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Title: Horizontal gene acquisitions, mobile element proliferation, and genome decay in the host-restricted plant pathogen erwinia tracheiphila

Author
item SHAPIRO, LORI - Harvard University
item Scully, Erin
item STRAUB, TIMOTHY - Dartmouth College
item PARK, JIHY - Massachusetts General Hospital
item STEPHENSON, ANDREW - Pennsylvania State University
item BEATTIE, GWYN - Iowa State University
item GLEASON, MARK - Iowa State University
item KOLTER, ROBERTO - Harvard University
item COELHO, MIGUEL - Harvard University
item DE MORAES, CONSEULO - Eth Zurich
item MESCHER, MARK - Eth Zurich
item ZHAXYBAYEVA, OLGA - Dartmouth College

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/26/2016
Publication Date: 2/7/2016
Publication URL: https://handle.nal.usda.gov/10113/62710
Citation: Shapiro, L.R., Scully, E.D., Straub, T.J., Park, J., Stephenson, A.G., Beattie, G., Gleason, M., Kolter, R., Coelho, M., De Moraes, C.M., Mescher, M.C., Zhaxybayeva, O. 2016. Horizontal gene acquisitions, mobile element proliferation, and genome decay in the host-restricted plant pathogen erwinia tracheiphila. Genome Biology and Evolution. 8(3):649-664.

Interpretive Summary: Modern agricultural practices rely on growing dense populations of genetically identical plants, which can promote the emergence and spread of pathogenic bacteria. Erwinia tracheilphila has recently emerged as an economically devastating bacterial pathogen of squashes and gourds in the Northeastern and Midwestern United States. It is transmitted from plant to plant by striped cucumber beetles, which deposit the bacteria on plant surfaces while feeding. This pathogen has already caused large scale agricultural losses, but little is known about how this pathogen circumvents plant immune systems, interacts with striped cucumber beetles, and invades plant tissues. Recently, the genomes of four different strains of this bacterial pathogen collected from infected plants in New York and Pennsylvania were sequenced, allowing us to investigate the mechanisms by which this pathogen evolved to occupy its current role. The genomes of the strains that infect squashes have acquired large numbers of genes from other bacterial species, which are predicted to have key roles in attaching to insects, evading host plant immune systems, and infecting plant tissues. The genome also contains large numbers of mobile elements. These features lead us to hypothesize that the Erwinia tracheilphila strains that infect squashes emerged recently and are still rapidly evolving. Understanding how this pathogen emerged and how it interacts with its insects and plants will allow us to determine why it causes such severe symptoms in infected plants and subsequently, to develop better control mechanisms.

Technical Abstract: Modern industrial agriculture depends on high-density cultivation of genetically similar crop plants, creating favorable conditions for the emergence of novel pathogens with increased fitness in managed compared with ecologically intact settings. Here, we present the genome sequence of six strains of the cucurbit bacterial wilt pathogen Erwinia tracheiphila (Enterobacteriaceae) isolated from infected squash plants in New York, Pennsylvania, Kentucky, and Michigan. These genomes exhibit a high proportion of recent horizontal gene acquisitions, invasion and remarkable amplification of mobile genetic elements, and pseudogenization of approximately 20% of the coding sequences. These genome attributes indicate that E. tracheiphila recently emerged as a host-restricted pathogen. Furthermore, chromosomal rearrangements associated with phage and transposable element proliferation contribute to substantial differences in gene content and genetic architecture between the six E. tracheiphila strains and other Erwinia species. Together, these data lead us to hypothesize that E. tracheiphila has undergone recent evolution through both genome decay (pseudogenization) and genome expansion (horizontal gene transfer and mobile element amplification). Despite evidence of dramatic genomic changes, the six strains are genetically monomorphic, suggesting a recent population bottleneck and emergence into E. tracheiphila’s current ecological niche.