Characterization of <i>Pseudomonas alliivorans</i> strains isolated from Georgia, USA: insights into genomic diversity and pathogenicity in onions

<i>Pseudomonas alliivorans</i> is an important emerging pathogen affecting numerous crops. The species is closely related to <i>Pseudomonas viridiflava,</i> with which <i>P. alliivorans</i> strains were often misidentified in the past. Here, we investigated the genetic and pathogenic characteristics of <i>P. alliivorans</i> strains isolated primarily from onions and weeds in Georgia, USA, using whole-genome sequencing, comparative genomics, and functional assays. We delineated the core genome and genetic diversity of these isolates, assessed their pathogenicity on onion foliage and red onion scales, and examined the roles of key virulence determinants (Hrp1-type III secretion system [T3SS], rhizobium-T3SS, type II secretion systems [T2SSs], and thiosulfinate [allicin]-tolerance <i>alt</i> cluster). Our results showed that the Hrp1-T3SS is pivotal for pathogenicity in <i>P. alliivorans</i>, whereas the rhizobium-T3SS, T2SSs, and <i>alt</i> cluster do not contribute to symptom development on red onion scales. Notably, the <i>alt</i> cluster confers <i>in vitro</i> thiosulfinate tolerance, supporting bacterial survival against onion-derived antimicrobial compounds. Additionally, homologous recombination in <i>P. alliivorans</i> occurs infrequently (at approximately one-tenth the rate of point mutations) and involves divergent DNA segments. The <i>alt</i> cluster is acquired through horizontal gene transfer, as evidenced by its lower GC content and the presence of adjacent transposases. In summary, our research provides valuable insights into the genetic diversity, evolutionary dynamics, and virulence mechanisms of <i>P. alliivorans</i> strains from Georgia, USA.IMPORTANCE<i>Pseudomonas alliivorans</i> is an emerging plant pathogen that threatens onion and other plants of economic importance. This study identifies key traits that help this bacterium cause disease, such as a specific secretion system critical for infecting onions, and a gene cluster that aids bacterial survival in onion tissues. Beyond highlighting weed as a potential inoculum source and supporting better weed management, the findings of this research open avenues for more targeted disease menegement. By unraveling the genetics of this pathogen, we can develop improved ways to detect, prevent, and reduce its impact, protecting crop health and yields.