv. tomato DC3000 Reveals Overlapping and Distinct Pathways Regulated by hrpL and hrpRS Lan, Lefu; Deng, Xin; Zhou, Jianmin Molecular Plant-Microbe Interactions, Vol. 19, Issue 9 https://doi.org/10.1094/MPMI-19-0976	journal	September 2006
Components of the Pseudomonas syringae Type III Secretion System Can Suppress and May Elicit Plant Innate Immunity Oh, Hye-Sook; Park, Duck Hwan; Collmer, Alan Molecular Plant-Microbe Interactions, Vol. 23, Issue 6 https://doi.org/10.1094/MPMI-23-6-0727	journal	June 2010
Impact of Temperature on In Planta Expression of Genes Involved in Synthesis of the Pseudomonas syringae Phytotoxin Coronatine Weingart, Helge; Stubner, Stephan; Schenk, Alexander Molecular Plant-Microbe Interactions, Vol. 17, Issue 10 https://doi.org/10.1094/MPMI.2004.17.10.1095	journal	October 2004
Perturbation of spermine synthase Gene Expression and Transcript Profiling Provide New Insights on the Role of the Tetraamine Spermine in Arabidopsis Defense against Pseudomonas viridiflava Gonzalez, María Elisa; Marco, Francisco; Minguet, Eugenio Gómez Plant Physiology, Vol. 156, Issue 4 https://doi.org/10.1104/pp.110.171413	journal	May 2011
Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation Lou, Yann-Ru; Bor, Melike; Yan, Jian Plant Physiology https://doi.org/10.1104/pp.16.00446	journal	April 2016
The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants Kunze, Gernot; Zipfel, Cyril; Robatzek, Silke The Plant Cell, Vol. 16, Issue 12 https://doi.org/10.1105/tpc.104.026765	journal	November 2004
The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception Chinchilla, Delphine; Bauer, Zsuzsa; Regenass, Martin The Plant Cell, Vol. 18, Issue 2 https://doi.org/10.1105/tpc.105.036574	journal	December 2005
Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Knight, H.; Trewavas, A. J.; Knight, M. R. The Plant Cell, Vol. 8, Issue 3 https://doi.org/10.1105/tpc.8.3.489	journal	March 1996
The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infection Oh, Chang-Sik; Kim, Jihyun F.; Beer, Steven V. Molecular Plant Pathology, Vol. 6, Issue 2 https://doi.org/10.1111/j.1364-3703.2005.00269.x	journal	March 2005
Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis de Torres, Marta; Mansfield, John W.; Grabov, Nina The Plant Journal, Vol. 47, Issue 3 https://doi.org/10.1111/j.1365-313X.2006.02798.x	journal	August 2006
The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana: Virulence action of Pst DC3000 effector HopAO1 Underwood, William; Zhang, Shuqun; He, Sheng Y. The Plant Journal, Vol. 52, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03262.x	journal	September 2007
Recombineering and stable integration of the Pseudomonas syringae pv. syringaeâ€ƒ61 hrp/hrc cluster into the genome of the soil bacterium Pseudomonas fluorescens Pf0-1: Stable integration of a T3SS-locus into Pf0-1 Thomas, William J.; Thireault, Caitlin A.; Kimbrel, Jeffrey A. The Plant Journal, Vol. 60, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.03998.x	journal	December 2009
The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato: The metabolic transition during disease following infection of Arabidopsis Ward, Jane L.; Forcat, Silvia; Beckmann, Manfred The Plant Journal, Vol. 63, Issue 3 https://doi.org/10.1111/j.1365-313X.2010.04254.x	journal	May 2010
A Bacterial Virulence Protein Suppresses Host Innate Immunity to Cause Plant Disease Nomura, K. Science, Vol. 313, Issue 5784 https://doi.org/10.1126/science.1129523	journal	July 2006
The Mangotoxin Biosynthetic Operon ( mbo ) Is Specifically Distributed within Pseudomonas syringae Genomospecies 1 and Was Acquired Only Once during Evolution Carrión, Víctor J.; Gutiérrez-Barranquero, José A.; Arrebola, Eva Applied and Environmental Microbiology, Vol. 79, Issue 3 https://doi.org/10.1128/AEM.03007-12	journal	November 2012
The Pseudomonas syringae pv. tomato HrpW Protein Has Domains Similar to Harpins and Pectate Lyases and Can Elicit the Plant Hypersensitive Response and Bind to Pectate Charkowski, Amy O.; Alfano, James R.; Preston, Gail Journal of Bacteriology, Vol. 180, Issue 19 https://doi.org/10.1128/JB.180.19.5211-5217.1998	journal	October 1998
Pseudomonas syringae Phytotoxins: Mode of Action, Regulation, and Biosynthesis by Peptide and Polyketide Synthetases Bender, Carol L.; Alarcón-Chaidez, Francisco; Gross, Dennis C. Microbiology and Molecular Biology Reviews, Vol. 63, Issue 2 https://doi.org/10.1128/MMBR.63.2.266-292.1999	journal	June 1999
From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition Yu, Xiao; Feng, Baomin; He, Ping Annual Review of Phytopathology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev-phyto-080516-035649	journal	August 2017
Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners Toruño, Tania Y.; Stergiopoulos, Ioannis; Coaker, Gitta Annual Review of Phytopathology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev-phyto-080615-100204	journal	August 2016
Defense-Related Proteins in Higher Plants Bowles, D. J. Annual Review of Biochemistry, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.bi.59.070190.004301	journal	June 1990
Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S. Genome Biology, Vol. 10, Issue 5 https://doi.org/10.1186/gb-2009-10-5-r51	journal	January 2009
The Arabidopsis Thaliana-Pseudomonas Syringae Interaction Katagiri, Fumiaki; Thilmony, Roger; He, Sheng Yang The Arabidopsis Book, Vol. 1 https://doi.org/10.1199/tab.0039	journal	January 2002
A Novel L -Amino Acid Ligase Is Encoded by a Gene in the Phaseolotoxin Biosynthetic Gene Cluster from Pseudomonas syringae pv. phaseolicola 1448A Arai, Toshinobu; Kino, Kuniki Bioscience, Biotechnology, and Biochemistry, Vol. 72, Issue 11 https://doi.org/10.1271/bbb.80439	journal	November 2008
Correction: Genomic Analysis of the Kiwifruit Pathogen Pseudomonas syringae pv. actinidiae Provides Insight into the Origins of an Emergent Plant Disease McCann, Honour C.; Rikkerink, Erik H. A.; Bertels, Frederic PLoS Pathogens, Vol. 9, Issue 9 https://doi.org/10.1371/annotation/af157ddc-200a-4105-b243-3f01251cc677	journal	September 2013
The mbo Operon Is Specific and Essential for Biosynthesis of Mangotoxin in Pseudomonas syringae Carrión, Víctor J.; Arrebola, Eva; Cazorla, Francisco M. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036709	journal	May 2012
Deletions in the Repertoire of Pseudomonas syringae pv. tomato DC3000 Type III Secretion Effector Genes Reveal Functional Overlap among Effectors Kvitko, Brian H.; Park, Duck Hwan; Velásquez, André C. PLoS Pathogens, Vol. 5, Issue 4 https://doi.org/10.1371/journal.ppat.1000388	journal	April 2009
Dynamic Evolution of Pathogenicity Revealed by Sequencing and Comparative Genomics of 19 Pseudomonas syringae Isolates Baltrus, David A.; Nishimura, Marc T.; Romanchuk, Artur PLoS Pathogens, Vol. 7, Issue 7 https://doi.org/10.1371/journal.ppat.1002132	journal	July 2011
Genomic Analysis of the Kiwifruit Pathogen Pseudomonas syringae pv. actinidiae Provides Insight into the Origins of an Emergent Plant Disease McCann, Honour C.; Rikkerink, Erik H. A.; Bertels, Frederic PLoS Pathogens, Vol. 9, Issue 7 https://doi.org/10.1371/journal.ppat.1003503	journal	July 2013
Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny Mucyn, Tatiana S.; Yourstone, Scott; Lind, Abigail L. PLoS Pathogens, Vol. 10, Issue 1 https://doi.org/10.1371/journal.ppat.1003807	journal	January 2014
Dynamic Evolution of Pathogenicity Revealed by Sequencing and Comparative Genomics of 19 Pseudomonas syringae Isolates Jeff, Roach,; Karen, Cherkis,; D., Jones, Corbin The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/0nga-kz54	text	January 2011
Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny Scott, Yourstone,; H., Chang, Jeff; R., Grant, Sarah The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/640s-h976	text	January 2014
Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 pseudomonas syringae isolates M. T., Nishimura,; D. A., Baltrus,; J. H., Chang, Public Library of Science https://doi.org/10.17615/kjke-5e64	text	January 2011
Cold Calcium Signaling in Arabidopsis Involves Two Cellular Pools and a Change in Calcium Signature after Acclimation Knight, Heather; Trewavas, Anthony J.; Knight, Marc R. The Plant Cell, Vol. 8, Issue 3 https://doi.org/10.2307/3870327	journal	March 1996
Physiological and molecular implications of plant polyamine metabolism during biotic interactions JimÃ©nez-Bremont, Juan F.; Marina, MarÃa; Guerrero-GonzÃ¡lez, MarÃa de la Luz Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00095	journal	March 2014
How Microbes Twist Jasmonate Signaling around Their Little Fingers Gimenez-Ibanez, Selena; Chini, Andrea; Solano, Roberto Plants, Vol. 5, Issue 1 https://doi.org/10.3390/plants5010009	journal	January 2016

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Host Range Determinants of Pseudomonas savastanoi Pathovars of Woody Hosts Revealed by Comparative Genomics and Cross-Pathogenicity Tests Moreno-Pérez, Alba; Pintado, Adrián; Murillo, Jesús Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00973	journal	July 2020
Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production Majumdar, Rajtilak; Minocha, Rakesh; Lebar, Matthew D. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00692	journal	May 2019

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