Pangenomic Analysis of Dickeya Dianthicola Strains Reveals the Outbreak of Blackleg and Soft Rot of Potatoes in USA

Authors: GE, T. - University Of Maine; JIANG, H. - University Of Maine; TAN, E. - University Of Maine; JOHNSON, S. - University Of Maine Cooperative Extension; Larkin, Robert - Bob; CHARKOWSKI, A. - Colorado State University; SECOR, G. - North Dakota State University; HAO, J. - University Of Maine

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/30/2021
Publication Date: 7/2/2021
Citation: Ge, T., Jiang, H., Tan, E.H., Johnson, S.B., Larkin, R.P., Charkowski, A.O., Secor, G., Hao, J. 2021. Pangenomic analysis of Dickeya dianthicola strains reveals the outbreak of blackleg and soft rot of potatoes in USA. Plant Disease. https://doi.org/10.1094/PDIS-03-21-0587-RE.
DOI: https://doi.org/10.1094/PDIS-03-21-0587-RE

Interpretive Summary: A major outbreak of a serious and damaging disease of potato plants, known as blackleg and soft rot of potato, caused primarily by the bacterial pathogen Dickeya dianthicola, has resulted in significant economic losses in the Northeastern United States since 2015. To investigate the genetic diversity among the strains involved in this outbreak and to compare these to previously reported strains of the pathogen, a comparative analysis was conducted on whole genomes of D. dianthicola strains isolated from outbreak samples with database reference strains. Whole genomes of 16 strains from the U.S. outbreak were fully assembled for this study and compared to 16 reference genomes from previously observed strains from around the world. Among the 32 strains, eight distinct clades were distinguished based on phylogenomic analysis. The outbreak strains were grouped into three clades, with most of the strains in clade I. All clade I strains were nearly identical and distinctly different from all previously known strains of D. dianthicola strains, suggesting a recent development and introduction of this strain into potato production. Some genes associated with pathogen virulence were found to be enhanced in this clade compared to others, and may be related to the dominant role this strain played in the outbreak. This research is useful for researchers to identify and understand the genetic variability of this pathogen and disease epidemiology, and can be used to improve control strategies and mitigate disease losses.

Technical Abstract: The bacterial pathogen Dickeya dianthicola has caused a serious outbreak of blackleg and soft rot (BSR) disease of potato throughout the eastern half of the U.S. since 2015. To investigate genetic diversity of the strains involved in this outbreak, a comparative analysis was conducted on whole genomes of D. dianthicola strains isolated from outbreak samples with reference strains. Whole genomes of 16 strains from the U.S. outbreak were fully assembled for this study and compared to 16 reference genomes retrieved from the NCBI GenBank. Among the 32 strains, eight distinct clades were distinguished based on phylogenomic analysis. The outbreak strains were grouped into three clades, with most of the strains in clade I. Clade I strains were homogeneous and distinct from previously reported D. dianthicola strains, suggesting a recent incursion of this strain into potato production from alternative hosts or environmental sources. The 32 D. dianthicola strains shared 3377 core proteins and 6693 pan-proteins. We screened and identified primary protein subunits associated with virulence from all three clades on U.S. strains. Virulence-related gene clusters, such as plant cell wall degrading enzyme genes, flagellar and chemotaxis related genes, two-component regulatory genes, and type I/II/III secretion system genes were highly conserved. But type IV and type VI secretion system genes varied among strains. Our whole genome analysis revealed that the virulent clade I strains encoded two type IV secretion systems, while clade II and III strains encoded only one cluster. Clade I and II strains encoded one more VgrG/PAAR spike protein than clade III. Thus, the presence of additional virulence-related genes may have enabled the unique clade 1 strain to become the predominant source of the US outbreak.