Abstract
The study of host range determinants within the Pseudomonas syringae complex is gaining renewed attention due to its widespread distribution in non-agricultural environments, evidence of large variability in intra-pathovar host range, and the emergence of new epidemic diseases. This requires the establishment of appropriate model pathosystems facilitating integration of phenotypic, genomic and evolutionary data. Pseudomonas savastanoi pv. savastanoi is a model pathogen of the olive tree, and here we report a closed genome of strain NCPPB 3335, plus draft genome sequences of three strains isolated from oleander (pv. nerii), ash (pv. fraxini) and broom plants (pv. retacarpa). We then conducted a comparative genomic analysis of these four new genomes plus 16 publicly available genomes, representing 20 strains of these four P. savastanoi pathovars of woody hosts. Despite overlapping host ranges, cross-pathogenicity tests using four plant hosts clearly separated these pathovars and lead to pathovar reassignment of two strains. Critically, these functional assays were pivotal to reconcile phylogeny with host range and to define pathovar-specific genes repertoires. We report a pan-genome of 7,953 ortholog gene families and a total of 45 type III secretion system effector genes, including 24 core genes, four genes exclusive of pv. retacarpa and several genes encoding pathovar-specific truncations. Noticeably, the four pathovars corresponded with well-defined genetic lineages, with core genome phylogeny and hierarchical clustering of effector genes closely correlating with pathogenic specialization. Knot-inducing pathovars encode genes absent in the canker-inducing pv. fraxini, such as those related to indole acetic acid, cytokinins, rhizobitoxine, and a bacteriophytochrome. Other pathovar-exclusive genes encode type I, type II, type IV, and type VI secretion system proteins, the phytotoxine phevamine A, a siderophore, c-di-GMP-related proteins, methyl chemotaxis proteins, and a broad collection of transcriptional regulators and transporters of eight different superfamilies. Our combination of pathogenicity analyses and genomics tools allowed us to correctly assign strains to pathovars and to propose a repertoire of host range-related genes in the P. syringae complex.
Highlights
The Pseudomonas syringae species complex is considered the most relevant phytopathogenic bacterium worldwide, as a prominent research model and as an economically important phytopathogen (Mansfield et al, 2012)
To use this genome as a reference in this and future comparative genomic analyses, we obtained the complete sequence of the pv. savastanoi (Psv) NCPPB 3335 chromosome
Genomics-based methods offer unprecedented resolution to analyze strain diversity and evolutionary relationships within the P. syringae complex, besides identifying candidate genes involved in pathogenicity and host range definition (Lindeberg et al, 2009; Baltrus et al, 2011; Bartoli et al, 2015; Monteil et al, 2016; Baltrus et al, 2017; Dillon et al, 2019a; Dillon et al, 2019b)
Summary
The Pseudomonas syringae species complex is considered the most relevant phytopathogenic bacterium worldwide, as a prominent research model and as an economically important phytopathogen (Mansfield et al, 2012) It comprises at least 13 phylogroups (PGs) encompassing 15 different Pseudomonas species associated with plants and the water cycle (Berge et al, 2014; Gomila et al, 2017). A recent study showed that P. syringae strains form an overlapping continuum of host range potential and that pathovar denominations do not correspond to the P. syringae biology (Morris et al, 2019). Understanding this complexity at the different levels requires the establishment of appropriate pathosystems, facilitating integration of phenotypic, genomic, and evolutionary data. The P. syringae complex emerged as one of the most relevant models to study host specificity in bacterial phytopathogens (Vinatzer et al, 2014; Baltrus et al, 2017; Dillon et al, 2019b)
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