Pseudomonas syringae is one of the most common plant pathogens that infect the phyllosphere. P. syringae can live on the plant surface as an epiphyte. To cause disease, it enters the plant, through wounds or natural openings such as stomata, and multiplies within the apoplast. P. syringae is an insightful model for understanding bacterial virulence mechanisms and host adaptation of pathogens as well as microbial evolution, ecology and epidemiology.
The P. syringae species complex forms a monophyletic group in the Pseudomonas fluorescens-like division of Pseudomonas. P. syringae strains are split into 13 phylogroups, which separate between early-branching and canonical lineages. Members of the canonical lineages have conserved virulence-associated and phenotypic features and include several plant-specialist phylogroups. P. syringae has also been subdivided into more than 60 pathovars on the basis of host of isolation, host range and other properties.
P. syringae attacks plants using a variety of virulence factors, including effector proteins that are translocated into the plant cell via the type III secretion system (T3SS), small-molecule toxins, exopolysaccharides, cell-wall-degrading enzymes and plant hormones (or hormone mimics). Whereas all pathogenic strains of P. syringae possess the T3SS and effectors, they may or may not produce other virulence factors.
Plants have evolved a defence mechanism (stomatal closure) to reduce bacterial entry through stomata by detection of pathogen-associated molecular patterns (PAMPs). To defeat stomatal defence, P. syringae uses toxins and T3SS effector proteins to overcome PAMP-induced stomatal closure. Stomatal closure is sensitive to high atmospheric humidity, which could promote bacterial entry into the plant.
After entry into the plant, P. syringae encounters the apoplast, a potentially carbohydrate-rich but heavily defended living space for microorganisms. Recent advances in the identification of a minimal repertoire of T3SS effectors and host-mutation-based disease reconstitution experiments provide evidence that immune suppression and establishment of aqueous apoplast are two principal pathogenic processes required for P. syringae growth inside the apoplast.
P. syringae infection is profoundly influenced by external environmental conditions, such as air humidity, temperature and microbiota that live on healthy plants. Understanding how abiotic and biotic environmental conditions shape P. syringae infection at the mechanistic level may become an important aspect of future research. A complete understanding of the multidimensional plant–P. syringae–environment–microbiota interactions will infer innovative approaches for controlling diseases on crop plants.
Pseudomonas syringae is one of the best-studied plant pathogens and serves as a model for understanding host–microorganism interactions, bacterial virulence mechanisms and host adaptation of pathogens as well as microbial evolution, ecology and epidemiology. Comparative genomic studies have identified key genomic features that contribute to P. syringae virulence. P. syringae has evolved two main virulence strategies: suppression of host immunity and creation of an aqueous apoplast to form its niche in the phyllosphere. In addition, external environmental conditions such as humidity profoundly influence infection. P. syringae may serve as an excellent model to understand virulence and also of how pathogenic microorganisms integrate environmental conditions and plant microbiota to become ecologically robust and diverse pathogens of the plant kingdom.
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Young, J. M. Pathogenicity and identification of the lilac pathogen, Pseudomonas syringae pv. syringae van Hall 1902. Ann. Appl. Biol. 118, 283–298 (1991).
Hirano, S. S. & Upper, C. D. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64, 624–653 (2000).
Bull, C. T. et al. Comprehensive list of names of plant pathogenic bacteria, 1980–2007. J. Plant Pathol. 92, 551–592 (2010).
McCann, H. C. et al. Genomic analysis of the Kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease. PLoS Pathog. 9, e1003503 (2013).
Mazzaglia, A. et al. Pseudomonas syringae pv. actinidiae (PSA) isolates from recent bacterial canker of kiwifruit outbreaks belong to the same genetic lineage. PLoS ONE 7, e36518 (2012).
Butler, M. I. et al. Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PLoS ONE 8, e57464 (2013).
Xin, X. F. & He, S. Y. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol. 51, 473–498 (2013).
Rouse, D. I., Nordheim, E. V., Hirano, S. S. & Upper, C. D. A model relating the probability of foliar disease incidence to the population frequencies of bacterial plant pathogens. Phytopathology 75, 505–509 (1985).
Lindow, S. E., Arny, D. C. & Upper, C. D. Bacterial ice nucleation: a factor in frost injury to plants. Plant Physiol. 70, 1084–1089 (1982).
Skirvina, R. M. et al. The use of genetically engineered bacteria to control frost on strawberries and potatoes. Whatever happened to all of that research? Sci. Hortic. 84, 179–189 (2000).
Morris, C. E., Monteil, C. L. & Berge, O. The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu. Rev. Phytopathol. 51, 85–104 (2013).
Lindow, S. E. & Brandl, M. T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69, 1875–1883 (2003).
Baltrus, D. A., McCann, H. C. & Guttman, D. S. Evolution, genomics and epidemiology of Pseudomonas syringae: challenges in bacterial molecular plant pathology. Mol. Plant Pathol. 18, 152–168 (2017). This review summarizes the current knowledge of P. syringae species from an ecological, genomic and evolutionary point of view.
Vinatzer, B. A., Monteil, C. L. & Clarke, C. R. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu. Rev. Phytopathol. 52, 19–43 (2014).
Stavrinides, J., McCloskey, J. K. & Ochman, H. Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl. Environ. Microbiol. 75, 2230–2235 (2009).
Dutta, B., Gitaitis, R., Smith, S. & Langston, D. Jr. Interactions of seedborne bacterial pathogens with host and non-host plants in relation to seed infestation and seedling transmission. PLoS ONE 9, e99215 (2014).
Jun, S. R. et al. Diversity of Pseudomonas genomes, including populus-associated isolates, as revealed by comparative genome analysis. Appl. Environ. Microbiol. 82, 375–383 (2015).
Garrido-Sanz, D. et al. Genomic and genetic diversity within the Pseudomonas fluorescens complex. PLoS ONE 11, e0150183 (2016).
Berge, O. et al. A user's guide to a data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLoS ONE 9, e105547 (2014). This paper delineates 13 PGs among the P. syringae species complex and outlines phenotypic traits common among the various PGs.
Adamczyk, L. et al. Directed flow of identified particles in Au+Au collisions at √SNN = 200 GeV at RHIC. Phys. Rev. Lett. 108, 202301 (2012).
Clarke, C. R., Cai, R., Studholme, D. J., Guttman, D. S. & Vinatzer, B. A. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol. Plant Microbe Interact. 23, 198–210 (2010).
Galan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).
Buttner, D. & He, S. Y. Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150, 1656–1664 (2009).
Glickmann, E. et al. Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol. Plant Microbe Interact. 11, 156–162 (1998).
O'Brien, H. E. et al. Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol. 12, 141 (2012). This paper describes the convergent evolution of phylogenetically distant P. syringae strains onto a common host and estimates the time of divergence for the P. syringae LCA.
Bell, C. D., Soltis, D. E. & Soltis, P. S. The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296–1303 (2010).
Bell, C. D., Soltis, D. E. & Soltis, P. S. The age of the angiosperms: a molecular timescale without a clock. Evolution 59, 1245–1258 (2005).
Lindow, S. E. & Leveau, J. H. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13, 238–243 (2002).
Keith, L. M. & Bender, C. L. AlgT (sigma22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J. Bacteriol. 181, 7176–7184 (1999).
Schreiber, K. J. & Desveaux, D. AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol. Microbiol. 80, 364–377 (2011).
Castillo-Lizardo, M. G. et al. Contribution of the non-effector members of the HrpL regulon, iaaL and matE, to the virulence of Pseudomonas syringae pv. tomato DC3000 in tomato plants. BMC Microbiol. 15, 165 (2015).
Baltrus, D. A. et al. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog. 7, e1002132 (2011). This paper describes the diversity and distribution of T3Es and other key virulence factors in a cross-section of 19 P. syringae isolates.
Aragon, I. M., Perez-Martinez, I., Moreno-Perez, A., Cerezo, M. & Ramos, C. New insights into the role of indole-3-acetic acid in the virulence of Pseudomonas savastanoi pv. savastanoi. FEMS Microbiol. Lett. 356, 184–192 (2014).
Araki, H. et al. Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proc. Natl Acad. Sci. USA 103, 5887–5892 (2006).
Godfrey, S. A. et al. The stealth episome: suppression of gene expression on the excised genomic island PPHGI-1 from Pseudomonas syringae pv. phaseolicola. PLoS Pathog. 7, e1002010 (2011).
Kunkeaw, S., Tan, S. & Coaker, G. Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol. Plant Microbe Interact. 23, 415–424 (2010).
Hockett, K. L., Nishimura, M. T., Karlsrud, E., Dougherty, K. & Baltrus, D. A. Pseudomonas syringae CC1557: a highly virulent strain with an unusually small type III effector repertoire that includes a novel effector. Mol. Plant Microbe Interact. 27, 923–932 (2014).
Melotto, M., Underwood, W., Koczan, J., Nomura, K. & He, S. Y. Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969–980 (2006).
Melotto, M., Zhang, L., Oblessuc, P. R. & He, S. Y. Stomatal defense a decade later. Plant Physiol. 174, 561–571 (2017).
Zeng, W., Melotto, M. & He, S. Y. Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr. Opin. Biotechnol. 21, 599–603 (2010).
Melotto, M. et al. A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J. 55, 979–988 (2008).
Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y. & Howe, G. A. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl Acad. Sci. USA 105, 7100–7105 (2008).
Zheng, X. Y. et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587–596 (2012).
Gimenez-Ibanez, S. et al. JAZ2 controls stomata dynamics during bacterial invasion. New Phytol. 213, 1378–1392 (2017).
Du, M. et al. Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26, 3167–3184 (2014). References 43 and 45 show that coronatine activates jasmonate signalling to turn on the expression of specific NAM, ATAF and CUC (NAC) family transcription factors in Arabidopsis and tomato, which are required for coronatine-mediated stomatal opening and/or immune suppression in the apoplast.
Toum, L. et al. Coronatine inhibits stomatal closure through guard cell-specific inhibition of NADPH oxidase-dependent ROS production. Front. Plant Sci. 7, 1851 (2016).
Panchal, S. et al. Coronatine facilitates Pseudomonas syringae infection of Arabidopsis leaves at night. Front. Plant Sci. 7, 880 (2016).
Allu, A. D., Brotman, Y., Xue, G. P. & Balazadeh, S. Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection. EMBO Rep. 17, 1578–1589 (2016).
Gimenez-Ibanez, S. et al. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS Biol. 12, e1001792 (2014).
Jiang, S. et al. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 9, e1003715 (2013).
Yang, L. et al. Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microbe 21, 156–168 (2017). This recent paper describes P. syringae T3E HopBB1 directly interacting with and degrading JAZ proteins, thereby activating jasmonate signalling and promoting disease. This represents one of an increasing number of studies (for examples, see references 49 and 50) showing that, similar to coronatine toxin, T3Es also induce jasmonate signalling.
Lee, D., Bourdais, G., Yu, G., Robatzek, S. & Coaker, G. Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H(+)-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27, 2042–2056 (2015).
Zhou, Z. et al. An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion. Plant Cell 27, 2032–2041 (2015).
Hurley, B. et al. The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. PLoS ONE 9, e114921 (2014).
Lozano-Duran, R., Bourdais, G., He, S. Y. & Robatzek, S. The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol. 202, 259–269 (2014).
Henry, E., Toruno, T. Y., Jauneau, A., Deslandes, L. & Coaker, G. Direct and indirect visualization of bacterial effector delivery into diverse plant cell types during infection. Plant Cell 29, 1555–1570 (2017).
Park, E., Lee, H. Y., Woo, J., Choi, D. & Dinesh-Kumar, S. P. Spatiotemporal monitoring of Pseudomonas syringae effectors via type III secretion using split fluorescent protein fragments. Plant Cell 29, 1571–1584 (2017). References 56 and 57 report an innovative GFP-based fusion approach to monitor type III translocation of P. syringae T3E in vivo.
Jones, J. D., Vance, R. E. & Dangl, J. L. Intracellular innate immune surveillance devices in plants and animals. Science 354, aaf6395 (2016).
Couto, D. & Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16, 537–552 (2016).
Meng, X. & Zhang, S. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51, 245–266 (2013).
Yamada, K., Saijo, Y., Nakagami, H. & Takano, Y. Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science 354, 1427–1430 (2016). This paper provides evidence that activation of PTI involves direct interaction between FLS2, a PRR for bacterial flagellin, and sugar transporter proteins STP1 and STP13, resulting in removal of sugars from the apoplast as a plant defence mechanism.
Mine, A. et al. Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity. Proc. Natl Acad. Sci. USA 114, 7456–7461 (2017).
Hutchison, M. L., Tester, M. A. & Gross, D. C. Role of biosurfactant and ion channel-forming activities of syringomycin in transmembrane ion flux: a model for the mechanism of action in the plant-pathogen interaction. Mol. Plant Microbe Interact. 8, 610–620 (1995).
Vaughn, V. L. & Gross, D. C. Characterization of salA, syrF, and syrG genes and attendant regulatory networks involved in plant pathogenesis by Pseudomonas syringae pv. syringae B728a. PLoS ONE 11, e0150234 (2016).
Bender, C. L., Alarcon-Chaidez, F. & Gross, D. C. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63, 266–292 (1999).
Roine, E. et al. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl Acad. Sci. USA 94, 3459–3464 (1997).
Lindeberg, M., Cunnac, S. & Collmer, A. Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 20, 199–208 (2012).
Cunnac, S. et al. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl Acad. Sci. USA 108, 2975–2980 (2011). This paper describes a minimum repertoire of eight T3Es that can largely rescue the growth defect of an 'effector-less' Pst DC300 strain in N. benthamiana plants.
Toruno, T. Y., Stergiopoulos, I. & Coaker, G. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54, 419–441 (2016).
Macho, A. P. & Zipfel, C. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23, 14–22 (2015).
Dou, D. & Zhou, J. M. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484–495 (2012).
Block, A. & Alfano, J. R. Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Microbiol. 14, 39–46 (2011).
He, P. et al. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563–575 (2006).
Rosebrock, T. R. et al. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448, 370–374 (2007).
Shan, L. et al. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17–27 (2008).
Gimenez-Ibanez, S. et al. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423–429 (2009).
Gohre, V. et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824–1832 (2008).
Zeng, L., Velasquez, A. C., Munkvold, K. R., Zhang, J. & Martin, G. B. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 69, 92–103 (2012).
Wei, H. L. et al. Pseudomonas syringae pv. tomato DC3000 type III secretion effector polymutants reveal an interplay between HopAD1 and AvrPtoB. Cell Host Microbe 17, 752–762 (2015).
Shimono, M. et al. The Pseudomonas syringae type III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection. Plant Physiol. 171, 2239–2255 (2016).
Block, A. et al. The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell. Microbiol. 12, 318–330 (2010).
Guo, M., Kim, P., Li, G., Elowsky, C. G. & Alfano, J. R. A bacterial effector co-opts calmodulin to target the plant microtubule network. Cell Host Microbe 19, 67–78 (2016). This paper describes the T3E HopE1 dampening plant immunity by disrupting the plant microtubule network. HopE1 interacts with a microtubule-associated protein (MAP65) and causes its dissociation from microtubules.
Rodriguez-Herva, J. J. et al. A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cell. Microbiol. 14, 669–681 (2012).
Goel, A. K. et al. The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol. Plant Microbe Interact. 21, 361–370 (2008).
Hauck, P., Thilmony, R. & He, S. Y. A. Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl Acad. Sci. USA 100, 8577–8582 (2003).
Jakobek, J. L., Smith, J. A. & Lindgren, P. B. Suppression of bean defense responses by Pseudomonas syringae. Plant Cell 5, 57–63 (1993).
Jin, L. et al. Direct and indirect targeting of PP2A by conserved bacterial type-III effector proteins. PLoS Pathog. 12, e1005609 (2016).
DebRoy, S., Thilmony, R., Kwack, Y. B., Nomura, K. & He, S. Y. A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc. Natl Acad. Sci. USA 101, 9927–9932 (2004).
Xin, X. F. et al. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539, 524–529 (2016). This paper shows that two highly conserved T3Es, HopM1 and AvrE, induce aqueous apoplast during P. syringae infection as a critical virulence mechanism. This study also provides insight into the high-humidity dependence of P. syringae infection, consistent with the 'disease triangle' concept.
Nomura, K. et al. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313, 220–223 (2006).
Wright, C. A. & Beattie, G. A. Pseudomonas syringae pv. tomato cells encounter inhibitory levels of water stress during the hypersensitive response of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 101, 3269–3274 (2004).
Oh, H. S. & Collmer, A. Basal resistance against bacteria in Nicotiana benthamiana leaves is accompanied by reduced vascular staining and suppressed by multiple Pseudomonas syringae type III secretion system effector proteins. Plant J. 44, 348–359 (2005).
Freeman, B. C. & Beattie, G. A. Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Mol. Plant Microbe Interact. 22, 857–867 (2009).
Stevens, R. B. in Plant Pathology, An Advanced Treatise (ed. Horsfall, J. G. ) 357–429 (Academic Press, New York, 1960).
Hacquard, S., Spaepen, S., Garrido-Oter, R. & Schulze-Lefert, P. Interplay between innate immunity and the plant microbiota. Annu. Rev. Phytopathol. 55, 565–589 (2017).
Lindemann, J., Arny, D. C. & Upper, C. D. Epiphytic populations of Pseudomonas syringae pv. syringae on snap bean and nonhost plants and the incidence of bacterial brown spot disease in relation to cropping patterns. Phytopathology 74, 1329–1333 (1984).
Hirano, S. S. & Upper, C. D. Population biology and epidemiology of Pseudomonas syringae. Annu. Rev. Phytopathol. 28, 155–177 (1990).
Yu, J., Penaloza-Vazquez, A., Chakrabarty, A. M. & Bender, C. L. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 33, 712–720 (1999).
Burch, A. Y., Zeisler, V., Yokota, K., Schreiber, L. & Lindow, S. E. The hygroscopic biosurfactant syringafactin produced by Pseudomonas syringae enhances fitness on leaf surfaces during fluctuating humidity. Environ. Microbiol. 16, 2086–2098 (2014).
Monier, J. M. & Lindow, S. E. Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl. Environ. Microbiol. 70, 346–355 (2004).
Dechesne, A. & Smets, B. F. Pseudomonad swarming motility is restricted to a narrow range of high matric water potentials. Appl. Environ. Microbiol. 78, 2936–2940 (2012).
Bjorklof, K., Nurmiaho-Lassila, E. L., Klinger, N., Haahtela, K. & Romantschuk, M. Colonization strategies and conjugal gene transfer of inoculated Pseudomonas syringae on the leaf surface. J. Appl. Microbiol. 89, 423–432 (2000).
Panchal, S. et al. Regulation of stomatal defense by air relative humidity. Plant Physiol. 172, 2021–2032 (2016).
Smirnova, A. et al. Thermoregulated expression of virulence factors in plant-associated bacteria. Arch. Microbiol. 176, 393–399 (2001).
Palmer, D. A. & Bender, C. L. Effects of environmental and nutritional factors on production of the polyketide phytotoxin coronatine by Pseudomonas syringae pv. glycinea. Appl. Environ. Microbiol. 59, 1619–1626 (1993).
Weingart, H., Stubner, S., Schenk, A. & Ullrich, M. S. Impact of temperature on in planta expression of genes involved in synthesis of the Pseudomonas syringae phytotoxin coronatine. Mol. Plant Microbe Interact. 17, 1095–1102 (2004).
Rowley, K. B., Clements, D. E., Mandel, M., Humphreys, T. & Patil, S. S. Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production. Mol. Microbiol. 8, 625–635 (1993).
Hockett, K. L., Burch, A. Y. & Lindow, S. E. Thermo-regulation of genes mediating motility and plant interactions in Pseudomonas syringae. PLoS ONE 8, e59850 (2013).
Li, H., Schenk, A., Srivastava, A., Zhurina, D. & Ullrich, M. S. Thermo-responsive expression and differential secretion of the extracellular enzyme levansucrase in the plant pathogenic bacterium Pseudomonas syringae pv. glycinea. FEMS Microbiol. Lett. 265, 178–185 (2006).
van Dijk, K. et al. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J. Bacteriol. 181, 4790–4797 (1999).
Wang, Y., Bao, Z., Zhu, Y. & Hua, J. Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant Microbe Interact. 22, 498–506 (2009).
Huot, B. et al. Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat. Commun. 8, 1808 (2017).
Menna, A., Nguyen, D., Guttman, D. S. & Desveaux, D. Elevated temperature differentially influences effector-triggered immunity outputs in Arabidopsis. Front. Plant Sci. 6, 995 (2015).
Kim, Y. S. et al. CAMTA-mediated regulation of salicylic acid immunity pathway genes in Arabidopsis exposed to low temperature and pathogen infection. Plant Cell 29, 2465–2477 (2017).
Cheng, C. et al. Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4, 2530 (2013). This paper shows that two major branches of plant immunity, PTI and ETI, respond to changing temperatures in distinct ways and suggests interesting interplays between plant immunity, temperature and pathogen physiology.
Frampton, R. A. et al. Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Appl. Environ. Microbiol. 80, 2216–2228 (2014).
Andreote, F. D. et al. Endophytic colonization of potato (Solanum tuberosum L.) by a novel competent bacterial endophyte. Pseudomonas putida strain P9, and its effect on associated bacterial communities. Appl. Environ. Microbiol. 75, 3396–3406 (2009).
Bais, H. P., Fall, R. & Vivanco, J. M. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134, 307–319 (2004).
Raaijmakers, J. M. & Mazzola, M. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50, 403–424 (2012).
Grosskinsky, D. K. et al. Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci. Rep. 6, 23310 (2016).
Yedidia, I. et al. Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl. Environ. Microbiol. 69, 7343–7353 (2003).
Wilson, M. & Lindow, S. E. Release of recombinant microorganisms. Annu. Rev. Microbiol. 47, 913–944 (1993).
Wensing, A. et al. Impact of siderophore production by Pseudomonas syringae pv. syringae 22d/93 on epiphytic fitness and biocontrol activity against Pseudomonas syringae pv. glycinea 1a/96. Appl. Environ. Microbiol. 76, 2704–2711 (2010).
Dulla, G. F., Krasileva, K. V. & Lindow, S. E. Interference of quorum sensing in Pseudomonas syringae by bacterial epiphytes that limit iron availability. Environ. Microbiol. 12, 1762–1774 (2010).
Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).
Muller, D. B., Vogel, C., Bai, Y. & Vorholt, J. A. The Plant microbiota: systems-level insights and perspectives. Annu. Rev. Genet. 50, 211–234 (2016).
Islam, M. T. et al. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 14, 84 (2016).
Agrios, G. N. Plant Pathology 5th edn (Academic Press, 2005).
Ham, J. H., Majerczak, D. R., Arroyo-Rodriguez, A. S., Mackey, D. M. & Coplin, D. L. WtsE, an AvrE-family effector protein from Pantoea stewartii subsp. stewartii, causes disease-associated cell death in corn and requires a chaperone protein for stability. Mol. Plant Microbe Interact. 19, 1092–1102 (2006).
Asselin, J. E. et al. Perturbation of maize phenylpropanoid metabolism by an AvrE family type III effector from Pantoea stewartii. Plant Physiol. 167, 1117–1135 (2015).
Schwartz, A. R., Morbitzer, R., Lahaye, T. & Staskawicz, B. J. TALE-induced bHLH transcription factors that activate a pectate lyase contribute to water soaking in bacterial spot of tomato. Proc. Natl Acad. Sci. USA 114, E897–E903 (2017). This paper reports that a T3E from X. gardneri induces strong water soaking in plant leaves and does so by activating plant cell-wall-modifying enzymes.
Cox, K. L. et al. TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton. Nat. Commun. 8, 15588 (2017).
Cohn, M. et al. Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol. Plant Microbe Interact. 27, 1186–1198 (2014).
Lindeberg, M. et al. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol. Plant Microbe Interact. 19, 1151–1158 (2006).
Alfano, J. R. et al. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl Acad. Sci. USA 97, 4856–4861 (2000).
Deng, W. L., Rehm, A. H., Charkowski, A. O., Rojas, C. M. & Collmer, A. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J. Bacteriol. 185, 2592–2602 (2003).
Gazi, A. D. et al. Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol. 12, 188 (2012).
Lan, L., Deng, X., Zhou, J. & Tang, X. Genome-wide gene expression analysis of Pseudomonas syringae pv. tomato DC3000 reveals overlapping and distinct pathways regulated by hrpL and hrpRS. Mol. Plant Microbe Interact. 19, 976–987 (2006).
Jovanovic, M. et al. Regulation of the co-evolved HrpR and HrpS AAA+ proteins required for Pseudomonas syringae pathogenicity. Nat. Commun. 2, 177 (2011).
Brencic, A. & Winans, S. C. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69, 155–194 (2005).
Bartoli, C. et al. The Pseudomonas viridiflava phylogroups in the P. syringae species complex are characterized by genetic variability and phenotypic plasticity of pathogenicity-related traits. Environ. Microbiol. 16, 2301–2315 (2014). This paper explores the mutual exclusivity and variation in genetic architecture of the T-PAI and S-PAI among P. viridiflava PGs.
Guttman, D. S., Gropp, S. J., Morgan, R. L. & Wang, P. W. Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol. Biol. Evol. 23, 2342–2354 (2006).
Tegli, S., Gori, A., Cerboneschi, M., Cipriani, M. G. & Sisto, A. Type three secretion system in Pseudomonas savastanoi pathovars: does timing matter? Genes 2, 957–979 (2011).
Monteil, C. L. et al. Population-genomic insights into emergence, crop adaptation and dissemination of Pseudomonas syringae pathogens. Microb. Genom. 2, e000089 (2016).
Munkvold, K. R., Russell, A. B., Kvitko, B. H. & Collmer, A. Pseudomonas syringae pv. tomato DC3000 type III effector HopAA1-1 functions redundantly with chlorosis-promoting factor PSPTO4723 to produce bacterial speck lesions in host tomato. Mol. Plant Microbe Interact. 22, 1341–1355 (2009).
Charity, J. C., Pak, K., Delwiche, C. F. & Hutcheson, S. W. Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: evidence for integron-like assembly from transposed gene cassettes. Mol. Plant Microbe Interact. 16, 495–507 (2003).
Xiang, T. et al. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18, 74–80 (2008).
Xiang, T. et al. BAK1 is not a target of the Pseudomonas syringae effector AvrPto. Mol. Plant Microbe Interact. 24, 100–107 (2011).
Cheng, W. et al. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III Effector. Cell Host Microbe 10, 616–626 (2011).
Li, L. et al. Activation-dependent destruction of a co-receptor by a Pseudomonas syringae effector dampens plant immunity. Cell Host Microbe 20, 504–514 (2016).
Zhang, J. et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7, 290–301 (2010).
Wu, S. et al. Bacterial effector HopF2 suppresses arabidopsis innate immunity at the plasma membrane. Mol. Plant Microbe Interact. 24, 585–593 (2011).
Wang, Y. et al. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22, 2033–2044 (2010).
Zhou, J. et al. The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Plant J. 77, 235–245 (2013).
Zhang, J. et al. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175–185 (2007).
Zhang, Z. et al. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253–263 (2012).
Eschen-Lippold, L. et al. Bacterial AvrRpt2-like cysteine proteases block activation of the Arabidopsis mitogen-activated protein kinases, MPK4 and MPK11. Plant Physiol. 171, 2223–2238 (2016).
Sarris, P. F. et al. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161, 1089–1100 (2015).
Le Roux, C. et al. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161, 1074–1088 (2015). References 158 and 159 show that P. syringae T3E AvrRps4 and Ralstonia solanacearum T3E Pop2 target plant immunity-associated WRKY transcription factors to dampen PTI.
Block, A. et al. The Pseudomonas syringae type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9. New Phytol. 201, 1358–1370 (2014).
Cui, H. et al. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7, 164–175 (2010).
Chen, Z. et al. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl Acad. Sci. USA 104, 20131–20136 (2007).
Cui, F. et al. The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover. Plant Physiol. 162, 1018–1029 (2013).
de Torres-Zabala, M. et al. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26, 1434–1443 (2007).
Hann, D. R. et al. The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol. 201, 585–598 (2014).
Washington, E. J. et al. Pseudomonas syringae type III effector HopAF1 suppresses plant immunity by targeting methionine recycling to block ethylene induction. Proc. Natl Acad. Sci. USA 113, E3577–E3586 (2016).
Jelenska, J., van Hal, J. A. & Greenberg, J. T. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc. Natl Acad. Sci. USA 107, 13177–13182 (2010).
Jelenska, J. et al. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17, 499–508 (2007).
Kang, Y. et al. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog. 10, e1004232 (2014).
Lee, A. H. et al. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS Pathog. 8, e1002523 (2012).
Li, G. et al. Distinct Pseudomonas type-III effectors use a cleavable transit peptide to target chloroplasts. Plant J. 77, 310–321 (2014).
Kim, M. G. et al. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121, 749–759 (2005).
Axtell, M. J. & Staskawicz, B. J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369–377 (2003).
Mackey, D., Holt, B. F. 3rd, Wiig, A. & Dangl, J. L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002).
Luo, Y., Caldwell, K. S., Wroblewski, T., Wright, M. E. & Michelmore, R. W. Proteolysis of a negative regulator of innate immunity is dependent on resistance genes in tomato and Nicotiana benthamiana and induced by multiple bacterial effectors. Plant Cell 21, 2458–2472 (2009).
Wilton, M. et al. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc. Natl Acad. Sci. USA 107, 2349–2354 (2010).
Bhattacharjee, S., Halane, M. K., Kim, S. H. & Gassmann, W. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334, 1405–1408 (2011).
Heidrich, K. et al. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334, 1401–1404 (2011).
Fu, Z. Q. et al. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284–288 (2007).
Nicaise, V. et al. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32, 701–712 (2013).
Zhou, H. et al. Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host Microbe 9, 177–186 (2011).
Ustun, S., Konig, P., Guttman, D. S. & Bornke, F. HopZ4 from Pseudomonas syringae, a member of the HopZ type III effector family from the YopJ superfamily, inhibits the proteasome in plants. Mol. Plant Microbe Interact. 27, 611–623 (2014).
Ustun, S. et al. The Proteasome acts as a hub for plant immunity and is targeted by Pseudomonas type III effectors. Plant Physiol. 172, 1941–1958 (2016).
This work was supported by grants from the Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Science, Chinese Academy of Sciences (X.-F.X.), the National Key Laboratory of Plant Molecular Genetics, China (X.-F.X.), the US National Institute of Food and Agriculture (NIFA) HATCH (Project: GEO00791 (B.K.)), the State of Georgia (B.K.), the Gordon and Betty Moore Foundation (GBMF3037 (S.Y.H.)), the US National Institute of General Medical Sciences (GM109928 (S.Y.H.)) and the US Department of Agriculture — NIFA (2015-67017-23360 and 2017-67017-26180 (S.Y.H)). The authors thank colleagues K. Aung and C. D. M. Castroverde at Michigan State University for comments on this manuscript and D. Baltrus at the University of Arizona for helpful discussions.
The authors declare no competing financial interests.
A bacterial strain or set of strains with the same or similar characteristics that is differentiated from other strains of the same species or subspecies on the basis of distinctive pathogenicity to one or more plant hosts.
- Endophytic phase
The life cycle phase when a microorganism lives within a plant.
(PGs). A phylogenetically related group of organisms. In the Pseudomonas syringae species complex, phylogroups have been delineated on the basis of genetic distance of less than 5% in conserved housekeeping genes.
- Multilocus sequence analysis
(MLSA). A technique to determine genetic relatedness and predict phylogeny on the basis of the analysis of concatenated sequences of multiple housekeeping genes. MLSA can be used to determine phylogenetic relationships within a closely related group of organisms.
- Rarefaction curve
A tool used to estimate genetic diversity. Rarefaction curves plot total 'genetic units' against the number of individuals analysed. The genetic unit can be set to different thresholds from SNP to species. As the curve flattens, predictions can be made about the extent of genetic diversity yet to be identified at the particular measured threshold.
A phenotypic scheme developed to distinguish species of phytopathogenic fluorescent pseudomonads. Canonical Pseudomonas syringae are positive for levan (L), negative for cytochrome C oxidase (O), negative for potato soft rot (P), negative for arginine dihydrolase (A) and positive for the hypersensitive response on tobacco (T).
- Type III secretion system
(T3SS). A proteinaceous supramolecular complex produced by many Gram-negative bacteria infecting plants or animals. It functions as a syringe-like structure and delivers virulence proteins, called T3SS effectors (T3Es), into the host cell and has essential roles in bacterial virulence.
- Hypersensitive response
A programmed cell death response of plants, mediated by recognition of pathogen effectors by the corresponding plant resistance proteins and activation of effector-triggered immunity (ETI).
Mutations in hrp genes lead to the loss of the host hypersensitive response in resistant plants and the loss of pathogenic potential in susceptible host plants. A subset of hrp genes were subsequently renamed to hrc (hrp conserved) genes on the basis of conservation with Yersinia spp. type III secretion system (T3SS) genes. Many of the hrp–hrc genes encode structural components of theT3SS.
(EPS). High-molecular-mass polymers that are composed of sugar residues and are secreted by a microorganism into the surrounding environment.
- T3SS effector
(T3E). Virulence proteins that are produced in many Gram-negative bacterial pathogens and delivered into the plant cell via the type III secretion system (T3SS). T3Es manipulate various plant processes to promote infection.
A toxin produced by Pseudomonas syringae; its chemical structure consists of two moieties — coronafacic acid and coronamic acid.
A class of lipodepsinonapeptide molecules that are secreted by Pseudomonas syringae. Syringomycins are virulence determinants required for the manifestation of disease symptoms in a number of plants.
Microscopic pores found in the epidermis of leaves, stems and other plant organs that facilitate gas exchange. Pores are bordered by specialized epidermal cells known as guard cells that are responsible for regulating the size of the stomatal opening.
- Pathogen-associated molecular patterns
(PAMPs). Also known as microorganism-associated molecular pattern (MAMPs). These are conserved microbial molecular structures and can elicit immune responses in the host.
- Guard cell
A specialized epidermal cell that surrounds the stomatal pore and enables it to open and close.
- Pattern-triggered immunity
(PTI). A branch of plant innate immunity, sometimes referred to as basal defence. PTI signalling is initiated by recognition of conserved microbial structures by plant membrane-localized receptors and transduced by downstream components, including the MAP kinase cascade and WRKY transcription factors, and finally leads to expression of plant immunity genes.
- Salicylic acid
A phenolic plant defence hormone that mediates plant defence against infections by biotrophic and hemibiotrophic pathogens.
- Abscisic acid
An isoprenoid plant stress hormone that functions in plant developmental processes such as seed dormancy and mediates plant response to water desiccation.
A lipid-based plant hormone that mediates plant defence against attacks by herbivory and necrotrophic pathogens as well as regulating plant growth and development.
- Mesophyll cells
Cells located between the upper and lower epidermis in the plant leaf; the primary cell type for photosynthesis in the plant.
- Effector-triggered immunity
(ETI). Another branch of plant innate immunity, formerly called 'gene-for-gene' resistance. It is triggered by recognition of specific type III secretion system effector (T3E) proteins by the corresponding plant resistance proteins through direct or indirect interaction. ETI evokes strong plant immune responses that often culminate in programmed cell death (that is, the hypersensitive response).
- Induced systemic resistance
(ISR). An important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the entire plant body for enhanced defence against a broad range of pathogens and insect herbivores.
A distinct phylogenetic lineage of eukaryotic microorganisms. Oomycetes include some of the most notorious pathogens of plants, causing devastating diseases such as late blight of potato and sudden oak death.
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Xin, XF., Kvitko, B. & He, S. Pseudomonas syringae: what it takes to be a pathogen. Nat Rev Microbiol 16, 316–328 (2018). https://doi.org/10.1038/nrmicro.2018.17
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