An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen Erwinia tracheiphila

Abstract

<i>Erwinia tracheiphila</i> is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting an economically important phytopathogen affecting few cultivated Cucurbitaceae few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about <i>E. tracheiphila</i> population structure or genetic diversity. To address this shortcoming, a representative collection of 88 <i>E. tracheiphila</i> isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct <i>hrp</i>T3SS virulence gene repertoires, host plant association patterns, and geographic distributions. Low genetic heterogeneity within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber (<i>Cucumis sativus</i>), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible <i>C. sativus</i> in temperate eastern North America may have facilitated the original emergence of <i>E. tracheiphila</i> into cucurbit agroecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification, and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens.<b>IMPORTANCE</b><i>Erwinia tracheiphila</i> is a virulent phytopathogen that infects two genera of cucurbit crop plants, <i>Cucurbita</i> spp. (pumpkin and squash) and <i>Cucumis</i> spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an <i>E. tracheiphila</i> isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced <i>Cucumis</i> spp. crop plants are driving the diversification of <i>E. tracheiphila</i> into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.