Pseudomonas syringae: what it takes to be a pathogen

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.

Figure 1. The phylogeny of P. syringae and common phylogroup features

On the left, proposed phylogenetic branching order for major species groups within the P. fluorescens-like major branch of Pseudomonas^, . On the right, thirteen identified phylogroups (PGs) in the P. syringae species complex, based on multi-locus sequence analysis (MLSA). Phylogroups representing monophyletic species within the complex are noted. Characteristic PG members are listed along with general phylogroup-associated features when known. S-PAI, single-part pathogenicity islands lack a canonical CEL but may carry CEL T3SS effectors within the hrp/hrc cluster. IaaL, presence of the indole acetic acid lysine synthetase gene for the inactivation of auxin. Hab, common habitat, strains are isolated mostly from plants (P) or the environment (E), or both/ubiquitous (U). INA, reported ice nucleation capacity or the presence of the inaW ice-nucleation gene. IaaL, Hab and INA traits vary on a strain-to-strain basis. *, PG 2 clade c and PG 13 have A-typical S-PAIs (A-PAI) with distinct genomic locations.

Figure 2. Potential steps to patho-adaptation in P. syringae evolution

Hypothesized ancestry of important traits in the P. syringae species complex. The S-PAI encodes AvrE and/or HopM effectors associated with apoplast water-soaking. T-PAI effector loci genes are associated with JA manipulation and defense suppression in addition to apoplast water-soaking. In addition to trait name abbreviations in Figure 1, Alg, genes for the regulation and production of alginate. iaaM/iaaH, genes for auxin synthesis, Pel, pectate lyase. T3Es, expansion and diversification of T3E repertoires. Tox, toxin packages of broad-host-range pathogens.

Figure 3. Battle during bacterial entry

Upper panel, P. syringae bacteria enter a section of a plant leaf through natural opening stomata. Lower panel, perception of bacterial PAMPs stimulates PAMP immune signaling in a stomatal guard cell leading to SA signaling and eventual stomatal closure; P. syringae phytotoxin coronatine and several T3Es (i.e. AvrB, HopBB1, HopX1 and HopZ1a) target the COI1 receptor or JAZ transcriptional repressors to activate JA signaling. Activation of JA signaling leads to modulation of the expression of ANAC transcription factors and ICS1 and BSMT1, which are involved in SA biosynthesis and metabolism, respectively, resulting in lowered SA accumulation and inhibition of PAMP-triggered stomatal closure.

Figure 4. Battle inside the leaf apoplast after bacterial entry

a. A diagram depicting the host targets of eight “core” T3Es in a susceptible Arabidopsis cell. AvrPtoB targets PRR complex to inhibit PTI. HopG1 and HopE1 target actin and microtubule networks through interaction with kinesin and MAP65, respectively. HopAM1 induces ABA hypersensitivity in the plant and enhances virulence on drought-condition plants, and HopN1 targets the chloroplast protein PsbQ. These five T3Es appear to be primarily involved in suppression of host immunity responses. Two conserved T3Es, HopM1 and AvrE, induce an aqueous apoplast. HopM1 targets a trans-Golgi network (TGN)/early endosome (EE)-localized ARF guanine exchange factor, MIN7, and AvrE interacts with protein phosphatase 2A (PP2A). The host target of HopAA1 (not shown) is not known. b. A conceptual model illustrating two basic aspects of host biology perturbed by P. syringae post epiphytic growth. Suppression of plant immunity and creation of an aqueous apoplast are two principal features of P. syringae infection in the leaf.

Figure 5. Interactions between plant, P. syringae and abiotic and biotic environment

a. A diagram illustrating the plant-pathogen-environment triangular interactions formally known as the “disease triangle”. b–d. Effects of temperature (b), humidity (c) and the microbiome (d) on P. syringae, the plant and disease outcome. Normal arrows indicate positive effects and block arrows indicate negative effects.