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Pseudomonas syringae: what it takes to be a pathogen

Nature Reviews Microbiology volume 16, pages 316–328 (2018)Cite this article

Subjects

Key Points

  • 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.

Abstract

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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Figure 1: The phylogeny of Pseudomonas syringae and common features of phylogroups.
Figure 2: Pseudomonas syringae evolution and steps towards pathoadaptation.
Figure 3: Entry of Pseudomonas syringae into leaves and overcoming stomatal closure.
Figure 4: Pseudomonas syringae immune evasion and water soaking inside leaves.
Figure 5: Interactions between Pseudomonas syringae, plants and the abiotic and biotic environment.

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Acknowledgements

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.

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Authors and Affiliations

  1. Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Science and Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS) and CAS John Innes Centre of Excellence for Plant and Microbial Sciences, Shanghai, China

    Xiu-Fang Xin

  2. Department of Plant Pathology, University of Georgia, Athens, GA, USA

    Brian Kvitko

  3. Department of Energy Plant Research Laboratory, Department of Plant Biology, Plant Resilience Institute and Howard Hughes Medical Institute, Michigan State University, East Lansing, MI, USA

    Sheng Yang He

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  1. Xiu-Fang Xin
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X.-F.X. and B.K. researched data for the article. X.-F.X., B.K. and S.Y.H. substantially contributed to discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Xiu-Fang Xin or Sheng Yang He.

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Glossary

Pathovars

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.

Phylogroups

(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.

LOPAT

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).

hrp–hrc

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.

Exopolysaccharide

(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.

Coronatine

A toxin produced by Pseudomonas syringae; its chemical structure consists of two moieties — coronafacic acid and coronamic acid.

Syringomycin

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.

Stomata

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.

Jasmonate

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.

Oomycete

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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