The overlapping continuum of host range among strains in the Pseudomonas syringae complex

Abstract

Pseudomonas syringae is the most frequently emerging group of plant pathogenic bacteria. Because this bacterium is ubiquitous as an epiphyte and on various substrates in non-agricultural settings, there are many questions about how to assess the risk for plant disease posed by strains in the environment. Although P. syringae is considered to have discrete host ranges in defined pathovars, there have been few reports of comprehensive comparisons of host range potential. Here we present results of host range tests for 134 strains, representing eight phylogroups, from epidemics and environmental reservoirs on 15 to 22 plant species per test conducted in four separate tests to determine the patterns and extent of host range. We sought to identify trends that are indicative of distinct pathotypes and to assess if strains in the P. syringae complex are indeed restricted in their host range. We show that for each test, strains display a diversity of host ranges from very restricted to very broad regardless of the gamut of phylogroups used in the test. Overall, strains form an overlapping continuum of host range potential with equal representation of narrow, moderate and broad host ranges. Groups of distinct pathotypes, including strains with currently the same pathovar name, could not be identified. The absence of groupings was validated with statistical tests for pattern recognition. The extent of host range was positively correlated with the capacity of strains to swarm on semi-solid agar medium and with the abundance of genes in biosynthetic clusters and was inversely correlated with the abundance of genes for proteins with transmembrane domains in their genomes. Our results are consistent with the current paradigm that disease symptoms are the result of multiple molecular interactions between P. syringae and its plant host that are modulated by abiotic and biotic conditions. This leads us to propose that pathovar denominations do not correspond to the underlying biology of P. syringae. A new concept of pathogenicity that accounts for the continuum of pathogenic potential in P. syringae would open new perspectives to understand the evolution of pathogenicity in this bacterium and new insights to anticipate disease and to manage plant health.

Differential virulence contributions of the efflux transporter MexAB-OprM inPseudomonas syringaeinfecting a variety of host plants

“…Considering the relatively low population sizes that were achieved in several of these species it is not surprising that symptoms were not seen in this study nor have they been typically seen under field conditions. These results however do add to the growing perspective that not all strains of P. syringae , and perhaps other plant pathogenic bacteria, are as host-specific as once thought (Morris et al 2019).…”

“…It is possible that some of the hosts tested here, such as tomato, in which mexB appears dispensable, are simply producing one or more synergistically acting efflux pump inhibitors. This has been seen in barberry ( Berberis) species, which produce the alkaloid berberine as well as the multidrug inhibitor 5’-methoxyhydnocarpin (Morris et al 2019). In addition, we observed substantial variation in the amount of bacterial growth in the apoplast of the plants tested here, with some plant species such as N. benthamiana supporting more than 10,000-fold more multiplication than in species such as V. faba or B. nigra (Fig.…”

“…P. syringae pv. syringae B728a (B728a) is pathogenic to common bean ( Phaseolus vulgaris ) and Nicotiana benthamiana (Vinatzer et al 2006), and was recently reported to cause disease symptoms on pepper ( Capsicum annuum ) (Morris et al 2019). Strain B728a has also been reported to be a poor colonizer of tomato ( Solanum lycopersicum ) (Lin and Martin 2007).…”

“…Most previous attention to the process of infection has focused on particular model plants that interact with a given pathogen. Many plant pathogenic bacteria, particularly those in P. syringae phylogroup 2, are now recognized to have relatively broad host ranges (Morris et al 2019), and yet it remains unclear to what extent a given virulence factor such as an efflux transporter would contribute to virulence on plants that would be expected to differ substantially in their chemical defenses. In this study, we will address the extent to which a given P. syringae strain is a promiscuous colonizer of a variety of plants and the relative importance of MexAB-OprM to its virulence on these hosts.…”

Genome-wide identification ofPseudomonas syringaegenes required for competitive fitness during colonization of the leaf surface and apoplast

“…In addition, phylogroup II contains many strains with broad host ranges (19). Strain B728a is also pathogenic on Nicotiana benthamiana (20) and pepper ( Capsicum annuum ) (21). Like other ice nucleation active strains of P. syringae , this strain contributes to frost damage in frost sensitive plant species by limiting their ability to supercool and avoid damaging ice formation (22).…”